Bio e Stimulant Es

Scientia Horticulturae 267 (2020) 109330
Contents lists available at ScienceDirect
Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti
Review
Appraisal of emerging crop management opportunities in fruit trees, T

grapevines and berry crops facilitated by the application of biostimulants
Boris Basilea,*, Youssef Rouphaela, Giuseppe Collab, Sebastian Soppelsac,1, Carlo Andreottic,*
a
Department of Agricultural Sciences, University of Naples Federico II, Portici (Naples), Italy
b
Department of Agriculture and Forest Sciences, University of Tuscia, 01100 Viterbo, Italy
c
Faculty of Science and Technology, Free University of Bozen-Bolzano, Piazza Università, 5-39100 Bozen-Bolzano, Italy
ARTICLE INFO ABSTRACT
Keywords: The fruit crop industry is continuously seeking for new technologies able to improve the overall sustainability of
Fruit species the production systems together with an enhancement of quality and safety of the products. Over the last 10
Nutrient use efficiency years, plant biostimulants have emerged as new and promising production tool able to increase the use efficiency
Abiotic stress of other agronomical inputs (i.e. irrigation water and fertilizers), to promote crop tolerance toward different
Drought tolerance
abiotic stressors (i.e. drought, salinity, extreme temperature and radiation) and to enhance the final quality of
AMF
food products. Despite the considerable amount of researches that have been conducted to elucidate the mode of
PGPR
Fruit quality action of plant biostimulants and their agronomical performances, the number of studies focusing on fruit crops
is relatively limited and the current knowledge on the interaction of these substances with the fruit tree growth
and physiology is still largely incomplete. This review provides a complete scientific overview of the available
literature on the experimental application and the physiological mechanisms of plant biostimulants on the most
relevant fruit crops, including berry crops, grapevine, olive, citrus fruits, pome fruits, stone fruits and other fruit
species. Following the functional claims currently used for the biostimulants definition at European level, the
review is articulated in sections focusing on i) the evidences of the biostimulants implication for fruit tree
resistance toward abiotic stresses (drought, salinity and thermal extremes); ii) the evidences of the biostimulants
capacity to enhance nutrients use efficiency in fruit crops; iii) the evidences of the biostimulants effects on tree
yield and final fruit quality. Overall, the potentiality of plant biostimulants to be successfully integrated within
the current management of modern orchards and vineyards emerges as clear. There are anyway aspects typically
linked to the perennial nature of fruit trees (i.e. the carry-over effect of previous seasons on the tree internal
reserves) or the different environmental conditions imposed by the open-field cultivation systems that need to be
further investigated and that represent the future challenges for the research applied on the use of plant bios-
timulants for fruit crops.
1. Rationale (Rouphael and Colla, 2018; Xu and Geelen, 2018). Bio-based products
such as plant biostimulants, represent a sustainable and effective
Nowadays, the horticultural and agricultural sectors are facing complement for their synthetic counterparts (i.e, inorganic and organo-
concurrent challenges to boost crop productivity in order to feed the mineral fertilizers), bringing benefits to the biodiversity, environment,
increasing global population, that is foreseen to reach roughly 10 bil- human health and economy (Xu and Geelen, 2018; Souri and
lion by 2050 (UN, 2019); and concomitantly to minimize the excessive Bakhtiarizade, 2019).
use of agrochemicals (fertilizers and pesticides) which can negatively The definition of plant biostimulants has been rigorously debated
impact human health and the ecosystems (Searchinger et al., 2013; over the last 8 years, substantially regarding regulatory framework
Noroozlo et al., 2019). To this end, modern horticulture needs to review purposes (du Jardin, 2012, 2015; Traon et al., 2014; La Torre et al.,
and broaden its practices, by integrating opportunities and technolo- 2016; Yakhin et al., 2017; Caradonia et al., 2019). In the recent reg-
gical innovations deriving from different adjacent sectors and value ulation (EU) 2019/1009 of the European Parliament and of the Council
chains, including the bio-based industry, in a circular economy strategy of 5 June 2019, plant biostimulants are defined as EU fertilizing
⁎
Corresponding authors.
E-mail addresses: boris.basile@unina.it (B. Basile), carlo.andreotti@unibz.it (C. Andreotti).
1
Present address: Laimburg Research Centre, 39051 Vadena-Pfatten, Italy.
https://doi.org/10.1016/j.scienta.2020.109330
Received 7 November 2019; Received in revised form 27 February 2020; Accepted 28 February 2020
0304-4238/ © 2020 Elsevier B.V. All rights reserved.
B. Basile, et al. Scientia Horticulturae 267 (2020) 109330
products (EU, 2019). Under the new regulation, plant biostimulants are optimized fertilizers application. To our knowledge, this is the first
defined as follows: ‘A plant biostimulant shall be an EU fertilising product review paper concerning the impact of microbial and non-microbial
the function of which is to stimulate plant nutrition processes independently plant biostimulants on fruit trees, grapevines and berry crops. The main
of the product’s nutrient content with the sole aim of improving one or more objective of the current review is to provide an updated scientific
of the following characteristics of the plant or the plant rhizosphere: i) nu- overview on the potential benefits of plant biostimulants on growth,
trient use efficiency, ii) tolerance to abiotic stress, iii) quality traits, or iv) yield potential, nutritional and functional quality of citrus, grapevine,
availability of confined nutrients in the soil or rhizosphere’ (EU, 2019). pome fruits, stone fruits, other fruit tree species and berry crops. As well
Based on this definition, plant biostimulants are specified on the basis as to unravel the physiological and molecular mechanism(s) mediating
of agricultural functions claims (Rouphael et al., 2018a) and include these stimulation effects and the impact of plant biostimulants appli-
diverse bioactive natural substances (humic and fluvic acids, animal cation on the resilience to abiotic stressors and the modulation of pri-
and vegetal protein hydrolysates, macroalgae [seaweeds] extracts and mary and secondary metabolism. This review paper concludes by pro-
silicon) as well as beneficial microorganisms (arbuscular mycorrhizal posing further investigation and research that scientists, extension
fungi and N-fixing bacteria of strains belonging to the genera Rhizobium specialists and private industries should focus on to increase the effi-
spp. Azotobacter and Azospirillum) (Calvo et al., 2014; Battacharyya cacy of plant biostimulants.
et al., 2015; Canellas et al., 2015; Colla et al., 2015, 2017; Haplern
et al., 2015; Rouphael et al., 2015; Ruzzi and Aroca, 2015; Bitterlich 2. Implications of plant biostimulants for tolerance to abiotic
et al., 2018). stresses
In general, plant biostimulants at low concentrations are even
capable of inducing an array of biochemical, physiological and mole- Abiotic stressors in particular drought, extreme temperatures and
cular plant responses such as improving flowering, plant growth and salinity in soil and water are responsible for 60–70 % of the yield gap
yield, boosting the nutritional and functional quality of the edible (i.e., the gap between actual and yield potential) dictated by global
product and its shelf life. Furthermore, the applications of microbial climate changes (Rouphael et al., 2012; Rouphael et al., 2017a). Oxi-
and non-microbial plant biostimulants have been reported to enhance dative stress, which frequently accompanies environmental stresses, has
nutrient use efficiency and tolerance to abiotic stressors such as been reported to disturb several morpho-anatomical, biochemical,
drought, extreme temperatures and salinity (Calvo et al., 2014; Bulgari metabolomic, molecular and physiological processes leading to stunted
et al., 2015; Haplern et al., 2015; Povero et al., 2016; Yakhin et al., growth and economically relevant yield losses (Wang et al., 2003). In
2017). Recent review papers aimed at uncovering the physiological and order to overcome the current situation, plant biostimulants has been
molecular mechanisms that regulate the biostimulation action of these suggested as one of the most promising drives for securing yield sta-
products, which can i) stimulate the C and N metabolism by triggering bility under unfavorable environmental and soil conditions (Rouphael
key enzymes, ii) increase the antioxidant defense system and the pro- et al., 2018b). The effectiveness of plant biostimulants in imparting
duction of secondary metabolites, iii) improve the photosynthetic ac- tolerance/avoidance of agricultural and horticultural crops against
tivity and water relations, iv) enhance the soil chemical and physical abiotic stressors has been associated to several direct and indirect me-
characteristics, v) trigger hormone-like activities in particular auxins, chanisms affecting plant biochemistry and physiology, including: i)
cytokinins and gibberellins), vi) enhance the epiphytic and rhizosphere improved nutrient uptake and assimilation due to a more vigorous root
microbial populations and vii) modulate the root system apparatus in system architecture (higher root biomass, length, volume and
terms of biomass, root hair branching, density, diameter, length and branching), ii) enhanced photosynthetic efficiency and leaf water re-
volume of soil/substrate exploited (García-Mina et al., 2004; Calvo lations, iii) increased accumulation of osmolytes such as glycine be-
et al., 2014; Haplern et al., 2015; Rouphael et al., 2017a, b, c, 2018b; taine, proline and sorbitol, iv) fortified antioxidant defense system
Bulgari et al., 2017; Ertani et al., 2017, 2018; Souri and Hatamian, (higher activity of antioxidant enzymes: superoxide dismutase (SOD)
2019). Despite the prominent advancements that have been elucidated and catalase (CAT) and lower oxidative stressors hydrogen peroxide
on the molecular and physiological mechanisms of microbial and non- (H2O2) and malondialdehyde (MAD), v) improved intrinsic water use
microbial plant biostimulants, many remaining issues warrant further efficiency (reduced transpiration and stomatal resistance and increased
investigations concerning their optimal application method (foliar or root-to-shoot ratio), vi) differential regulation of key genes involved in
drench), intervention time (before, during or after stress and phenolo- detoxification of Reactive Oxygen Species (ROS) and the production of
gical stages), application rate (Souri and Tohidloo, 2019), environ- osmolytes and vii) modulated epiphytic microbial populations that
mental conditions, crop management practices, and species/cultivars enhance plant growth (Calvo et al., 2014; Battacharyya et al., 2015;
response and how the biostimulation action may change in relation to Colla et al., 2015, 2017; Rouphael et al., 2015; Rouphael and Colla,
those interacting variables. 2018; Fiorentino et al., 2018; Luziatelli et al., 2019; Souri and
The beneficial effect of plant biostimulants cannot be generalized Hatamian, 2019). The literature concerning the use of plant biostimu-
for all types of crops. For instance, the stimulation action of plant lants to enhance tolerance toward abiotic stresses of selected fruit
biostimulants in the fruit production industry is not always consistent in species is summarized in Table 1.
terms of efficacy, compared to other crops (annual species, ornamentals
and vegetable) grown under greenhouse conditions. This could be at- 2.1. Drought
tributed to the higher application frequency and the favorable climatic
conditions in controlled environments (i.e., higher relative humidity) 2.1.1. Citrus
which may improve the leaf permeability and consequently the bios- The available literature reporting on the use of plant biostimulants
timulant efficacy (Colla and Rouphael, 2019). In addition, the carry- to contrast water stress effects is still limited for many fruit crops, even
over effect of the previous seasons on the organic and inorganic tree though some interesting indications are already available especially for
reserves can interfere with the direct potency of the applied biostimu- the citrus group of species. The application, both as foliar spray or as
lant, hindering their potentialities on plant metabolism. Moreover, the soil drench, of a seaweed extract from Ascophyllum nodosum was found
results consistency can be affected by the different climatic conditions to mitigate the negative effects of water stress in young orange (Citrus
occurring year after year in open-field cultivation systems. Despite sinensis (L.) Osbeck) trees (cv. ‘Hamlin’) grafted on citrange (cvs.
these limitations, interest in plant biostimulants in fruit trees, grape- ‘Carrizo’ and ‘Swingle’) and subjected to two differential water regimes
vines and berry crops sector is on the rise and urged by the high interest (100 % and 50 % of the evapotranspiration) (Spann and Little, 2011).
of fruit production industry, private companies and scientists, in en- Trees grown under pot conditions and treated with the seaweed extract
hancing quality, yield under optimal and sub-optimal conditions, and had higher vegetative growth (longer shoots, bigger leaf area and
2
Table 1
Effects of microbial and non-microbial biostimulants on the agronomical, biochemical, molecular and physiological performances of fruit crops under abiotic stress conditions.
Fruit crop Biostimulant Mode and rate of application Growing conditions Abiotic stress (drought) Stress tolerance mechanism(s) References
B. Basile, et al.
Grapevine Marine active substances Foliar application Potted plants in One water regime (irrigation Increased midday leaf water potential, stomatal conductance and Mancuso et al.
extracted from seaweeds Dosage: 0.1 % greenhouse was withheld for 6 days and leaf net-CO2 exchange rates. (2006)
then reapplied)
Grapevine AMF (Glomus mosseae) Soil application (50 cm3 of Potted plants Two water regimes (100 % Increased pre-dawn leaf water potential, stomatal conductance Nikolaou et al.
inoculum per pot) field capacity and no irrigation and leaf net-CO2 exchange rates (2003)
applied)
Loquat AMF (Funneliformis mosseae) 300 g of mycorrhizal Potted plants in Two water regimes (75 % and Increased dry biomass and leaf water potential. Zhang et al.
inoculum per plant, added growth chamber 45 % of field capacity) Increased water stress tolerance due to osmotic adjustments at (2015)
near roots root level (high proline concentration) and to the anti-oxidative
molecule (i.e. glutathione).
Mango Potassium silicate Drench application, every Field trial Two water regimes (water Enhanced vegetative and productive growth. Increased tolerance Helaly et al.
two weeks at the rate of 1.5 potential Ψs: -0.18 and -0.77 to water stressed conditions. Reduced harmful effects of Reactive (2017)
mM Si bars) Oxygen Species.
Orange Seaweed extract (Ascophyllum 5 ml L−1 as a soil drench or Unshaded Two irrigation regimes (100 % Increased vegetative growth and water use efficiency. Spann and Little
nodosum) foliar spray, once per week greenhouse and 50 % of ET) (2011)
Pistachio AMF (Glomus etunicatum) 100 g of mycorrhizal Potted plants in Two water regimes (100 % and Enhanced drought tolerance. Increased plant growth and shoot Abbaspour et al.
inoculum per plant, applied greenhouse 50 % of water holding nutrient concentration (P, K, Zn and Cu). Enhancement of (2012)
to soil capacity) antioxidant enzyme activities and osmotic adjustment (high level
of soluble sugars, proline in leaves).
Strawberry AMF (Funneliformis mosseae A single soil application Potted plants Two irrigation regimes (100 % Improved plant growth (root and shoot weight) and water use Boyer et al.
BEG25, Funneliformis geosporus and 60–70 % of ETc) efficiency. (2015)
BEG11)
Strawberry Seaweed extract (species not Four foliar sprays. Dosage: High tunnel Four irrigation regimes (0.5, Improved total soluble solids, fructose, sucrose and quercetin Kapur et al.
reported) 1.33 g L−1 0.75, 1.00 and 1.25 of ETc) content of the fruit. (2018)
Tangerine orange AMF (Glomus mosseae) Soil application (0, 5, 10, 20 Potted plants No stress Mycorrhization increased root system architecture traits (e.g. Wu et al. (2012)
3
and 40 g of inoculum per total length, surface area, volume). Leaf and root arginine and
pot) ornithine decarboxylase (ADC and ODC) activity were increased.
Stimulated the synthesis of polyamines (e.g. putrescine).
Tangerine orange AMF (Glomus versiforme) Soil application (30 g of Potted plants in Two water regimes (75 % and AM symbiosis stimulated plant growth and induced osmotic Wu et al. (2006)
inoculum per pot) greenhouse 55 % of relative soil water adjustments (not from proline, but from non-structural
content) carbohydrates, K+, Ca2+ and Mg2+). Increased leaf water
potential, transpiration rates, photosynthetic rate, stomatal
conductance, relative water content and reduced leaf
temperature.
Trifoliate orange AMF (Funneliformis mosseae and Soil application (1000 spores Potted plants in Two water regimes (70 % and AM-hyphal system contributed to water absorption. Increased Zhang et al.
Paraglomus occultum) per pot) greenhouse 50 % field capacity) leaf water potential. (2018)
Trifoliate orange, AMF (Funneliformis mosseae) Soil application (20 g of Potted plants in No stress Improved structure and aggregate stability of rhizospheric soils Wu et al. (2014)
Tangerine orange, inoculum per pot) greenhouse with positive consequences on water availability, plant growth
Kumquat performances and root morphological traits. Glue-functioning
mechanism promoted by AM at the rhizospheric level, with
positive effect on the soil structure development.
Trifoliate orange AMF (Funneliformis mosseae and Soil application (1000 spores Potted plants in Two water regimes (70 % and AMF-treated seedlings increased leaf sucrose, glucose and Wu et al. (2017)
Paraglomus occultum) per pot) greenhouse 50 % field capacity) fructose. Lower proline accumulation in AMF plants under
drought stress.
Trifoliate orange AMF (Funneliformis mosseae) Soil application (120 g of Potted plants in Two water regimes (75 % and Enhanced leaf relative water content, leaf water potential, and Jia-Dong et al.
inoculum per pot) greenhouse 55 % field capacity) plant growth performance, as well as root ABA levels. Up- and (2019)
down-regulation of some aquaporin genes.
Fruit crop Biostimulant Mode and rate of application Growing Abiotic stress (salinity) Stress tolerance mechanism(s) References
conditions
(continued on next page)

