Co-evolution within the plant holobiont drives host performance

EMBO Rep. 2023 Sep 6;24(9):e57455. doi: 10.15252/embr.202357455. Epub 2023 Jul 20.

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.

Keywords: ecosystem; fitness; immunity; metaorganism; microbiome.

Publication types

  • Review
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Microbiota* / physiology
  • Plants*
  • Symbiosis