The genetic architecture of adaptation to leaf and root bacterial microbiota in<i>Arabidopsis thaliana</i>

Roux, Fabrice; Frachon, Léa; Bartoli, Claudia

doi:10.1101/2022.09.26.509609

Cited by 5 publications

(7 citation statements)

References 101 publications

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“…Our results highlight the significant influence of plant compartment, site loca[on, and sampling season on shaping microbial communi[es, elucida[ng 14.6-25.7% of their variability, including bacteria, fungi, and non-fungal eukaryotes (Fig. 2), consistent with results from previous studies [30,[34][35][36][37][38][39].…”

Section: Discussionsupporting

confidence: 90%

Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues

Mahmoudi,

Almario,

Lutap

et al. 2023

Preprint

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The leaf-associated microbiome plays a crucial role in plant health and persistence to biotic and abiotic perturbations. However, factors that drive long-term seasonal adaptations of the leaf microbiome, particularly in response to combined stresses, are not well understood. To investigate seasonal adaptation of the leaf microbiome over five years, we analyzed changes in bacterial, fungal and general eukaryotic communities in and onArabidopsis thalianaleaves from natural populations using molecular markers. We collected samples during spring and fall and used linear regression models and co-occurrence networks to examine the roles of abiotic perturbations, space, and time in shaping the microbiome. Consistent with previous studies, time, space, and host compartment explained more than 18% of microbial community variation. Moreover, we dissect environmental factors that significantly impact microbial community variation. Additionally, we explored the effects of diversity and environmental factors on microbial network complexity and found that decreased diversity was correlated with increased complexity of microbial networks over growing seasons. We were thus able to identify individual microbial taxa that are adapted to specific seasons and their response to abiotic perturbations. We conclude that seasonality adaptation of leaf microbiota is significantly shaped by three environmental factors: radiation, wind speed and drought. Based on our findings we therefore hypothesize that beside space, time and compartment, diversity and stability of microbe-microbe interactions in the phyllosphere are predominantly shaped by a small set of environmental perturbations. Our findings have practical implications for the selection and development of field-adapted probiotics for agricultural applications.

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Section: Discussionsupporting

confidence: 90%

Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues

Mahmoudi,

Almario,

Lutap

et al. 2023

Preprint

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“…GEA analysis was performed on microbiota descriptors (species richness, Shannon’s diversity, PCoA first four axes and abundance of the most prevalent fungal and bacterial OTUs) as described in Roux et al ., 2023 and Frachon et al ., 2023 (10, 12). Detailed information about GEA analysis and related scripts are provided in the SI Appendix.…”

Section: Methodsmentioning

confidence: 99%

“…Recently, studies showed the power of GEA to identify plant loci associated with biotic communities. This has been demonstrated both in the non-model plant species B. incana and its associated pollinator communities (10), and in the model plant species Arabidopsis thaliana and its plant-plant (11) and plant-microbiome (12) interactions. The latter study is the only describing adaptive loci associated with bacterial descriptors in natural plant populations.…”