Table 1 (continued)
Fruit crop Biostimulant Mode and rate of application Growing Abiotic stress (salinity) Stress tolerance mechanism(s) References
conditions
B. Basile, et al.
Apple AMF (Glomus versiforme) Drench application (100 ml of Potted plants Four salinity levels (NaCl: 0, Higher leaf turgidity. Increased root length colonization Yang et al.
inoculum) 2‰, 4‰ and 6‰) of AMF apple plants. Defence mechanism against reactive (2014)
oxidative species developed by AMF plants (high
ascorbate peroxidase and catalase activities). High
K+/Na+ ratio.
Date palm AMF (Glomus mosseae), PGPB (Azospirillum Soil drench application with 85 ml Field trial Plants were irrigated with Reduced salt-induced oxidative damage. Increased Naser et al.
lipoferum, Paenibacillus polymyxa and Bacillus (108 cells ml−1) per plant saline water and grown in photosynthetic pigments, antioxidant enzyme activity, (2016)
circulans) and putrescine amine reclaimed saline soil organic solutes and promoting growth substances (e.g.
gibberellic acid, auxins and cytokinin). Decreased lipid
peroxidation and abscisic acid level.
Grapevine Potassium silicate (K2SiO3ˑ9H2O) Soil application Potted plants in Plants exposed to 0 and 100 Increased leaf-area expansion rates, plant height growth, Qin et al.
Dosage: (2 mM) greenhouse mM NaCl leaf photosynthesis, maximum yield and potential (2016)
photochemical efficiency of the photochemical reactions
in photosystem II.
Persimmon Protein hydrolysate (from animal origin) Soil drench application (5 L ha−1, Field trial Soil in salinity condition Reduced Cl− uptake, leaf necrosis, and leaf water Visconti et al.
neutralised with calcium salts every 8 days, 7 times in 2012 and 23 L potential. Enhanced biosynthesis of salt-stress-response (2015)
ha−1, every 6 days, 24 times in 2013) proteins.
Strawberry AMF (Funneliformis caledonius, Funneliformis Soil application (100 or 50 fungal Potted plants in Four salinity levels (100 ml of AMF improved salt tolerance and increased shoot and Sinclair et al.
mosseae and Rhizophagus irregularis) propagules per plant) greenhouse salt solution containing 0, 50, root mass in treated plants. Genotype-specific effect of (2014)
100 or 200 mM NaCl) AMF inoculation.
Strawberry Potassium silicate Soil drench application. Once per Potted plants in Two salinity level (0 and 50 Increased peroxidase and superoxide dismutase enzyme Yaghubi et al.
week. Dosage: 1000 or 1500 ppm greenhouse mM NaCl, added to nutrient activity. Reduction of proline content. Increased fruit (2016)
solution) yield.
Strawberry PGPB (Bacillus subtilis EY2, Bacillus atrophaeus Root dipping in bacterial suspensions Potted plants in Two salinity levels (0 and 35 Sodium and chloride leaf and root content was reduced Karlidag et al.
EY6, Bacillus spharicus GC subgrup B EY30, (108 CFU ml−1) for 30 min. greenhouse mM of NaCl, added to the by PGPR inoculation. Increased leaf relative water (2011)
4
Staphylococcus kloosii EY37 and Kocuria nutrient solution) content and final yield.
erythromyxa EY43)
Tangerine AMF (Glomus mosseae and Paraglomus occultum) Soil application Potted plants in Plants exposed to 0 and 100 Increased plant growth (height, stem diameter, shoot, Wu et al.
orange greenhouse mM NaCl root and total plant biomass) and physiological (2010)
performances (photosynthetic rate, transpiration rate and
stomatal conductance) by AMF plants.
Fruit crop Biostimulant Mode and rate of application Growing conditions Abiotic stress (thermal Stress tolerance mechanism(s) References
stress)
Apple Carnauba wax Three foliar applications at 12.5 % (v/v) with Field trial High solar radiation and Reduced sunburn damage. Decreased fruit surface temperature and Schrader (2011)
water high temperature stress transmission of ultraviolet radiation.
Blueberry AMF (Glomus mosseae) Soil application Potted plants in Cold stress Higher superoxide dismutase, ascorbate peroxidase, guaiacol Liu et al. (2017)
greenhouse and growth peroxidase activities in AMF inoculated plants. Enhanced soluble
chamber sugar, proline ascorbate and glutathione accumulation in AMF
treated plants.
Grapevine PGPB (Burkholderia Immersion of the nodal explants (106 CFU In vitro Cold stress Increased plant biomass, leaf photosynthesis and levels of cold- Ait Barka et al.
phytofirmans PsJN) ml−1 bacterial suspension) stress-related metabolites (starch, proline, and phenolics); (2006)
decreased electrolyte leakage from leaves.
higher shoots and leaves dry weight), independently of the type of
Marfà et al. (2009)
Gunes et al. (2016)

rootstock used. Differently, the calculated water use efficiency (either
Theocharis et al.
Bogunovic et al.
Fernandez et al.
Sharma et al.
intrinsic or agronomical based on the whole biomass produced) was
References
(2012) significantly higher for the treated trees which were water-stressed and
(2012)
(2018)
(2016)
grafted on the ‘Swingle’ rootstock. The authors explained these out-
comes as a consequence of the different rootstocks susceptibility to
water stress and indicated the changes in the hormonal metabolism and
Increased yield, antioxidant enzyme activities and decreased freeze

Increased plant biomass. Early flowering, and early production of
Reduced sunburn, fruit cracking and incidence of fruit borer and
related sugars (glucose, sucrose, and raffinose with its precursor,
bacterial blight. Treated fruits showed higher red colour, sugar, phenolics accumulation as a possible physiological putative mechanism
Increased total soluble sugars, starch and single cold-tolerance
Stress-related gene transcripts and metabolite levels increased
(Spann and Little, 2011). Microbial biostimulants based on arbuscular

mycorrhizal fungi (AMF) were also reported to promote tolerance of
citrus plants toward drought stress. The mechanisms involved in such
tolerance are different and have been exhaustively reviewed by Wu
et al. (2013). The citrus root system architecture (root length, surface
earlier and faster, and reached higher levels
area and volume) can be altered by the AMF inoculation, leading to an

increased water uptake (Wu et al., 2012). Moreover, the contribution of
Enhanced resistance to frost damages.
phenolic and anthocyanin content.
the hyphal system to the water absorption was found significantly

higher (2–7 times) for citrus plants under water stress (irrigation sup-
Stress tolerance mechanism(s)
plies at 55 % of maximum water holding capacity of soils) than in well

water conditions (75 % of maximum water holding capacity), in-
fruit under cold stress.
dependently from the AMF used for the inoculum (Zhang et al., 2018).
AMF inoculation also induced osmotic adjustments in trifoliate orange
[Poncirus trifoliata (L.) Raf.] trees grown in controlled substrate condi-
galactinol).
tions, allowing improved plant growth performances and higher leaf

injury.
relative water content under drought stress (Wu et al., 2006, 2017). In
more detail, the concentration of osmotically active substances, both
inorganic (K+ and Ca2+) and organic (sucrose, glucose and fructose),
High solar radiation and
high temperature stress
were found higher in leaves of AMF-inoculated plants under drought

Abiotic stress (thermal
stress, whereas proline (also involved in the osmotic adjustment) was

reduced as compared with non-inoculated plants because of a higher
activity of the proline-catabolic enzymes. AMF were also able to im-
Cold stress
Cold stress
Cold stress
Cold stress
Cold stress
prove structure and aggregate stability of rhizospheric soils with posi-

stress)
tive consequences on water availability and plant growth performances.

