Autopolyploidy alters nodule‐level interactions in the legume–rhizobium mutualism

Abstract

Premise Polyploidy is a major genetic driver of ecological and evolutionary processes in plants, yet its effects on plant interactions with mutualistic microbes remain unresolved. The legume–rhizobium symbiosis regulates global nutrient cycles and plays a role in the diversification of legume species. In this mutualism, rhizobia bacteria fix nitrogen in exchange for carbon provided by legume hosts. This exchange occurs inside root nodules, which house bacterial cells and represent the interface of legume–rhizobium interactions. Although polyploidy may directly impact the legume–rhizobium mutualism, no studies have explored how it alters the internal structure of nodules. Methods We created synthetic autotetraploids using Medicago sativa subsp. caerulea. Neotetraploid plants and their diploid progenitors were singly inoculated with two strains of rhizobia, Sinorhizobium meliloti and S. medicae. Confocal microscopy was used to quantify internal traits of nodules produced by diploid and neotetraploid plants. Results Autotetraploid plants produced larger nodules with larger nitrogen fixation zones than diploids for both strains of rhizobia, although the significance of these differences was limited by power. Neotetraploid M. sativa subsp. caerulea plants also produced symbiosomes that were significantly larger, nearly twice the size, than those present in diploids. Conclusions This study sheds light on how polyploidy directly affects a plant–bacterium mutualism and uncovers novel mechanisms. Changes in plant–microbe interactions that directly result from polyploidy likely contribute to the increased ability of polyploid legumes to establish in diverse environments.

Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism

“…Furthermore, although not tested directly here, a separate analysis of internal nodule traits of diploid and neotetraploid M. sativa subsp. caerulea found that polyploidy directly increased the size of rhizobia (bacteroids) hosted within nodules (Forrester & Ashman, 2019), a metric positively correlated with the amount of N provided to plant hosts (Oono & Denison, 2010). Thus, multiple mechanisms may have led to the polyploid advantage observed here.…”

“…Comparing established diploid and polyploid plants of the same species provides insight into how polyploidy might impact the evolutionary trajectory of plant species in natural populations (Spoelhof et al, 2017;Baduel et al, 2018;Forrester & Ashman, 2019). Medicago experienced multiple polyploidization events throughout its history, including an event 58 million years ago (Cannon et al, 2006;Young et al, 2011).…”

“…In addition, polyploid plants have larger cells, which might allow them to host a greater quantity of rhizobia, thereby increasing the amount of N obtained (Forrester & Ashman, 2018). These changes might enable polyploid plants to establish mutualisms with a broader range of rhizobial partners and/or host more or higher quality symbionts relative to diploids (reviewed by Forrester & Ashman, 2018;Forrester & Ashman, 2019). However, it remains unclear whether these differences translate to greater generalization in taxonomic niche breadth and host benefits obtained by polyploids across diverse rhizobial environments (Forrester & Ashman, 2018).…”

“…We conducted an inoculation experiment using a geographically widespread sampling of diploid (2x) and autotetraploid (4x) lineages of the plant species complex Medicago sativa and a diverse panel of Sinorhizobium bacterial symbionts. While synthetic neopolyploid plants can be used to isolate the immediate effects of polyploidy (Husband et al, 2008;Ramsey, 2011), with some caveats (see M€ unzbergov a, 2017), established polyploid lineages shed light onto the evolutionary consequences of genome duplication (Spoelhof et al, 2017;Baduel et al, 2018;Forrester & Ashman, 2019) and thus contribute to our understanding of successful polyploids. Ancient polyploidy is hypothesized to have enhanced legume mutualisms with rhizobia by duplicating genes that function in the establishment and maintenance of mutualism (Young et al, 2011;Li et al, 2013), yet no studies have tested biotic niche divergence in a polyploid (e.g.…”

Differential Gene Expression with an Emphasis on Floral Organ Size Differences in Natural and Synthetic Polyploids of Nicotiana tabacum (Solanaceae)

“…While natural polyploids have been used to investigate evolutionary and ecological questions including ecological niche differentiation, defense against herbivores, and stress tolerance [72][73][74][75][76][77], the production of synthetic allopolyploids allows for the study of traits instantaneously after genome merger. Many recent papers have used synthetic polyploids to study functional traits and inflorescence morphology in a variety of species [78][79][80][81][82][83]. By comparing natural and synthetic polyploids, the immediate consequences of polyploidy can be disentangled from the changes that occur via subsequent evolution following whole genome duplication.…”