Association mapping of ectomycorrhizal traits in loblolly pine (Pinus taedaL.)

Abstract

To understand how diverse mutualisms coevolve and how species adapt to complex environments, a description of the underlying genetic basis of the traits involved must be provided. For example, in diverse coevolving mutualisms, such as the interaction of host plants with a suite of symbiotic mycorrhizal fungi, a key question is whether host plants can coevolve independently with multiple species of symbionts, which depends on whether those interactions are governed independently by separate genes or pleiotropically by shared genes. To provide insight into this question, we employed an association mapping approach in a clonally replicated field experiment of loblolly pine (Pinus taeda L.) to identify genetic components of host traits governing ectomycorrhizal (EM) symbioses (mycorrhizal traits). The relative abundances of different EM fungi as well as the total number of root tips per cm root colonized by EM fungi were analyzed as separate mycorrhizal traits of loblolly pine. Single‐nucleotide polymorphisms (SNPs) within candidate genes of loblolly pine were associated with loblolly pine mycorrhizal traits, mapped to the loblolly pine genome, and their putative protein function obtained when available. The results support the hypothesis that ectomycorrhiza formation is governed by host genes of large effect that apparently have independent influences on host interactions with different symbiont species.

Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes

“…Ecological effects of context-dependency in mutualism have been recognized for a long time, i.e., traits and mutualism benefits often shift across environmental conditions such as nutrient availability or light environments ( 97 – 99 ), although not ubiquitously for all traits (e.g., 100 , 101 ). More recent studies have begun to document the evolutionary changes that can result from these ecological effects, e.g., divergence of host and/or symbiont symbiosis traits across strong ecological gradients ( 59 , 102 – 105 ). Evolutionary change in response to environments implies that the loci underlying selected traits have differential effects on fitness across environments.…”

Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

“…Ecological effects of context-dependency in mutualism have been recognized for a long time, i.e., traits and mutualism benefits often shift across environmental conditions such as nutrient availability or light environments (97, 98, 99), although not ubiquitously for all traits (e.g., 100, 101). More recent studies have begun to document the evolutionary changes that can result from these ecological effects, e.g., divergence of host and/or symbiont symbiosis traits across strong ecological gradients (59, 102, 103, 104, 105). Evolutionary change in response to environments implies that the loci underlying selected traits have differential effects on fitness across environments.…”

“…traits (e.g.,93,94). More recent studies have begun to document the evolutionary changes that can result from these ecological effects, e.g., divergence of host and/or symbiont symbiosis traits across strong ecological gradients(95,96, 59,97,98). Evolutionary change in response to environments implies that the loci underlying selected traits have differential effects on fitness across environments.…”

Interspecific selection in a diverse mycorrhizal symbiosis

“…Because mycorrhizal symbioses are diverse, multispecies interactions in which multiple fungi can associate with the same plant and vice versa 17 , 18 , it is not clear whether we expect them to evolve towards a core set of shared mutualistic traits (as predicted for purely free-living mutualisms) or towards a set of complementary non-competing symbionts that have unique modes of interaction with each other (as predicted for intimate symbiosis 13 ). Experiments with pines and ectomycorrhizal (ECM) fungi suggest that pine populations have evolved preferences for particular fungal species 19 , 20 and that some of these interactions may be controlled in plants by independent loci of large effect 21 . Estimates of natural selection by ECM fungi on plant traits could lend insight into how interspecific selection may operate in such multispecific mutualistic species interactions, yet we lack direct field estimates of natural selection in these diverse interactions.…”