These effects were measured on trifoliate orange where a positive
correlation was obtained between root colonization or soil hyphal
length and the extractable soil glomalin concentration (Wu et al.,
Growing conditions
2014). Glomalin is a glycoprotein released by an AMF into soil during

hyphal turnover or death, and is considered responsible for the glue-
functioning mechanism at the rhizospheric level with positive effect on
Field trial
Field trial
Field trial
Field trial
the soil structure development (Wu et al., 2013). Recently, Jia-Dong

In vitro
In vitro
et al. (2019) investigated the role of aquaporins (i.e. proteinaceous

pores present in cell membrane and involved on water transport in
Four drench applications. Dosage: 0.5, 1.0 and
Foliar spray and soil application (10 % boron

Root immersion (3 × 108 CFU ml−1 bacterial
Five foliar sprays (3% concentration), applied
Soil drench application (5 times). Dosage: 2.5
plants) at root level in the enhanced growth performances and water

Root dipping (3 × 108 CFU ml−1 bacterial
status of trifoliate orange plants subjected to water stress and AMF

and 109 CFU ml−1 bacterial suspension).
inoculation. Aquaporin genes were found both up and down regulated,

underlining the diverse response and complex mechanisms of aqua-
porins to mycorrhization and drought stress.
Mode and rate of application
2.1.2. Grapevine
at fortnightly intervals
Some studies have focused on the possible application of different

Dosage: 90 L ha−1
classes of plant biostimulants for mitigating the effects of drought stress

1.5 g plant−1
also on grapevines (Vitis vinifera L.). Mancuso et al. (2006) reported

suspension)
suspension)
that, in a water stress experiment conducted in pots under controlled

g L−1
conditions (greenhouse), the foliar application (twice a week) of a

commercial seaweed extract of unspecified origin and composition in-
duced a significant increase in midday leaf water potential of ‘San-
Protein hydrolysate from
Boron and plant growth

Amino-acids of animal
giovese’ grapevines (grafted onto 420A) compared to the untreated

PGPB (Burkholderia
PGPB (Burkholderia
promoting bacteria
phytofirmans PsJN)
phytofirmans PsJN)
control vines. This improvement in vine water status of treated plants

was translated in increased values of stomatal conductance and leaf net-
animal origin
Biostimulant
CO2 exchange rates. In another research carried out in pots, Nikolaou

et al. (2003) studied the effects of pre-transplant soil inoculation with
Kaolin
origin
Table 1 (continued)
the mycorrhizal fungi Glomus mosseae on the drought tolerance of

‘Cabernet sauvignon’ vines grafted onto eight rootstocks. The results
Pomegranate
indicated that, after 5–8 days without irrigation, mycorrhizal vines had
Strawberry
Strawberry
Strawberry
Grapevine
Grapevine
Fruit crop
higher pre-dawn leaf water potential, stomatal conductance and leaf

