Rapid evolution in plant–microbe interactions – an evolutionary genomics perspective

Abstract

Summary Access to greater genomic resolution through new sequencing technologies is transforming the field of plant pathology. As scientists embrace these new methods, some overarching patterns and observations come into focus. Evolutionary genomic studies are used to determine not only the origins of pathogen lineages and geographic patterns of genetic diversity, but also to discern how natural selection structures genetic variation across the genome. With greater and greater resolution, we can now pinpoint the targets of selection on a large scale. At multiple levels, crypsis and convergent evolution are evident. Host jumps and shifts may be more pervasive than once believed, and hybridization and horizontal gene transfer (HGT) likely play important roles in the emergence of genetic novelty.

Flourishing in water: the early evolution and diversification of plant receptor‐like kinases

“…Host–microbe conflicts can drive the everlasting arms race between hosts and microbes (Stukenbrock and McDonald, 2009; Han, 2019; de Vries et al ., 2020). The relevant genes from both parts that are involved in the conflicts may exhibit signs of positive selection (Han, 2019; de Vries et al ., 2020).…”

“…Host–microbe conflicts can drive the everlasting arms race between hosts and microbes (Stukenbrock and McDonald, 2009; Han, 2019; de Vries et al ., 2020). The relevant genes from both parts that are involved in the conflicts may exhibit signs of positive selection (Han, 2019; de Vries et al ., 2020). To detect selection pressure acting on RLKs from charophytes and land plants, we calculated the ratio of non‐synonymous to synonymous nucleotide substitution rates (dN/dS) and detected positively selected sites for 82 paralog groups from 40 RLK lineages (Table S4).…”

“…As a classical example of the ‘Red Queen’ dynamics, the evolutionary conflicts between plants and microbes result in everchanging co‐evolutionary cycles, imposing strong selective pressure on the evolution of relevant molecules of both parts (for instance, NBS‐LRRs and RLKs of plants and effector genes of pathogens) (Stukenbrock and McDonald, 2009; Han, 2019; de Vries et al ., 2020). The plant–microbe conflicts can drive cycling selective sweeps in both plant and microbe populations, or maintain allele frequency fluctuating in both plant and microbe populations through balancing selection (Stukenbrock and McDonald, 2009; Han, 2019; de Vries et al ., 2020). Plant–microbe interactions have recently been studied in both the evolutionary and mechanistic context, promoting an emerging field known as ‘evolutionary molecular plant–microbe interactions’ (de Vries et al ., 2018; Upson et al ., 2018).…”

Mutualist and pathogen traits interact to affect plant community structure in a spatially explicit model

“…This result is relevant to the interpretation of empirical studies that increasingly show that functionally specific pathogens with broad host ranges are the norm 32,48 . An additional possibility is that such generalist pathogens rapidly adapt or evolve to exploit a host occupying a given site 49 . In this case, the model results referring to microbial abundance could be interpreted as the degree of adaptation to a specific host species.…”

A multi-omics approach to solving problems in plant disease ecology

“…In addition to elucidating genomic architecture, phylogenomics and population genomics address similar questions, but at different biological scales: relationships among species, and individuals and populations within species, respectively. The types of questions addressed include genome-wide evolutionary and demographic processes affecting population structure, evolutionary processes affecting speciation and the divergence of closely related taxa, and locus-specific effects, acting on specific genes or chromosomes that affect adaptation or defined phenotypes [ 26 , 29 , 30 ]. Such data provide a foundation for understanding the evolutionary potential of plant pathogens.…”