Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism

Abstract

Polyploidy is a key driver of ecological and evolutionary processes in plants, yet little is known about its effects on biotic interactions. This gap in knowledge is especially profound for nutrient acquisition mutualisms, despite the fact that they regulate global nutrient cycles and structure ecosystems. Generalism in mutualistic interactions depends on the range of potential partners (niche breadth), the benefits obtained and ability to maintain benefits across a variety of partners (fitness plasticity). Here, we determine how each of these is influenced by polyploidy in the legume-rhizobium mutualism. We inoculated a broad geographic sample of natural diploid and autotetraploid alfalfa (Medicago sativa) lineages with a diverse panel of Sinorhizobium bacterial symbionts. To analyze the extent and mechanism of generalism, we measured host growth benefits and functional traits. Autotetraploid plants obtained greater fitness enhancement from mutualistic interactions and were better able to maintain this across diverse rhizobial partners (i.e. low plasticity in fitness) relative to diploids. These benefits were not attributed to increases in niche breadth, but instead reflect increased rewards from investment in the mutualism. Polyploid plants displayed greater generalization in bacterial mutualisms relative to diploids, illustrating another axis of advantage for polyploids over diploids.

Polyploidy: A Biological Force From Cells to Ecosystems

“…Such injury-triggered WGD may enable rapid tissue regrowth without compromising the integrity of a tissue barrier during cell division [26] or provide necessary mechanical force [27]. Similarly, in plants, endoreplication responses (cell cycle activation without mitosis) can be stimulated by both major pathogens of agricultural crops (e.g., powdery mildew, root knot nematodes [28]) and ancient mutualistic associations (e.g., mycorrhizal fungi and nitrogen-fixing rhizobia) in which most plants engage [29,30]. While endoreplication can arise via various shortcuts in the cell cycle, endoreplication in response to biotrophic interactions that involve penetration of the plant tissue results in upregulation of the same genes, suggesting that the effectors involved are generic reactions to cell stress [29].…”

A multilayered cross-species analysis of GRAS transcription factors uncovered their functional networks in plant adaptation to the environment

“…Polyploidy, or whole-genome duplication (WGD), is one of the key forces of ecological and evolutionary processes in plants [2] . Caused by abnormal environments, polyploidization, or WGD, can increase the adaptive plasticity of plants to environments and the genetic variability of plants [3] .…”

“…Caused by abnormal environments, polyploidization, or WGD, can increase the adaptive plasticity of plants to environments and the genetic variability of plants [3] . Polyploidy is particularly common in plants, with all angiosperms sharing ancestral polyploid events and 24% of existing plant species being recent polyploids [2] , [4] . During evolution and genome diploidization, many duplicated genes have been lost or highly modified, and the number of duplicated chromosomes has been rearranged and reduced, leaving multiple duplicated genes without obvious cytological evidence of WGD [5] .…”

When everything changes at once: finding a new normal after genome duplication

“…Increased cell size may have additional context-specific consequences such as the relationship of legumes with their nitrogen-fixing symbiotic partners. For example, polyploids gain more vigour from mutualism with a wide range of Sinorhizobium strains than diploids [44][45][46]. For autotetraploid Medicago sativa, this is mediated by larger nodules with larger nitrogen (N)-fixation zones, which leads to greater N-fixation.…”