Available online at www.sciencedirect.

com Current Opinion in

ScienceDirect Plant Biology

The core microbiota across the green lineage

Paloma Durán

Abstract Introduction
The study of plant–microbe interactions and the character- Plant hosts interact with a multitude of microbes in
ization of plant-associated microbiota has been the focus of their natural environment, including bacteria and fungi.
plant researchers in the last decades due to its importance for These interactions are often key for the survival of the
plant health in natural conditions. Here, I explore the persistent host under stressful conditions, while hosts create hab-
core microbiota associated with different plant species and itats for the associated microbes, giving them access to
across different environments by performing a meta-analysis of released nutrients [1]. In addition, microbeemicrobe
publicly available datasets. Intra-specific analyses revealed interactions are yet another layer of complexity that
that diverse plant genotypes growing in similar habitats interact affects plant survival [2,3]. The study of plantemicrobe
with a common set of microbial groups but that some of these interactions has grown exponentially with the develop-
core groups are species- or environment-specific. Further- ment of next-generation sequencing technologies,
more, interspecific meta-analysis demonstrates the conserva- which has allowed the description of the microbiota
tion of seven bacterial orders across diverse photosynthetic associated with plant species in their natural habitats, as
organisms, including microalgae, suggesting a conserved ca- well as the correlation of microbial composition with
pacity for interaction with these core microbes throughout environmental variables and host traits [4e6]. More-
evolutionary history. However, the specific functions of these over, the generation of representative microbial culture
core members and whether these functions are conserved collections helped to move forward the plant microbiota
across hosts remain largely unexplored. I therefore discuss the field by tackling the functionality of these microbes in a
importance of understanding the roles of the core microbiota community context [7]. For example, by using synthetic
and propose future research directions, including the explora- biology and microbiota reconstitution experiments, it
tion of microbial interactions across different kingdoms. By has been recently shown how specific bacterial metab-
investigating the core microbiota and its functions, it will be olites are key for root microbiota structure [8], that
possible to leverage this knowledge for sustainable agricultural multiple bacterial groups are key for plant root archi-
management and conservation goals. tecture [9], or that interkingdom microbeemicrobe in-
teractions are crucial to maintain host health [10e12].
Addresses In addition to understanding the basis of microbiota
Laboratoire des Interactions Plantes-Microbes-Environnement, Institut
structure, the next milestone of plant microbiota
National de Recherche pour l’Agriculture, l’Alimentation et l’Envir-
onnement, CNRS, Université de Toulouse, Castanet-Tolosan, France research is to investigate how to leverage their proper-
ties for a more sustainable management of agriculture as
Corresponding author: Durán, Paloma (paloma.duran@inrae.fr) well as conservation goals [13e17].

Current Opinion in Plant Biology 2024, 77:102487 The persistent plant microbiota
This review comes from a themed issue on Biotic interactions 2024
In order to manage plant-associated microbial systems,
it is important to understand how these microbial
Edited by Pierre-Marc Delaux and Jacqueline Monaghan
communities change across ecological and host envi-
For complete overview of the section, please refer the article collection - ronments and the fraction of these communities that
Biotic interactions 2024
remains persistent. Indeed, a remarkable observation
Available online 5 December 2023 from all the work mentioned earlier is that despite dif-
https://doi.org/10.1016/j.pbi.2023.102487 ferences in habitat, environmental conditions, host ge-
1369-5266/© 2023 The Author. Published by Elsevier Ltd. This is an netics, or microbeemicrobe interactions, a subset of
o p e n a c c e s s a r t i c l e u n d e r t h e C C B Y- N C l i c e n s e ( h t t p : / / these microbial groups is invariably found in association
creativecommons.org/licenses/by-nc/4.0/). with all land plant species: the so-called persistent or
core microbiota [18]. Most microbiota studies highlight
Keywords a persistent microbiota associated with their system of
Plant microbiota, Core microbiota, Plant–microbe interactions, Sus- study, but despite the importance of these observations,
tainable agriculture, Photosynthetic organisms.

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2 Biotic interactions 2024

few studies have compiled data from multiple micro- groups with variable relative abundances that are
biota surveys to find commonalities. Therefore, to have reduced if the comparison is done across multiple en-
a global view, I have gathered and re-analyzed microbial vironments (Figure 1). Importantly, a subset of microbial
profiling data of plants growing in natural or seminatural groups (for example, Rokubacteriales in barley,
conditions, at different levels: 1) intraspecific: repre- Gemmatales in switchgrass, or Polyangiales in maize) are
sentative of multiple genotypes or multiple habitats of considered persistent within their own species but not
the same plant species and 2) interspecific: represen- for other species, suggesting that these are either
tative of multiple plant species. species-specific or site-specific (Figure 1).

