Co‐evolution within the plant holobiont drives host performance

Abstract

Plants interact with a diversity of microorganisms that influence their growth and resilience, and they can therefore be considered as ecological entities, namely “plant holobionts,” rather than as singular organisms. In a plant holobiont, the assembly of above‐ and belowground microbiota is ruled by host, microbial, and environmental factors. Upon microorganism perception, plants activate immune signaling resulting in the secretion of factors that modulate microbiota composition. Additionally, metabolic interdependencies and antagonism between microbes are driving forces for community assemblies. We argue that complex plant–microbe and intermicrobial interactions have been selected for during evolution and may promote the survival and fitness of plants and their associated microorganisms as holobionts. As part of this process, plants evolved metabolite‐mediated strategies to selectively recruit beneficial microorganisms in their microbiota. Some of these microbiota members show host‐adaptation, from which mutualism may rapidly arise. In the holobiont, microbiota members also co‐evolved antagonistic activities that restrict proliferation of microbes with high pathogenic potential and can therefore prevent disease development. Co‐evolution within holobionts thus ultimately drives plant performance.

Adding experimental precision to the realism of field observations: Plant communities structure bacterial communities in a glacier forefield

“…By experimentally controlling plant species composition and richness, we can—to a large extent—exclude other factors apart from plant communities as causes for differences in bacterial communities at the end of the experiment. Plant species evolved multiple strategies to shape the microbes colonizing the soil that involve the plant immune system, phytohormone signalling and metabolites facilitating or preventing microbial growth indicating the plants' necessity to modulate the bacteria they interact with (Bulgarelli et al, 2013; Gaube et al, 2023; Junker & Tholl, 2013; Mesny et al, 2023). Bacteria often determine the fate of plants in ecosystems either by pathogenic functions reducing the plants' chance to establish or by growth‐promoting functions that provide higher competitive abilities (Berendsen et al, 2012; Delaux & Schornack, 2021).…”

“…The long shared evolutionary history of plants and microbes underlies the close ecological relationships between both partners as observed in extant ecosystems (Delaux & Schornack, 2021). Plant adaptations that facilitate the establishment of beneficial microbiota and those that restrict the growth of pathogens shape the microbial communities associated with plants and the surrounding substrate (Mesny et al, 2023). These adaptations involve the plant immune system, phytohormone signalling and metabolite‐mediated structuring mechanisms such as root exudates that shape plant species‐specific soil microbiomes (Bulgarelli et al, 2013; Gaube et al, 2023; Junker & Tholl, 2013; Mesny et al, 2023).…”

“…Plant adaptations that facilitate the establishment of beneficial microbiota and those that restrict the growth of pathogens shape the microbial communities associated with plants and the surrounding substrate (Mesny et al, 2023). These adaptations involve the plant immune system, phytohormone signalling and metabolite‐mediated structuring mechanisms such as root exudates that shape plant species‐specific soil microbiomes (Bulgarelli et al, 2013; Gaube et al, 2023; Junker & Tholl, 2013; Mesny et al, 2023). Consequently, plant species composition has often been reported to explain variation in the composition of microbial communities (e.g.…”

Symbiont plasticity as a driver of plant success

“…Plants have evolved complex metabolite‐mediated strategies, including those acting via the immune system, to selectively recruit beneficial microorganisms in their microbiota and suppress harmful microbes; either directly or via facilitation of microbes that restrict the proliferation of strong parasites (Hacquard et al ., 2017; Mesny et al ., 2023). Plants possessing these strategies are able to influence the relative proportions of different microbiome members or lead some microbes to disappear and others to colonize.…”

A fungal transcription factorBOT6facilitates the transition of a beneficial root fungus into an adapted anthracnose pathogen

“…Although it is little known how these endophytes can colonize inside plant tissues, they must overcome a durable and sophisticated defense system called nonhost resistance 2, 3, 4 . Even after they successfully enter host tissues, they simultaneously adapt their infection strategies, ranging from mutualistic to pathogenic, under changing host environments (changes in nutrients, host gene expression, or microbiota) 5, 6, 7, 8, 9 . Several reports have documented that host immune responses can drastically regulate the lifestyle of adapted microbes toward beneficial ones by restricting microbial colonization 10, 11, 12, 13 .…”