net-CO2 exchange rates compared to non-mycorrhizal vines, even
though the intensity and the significance of these effects strongly
5
depended on the rootstock. The importance of the mycorrhizal sym- The authors also suggested 2‰ and 4‰ salt concentration as the upper
biosis for grapevines under water stress was also highlighted by the thresholds of salinity tolerance for non-mycorrhizal and mycorrhizal
results of Schreiner et al. (2007). The authors reported that, in own- apple seedlings (Yang et al., 2014).
rooted ‘Cabernet sauvignon’ vines, deficit irrigation applied early or
late in berry development caused a decrease in fine root density, but 2.2.2. Citrus
this appeared to be compensated by an increase in arbuscular coloni- Salt tolerance was enhanced by mycorrhization in red tangerine
zation. (Citrus tangerine Hort. ex Tanaka) seedlings (Wu et al., 2010). Plants
inoculated with G. mossae and Pyrodictium occultum showed greater
2.1.3. Other fruit crops vegetative growth (higher plant height, stem diameter and total bio-
As for the use of plant biostimulants to mitigate water stress on mass) and physiological performances (better photosynthetic and
other fruit crops, the repeated canopy application of a commercial ex- transpiration rates, stomatal conductance) under both non-saline and
tract of undefined seaweed species on strawberries (Fragaria × ana- saline stress conditions (0 and 100 mM NaCl, respectively). Authors
nassa Duch. cv. ‘Rubygem’) allowed to increase significantly the final explained the enhanced tolerance to salinity stress as the result of the
yield of treated plants under drought conditions (Kapur et al., 2018). combined effect of AMF on root morphology and the ionic status of the
The benefit obtained with the use of the plant biostimulants decreased cells (higher K+/Na+ and Ca2+/ Na+ ratios).
with the increase of the irrigation water applied. These results have to
be ascribed to the positive effect of the seaweed applications on the 2.2.3. Grapevine
plants canopy surface development (higher leaf area) and, conse- Recent research suggests that silicon can mitigate the negative ef-
quently, on their light interception and photosynthetic performances. fects of salinity on grapevine physiology (Qin et al., 2016). The authors
AMF inoculation also improved the vegetative growth of strawberry reported that soil application of potassium silicate (2 mM solution of
plants (cv. Everest) under dry or wet regime (Boyer et al., 2015). More K2SiO3ˑ9H2O) significantly stimulated leaf-area expansion rates and
in detail, the use of two AMF (Funnelliformis mosseae and Funnelliformis plant height growth of 1-year old ‘Cabernet sauvignon’ cuttings exposed
geosporus), alone or in combination, restored plant growth under dry to saline stress (100 mM of NaCl). These effects were associated with
conditions at the same or higher levels than the fully irrigated control. the mitigation of the negative influence of salinity on leaf photo-
AMF increased dry biomass accumulation and leaf water potential synthesis, probably because silicon plays a significant role in the pro-
of drought-stressed loquat (Eriobotrya japonica Lindl.) plants grown in tection of the photosynthetic machinery. This effect was also suggested
pots (Zhang et al., 2015). The higher drought tolerance of AMF-in- by the increase in maximum yield and potential photochemical effi-
oculated plants was linked to osmotic adjustments at root level as ciency of the photochemical reactions in photosystem II obtained after
shown by the higher concentration of proline as compared to non-in- the application of potassium silicate in salt stressed vines.
oculated control. Moreover, the anti-oxidative molecule glutathione
was found higher in inoculated loquat plants under drought stress, 2.2.4. Other fruit crops
therefore signaling a protection reaction against the ROS typical of The use of a biostimulant product based on a calcium protein hy-
stress conditions. This result, in combination with the lower activity of drolysate (CPH) of animal origin was tested on persimmon [Diospyros
the antioxidant enzyme SOD, proved that the AMF-inoculated plants kaki (cv. ‘Rojo Brillante’)] trees grafted onto D. lotus and it was found
were less damaged by the drought (Zhang et al., 2015). Similar results able to improve the tolerance of persimmon trees to salt stress condi-
were also obtained on AMF-inoculated pistachio (Pistacia vera L.) tions (Visconti et al., 2015). In both years of the study, treated trees
seedlings under water shortage (Abbaspour et al., 2012). These evi- showed a significant decrease in chloride uptake and leaf necrosis and
dences suggest the existence of a complex metabolic reaction, which an increase in stem water potential in both years of the study. The
includes the enhancement of the antioxidant enzyme activities (POD at authors proposed two possible mechanisms able to explain the en-
shoot and root level and CAT at shoot level only), the osmotic adjust- hanced salt tolerance of CPH treated trees: i) the capacity of Ca2+ (one
ment (high soluble sugars in leaves) and the improvement of plant of the hydrolysate components) to promote plant ability to exclude the
nutritional status (higher accumulation of P, K, Zn and Cu). chloride ions from the root cells; and ii) the enhanced expression of the
Beneficial elements are those inorganic compounds that promote salt-stress response proteins triggered by the amino acids (proline,
plant growth and tolerance toward abiotic stress (Pilon-Smits et al., glycine, betaine) included in the CPH (Visconti et al., 2015).
2009). Among them, silicon (Si) is considered as a multi-function ele- The growth of plants of three strawberry cultivars (‘Albion’,
ment, often involved in different plant reaction mechanisms against ‘Charlotte’ and ‘Seascape’) under salt stress (NaCl concentration in the
stress conditions. Si applications supplied as K2SiO3 with the irrigation solution ranging from 0 to 200 mM) was enhanced by an AMF inoculum
system were reported to enhance the tolerance toward drought stress in with the species F. caledonius, F. mosseae and Rhizophagus irregularis
mango (Mangifera indica L.) trees of different cultivars (Helaly et al., (Sinclair et al., 2014). The mitigation effect at the highest NaCl con-
2017). Si supplies had an effect on metabolic pathways of mango plants centration was higher for R. irregularis, showing that AMF effectiveness
exposed to drought stress by increasing the efficacy of the scavenging was genotype- and condition-dependent. Drench applications of po-
system of the ROS and therefore improving the capacity of trees to tassium silicate in the nutrient solution (1000 ppm and 1500 ppm)
withstand arid conditions. counteracted the negative effect of saline stress (50 mM NaCl) in
strawberry plants cvs. ‘Kurdistan’ and ‘Paros’ (Yaghubi et al., 2016).
2.2. Salinity Salt-stressed plants treated with potassium silicate reduced the proline
content (osmotic adjustment) and improved the activation of anti-
2.2.1. Apple oxidant enzymes leading to a higher salt tolerance index for both cul-
The inoculum with the AMF can be considered as a possible way to tivars. On the majority of the tested variables, drench application of
enhance plant tolerance to salinity. Apple seedlings (Malus hupehensis 1000 ppm K2O3Si resulted as the most effective, allowing treated plants
Rehd.) under salinity stress and inoculated with AMF (Glomus versi- to increase final yield by 50 % compared to untreated salt-stressed
forme) maintained higher leaf turgidity despite a lower leaf osmotic plants (Yaghubi et al., 2016). Plant growth promoting bacteria (PGPB)
potential as compared to non-mycorrhizal plants (Yang et al., 2014). belonging to different genera (Bacillus, Staphylococcus and Kocuria)
The inoculated apple seedlings presented a more effective defense significantly increased (by 51%–94%) the final yield of strawberry
mechanism against ROS resulting from the salinity stress (higher as- plants cv. ‘Fern’ under saline conditions (35 mM NaCl added to the
corbate peroxidase and catalase activities) and showed a higher K+/ nutrient solution; Karlidag et al., 2011). Leaves of salt-stressed plants
Na+ ratio, therefore confirming a better adaptation to salinity stress. treated with the PGPB showed higher values of leaf relative water
6
content (approximately +15 % as compared to control) and N content. 2.3.3. Other fruit crops
Na+ and Cl− concentrations in leaves and Cl− content in roots were Lower fruit superficial temperature and reduced sunburn damages
significantly reduced by PGPB applications in comparison with stressed were obtained with kaolin, a particle film technology based on silicate
plants (control). This result suggests that the possible changes in the and alumina minerals, applied on pomegranate (Punica granatum L.)
exopolysaccharides produced in the rhizosphere by bacterial inocula- trees (Sharma et al., 2018). Treated pomegranates showed around 50 %
tion could have contributed to the enhanced plant tolerance to saline less sunburn and fruit cracking symptoms, as well as a reduced in-
stress (Karlidag et al., 2011). cidence of bacterial blight leading to high commercial value of the fruit
PGPB (Azospirillum lipoferum, Paenibacillus polymyxa and Bacillus on the market (Sharma et al., 2018).
ciraulans) alone or in combination with AMF and putrescine amine in- Drench application of a biostimulant based on amino acids of an-
creased nutritional status and sugar content of date palm (Phoenix imal origin enhanced growth and resistance to frost damages in
dactylifera L.) trees irrigated with saline water (Naser et al., 2016). The strawberry plants (cvs. ‘Alba’, ‘Asia’ and ‘Clery’; Bogunovic et al.,
enhanced tolerance of date palm trees was combined with a decreased 2015). Similarly, Marfà et al. (2009) found, under cold conditions, a
lipid peroxidation measured at young leaf level and with an increased higher dry mass accumulation in roots of newly transplanted straw-
activity of diamine oxidase and polyamine oxidase. The authors con- berry plants treated with an enzymatic hydrolysate obtained from an-
cluded that these results might be the consequence of different factors imal hemoglobin. In addition, freeze injuries of strawberry plants (cv.
(higher concentration of photosynthetic pigments, organic solutes and/ ‘Fern’) were reduced by foliar and/or soil applications of a biostimulant
or selected hormones, reduced production of polyamines), even though containing PGPR and 10 % boron (Gunes et al., 2016). Treated plants
the exact physiological mechanisms of date palm resistance toward salt had a significantly higher yield (+55 % as compared to untreated
stress remain unclear. control) and were characterized by a higher antioxidant enzyme ac-
tivity (CAT, POD and SOD) measured at leaf level. The use of AMF to
2.3. Thermal stress protect crops against low temperature stress was also studied on two
blueberry cultivars, respectively, from Vaccinium ashei (‘Britewell’) and
Extreme high or low temperatures are often limiting factors for V. corymbosum (‘Misty’) (Liu et al., 2017). The low temperature treat-
plant growth and crop productivity (Źróbek-Sokolnik, 2012). Plant re- ment (10 °C) decreased AMF (G. mosseae) development in both cultivars
sponse to thermal stress is generally represented by changes in the lipid as compared to optimal temperature (25 °C). ‘Britewell’ plants were
composition of cell membranes and by the activation of endogenous more dependent on AMF inoculation than ‘Misty’ plants, suggesting a
detoxification mechanisms (Iba, 2002). Very few studies investigating possible relevant role of the specific AFM-host interaction for the en-
these physiological responses are available for fruit crops. hanced tolerance toward low temperature stress. Inoculated blueberry
plants presented an enhanced tolerance toward low temperature as a
2.3.1. Apple result of an increased activity of antioxidant enzymes (SOD, APX,
The excessive solar radiation, often linked to global warming and GMX), lower superoxide and hydrogen peroxide production and higher
climate change, can cause a sharp increase of temperature at fruit level osmo-protectants accumulation (proline and soluble sugars). In addi-
leading to skin sunburns and overall loss of fruit quality (Racsko and tion, as described for other crops, AMF inoculations allowed an in-
Schrader, 2012). As protective system, apple fruits are generally char- creased uptake and accumulation of P and K in blueberry stems and
acterized by natural waxes located in the cuticle and pigments of the leaves under low temperature conditions, allowing inoculated plants to
epidermis, which are able to reflect and absorb ultraviolet (UV) ra- present a higher overall growth (Liu et al., 2017).
diations, therefore attenuating the harmful effect of UV (Schrader,
2011). Following this observation, the application of an emulsified
natural wax from carnauba palm (Copernicia prunifera) allowed to sig- 3. Implications of plant biostimulants for enhancing nutrient use
nificantly reduce sunburn incidence in different apple cultivars (‘Jo- efficiency
nagold’, ‘Fuji’ and ‘Cameo’) in orchard conditions (Schrader, 2011).
This effect was the result of the UV filtering property of the wax that did The use of natural substances (e.g. humic acids, protein hydro-
not cause neither phytotoxicity in leaves nor changes in the leaf gas lysates, seaweeds extracts) and/or microbial inoculants (PGPR and
exchanges. AMF) can represent a valuable tool to overcome nutrient limitation in
different crop systems by enhancing plant resilience and also by im-
2.3.2. Grapevine proving nutrient uptake and assimilation (De Pascale et al., 2017;
Different studies reported that the inoculation with plant growth- Mohammadipour and Souri, 2019; Souri and Bakhtiarizade, 2019).
promoting rhizobacterium (PGPR) can increase vine tolerance to low Biostimulant substances can increase nutrient availability for specific
temperatures in grapevines (Ait Barka et al., 2006; Fernandez et al., mineral nutrients through a partial modification of the soil physico-
2012; Theocharis et al., 2012). In an in-vitro experiment, Ait Barka chemical properties (e.g. pH, cation exchange capacity and/or reduc-
et al. (2006) reported that, in chilled Chardonnay plantlets, bacteriza- tion of the nutrient losses due to leaching) or by preventing in-
tion with Burkholderia phytofirmans (strain PsJN) induced an increase in solubilization of plant nutrients into the soil solution (e.g., metal-pep-
plant biomass and in leaf photosynthesis and a decrease in electrolyte tides/amino acids or metal-humic/fulvic acids complexation) (De
leakage from leaves compared to non-inoculated vines. These positive Pascale et al., 2017; Souri and Hatamian, 2019). Plant biostimulants
responses were associated with an increase, measured in chilled in- can also enhance root growth increasing root surface for nutrient up-
oculated-vines, in the levels of cold-stress-related metabolites (starch, take (Colla et al., 2015). Microbial-based biostimulants can increase
proline, and phenolics). Fernandez et al. (2012) confirmed that the nutrient uptake by enhancing the soil volume accessible to plant roots
increase in the cold tolerance in ‘Chardonnay’ vines bacterized with B. (e.g., mycorrhizae) and by making unavailable nutrient forms available
phytofirmans appeared mediated by significant changes in carbohydrate for plant uptake (e.g., nitrogen-fixation bacteria, PGPB able to solubi-
metabolism that lead to an increase in total soluble sugars, starch and in lize P, Fe, Mn, Zn). Increasing nutrient use efficiency, in particular for
single cold-tolerance related sugars such as glucose, sucrose, and raf- nitrogen, is fundamental for both economic and environmental reasons.
finose with its precursor, galactinol. An additional study focusing on the To underline the relevance of this specific property, the capacity of
metabolism of stress-related metabolites (proline, MDA, aldehydes and plant biostimulants to increase nutrient use efficiency has been listed
hydrogen peroxide) suggested that the cold acclimation induced by the among one of the claims supporting their placement on the market. In
B. phytofirmans endophyte in ‘Chardonnay’ vines occurs via the Table 2 are summarized studies about the use of plant biostimulants to
scavenging system (Theocharis et al., 2012). enhance the nutrient use efficiency of different fruit species.
7
Table 2
Effects of microbial and non-microbial biostimulants on nutrient uptake and nutrient use efficiency of fruit crops.
Fruit crop Biostimulant Mode and rate of application Growing conditions Crop performance and nutrient use/uptake efficiency References
B. Basile, et al.
Almond Seaweed extracts (Ascophyllum nodosum) Foliar application Potted plants in Increased vegetative growth and potassium uptake under Saa et al. (2015)
greenhouse potassium deficient conditions.
Apple AMF (Glomus mosseae, Glomus intraradices and Glomus Soil application Potted plants in Increase growth and percentage of actively growing apices Fortuna et al.
viscosum) greenhouse shown by AMF inoculated plants (similar results obtained (1996)
in plants fertilized with P).
Apple AMF (Glomus mosseae) Soil application Potted plants in Inoculation increased P uptake in all substrates. Plant Schubert and
greenhouse growth was enhanced by inoculation in two out of the Lubraco (2000)
three tested substrates.
Apple AMF (different commercial AMF inocula) Soil application and root dipping Potted plants in Increased plant growth. AMF inoculated plants showed Gąstoł et al.
greenhouse higher content of N, K, P and B in the shoots and N, S, Cu, (2016)
Fe, Mn, Mo and Ti in the roots.
Apple PGPB (Pseudomonas BA-8 and Bacillus OSU-142) Floral and foliar applications of bacterial suspension Field trial Stimulated plant growth and yield. Increased leaf nutrient Pirlak et al. (2007)
(109 CFU ml−1) concentration (N, P, K, Fe, Mn and Zn).
Apple PGPB (Bacillus OSU-142, Bacillus M-3, Burkholderia OSU-7 Root dipping in bacterial suspension (109 CFU ml−1) Field trial Increased vegetative and productive parameters. Higher Aslantaş et al.
and Pseudomonas BA-8) for 60 min. and syringe inoculation with 5 ml of level of plant growth hormones (e.g. indole-3-acetic acid, (2007)
bacterial suspension (109 CFU·ml−1) inoculated into cytokinins) in PGPR-treated plants.
the middle of the root plug
Apple PGPB (Klebsiella planticola TSHA-91 and Azotobacter, Soil application Field trial Increase of the fruit yield. Pešaković et al.
Pseudomonas and Bacillus genera with natural vitamins, (2017)
enzymes and growth stimulators)
Apricot AMF (Glomus fasciculatum) Soil application (50 g of inoculum per plant) Potted plants in Increased vegetative growth, leaf chlorophyll content, leaf Dutt et al. (2013)
growth chamber phenolic content, and nutrient content.
Grapevines Marine active substances extracted from seaweeds Foliar application Potted plants in Increased uptake rate per unit of root length of potassium Mancuso et al.
Dosage: 0.1 % greenhouse and calcium ions; increased magnesium leaf concentration (2006)
and vine growth.
8
Grapevines Marine active substances extracted from seaweeds Soil application Potted plants in Increased uptake rate per unit of root length of potassium Mugnai et al.
Dosage: 0.1 % greenhouse and ammonium ions; increased vine growth. (2008)
Grapevines AMF (Glomus mosseae, Glomus intraradices, and Soil application (20 g of inoculum per plant) Potted plants in Increased phosphorus uptake by roots and plant growth. Schreiner (2007)
Scutellospora calospora) greenhouse
Olive AMF (Glomus mosseae, G. intraradices, and G. claroideum) Soil application (5 g of inoculum; 40 fungus spores Potted plants in Increased vegetative growth and nitrogen, phosphorus and Porras-Soriano
g−1) open field potassium uptake under both non-saline and saline stress et al. (2009)
conditions conditions.
Peach PGPB (Alcaligenes 637Ca, Agrobacterium A18, Root dipping in bacterial suspension (109 CFU ml−1) Potted plants in Increased iron leaf concentration in calcareous soil. Arıkan et al.
Staphylococcus for 30 min. greenhouse (2018)
MFDCa1, MFDCa2, Bacillus M3 and Pantoea FF1
Prickly pear AMF (Glomus albidum, G. diaphanum, and G. clámides) Soil application Greenhouse Increased plant growth and nutrient uptake (P, B and Zn). Estrada-Luna and
cactus Davies (2001)
Sour orange AMF (Rhizophagus clarus) Soil application (5000 spores per plant) Potted plants in Increased growth parameters (shoot diameter, shoot Ortas et al. (2018
greenhouse length, and shoot and root dry weight). Inoculated plants a, b)
showed an increase in nutrient uptake as well as a higher
mycorrhizal dependency when fertilized with P.
Strawberry Seaweed extract Soil drench application (10 ml in 20 ml of tap water) Potted plants in Increased vegetative growth, leaf chlorophyll content, Spinelli et al.
greenhouse stomata density, photosynthetic rate and yield. Changed (2010)
root-associated microbial biocoenosis. Rhizosphere
acidification and higher iron ions uptake.
Strawberry AMF (Rhizophagus intraradices, Glomus aggregatum, Glomus Soil application Potted plants in Increased flower and fruit production, fruit size in plants Bona et al. (2015)
viscosum, Claroideoglomus etunicatum, and Claroideoglomus greenhouse grown in conditions of reduced fertilization. Improved
claroideum) and PGPB (Pseudomonas fluorescens strain Pf4 sugar, ascorbic acid and folic acid concentration.
and Pseudomonas sp. 5Vm1K)
Strawberry AMF (Rhizofagus intra-radices) and PGPB (Pseudomonas Soil application (5 g of mycelium spores; 400 fungus Potted plants in Increased crop yield. Enhancement of P content in fruits Ansari et al.
fluorescens strain R8, P.fluorescens strain R48, P. putida spores g−1). Root dipping in bacterial suspension (108 greenhouse from plants growing under P-deficiency. Increased (2018)
strain R108 and P.putida strain) CFU·ml−1) phenolic and antioxidant capacity in fruits from treated
plants.
3.1. Apple
Chen et al. (2017)
Xiao et al. (2015)

Abay and Pirlak
Yu et al. (2012)
Inoculation with AMF (G. viscosum and G. mosseae) in nursery
References
conditions may represent a useful tool to promote active growth of

(2017)
shoot apices and to overcome stunted growth of micropropagated

plantlets of the apple rootstock MM106 during the acclimation phase in
of Zn, P, K and Mg in shoots and roots of plants grown in a
greenhouse (Fortuna et al., 1996). AMF-inoculated plantlets were
photosynthesis in AMF inoculated plants, especially under
Increased plant height, shoot and root dry weight, P and N

Enhancement of plant growth, Mg concentration, and the
concentrations, root viability, acid phosphatase, catalase,
invertase and urease activities. Enhanced concentrations
characterized by a percentage of actively growing apices similar to P-

Crop performance and nutrient use/uptake efficiency
Increased plant biomass, leaf soluble protein, sugar
fertilized plantlets and significantly higher than the non-inoculated and

non-fertilized ones. In addition, P concentration in roots and shoots of
inoculated plants was also higher than control. Authors suggested
Increased zinc and iron leaf concentrations.
Zn-poor substrate. Decreased the soil pH.
mycorrhizal inoculation as a useful technique to reduce the use of

low Mg Availability in the substrate.
chemical fertilizer in nursery farms for the commercial production of

fruit trees (Fortuna et al., 1996). These indications were also largely
confirmed on similar plant material (micropropagated plantlets of the
apple rootstock MM106) inoculated with mycorrhizal fungi and trans-
planted on different commercial substrates based on peat and perlite
(Schubert and Lubraco, 2000). The use of different commercial AMF
inocula was found also effective for the promotion of plant growth and
nutritional status of apple seedlings (‘Antonovka’) grown in soil col-
uptake.
lected from an orchard showing apple replant disease symptoms (Gąstoł

et al., 2016). AMF-inoculated seedlings generally presented a higher
plant height, biomass accumulation and macronutrients (N, P, K) con-
Growing conditions
centration in leaves. Moreover, the AMF inoculation promoted a higher

Potted plants in
Potted plants in
Potted plants in
uptake of heavy metals (Pb and Cd) and their immobilization at the root
shade house
system level, therefore suggesting an interesting filtering-out me-

greenhouse
greenhouse
Field trial
chanism against these toxic ions (Gąstoł et al., 2016).