Intraspecific persistent microbiota Interspecific persistent microbiota

Initially, plant microbiota studies focused on one refer- Based on the intraspecific meta-analysis and observa-
ence genotype of a given plant species growing in one or tions in many previous studies, there are microbial
multiple habitats. In order to understand the genetic members that are shared across different species. In the
basis of host control over the microbiota, reverse ge- work of Yeoh et al. [26**], the authors performed one of
netics approaches have been mostly utilized (e.g., using the most extensive multispecies microbiotaeprofiling
mutant lines to test a specific hypothesis). Only studies, including root samples of 31 plant species
recently, the natural variation of the host has been uti- inhabiting the same soil chronosequence. By doing so,
lized as a tool to understand the role of host genetics on they observed that nine different bacterial orders were
microbiota establishment. For instance, several genome- commonly found in association with these diverse set of
wide association studies (GWASs) based on hundreds of plant species, spanning from lycopods to angiosperms.
genotypes have been recently performed for diverse These findings suggest that the capacity to interact
plant species, such as in Arabidopsis phyllosphere with a common set of microbial groups might be
[19e21], in switchgrass roots [22], in maize roots [6], or conserved across the evolutionary history of photosyn-
in barley rhizosphere [23] and sorghum rhizosphere thetic organisms. But, how far in the green lineage tree
[24]. Within a given plant species, it could be expected is this capacity conserved? In our recent work, we
that genetic variation of the host will drive microbiota extended these observations to the microbiota associ-
differentiation, but also that a high proportion of mi- ated with Chlamydomonas reinhardtii, which is a unicel-
crobial groups will be shared between different host lular microalgae inhabiting the soil. Using equivalent
genotypes. In addition, the proportion of these shared microbiota-profiling methods to those used previously
microbial groups could decrease when the plant host with land plants, we showed that this microalgae,
inhabits different environments. To investigate this, I as well as other microalgae species, associate with soil-
performed a meta-analysis combining recent studies derived bacterial communities, especially those that are
where the microbiota of multiple accessions of a plant common across land plants, including those described
species was analyzed, as well as studies containing in [26**,27**].
multiple habitats for the same host species (Table 1). I
selected those microbial groups at the order level To put all of these findings into context, I gathered
(bacterial for all, and fungal when available) that were these and other profiling data from recent studies where
present in more than 70% of the samples (Supplemen- the bacterial microbiota of multiple plant species has
tary information, Figure 1). This highlighted that been analyzed (Table 2) and retrieved those bacterial
despite microbiota composition differences driven by groups that were found in more than 70% of the samples
host genetics (as analyzed by each respective study), in a given species (Supplementary information,
genetically diverse plant hosts growing in similar habi- Figure 2a, b). In addition to species-specific bacterial
tats interact with a common set of bacterial and fungal groups, and those in association with a subset of species,

Table 1

Studies from which data were retrieved for intraspecific persistent microbiota data analysis. Within each study, there are multiple ge-
notypes, multiple sites surveyed, or both.

Host species Study type Citation Microbial groups

Arabidopsis thaliana Multiple habitats Karasov et al., 202325 Bacteria

Arabidopsis thaliana Multiple habitats Thiergart et al., 20204 Bacteria, fungi
Hordeum vulgare Multiple genotypes in one habitat Escudero-Martinez et al., 202223 Bacteria
Capsella Multiple habitats Karasov et al., 202325 Bacteria
Zea species Multiple genotypes in one habitat He et al., 20236 Bacteria, fungi
Panicum virgatum Multiple genotypes inmultiple habitats Edwards et al., 202322 Bacteria

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 The core microbiota across the green lineage Durán 3

Figure 1

a) b)

