Uncovering the reciprocal effects of plant polyploidy and the microbiome: implications for understanding of polyploid success

Abstract

Polyploidy plays a major role in diversification and speciation of almost all plants. Separately, the microbiome is recognized for its ubiquitous role in plant functioning. Despite the importance of both processes, we lack a synthetic picture of their reciprocal relationship. I forge this missing linkage by presenting the ways in which plant polyploidy can shape the microbiome and how the microbiome in turn can affect polyploid phenotype and fitness. I illustrate these interactions by drawing on the small, but compelling, set of comparisons of the plant-microbial community interaction with taxa representing different stages of the polyploid continuum and thereby shed light on how the advantages of polyploidy may be influenced by microbes. I use findings from a range of studies to build the case for plant-microbiome reciprocal interactions in both key pathways for polyploid persistence: overcoming their minority cytotype disadvantage and increasing competitive ability and/or niche shifts relative to diploids. I put forward how the microbiome likely plays a role in polyploid stress tolerance, abiotic niche breadth, range limits and coexistence. I conclude by identifying the research needed to test these hypotheses and how doing so could transform our understanding of polyploidy as a driver of plant ecology and evolution.

Keywords: coexistence; microbiome; minority cytotype; niche breadth; plant–microbe interaction; plasticity; polyploidy.

Fig. 1

Conceptual representation of and predictions for the microbiome and polyploidy interaction. (a) Schematic path diagram of reciprocal interactions of polyploidy and the microbiome described in this paper. Arrows reflect the direction of effects between any two elements in the diagram, and blue brackets denote emergent processes that result from the interactions enclosed within them. Specifically, whole genome duplication (WGD: center) that creates a polyploid plant (right side) with a phenotype that differs from the diploid (left side) may lead to a change in the structure of its microbial community, which in turn can feedback to modify the polyploid's phenotypic expression. The polyploid's stress tolerance may be enhanced relative to the diploid's either through its direct response to stress or responses mediated through its microbial community. Likewise, expression of phenotypic plasticity of the polyploid might exceed that of the diploid via plant response or microbially mediated response. Both diploid and polyploid plants may uniquely condition their soils in ways that could contribute pairwise plant–soil feedbacks that in turn promote diploid–polyploid coexistence or exclusion of one ploidy. (b) Schematic of predictions for degree of microbiome differentiation and strength of pairwise plant–soil feedbacks. Degree of differentiation (from same to different) between polyploid and diploid microbiomes (upper) and strength (from neutral to strong) of diploid–polyploid plant–soil feedbacks (lower) will scale with the stages of the polyploid continuum (from synthetic neo‐polyploid–diploid pairs to more phylogenetically differentiated allopatric polyploid–diploid species pairs).