Section: Introductionmentioning

confidence: 99%

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

Maillet,

Norest,

Kautsky

et al. 2023

Preprint

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Plants as animals are strictly associated with a cortege of microbial communities influencing their health, fitness and evolution. Therefore, scientists refer to all living organisms as holobionts; complex genetic units that coevolve simultaneously. This is what has been recently proposed as the hologenome theory of evolution. This exciting and attractive theory has important implications on animal and plant health; however, it still needs consistent proof to be validated. Indeed, holobionts are still poorly studied in their natural habitats where coevolution and natural selective processes occur. Compared to animals and crops, wild plant populations are an excellent and unique model to explore the hologenome theory. These sessile holobionts have strictly coevolved with their microbiota for decades and natural selection and adaptive processes acting on wild plants are likely to regulate the plant-microbe interactions. Here we conducted for the first time a microbiota survey, plant genome sequencing and Genome-Environmental Analysis (GEA) of 26 natural populations of the non-model plant speciesBrassica rapa. We collected plants over two seasons in Italy and France, and analyzed the microbiota on two plant compartments (root and rhizosphere). We identified that plant compartment and season modulateB. rapamicrobiota. More importantly, when conducting GEA we evidenced neat peaks of association correlating with both fungal and bacterial microbiota. Surprisingly, we found 13 common genes between fungal and bacterial diversity descriptors that we referred under the name of Holobiont Generalist Genes (HGG). These genes might strongly regulate the diversity and composition of plant microbiota at the inter-kingdom level.Significance StatementThe novel hologenome concept claims that hosts and their associated microbes (considered as holobionts) are a unique evolutionary unit on which natural selection acts. Thus, the hologenome theory assumes that hosts and microbiomes simultaneously coevolve. This novel vision of universal evolutionary entities is promising for both animal and plant health purposes. However, it is still quietly controversial as it suffers from a lack of tangible evidence. How can we enrich the debate on holobionts? How can we translate this concept in discoveries that can change farming practices? Our study is filling the gaps of the hologenome theory by showing that certain genes under natural selection and regulating plant microbiota are generalist in response to fungal and bacterial communities.

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“…In this study, we aimed to describe the genetic architecture of the adaptive potential of the response of the annual wild plant species A. thaliana to attacks from more southern strains of the P. syringae species complex. Besides being a model in plant genetics and molecular biology, A. thaliana is above all a wild plant species inhabiting contrasting environments for diverse abiotic (e.g., climate, soil physicochemical properties) and biotic (e.g., microbial communities, plant communities) factors (Frachon et al, 2019;Roux et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

“…Besides being a model in plant genetics and molecular biology, A . thaliana is above all a wild plant species inhabiting contrasting environments for diverse abiotic (e.g., climate, soil physicochemical properties) and biotic (e.g., microbial communities, plant communities) factors (Frachon et al., 2019; Roux et al., 2023). In addition, disease incidence has been commonly observed in natural populations of A .…”

Section: Introductionmentioning

confidence: 99%

The genetic architecture of the adaptive potential of Arabidopsis thaliana in response to Pseudomonas syringae strains isolated from south‐west France

Bartoli,

Rigal,

Huard‐Chauveau

et al. 2023

Plant Pathology

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Phytopathogens are a threat for global food production and security. Emergence or re‐emergence of plant pathogens is highly dependent on the environmental conditions affecting pathogen spread and survival. Under climate change, a geographic expansion of pathogen distribution poleward has been observed, potentially resulting in disease outbreaks on crops and wild plants. Therefore, estimating the adaptive potential of plants to novel epidemics and describing the underlying genetic architecture is a primary need to propose agricultural management strategies reducing pathogen outbreaks and to breed novel plant cultivars adapted to pathogens that might spread under climate change. To address this challenge, we inoculated Pseudomonas syringae strains isolated from Arabidopsis thaliana populations from south‐west of France on the highly genetically polymorphic TOU‐A A. thaliana population from north‐east France. While no adaptive potential was identified in response to most P. syringae strains, the TOU‐A population displayed a variable disease response to the JACO‐CL strain belonging to the P. syringae phylogroup 7 (PG7). This strain carried a reduced type III secretion system (T3SS) characteristic of the PG7 as well as flexible genomic traits and potential novel effectors. Genome‐wide association mapping on 192 TOU‐A accessions revealed a polygenic architecture of disease response to JACO‐CL. The main quantitative trait locus (QTL) region encompasses two R genes and the AT5G18310 gene encoding ubiquitin hydrolase, a target of the AvrRpt2 P. syringae effector. Altogether, our results pave the way for a better understanding of the genetic and molecular basis of the adaptive potential in an ecologically relevant A. thaliana–P. syringae pathosystem.

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The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

Cited by 5 publications

References 101 publications

Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues

Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

The genetic architecture of the adaptive potential of Arabidopsis thaliana in response to Pseudomonas syringae strains isolated from south‐west France

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