Current Opinion in Plant Biology

Intraspecific persistent bacterial and fungal orders across published datasets. a) Bacterial orders that are found across 70% of the samples of a
given genotype within each study, with an abundance of at least 0.05% across the dataset. Symbol sizes represent the average relative abundance
across the dataset and are color-coded based on their taxonomic assignment at the phylum level. Symbol shapes represent the microhabitat that was
analyzed in each study. The upper panel represents the number of bacterial persistent groups found across different types of approaches (sample
number: n = 992 P. virgatum samples in Ref. [22]; n = 137 H. vulgare samples in Ref. [23]; n = 379 Zea samples in Ref. [6]; n = 198 A. thaliana samples in
Ref. [25]; n = 208 A. thaliana samples in Ref. [4]; n = 108 Capsella samples in Ref. [25]). b) Fungal orders that are found across 70% of the samples of a
given genotype within each study, with an abundance of at least 0.05% across the dataset. Symbol sizes represent the average relative abundance
across the dataset and are color-coded based on their taxonomic assignment at the phylum level. Symbol shapes represent the microhabitat that was
analyzed in each study. The upper panel represents the number of fungal persistent groups found across different types of approaches (sample number:
n = 387 Zea samples in Ref. [6]; n = 216 A. thaliana samples in Ref. [4]).

there is a gradient that goes from three to seven bac- that these members are adapted to outcompete other
terial orders following the host’s evolutionary microbial groups, and more importantly, to interact with
distance that are found in association with all the one another in multiple environments. Remarkably, the
photosynthetic species included in this analysis: number of common bacterial orders tends to increase
Burkholderiales, Caulobacterales, Chitinophagales, with the distance to the common ancestor, but the
Frankiales, Rhizobiales, Sphingomonadales, and relative abundance that these members account for re-
Xanthomonadales (Figure 2a, c). This means that mains relatively stable across the green lineage
members of these core groups do not rely on complex (Figure 2a, b, d). One hypothesis for this increment in
anatomical structures such as leaves or roots to assemble core microbiota diversity from Chlorophytes to Magno-
in the surrounding area of their host but are adapted to liophyta would be that with more complex interactions
plant-associated microhabitats and basic structures, being formed, hosts would engage in interactions
such as their cell walls. Also, they make up between 20% with more diverse microbial communities. Also, it is
and 80% of the total microbial abundance, suggesting possible that with evolutionary distance, there may be

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4 Biotic interactions 2024

Table 2 core members for their host. For example, Luo et al.
[32], by using RNA-isotope probing, have shown that
Studies from which data were retrieved for interspecific persis-
bacteria associated with plant roots that actively uptake
tent and core microbiota data analysis.
root exudates overlap with the core rhizosphere micro-
Citation Host species analyzed biota. In another study, Qiu et al. [33] showed that the
core microbiota resisted and protected their host of the
Karasov et al., 202325 2 invasion by a pathogenic fungal strain in cotton plants.
Thiergart et al., 20204 1 These examples suggest that the core microbiota has
Escudero-Martinez et al., 202223 1 beneficial roles for its host and that different members
He et al., 20236 2
of the core may have different functions. To further
Edwards et al., 202322 1
Alcaraz et al., 201828 2 characterize these functions in an unbiased manner, it
Yeoh et al., 201726 31 will be key to go back to surveying natural sites and
Duran et al., 2022a27 4 using high-throughput omics methods, such as shotgun
sequencing, microbial transcriptomics, or microbial
metabolomics. Thereby, it will be possible to decipher
the metabolic and functional traits of these microbial
an increase and diversification of exudates and anato- groups. In addition, isotope labeling, as in Ref. [32],
mical complexes, and more microbial members are would inform on what are the metabolic exchanges be-
capable of associating with these photosynthetic hosts. tween core microbes and their host. Finally, generation
While this meta-analysis includes many different of comprehensive culture collections and reconstruction
photosynthetic species, it still lacks more examples of of core microbiota communities will enable to test and
specific host groups. Therefore, it would be interesting validate 1) the functions of an overall core community
in the future to use a “gradient” of photosynthetic and 2) the specific roles of each member within the
model systems with different levels of core microbiota core community.
diversity to test these hypothesis experimentally (for
example, Chlamydomonas as representative of chlor- Another question that remains is how conserved these
ophytes, Mesostigma of charophytes, Marchantia of bryo- functions are: are members of the same taxonomic group
phytes, Ephedra of gymnosperms [29], and Arabidopsis from different core communities interchangeable be-
thaliana and Lotus japonicus (capable of symbiotic in- tween different hosts? To advance in this context, it may
teractions) of angiosperms). be important to make use of the aforementioned culture
collections of core microbiomes across multiple geno-
This meta-analysis highlights that there are several types and multiple species. In this direction, Wippel
levels of persistent microbiota: (1) one that is common et al. [34**] used the reference root-derived bacterial
to multiple genotypes of the same species, thereby culture collection of A. thaliana and that of L. japonicus
being of primary importance for unraveling the host and selected those bacterial members that were equiv-
genetic drivers of microbiota establishment; (2) one that alent in the two collections. Then, they cross-inoculated
is common to multiple genotypes in multiple habitats, these microbial consortia, which showed that bacterial
which could be relevant from an agricultural manage- members preferentially colonize (higher relative abun-
ment perspective, whereby, knowing what the core dance) their own host in a community context but that
microbiota is and how it may be affected by applying a they are equally capable of colonizing both hosts. In
treatment to diverse landraces across multiple locations similar lines, in our own work, we selected equivalent
would be of critical importance; and (3) one that is bacterial strains from the C. reinhardtiiederived culture
persistent across multiple host species and habitats and collection to those of A. thaliana and showed that com-
can give us a deeper understanding about the in- munity structure remained unchanged in association
teractions between microbes and photosynthetic or- with both hosts [27]. Therefore, to fully understand the
ganisms as well as their evolutionary trajectory. conservation of core microbiota roles, the next steps
would include using multiple hosts together with
The functions of the core microbiota and their derived culture collections to perform exchange
future perspectives experiments microbial members across core microbi-
One important caveat is that the groups highlighted al communities.
here were selected based on their taxonomy and abun-
dance, common factors by which to select core micro- Finally, another question that needs tackling is how
biota [30]. But it is important to note that other factors different microbial kingdoms interact with one another
could be used to define this core microbiota (as for a stable core community. As shown in Figure 1, there
discussed by Risely [31**]), including the functions are fungal members that are also shared across different
that these microbial members may provide for the host plant species, but the surveying depth of other microbial
and the core community. However, very few studies groups is far from that of bacterial communities. Thus, it
have taken the step to understand the functional role of will be important to include these understudied taxa as
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 The core microbiota across the green lineage Durán 5