The application under orchard conditions of PGPR (Pseudomonas
and Bacillus strains) increased the nutrients concentration (N, P, K, Fe,
Mn and Zn) measured at leaf level of apple trees of two cultivars
Soil application (20 g of inoculum per plant containing
Soil application (50 g of inoculum per plant containing
suspension (109 CFU·ml−1) inoculated into the middle
(‘Starkrimson’ and ‘Granny Smith’; Pirlak et al., 2007). Beside the im-
Soil application (420 ml of a commercial product
provement of the nutrient status, trees that were treated by spraying

two times (at full bloom and after 60 days) a bacterial suspension on the
Syringe inoculation with 50 ml of bacterial
containing 12 % of humic plus fulvic acids
canopies resulted more productive, without any negative consequence

on the final apple composition (total soluble solids and titratable
acidity).
Mode and rate of application
3.2. Citrus
part of seedling roots
Seedlings of sour orange (Citrus aurantium L.) inoculated with the

about 240 spores)
about 600 spores)
AMF Rhizophagus clarus showed increased growth parameters (higher

shoot diameter, shoot length, and shoot and root dry weight) as well as
nutrient concentration (P, Zn, Mn and Cu) in leaves as compared to
non-inoculated plants (Ortas et al., 2018a). Moreover, the mycorrhizal
dependency (MD) percentage, defined as the ratio of the shoot dry
weight of the AMF-seedling and non-AMF seedlings, increased with
PGPB (Pseudomonas chlororaphis, Bacillus megaterium,
plant growth over time. In a further study, the same authors demon-
strated that mycorrhizal inoculation increased seedlings growth in both
Burkholderia cepacia and Arthrobacter pascens)
sterile and non-sterile soils (Ortas et al., 2018b). The MD applied to the
AMF (Glomus intraradices and G. versiforme)
total plant dry weight was higher for seedlings grown on sterilized than
on non-sterilized soils. Moreover, P addition had an effect on MD of
citrus plants, whereas Zn application had not (Ortas et al., 2018b). This
indication conflicts with Chen et al. (2017), who reported that the MD
of trifoliate orange seedlings was higher in inoculated plants grown in a
AMF (Glomus versiforme)
Zn-poor substrate as compared to the non-inoculated plants. In addi-

tion, trifoliate orange seedlings inoculated with the two AM fungi dis-
played different responses to low-Zn, therefore suggesting a specific AM
Biostimulant
Humic acids
fungi–host plant interaction effect. With a similar experimental ap-

proach, the same research group demonstrated the beneficial effects of
AMF inoculation with different Glomus species for the nutrient uptake
Table 2 (continued)
and growth performances of trifoliate orange seedlings grown under

