Abstract
Bacteria living on and in leaves and roots influence many aspects of plant health, so the extent of a plant's genetic control over its microbiota is of great interest to crop breeders and evolutionary biologists. Laboratory-based studies, because they poorly simulate true environmental heterogeneity, may misestimate or totally miss the influence of certain host genes on the microbiome. Here we report a large-scale field experiment to disentangle the effects of genotype, environment, age and year of harvest on bacterial communities associated with leaves and roots of Boechera stricta (Brassicaceae), a perennial wild mustard. Host genetic control of the microbiome is evident in leaves but not roots, and varies substantially among sites. Microbiome composition also shifts as plants age. Furthermore, a large proportion of leaf bacterial groups are shared with roots, suggesting inoculation from soil. Our results demonstrate how genotype-by-environment interactions contribute to the complexity of microbiome assembly in natural environments.
Highlights
Bacteria living on and in leaves and roots influence many aspects of plant health, so the extent of a plant’s genetic control over its microbiota is of great interest to crop breeders and evolutionary biologists
We focus on the following questions: first, how do bacterial communities change over the lifetimes of perennial plants? Second, how much do plant genotype and interactions of plant genotype with the local environment contribute to microbiome variation? Third, do above- and below-ground organs show similar patterns of genetic control over their resident bacterial communities? Here we show that root microbiomes change as plants age from 2 to 4 years old; the host genotype effect on the phyllosphere microbiome is environment-dependent; and despite strong overlap in community membership, leaf and root microbiomes are shaped by different sources of variation
To more stringently assess the degree of overlap between aboveground and belowground communities, we focused on the set of plants for which we had data from matched leaves and roots (N 1⁄4 237 plants) and reanalysed the raw reads to form operational taxonomic units (OTUs) based on a 99% sequence similarity threshold
Summary
Bacteria living on and in leaves and roots influence many aspects of plant health, so the extent of a plant’s genetic control over its microbiota is of great interest to crop breeders and evolutionary biologists. Quantitative trait locus mapping of field-grown maize exposed to low and high levels of ultraviolet-B radiation revealed multiple loci that controlled bacterial epiphyte diversity only under high ultraviolet-B, in addition to several loci with environment-independent (constitutive) effects[22] Such targeted experiments are useful for studying the genes underlying microbiome responses to specific environmental stimuli. Genetic variation for plastic responses to the suite of environmental factors that differentiate natural environments and agroecosystems should be assessed[23] Another understudied potential source of microbiome variation is host age, which can affect expression of plant functional traits that influence the microbiome (for example, defensive chemistry[15,24,25]). A more targeted experimental design is needed to learn how plant-associated microbial communities are maintained in aging perennial plants in the face of temporal variation
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