Figure 2

a) b) c)

d)

Current Opinion in Plant Biology

Core microbiota across the green lineage. a) Phylogenetic tree of photosynthetic organisms used in this meta-analysis. In shaded gray and green are
highlighted the domains to which each species belongs, and the leaves of each domain are collapsed for easier visualization. b) Average relative
abundance of intraspecies bacterial orders found in association with photosynthetic organisms. The shades of gray indicate whether they are species-
specific or core bacterial groups (dark red). c) Zoom-in of the average relative abundance of interspecies bacterial orders scaled at 100% abundance.
These abundances correspond to those in b colored with dark red. d) Number of bacterial core groups found in each domain of the green lineage (number
of core members found in b). Gray and green shades match those in a. Significant differences are depicted with letters (P < 0.05, ANOVA with Tukey HSD
post hoc test). Abbreviation: ANOVA = analysis of variance; HSD = Honestly Significant Difference.

another layer of complexity required in order to fully Acknowledgements

understand core microbiota dynamics and their role on I thank Fabrice Roux, Fabienne Vailleau and two anonymous reviewers for
constructive comments on the manuscript. P.D. is member of the “Labo-
plant host health. ratoires d’Excellences (LABEX)” TULIP (ANR-10-LABX-41) and of the
“École Universitaire de Recherche (EUR)” TULIP-GS (ANR-18-
EURE-0019).
Funding
This project has received funding from the European
Research Council (ERC) under the European Union’s Supplementary information. Materials and
Horizon 2020 research and innovation program (grant methods
agreement No 951444 ePATHOCOM). Meta-analysis of intraspecific and interspecific
overlap of microbial communities
For the meta-analysis of host-associated bacterial and
Declaration of competing interest fungal communities, data from previous studies were
The authors declare that they have no known competing retrieved directly as processed operational taxonomic
financial interests or personal relationships that could units or amplicon sequence variants tables from their
have appeared to influence the work reported in this respective publications (Tables 1 and 2). Given that
paper. these studies used nonoverlapping sequencing primers,
all datasets were combined after aggregating relative
Data availability abundances at the bacterial order taxonomic level. The
Data and scripts will be deposited and available at persistent and core groups of the host-associated micro-
https://github.com/duranpa/COPB_metanalysis.git biota were determined by identifying bacterial orders

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6 Biotic interactions 2024

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