low magnesium conditions (Xiao et al., 2015).
Sweet cherry
orange
orange
Fruit crop
Trifoliate
Trifoliate
3.3. Grapevine
Walnut
In two experiments carried out on potted ‘Sangiovese’ grapevines
9
grafted onto 420A, bi-weekly foliar application (Mancuso et al., 2006) biostimulant could have contributed to a more efficient mobilization
or weekly soil application (Mugnai et al., 2008) of seaweed extracts and uptake of the iron ions, therefore allowing to overcome the lime-
(unspecified origin in the case of Mancuso et al., 2006; from Ulvales in induced iron chlorosis (indirect effect). The overall effect of the sea-
the case of Mugnai et al., 2008) were reported to increase the uptake weed extract on stressed plants was found very similar to the one ob-
rate per unit of root length of potassium, ammonium and calcium ions tained with sequestrene, thus leading the authors to conclude that the
and this was translated in a stimulation of vine growth. Mancuso et al. tested biostimulant could represent a valid and environmental-friendly
(2006) also reported that bi-weekly foliar application of seaweed ex- substitute of the iron chelates (Spinelli et al., 2010). PGPR (Pseudo-
tracts increased nitrogen, potassium and phosphorus concentrations in monas sp.) alone or in combination with AMF (Glomus sp., Clar-
both roots and shoots, and, in addition, also induced an increase in leaf oideoglomus sp. and R. intraradices) affected growth, yield and quality of
concentration of magnesium. This result may be interesting, because strawberry (‘Selva’) in conditions of reduced nutrients supply (Bona
the incidence of bunch stem necrosis, a serious physiological disorder et al., 2015; Lingua et al., 2013). Indeed in an experiment in pots, in-
affecting grapevines, is often attributed to magnesium deficiency oculated strawberry plants fed with a solution containing about the 70
caused by the competition between the uptake of potassium and mag- % of the N and P2O5 used in the conventional practice (3.1 g plant−1 N
nesium by roots (Bondada and Keller, 2012). Moreover, Schreiner and 1.1 g plant−1 P2O5) showed higher number of flowers, yield per
(2007) reported that pre-transplant soil inoculation with a mix of arplant and average fruit weight compared to non-inoculated plants
buscular mycorrhizal fungi species (G. mosseae, G. intraradices, and (Bona et al., 2015). Moreover, the concentration of compounds with a
Scutellospora calospora) induced a significant increase in phosphorus high nutritional value (e.g. total sugars, ascorbic acid, folic acid and
uptake and in plant growth of potted ‘Pinot noir’ vines when these anthocyanins) were also found higher in strawberries harvested in
plants were grown in low fertility soil. The same author also reported in treated plants (Bona et al., 2015; Lingua et al., 2013). Similar effects of
a second experiment that similar effects could be obtained inoculating Pseudomonas strains and AMF application were also obtained on ‘Selva’
the soil only with G. mosseae isolates (Schreiner, 2007). strawberry plants grown in a P-deficient calcareous soil (Ansari et al.,
2018). Nutritional value of treated strawberries, including P content,
3.4. Stone fruits was improved. Authors suggested that the use of PGPR and AMF might
be combined with lower nutritional inputs without any detrimental
Soil application of humic and fulvic acids was reported to increase effect on plant growth and fruit quality, but resulting in a higher nu-
significantly zinc and iron leaf concentration in ‘0900-Ziraat’ sweet trient use efficiency in both organic and conventional production sys-
cherry (Prunus avium L.) trees grafted onto the Gisela 6 rootstocks (Abay tems (Ansari et al., 2018). Yu et al. (2012) investigated the use of
and Pirlak, 2017). The maintenance of a sufficient iron uptake by roots natural rock phosphate (RP) treated with phosphate-solubilizing bac-
is very important in calcareous soils for species like peach [Prunus teria (PSB) as valuable alternative to P fertilizer and for the definition of
persica (L.) Batsch], that, under these growing conditions, are highly more sustainable agricultural systems in highly contaminated regions in
sensitive to lime-induced iron chlorosis. Interestingly, Arıkan et al. China. PSB (Pseudomonas chlororaphis and Bacillus megaterium) were co-
(2018) reported that, in an experiment in pots, root inoculation with inoculated with a nitrogen-fixing bacteria (Arthrobacter pascens) ob-
PGPR induced a significant increase in active iron concentration in the taining a significant enhancement of phosphate solubilization as com-
leaves of ‘Elegant Lady’ peach trees grafted onto GF677 or Nemaguard pared to control. When the RP inoculated with the bacterial combina-
(rootstocks that are, respectively, tolerant or sensitive to lime-induced tion was mixed with P-deficient soil and used as growing media for
iron chlorosis) grown in a calcareous substrate (29.6 % CaCO3). This walnut (Juglans sigillata L.) seedlings in pot conditions, plant growth
response in inoculated trees was associated to increases, compared to (height and dry weight) and nutrients uptake (P, N and K) were found
control trees, in the activity of ferric chelate reductase (at both the root significantly higher than control. The authors concluded that the use of
and leaf level) and in the leaf concentration of organic acids, that are bacteria-inoculated RP as soil amendment could be seen as an alter-
considered to be two important physiological mechanisms used by native to the supply of N and P to walnut plants, even though additional
plants to reduce insoluble ferric cations (Fe3+) to the more soluble research will be needed to evaluate the effects of these bacteria on
ferrous ions (Fe2+). In a recent experiment, Saa et al. (2015) reported phosphate mobilization under field conditions (Yu et al., 2012). The
that foliar applications of an A. nodosum seaweed extract stimulated the positive application of AMF as a biotechnological tool that allows a
vegetative growth of potted ‘Nonpareil’ almond trees grafted onto Ne- more rapid growth and a more efficient usage of P was also described
maguard grown under deficient or good potassium availability in the for prickly-pear cactus (Opuntia albicarpa cv. ‘Reyna’) plantlets
soil (obtained applying to the substrate a fertigation solution with a K (Estrada-Luna and Davies, 2001). Growth enhancement was promoted
concentration of 5 or 125 μg g−1, respectively). In addition, the results by the ability of the AMF to enhance the uptake of selected nutrients
suggested that this biostimulant can enhance significantly potassium (including P, B and Zn). The authors underlined that an efficient use of
uptake when this nutrient was deficient in the soil. However, this study P inputs is particularly important for nursery production systems in
was inconclusive about the possible mechanism behind this interesting order to reduce chemical inputs and potential nutrient irrigation run-
result. Furthermore, soil inoculation with AMF of the species G. fasci- off, while maintaining the production of healthy plants (Estrada-Luna
culatum significantly improved vegetative growth, leaf chlorophyll and Davies, 2001).
content, leaf phenolic content, and nutrient content in apricot (Prunus At transplanting of semi hardwood olive (Olea europea L.) cuttings
armeniaca L.) seedlings at a nursery stage compared to non-inoculated into pots, the medium inoculation with AMF of the genus Glomus sti-
control (Dutt et al., 2013). mulated nutrient uptake and vegetative growth under both non-saline
and saline stress conditions (Porras-Soriano et al., 2009).
3.5. Other fruit crops
4. Implications of plant biostimulants for increasing yield and
Strawberry plants grown on a calcareous substrate and treated with modulating nutritional and functional quality traits
a seaweed extract from A. nodosum were characterized by a stronger
vegetative growth and a higher yield as compared to untreated plants Scientific studies on the effects of biostimulant applications on crop
(Spinelli et al., 2010). Treated plants showed a more developed root growth, yield and quality have provided variable results (Table 3). This
system that might have influenced positively nutrients uptake (direct probably because consistent results on fruit trees are generally more
effect). Moreover, kahydrin (a derivate of the K-vitamin that, when difficult to attain than in annual plants (e.g. vegetables and cereals) on
exogenously applied, induces the H+ secretion into the apoplast and account of the “carry over” effects and influences of growth, cropping
the consequent acidification of the rhizosphere) contained in the and metabolic reserves accumulation from one season to the next
10
Table 3
Effects of microbial and non-microbial biostimulants on quality and nutraceutical value of fruits.
Fruit crop Biostimulant Mode and rate of application Growing conditions Effects on nutritional and functional quality of fruit References
B. Basile, et al.
products
Apple Seaweed extract (Fucus spp.) Seven foliar sprays Field trial Increased red colour intensity and distribution. Malaguti et al. (2002)
Apple Seaweed extract (Ascophyllum nodosum), alfalfa protein Weekly foliar sprays, starting after full Field trial Increased intensity and extension of red coloration. Higher Soppelsa et al. (2018)
hydrolysate and B-group vitamins (B1, B2, B6) bloom anthocyanin content in the skin of treated apples.
until harvest (4.0, 3.0 and 1.5 kg ha−1)
Apple Seaweed extract (Ascophyllum nodosum) Seven foliar sprays at 3.51 L ha−1 and Field trial No effect on fruit yield. Tendency to reduce the incidence Bradshaw et al. (2013)
1.17 L ha−1 of sunburn and frost rings.
Apple PGPB (Bacillus M3, Bacillus OSU-142, Microbacterium FS01) Root dipping in bacterial suspension (109 Field trial Stimulated plant growth (shoot length and diameter), Karlidag et al. (2007)
CFU ml−1) for 30 min. yield and fruit weight.
Apple Seaweed extract (Ascophyllum nodosum) Four applications by fertirrigation at 30 L Field trial Increased fruit yield and number of fruits per tree in the Spinelli et al. (2009)
ha−1 “off” year of ‘Fuji’ trees. Positive effect on controlling the
alternate bearing.
Apricot Humic and fulvic acids Foliar application (Dosage: 500 g 100 Field trial Increased antioxidant activity of the fruit at harvest. Tarantino et al. (2018)
L−1)
Banana PGPR (Psuedomonas florescens) plus chitin Application of 400 ml of bacterial Field trial, rain fed Higher average fruit weight and overall yield. Kavino et al. (2010)
suspension (9 × 108 CFU ml−1) in chitin-
amended KBB medium
Blackberry PGPR (Pseudomonas fluorescence) Root and leaf inoculation with app. 1 × Greenhouse and Increased sugar accumulation in fruits. Higher phenolic García-Seco et al. (2012);
107 CFU ml−1 field conditions and flavonoid compounds. Ramos-Solano et al. (2014);
García-Seco et al. (2015)
Grapevine Humic acids Foliar applications (40−50 ml L−1) Field trial Increase berry weight, cluster weight, fruit yield per vine, Popescu and Popescu (2018)
soluble solids content at harvest.
Grapevine Humic acids Foliar application (100 mg L−1) Field trial Increased berry size and soluble solids concentration in Ferrara and Brunetti (2010)
the fruits at harvest.
Grapevine Protein hydrolysate (from vegetal origin) Soil application Field trial Increased in must total polyphenols and anthocyanins; Parrado et al. (2007)
11
more intense red color of the must; increased; induction of
the synthesis of petunidin.
Grapevine Seaweed extract (Ascophyllum nodosum) Foliar sprays (1.5 kg ha−1) Field trial Induced, at harvest, a significant increment of Frioni et al. (2018)
anthocyanin concentration in the berry skin.
Grapevine French-oak wood extracts Foliar spray (230 ml vine−1) Field trial Changed wine aroma (increased wooden aromatic notes) Martínez-Gil et al. (2011)
mainly due to the increased concentration of glycosidic
nonvolatile aroma precursors in the berries at harvest.
Grapevine French-oak wood extracts Foliar spray (250 ml vine−1) Field trial Changed wine aroma (increased caramel, butterscotch, Martínez-Gil et al. (2012)
and vanilla aromatic notes) mainly due to the increased
concentration of glycosidic nonvolatile aroma precursors
in the berries at harvest.
Grapevine French-oak wood extracts Foliar spray (300 ml vine−1) Field trial Increased polyphenolic content and improved color of the Pardo-García et al. (2014)
wine.
−1
Grapevine American-oak wood extracts Foliar spray (250 ml vine ) Field trial Changed glycosidic aroma profile of the grapes at harvest. Martínez-Gil et al. (2013)
Grapevine Vine-shoots extracts; French-oak wood extracts Foliar spray (300 ml vine−1) Field trial Increased wine amino acid content. Sánchez-Gómez et al. (2016a)
Grapevine Vine-shoots extracts; Foliar spray (300 ml vine−1) Field trial Increased concentration of fermentative aromas and Sánchez-Gómez et al. (2016b)
polyphenols in the wine.
Grapevine Phenylalanine Foliar sprays (200 ml vine−1) Field trial Increased must amino acid content. Garde-Cerdán et al. (2014)
Grapevine Phenylalanine Foliar sprays (200 ml vine−1) Field trial Increased concentration of stilbenes in the wine. Garde-Cerdán et al. (2014)
Grapevine Phenylalanine Foliar sprays (200 ml vine−1) Field trial Increased phenylalanine concentration and changed Garde-Cerdán et al. (2018)
aroma profile of the must.
Table 3 (continued)
Fruit crop Biostimulant Mode and rate of application Growing conditions Effects on nutritional and functional quality of fruit References
products
B. Basile, et al.
Mandarin Moringa oleifera extract Foliar sprays with 3% M. oleifera extract, Open field Increased fruit quality (phenolics and antioxidant Nasir et al. (2016)
alone or in combination with K and Zn potential) and final yield.
Olive Seaweed extract (Ascophyllum nodosum) Foliar sprays (3.5 L tree−1) Field trial Increased fruit oil content, and fruit maturity rate. Chouliaras et al. (2009)
Papaya AMF (Glomus mosseae and Entrophospora colombiana) Inoculum with app. 7300 spores kg−1 Open field Longer storability of fruits. No differences in fruit quality Vázquez-Hernández et al.
substrate parameters. Increased yield. (2011)
Peach Humic acids Foliar or soil application of a humic acid Field trial Increased fruit size, fruit yield per tree, fruit soluble solids, Abd El-Razek et al. (2012)
solution (0.25-0.50 %; 5 L tree−1) skin anthocyanin concentration, nitrogen, phosphorus,
and potassium and mineral content.
Pear Seaweed extract (Ascophyllum nodosum) Three foliar sprays at 3 L ha−1 Field trial Increased seed number per fruit, fruit weight and yield per Colavita et al. (2011)
tree. No effects on fruit maturity indices and vegetative
parameters.
Strawberry Humic acid and salicylic acid Foliar sprays Greenhouse Enhanced sugar, acidity, vitamin C content, red tone (a*) Aghaeifard et al. (2016)
experiment and leaf nutrient concentration (P, K, Ca, Mg). Reduced
the total antioxidant capacity. No effect on pH and fruit
luminosity (L*). Higher fruit yield.
Strawberry Seaweed extract (Ascophyllum nodosum) and silicon dioxide Four foliar sprays (20 ml 10 L−1 and 2 ml Slightly elevated Improved fruit quality (e.g. high anthocyanin content). Weber et al. (2018)
10 L−1) beds in greenhouse Increased total fruit yield and total number of fruits.
Strawberry AMF (Funneliformis mosseae, Septoglomus viscosum and Mycorrhizal inoculum (11 % v/v) mixed Potted plants in PGPR improved fruit yield and quality (sugar and Todeschini et al. (2018)
Rhizophagus irregularis) and PGPB (Pseudomonas fluorescens with plant growth medium. 8 ml of greenhouse anthocyanins accumulation). Modification of the aromatic
strain Pf4, Pseudomonas sp. 5Vm1K and P. fluorescens strain bacterial suspension (109 CFU ml−1) per profiles of treated fruits.
19Fv1t) plant
Strawberry PGPR (Bacillus amylolequefaciens and Paraburkholderia Root and foliar application with a solution Field conditions Higher total antioxidant activity and bioactive compounds Rahman et al. (2018)
fungorum) containing app. 1 × 109 CFU ml−1. (raised bed) concentrations: anthocyanins, carotenoids, flavonoids and
phenolics.
Strawberry PGPR (Phyllobacterium) Inoculation with 1 × 106 CFU ml−1 Potted plants in Higher content in vitamin C. Flores-Félix et al. (2015)
12
greenhouse
Strawberry AMF (Glomus sp.) and PGPB (Pseudomonas fluorescens strain Soil application with 100 ml of AMF Potted plants in Enhanced anthocyanin concentration in the fruits. Lingua et al. (2013)
Pf4 and Pseudomonas sp. 5Vm1K) inoculum and 5 ml of bacterial suspension greenhouse
(109 CFU·ml−1)
Strawberry Seaweeds extracts (from A. nodosum), alfalfa protein Weekly foliar sprays, starting from pre- Potted plants in Enhanced fruit firmness, external color and nutritional Soppelsa et al. (2019)
hydrolysates and chitosan flowering until harvest (4.0, 3.0 g L−1 and greenhouse values (content of phenolic compounds).
10 ml L−1)
Sweet cherry PGPB (Bacillus subtilis OSU-142, Pseudomonas putida BA-8) Foliar application of bacterial suspensions Field trial Improved tree nutritional status. Esitken et al. (2006)
(109 CFU ml−1)
Sweet cherry Seaweed extract Two-three foliar applications (5 L ha−1) Field trial Decreased percentage of cracked fruits. Vercammen et al. (2008)
Sweet cherry Potassium silicate Soil applications (1%) Field trial Increased fruit flesh firmness. Kaiser et al. (2014)
(Wertheim and Webster, 2005). This might partially explain the reason +20 %) as compared to control. Contrary to other studies on other fruit
for the more evident results achieved in trials conducted with biosti- crops, seaweed application did not have any significant effect on the
mulant products on trees under stress conditions (drought, nutrient main fruit quality traits.
limitation, pathogens), as shown in other sections of this review. Within
this framework, an interesting field of application of biostimulant 4.2. Stone fruits
compounds is therefore the one of the organic farming, which is gen-
erally characterized by lower yield as compared with conventional In ‘Flordaprince’ peach trees, foliar or soil applications of a humic
production system, mainly because of stress conditions induced in acid solution (0.25-0.50 %; 5 L per tree) at fruit set and in four fol-
plants by the limitation imposed on fertilization and plant defense lowing dates (every 15 days) induced a significant increase in fruit size
(Seufert et al., 2012). at harvest and fruit yield per tree (Abd El-Razek et al., 2012). Moreover,
fruit soluble solids were increased in fruit flesh as well as the antho-
4.1. Apple and pear cyanin concentration in fruit skin. These effects were particularly in-
teresting when the solution was applied at 0.50 % at both the soil and
Repeated foliar applications of an A. nodosum seaweed extract in- the canopy, since they induced a 77–78 % increase in fruit size (fruit
duced larger leaf area and photosynthetic capacity of organically grown fresh weight), that was translated in similar percent increases in fruit
apple trees (cv. ‘Jonathan’) (Soppelsa et al., 2018). In addition, the yield per tree. In addition, these effects were also associated to a sig-
seaweed extract applications induced a higher chlorophyll accumula- nificant increase in leaf chlorophylls, nitrogen, phosphorus, and po-
tion in leaves, therefore suggesting a possible role of this biostimulant tassium and mineral content. Similar results were also obtained in other
in slowing down the chlorophyll degradation process as also indicated studies on the same peach cultivar (El-Khawaga, 2011; Mansour et al.,
by Spinelli et al. (2009). The seaweed extract did not change the yield 2013). Tarantino et al. (2018) reported, for ‘Orange Ruby’ apricot trees,
performances of apple trees under balanced crop load conditions that the foliar application at three phenological stages (sepals closed
(Soppelsa et al., 2018; Bradshaw et al., 2013; Malaguti et al., 2002), forming a red ball, fruit set and during fruit development) of a com-
whereas it significantly increased fruit yield and number of fruits per mercial product containing vermicompost-derived humic and fulvic
tree in the “off” year of ‘Fuji’ trees showing alternate bearing (Spinelli acids induced a significant increase in the antioxidant activity of the
et al., 2009). Biostimulant products based on seaweed, protein hydro- fruit at harvest. Moreover, a significant, but quantitatively negligible,
lysate and B-group vitamins had a minor impact on primary apple positive effect on fruit yield was also recorded only in a year char-
quality traits (size, flesh firmness, acidity and total sugars), whereas acterized by very low crop load per tree. Conversely, the foliar appli-
they induced an improvement of the intensity and extension of red cation of a suspension of Bacillus subtilis (109 CFU ml−1) induced in
coloration in ‘Jonathan’ apples at harvest (Soppelsa et al., 2018). This apricot trees (cv. ‘Hacihaliloglu’) a significant increase in fruit yield per
result was obtained in two consecutive years and was, therefore, in- tree (+30 %) and in vegetative growth (+26 %) compared to un-
dependent from the effects of the seasonal climatic conditions. Apples sprayed trees (Esitken et al., 2003). Similarly, Esitken et al. (2006)
showing a more intense red color were also characterized by higher showed that foliar applications of a bacterial suspension of the genus
anthocyanins accumulation in the fruit skin. This evidence could be Pseudomonas e Bacillus (applied alone or in combination) could induce
probably ascribed to a modulation of the metabolism of plant en- an increase in fruit yield per tree and in the vegetative growth asso-
dogenous growth regulators (mainly cytokines and abscisic acid) which ciated with an improvement in the nutritional status of sweet cherry.
are involved in the control of anthocyanins biosynthesis in plant organs The biostimulation action induced by PGPR on tree vegetative and re-
(Wally et al., 2013). Treated apples presented also a higher antioxidant productive growth was also reported for sour cherry (Prunus cerasus L.)
potential of the pulp. This result was year-dependent and could be due (Arikan and Pirlak, 2016) and European plum (Prunus domestica L.)
to an up-regulation of genes responsible for the phenolic compounds (Karakurt et al., 2010).
biosynthesis at the fruit level as also described by Ertani et al. (2017) An interesting potential application of seaweed extracts was pro-
for tomato fruit. posed by Vercammen et al. (2008). The authors tested the suitability of
Bacterial application with Bacillus and Microbacterium strains to the this kind of biostimulants to reduce the incidence of fruit cracking due
root system of ‘Granny Smith’ trees grafted onto MM106 prior to to rainfalls in sweet cherry. The results of this study suggest that, for the
plantation in orchard conditions was reported to enhance vegetative cultivars ‘Kordia’ and ‘Sweetheart’, two-three foliar applications of a
growth (measured as average shoot length) by approximately 20 % and commercial product containing seaweed extracts of undefined compo-
cumulative yield by 26–88 %, depending on the type of PGPR used sition and origin (applied two-four weeks before harvest) induced a
(Karlidag et al., 2007). Similar results were also obtained with other decrease in the percentage of cracked fruits of up to around 10 %. In-
PGPR (Bacillus, Burkholderia and Pseudomonas strains) on young trees terestingly, this result was also obtained in the case of cracking due to
belonging to the same apple cultivar (Aslantaş et al., 2007). Authors water transport through the pedicel (i.e. water absorbed by the root
indicated a yield increase up to 100 % as compared to control, even system and not directly from fruit skin). Additional research is required
though results referred to one single productive year. In another study to confirm these results also in other cultivars. In addition, soil appli-
by Pešaković et al. (2017) it was found that a microbial biostimulant cation of potassium silicate repeated every three weeks (from bloom to
composed by PGPR (Azotobacter, Pseudomonas and Bacillus) as well as harvest) was reported to induce an increase in flesh firmness of sweet
vitamins, enzymes and growth stimulators had similar effects on all the cherry fruits at harvest, but these effects were not consistent for all
productive indices (flowering intensity, fruit set and yield per tree) as cultivars and experimental conditions (Kaiser et al., 2014).
those of a traditional chemical fertilizer based on N, P and K. Both the
mineral fertilizer and the biostimulant were applied using a drip irri- 4.3. Grapevine
gation system during the vegetative season. Despite the fact that results
refer to one single year of study, the authors support the introduction of The literature on the possible application of biostimulants to im-
biofertilization as a more sustainable mean for the apple industry. prove grapevine yield and berry, must and wine composition is rela-
Regarding the pear (Pyrus communis L.) cultivation, crop perfor- tively large as compared to other fruit crops. Popescu and Popescu
mances of the cv. ‘William’s’ were enhanced after seaweed (A. nodosum) (2018) reported that in two white grape cultivars (‘Feteasca Regala’ and
extract applications during two consecutive seasons (Colavita et al., ‘Riesling Italico’) the foliar application at pre-bloom and fruit set
2011). Authors found that three canopy treatments around blooming (40–50 ml L−1) of a commercial product containing vermicompost-
time (from early bloom to fruit set) resulted in 40 % increased seed derived humic acids induced an increase in berry weight, cluster weight
number per fruit, higher fruit weight and yield per tree (approximately and, consequently, in fruit yield per vine compared control vines. The
13
authors also reported an increase in sprayed vines of berry soluble so- (on the 7th day post-veraison) on vines of the white cultivar ‘Airén’
lids content at harvest. These effects of stimulation of berry growth and induced a significant increase in must amino acid concentration, that is
of carbohydrate accumulation in the fruits were associated with a associated to an interesting increase in the concentration of fermenta-
general improvement induced by humic acids of some vine physiolo- tive aromas and polyphenols in the wine.
gical parameters related to whole plant photosynthesis (increased leaf To increase amino acid concentration in must or in general to in-
net CO2 exchange rate, leaf chlorophyll concentration, and total vine crease yeast assimilable nitrogen (YAN) in the must, research activities
leaf area). A stimulating effect of a single foliar application of humic are recently focusing also on the possible use of protein hydrolysates as
acids (100 mg L−1 at full bloom) on berry size and on the accumulation foliar spray, even though the results reported in the literature are not
of carbohydrate in the fruits was also previously reported by Ferrara always consistent. It appears that the significance of these effects
and Brunetti (2010) for the white table grape cultivar ‘Italia’. In this strongly depends on the specific amino acid composition of the protein
latter study, less evident were the effects of humic acids on leaf hydrolysate applied. Studies conducted on ‘Tempranillo’ indicated that
chlorophyll concentration (measured with a nondestructive portable phenylalanine applications resulted in an increase in amino acid con-
chlorophyll meter). However, humic acids were reported previously to centration in the must and an increase in the concentration of stilbenes
increase leaf chlorophyll content and photosynthesis in different higher and aromatic compounds in the wine, whereas the foliar application of
plants (Nardi et al., 2002). proline does not appear to have any significant effects on these para-
Parrado et al. (2007) studied, for the wine grape cultivar ‘Tempra- meters (Garde-Cerdán et al., 2014, 2015, 2018). Some of these latter
nillo’, the effects of soil applications (20 L ha−1) of a protein hydro- responses appear to be more correlated to the nutritional status of the
lysate of vegetal origin (corn, sorghum and carob) on must composition vine (as a consequence of the nitrogen fertilization) than to real bios-
and color. Interestingly, the results highlighted that the biostimulant timulant action of the sprayed amino acids.
application induced increases in must total polyphenols and antho-
cyanins, respectively, by 28 % and 227 % compared to the untreated 4.4. Other fruit tree species
controls. These changes in composition were responsible for a more
intense red color of the must. In addition, the authors reported that the The number of scientific evidences of the positive effect of different
increase in anthocyanin concentration measured in the must obtained biostimulants on the growth and yield of strawberry plants is relatively
from treated vines was also associated to an induction of the synthesis large. Here we will concentrate mainly on the most recently published
of petunidin, an anthocyanin that was not detected in the must of un- researches. Organically cultivated strawberry treated with a combina-
treated controls. Similarly, Frioni et al. (2018) showed that five foliar tion of two commercial products based on silicon and an A. nodosum
sprays (applied between pre-veraison and harvest at a dose of 1.5 kg seaweed extract enhanced significantly total yield (+26 %) and the
ha−1) of a commercial A. nodosum seaweed extract induced, at harvest, ripening process (around +10 % of marketable fruits harvested earlier
a significant increase of anthocyanin concentration in the berry skin of in the season) (Weber et al., 2018). Treatments applied four times
three cultivars (‘Cabernet Franc’, ‘Pinot Noir’, ‘Sangiovese’). Since during the flowering and early fruit formation stages, had also a sig-
seaweed applications did not affect yield components, leaf photo- nificant effect on fruit quality by enhancing overall color and antho-
synthesis, vine leaf area, and other berry composition parameters (so- cyanins accumulation of early harvested strawberries. A similar yield
luble solids content in berry juice at harvest), this effect appeared increase was also found on strawberry plants foliarsprayed at full bloom
mainly due to direct stimulation of anthocyanin biosynthesis and ac- and 15 days later with a solution containing humic acids at different
cumulation. It is also important to highlight that these effects were concentrations (25−100 mg L−1) (Aghaeifard et al., 2016). Recently,
consistent in different cultivars grown in areas characterized by largely Soppelsa et al. (2019) found that the repeated applications of selected
different climates (‘Sangiovese’ in Mediterranean climate whereas biostimulants (A. nodosum extracts, alfalfa protein hydrolysates and
‘Pinot Noir’ and ‘Cabernet Franc’ in continental climate). This may chitosan) improved strawberry commercial (firmness and external
suggest that the medium-late application of seaweed extract may be a color) and nutritional (content of phenolic compounds) quality at
suitable vineyard management strategy to improve berry phenolic harvest.
composition for several red cultivars over a large range of climatic As for the use of microbial biostimulants (e.g. AMF and PGPR),
conditions (from cool to warm viticultural regions). there is currently a large consensus on their general positive effects on
Several authors reported that the foliar application of aqueous ex- different aspects related to the vegetative growth, yield and fruit quality
tracts of toasted French oak wood performed at the transition phase of in strawberry plants. In a study conducted on cv. ‘Elyana’ plants co-
berry development (veraison) can affect significantly the aroma of the inoculated with AMF (R. irregularis, F. mosseae, S. viscosum) and PGPR
wines obtained from the white cultivar ‘Verdejo’ (Martínez-Gil et al., (Pseudomonas sp.), the “fungus” component had an effect mostly on the
2011) and the red variety ‘Petit Verdot’ (Martínez-Gil et al., 2012). vegetative parameters (dry mass accumulation at different organs
These effects are mainly related to an increase in the berry in glycosidic level), whereas the “bacterium” component contributed largely to the
nonvolatile aroma precursors, while the volatiles are released during increase of fruit yield and quality (Todeschini et al., 2018). In addition,
the winemaking process (mainly during the post-fermentation fining). strawberries sampled from plants treated with the different micro-
Similar results were also reported about the effect of the foliar appli- organism combinations were characterized by a different volatile pro-
cation of American oak extracts on the concentration of glycosidic file, therefore resulting in an interesting enlargement of the final or-
aroma precursors in the berries of ‘Chardonnay’ and ‘Sirah’ grapevines ganoleptic typology of fruits. The nutritional value of strawberries
at harvest (Martínez-Gil et al., 2013). Furthermore, Pardo-García et al. largely depends on the concentration of numerous bioactive compounds
(2014) showed, for ‘Monastrell’ grapevines, that foliar sprayings at which are naturally present in the fruits and that can vary according to
veraison with French oak extracts induced a significant increase in many factors, including the genotype, the growing environment and the
polyphenolic content and better colour of the wines. Most of the de- cultivation techniques (Valentinuzzi et al., 2015). PGPR belonging to
scribed effects of the oak extracts on wine composition depended on the different species and strains have shown to be able to increase func-
cultivar and the specific phenological stage when the treatment is ap- tional quality of strawberry fruits at harvest (Flores-Félix et al., 2015;
plied. Oak extracts are food additives rich in volatile compounds Rahman et al., 2018). More into detail, the application of two different
(Martínez-Gil et al., 2012, 2013). plant probiotic bacteria (Bacillus sp. and Burkholderia sp.) significantly
Recently, other authors have evaluated the suitability of using increased the total antioxidant activity and the concentration of several
aqueous extracts of vine-shoots to improve berry composition at harvest bioactive compounds (anthocyanins, carotenoids, flavonoids and phe-
(Sánchez-Gómez et al., 2017). In more details, Sánchez-Gómez et al. nolics) in strawberry fruits cv. ‘Festival’ cultivated in open-field con-
(2016a, b) reported that the foliar application of vine-shoots extracts ditions (Rahman et al., 2018). Similarly, the application of the bacterial
14
strain of genus Phyllobacterium was found to increase by almost 100 % period (11 days) at 20 °C (Vázquez-Hernández et al., 2011). PGPR,
the vitamin C concentration of fruits harvested from strawberry seed- previously isolated from the rhizosphere, were inoculated on two-year-
lings (cv. ‘Camarosa’) (Flores-Félix et al., 2015). The use of PGPR was old potted mango trees in order to evaluate their effects on growth and
reported also to be effective in increasing yield and quality of black- flowering under greenhouse conditions (de los Santos-Villalobos et al.,
berry (Rubus fruticosus L.) fruits. The root inoculation with a bacterial 2013). Strains of Burkholderia caribensis and Rhizobium sp. induced
strain of Pseudomonas fluorescence resulted particularly efficient in growth promotion and a higher number of flower buds compared with
increasing yield per plant (by approximately 40 %) and the fruit total non-inoculated control. The higher number of floral buds and flowers
soluble solids content by 3°Brix (+20 % as compared to control) of was probably triggered by the up-regulation (2 folds higher as com-
field-grown blackberry plants, cv. Lochness (García-Seco et al., 2012). pared to control) of the FLOWERING LOCUS T (FT) gene expression
The authors hypothesized that an increased photosynthetic efficiency of that could, therefore, play a role as floral signal in mango. In banana
the inoculated plants could be a possible explanation for the obtained (Musa spp.), the application of two different strains of Pseudomonas
results, even though no direct measurements of photosynthetic rates fluorescens in combination with chitin resulted in improved plant
were reported in the paper. Similar effects on sugar accumulation in growth (plant height and leaf area index) and yield (bunch and fruit
blackberry fruits were also detected by the same research group on a weight) compared to control treatment (Kavino et al., 2010). Chitin
following experiment conducted under greenhouse conditions (Ramos- supply to bacterial strains resulted in higher chitinase secretion by the
Solano et al., 2014). Beside primary metabolites (sugars and organic bacteria, with potential positive effect on the PGPR performances for
acids), blackberry fruits from inoculated plants were also characterized the degradation of the chitin-rich cells of insects and fungi. Based on
by a higher total phenolics and flavonoids content as compared with this observation, the authors concluded that the addition of chitin in the
control. As demonstrated in a following study conducted on the same formulation of a PGPR product could enhance bacterial survival and its
plant material, the application to the root system of P. fluorescence re- efficacy also under open-field conditions (Kavino et al., 2010).
sulted in a promotion of the whole phenylpropanoid and flavonoid
pathways, leading to higher accumulation of secondary metabolites in 5. Final remarks and challenges beyond the state of art
blackberries, with positive consequences on the overall nutritional
value of the fruits (Garcia-Seco et al., 2015). Microbial and non-microbial plant biostimulants appear as novel
In olive trees, a foliar application (ten days after bloom) of A. no- and prominent category of agricultural input complementing synthetic
dosum seaweed extracts in combination with a nitrogen and boron fertilizers and able to act at multiple levels of crop production. Plants
fertilization (applied at the soil) resulted in significant increases in fruit biostimulants are known to modulate plant molecular and physiological
yield per tree, oil content in the fruits, and in an acceleration of fruit processes that boost plant growth, productivity, quality and alleviate
maturity compared to untreated controls and to trees that received only the impact of abiotic stressors. Studies on the use of biostimulant pro-
the nitrogen and boron fertilization (Chouliaras et al., 2009). Interest- ducts in the fruit production industry are still limited as compared to
ingly, this study was carried out in a low-yield year of the olive orchard herbaceous crops (vegetables, cereals, soybean, etc.) and the results
and the very positive effect of the biostimulant on fruit yield (8.4 and obtained until now are not always consistent in terms of efficacy and
1.5 times higher compared to untreated controls and to trees that re- repeatability. This evidence is probably linked to the perennial nature
ceived only the nitrogen and boron fertilization, respectively) was only of the woody tree species. Indeed, the effectiveness of the plant bios-
partially explained by an increase in fruit size, but it was more related timulants and the repeatability of the results obtained could be partially
to an increase in the number of fruit per tree. These results may be hidden by the availability of metabolic reserves located in the perma-
interesting for an alternate bearing species like olive. Positive effects of nent organs of the fruit tree (root, trunk, branches) which also depend
the soil application of a commercial product containing 20 % of humic on the climatic conditions occurring year after year in open-field cul-
acids on fruit yield of olive trees were also reported by Shahin et al. tivation systems. Despite these limitations, selected biostimulant pro-
(2015). ducts showed some interesting effects especially with regard to the
The use of biostimulants to improve growth and yield performances enhanced fruit yield under suboptimal growing conditions (e.g. nu-
was also tested on tropical and sub-tropical fruit species. Nasir et al. trients and water limitation) and to the higher commercial quality of
(2016) investigated the potential role of a leaf extract of Moringa olei- the products (e.g. nutritional and esthetical properties of fruits).
fera as biostimulant to enhance productivity and fruit quality of man- Therefore, plant biostimulants should not be considered as one-size-fits-
darin (Citrus nobilis L. × Citrus deliciosa T.) ‘Kinnow’ trees. This extract all solution and the major challenge will be to elucidate the best species/
is considered inexpensive and therefore it represents a good candidate genotype × environment × management practices (including biosti-
to substitute the more costly seaweed extracts and/or synthetic hor- mulants) in order to select best combinations. Finally, many remaining
mones. The composition of the moringa leaf extract was not directly issues warrant further investigation and should focus on:
investigated, even though the authors referred to a high concentration
of phytohormones (e.g. citokinins and auxins) and other growth pro- i fine characterization of the active ingredients inside the biostimu-
moting compounds such as ascorbate, phenolics and minerals (Ca, K, Zn lant products and of their mode of action/mechanism within the
and Fe). Moringa extract application, alone or in combination with fruit tree physiology;
potassium and zinc, boosted final yield of marketable fruits (+ 50 % as ii optimization of the way of application (time and rate of applica-
compared to untreated control) because of a significant increase in fruit tion), considering the specie/cultivar/rootstock combinations and
set and decrease in fruit drop. Moreover, fruit quality was also im- the different tree growing stages (age of trees and phenology);
proved, with treated mandarin showing higher antioxidant activity and iii test the efficacy of the biostimulants under real growing conditions
phenolics concentration compared to non-treated control treatment (open-field or protected cultivation), where multiple and combined
(Nasir et al., 2016). Improved growth performances and fruit quality biotic and abiotic stressors occurred;
were also measured in a plantation obtained with papaya seedlings iv evaluation of the impact of the climatic/seasonal conditions, also
previously inoculated with two AMF species (G. mosseae and En- taking the future scenarios of climatic changes into consideration
trophospora colombiana; Vázquez-Hernández et al., 2011). The final (increased temperature and the effect on the chill and heath re-
yield was particularly enhanced in the G. mosseae-inoculated plants (by quirement of the deciduous tree species, heath waves, prolonged
105 % compared to non-inoculated control). The main fruit quality drought periods, excessive radiation, etc.);
traits at harvest were not modified by the AMF applications, whereas v verify the occurrence of possible negative carry-over effects caused
both treatments affected positively the papaya post-harvest behavior, as by the biostimulants designing multiple-year trials;
shown by a significantly reduced loss of weight during the storage vi include analysis of cost-benefit indexes of the biostimulant
15
applications in order to evaluate also the economical sustainability crop responses: a review. Biol. Agric. Hortic. 31, 1–17. https://doi.org/10.1080/
of these agronomic tools for the fruit crop production systems. 01448765.2014.964649.
Bulgari, R., Morgutti, S., Cocetta, G., Negrini, N., Farris, S., Calcante, A., Spinardi, A.,
Ferrari, E., Mignani, I., Oberti, R., Ferrante, A., 2017. Evaluation of borage extracts as
Author contributions potential biostimulant using a phenomic, agronomic, physiological, and biochemical
approach. Front. Plant Sci. 8, 935. https://doi.org/10.3389/fpls.2017.00935.
Calvo, P., Nelson, L., Kloepper, J.W., 2014. Agricultural uses of plant biostimulants. Plant
CA, BB, GC and YR had the original idea, provided the intellectual Soil 383, 3–41. https://doi.org/10.1007/s11104-014-2131-8.
input and set up the review article. YR and GC wrote the Introduction Canellas, L.P., Olivares, F.L., Aguiar, N.O., Jones, D.L., Nebbioso, A., Mazzei, P., Piccolo,
section. CA and SS wrote the review text concerning pome fruits, citrus, A., 2015. Humic and fulvic acids as biostimulants in horticulture. Sci. Hortic. 196,
15–27. https://doi.org/10.1016/j.scienta.2015.09.013.
berry crops and other fruit species. BB wrote the review text concerning Caradonia, F., Battaglia, V., Righi, L., Pascali, G., La Torre, A., 2019. Plant biostimulant
grapevine, olive and stone fruits. All authors listed have made a sub- regulatory framework: prospects in Europe and current situation at international
stantial, direct and intellectual contribution to the final draft, and ap- level. J. Plant Growth Regul. 38, 438–448. https://doi.org/10.1007/s00344-018-
9853-4.
proved it for publication.
Chen, Y.Y., Hu, C.Y., Xiao, J.X., 2017. Effects of arbuscular mycorrhizal fungi on the
growth and zinc uptake of trifoliate orange (Poncirus trifoliata) seedlings grown in
Declaration of Competing Interest low-zinc soil. J. Plant Nutr. 40, 324–331. https://doi.org/10.1080/01904167.2016.
1240192.
Chouliaras, V., Tasioula, M., Chatzissavvidis, C., Tasioula-Margari, I., Tsabolatidou, E.,
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Scientia Horticulturae 267 (2020) 109330

Contents lists available at ScienceDirect

Appraisal of emerging crop management opportunities in fruit trees, T

ARTICLE INFO ABSTRACT

(continued on next page)

higher shoots and leaves dry weight), independently of the type of

Marfà et al. (2009)

Gunes et al. (2016)

Increased yield, antioxidant enzyme activities and decreased freeze

Stress-related gene transcripts and metabolite levels increased

(Spann and Little, 2011). Microbial biostimulants based on arbuscular

area and volume) can be altered by the AMF inoculation, leading to an

the hyphal system to the water absorption was found significantly

plies at 55 % of maximum water holding capacity of soils) than in well

tions, allowing improved plant growth performances and higher leaf

were found higher in leaves of AMF-inoculated plants under drought

stress, whereas proline (also involved in the osmotic adjustment) was

prove structure and aggregate stability of rhizospheric soils with posi-

tive consequences on water availability and plant growth performances.

2014). Glomalin is a glycoprotein released by an AMF into soil during

the soil structure development (Wu et al., 2013). Recently, Jia-Dong

et al. (2019) investigated the role of aquaporins (i.e. proteinaceous

Foliar spray and soil application (10 % boron

Five foliar sprays (3% concentration), applied

Soil drench application (5 times). Dosage: 2.5

plants) at root level in the enhanced growth performances and water

status of trifoliate orange plants subjected to water stress and AMF

inoculation. Aquaporin genes were found both up and down regulated,

Some studies have focused on the possible application of different

classes of plant biostimulants for mitigating the effects of drought stress

also on grapevines (Vitis vinifera L.). Mancuso et al. (2006) reported

that, in a water stress experiment conducted in pots under controlled

conditions (greenhouse), the foliar application (twice a week) of a

Boron and plant growth

giovese’ grapevines (grafted onto 420A) compared to the untreated

control vines. This improvement in vine water status of treated plants

CO2 exchange rates. In another research carried out in pots, Nikolaou

the mycorrhizal fungi Glomus mosseae on the drought tolerance of

higher pre-dawn leaf water potential, stomatal conductance and leaf

Chen et al. (2017)

Xiao et al. (2015)

conditions may represent a useful tool to promote active growth of

shoot apices and to overcome stunted growth of micropropagated

photosynthesis in AMF inoculated plants, especially under

Increased plant height, shoot and root dry weight, P and N

characterized by a percentage of actively growing apices similar to P-

Increased plant biomass, leaf soluble protein, sugar

fertilized plantlets and significantly higher than the non-inoculated and

Zn-poor substrate. Decreased the soil pH.

mycorrhizal inoculation as a useful technique to reduce the use of

chemical fertilizer in nursery farms for the commercial production of

lected from an orchard showing apple replant disease symptoms (Gąstoł

centration in leaves. Moreover, the AMF inoculation promoted a higher

system level, therefore suggesting an interesting filtering-out me-

chanism against these toxic ions (Gąstoł et al., 2016).

Soil application (50 g of inoculum per plant containing

suspension (109 CFU·ml−1) inoculated into the middle

provement of the nutrient status, trees that were treated by spraying

canopies resulted more productive, without any negative consequence

Seedlings of sour orange (Citrus aurantium L.) inoculated with the