Polyploidy: an evolutionary and ecological force in stressful times

Abstract

Polyploidy has been hypothesized to be both an evolutionary dead-end and a source for evolutionary innovation and species diversification. Although polyploid organisms, especially plants, abound, the apparent nonrandom long-term establishment of genome duplications suggests a link with environmental conditions. Whole-genome duplications seem to correlate with periods of extinction or global change, while polyploids often thrive in harsh or disturbed environments. Evidence is also accumulating that biotic interactions, for instance, with pathogens or mutualists, affect polyploids differently than nonpolyploids. Here, we review recent findings and insights on the effect of both abiotic and biotic stress on polyploids versus nonpolyploids and propose that stress response in general is an important and even determining factor in the establishment and success of polyploidy.

Figure 1

The nonrandom establishment of WGDs. Red crosses represent extinction, while orange circles represent successful polyploidy coinciding with environmental stress, and light orange triangles represent successful polyploidy following delayed rediploidization [responsible for lag times between the WGD event and its exerted effects {Schranz et al., 2012; Robertson et al., 2017}]. The dark blue diamond represents a diploid having survived environmentally challenging conditions. The two branches descending from a WGD event represent the duplicated genome, while the changing color in one branch denotes the divergence (and diploidization) of the subgenomes. Gray squares represent WGDs that coincide (purple) or seem to coincide (light gray) with a period of global change or extinction. If polyploidy by itself (without rediploidization, functional divergence of genes, or rewiring of networks) enables evolutionary innovation (e.g. through short-term gene expression changes, epigenetic remodeling), WGDs might become established even in the absence of rediploidization (represented by the light blue square). See text for details.

Figure 2

Representative examples of the effects of polyploidy on mutualistic and antagonistic species interactions. (A, B, and D), Examples of mutualistic interactions. (C), Antagonist interaction. (A) Root nodules of synthetic neotetraploid (left) and diploid (right) alfalfa (Medicago sativa subsp. caerulea) inoculated with rhizobia (Forrester and Ashman, 2020). The autotetraploid plants produced nodules that were 20% larger than diploids and these housed symbiosomes—each with enlarged bacteroids (white arrows)—that were nearly twice the size of those present in diploids. Nodules are stained with SYTO 13 bacteroid fluorescence is depicted in green and plant autofluorescence in blue, 10× lens was used for viewing. (B) Tetraploid (left) alfalfa subsp. sativa and diploid (right) alfalfa subsp. caerulea showing root nodule production (Forrester et al., 2020). Autotetraploid alfalfa produced more than twice as much total root nodule biomass (white arrows pointing to individual nodules) than diploids, and this leads to higher shoot biomass. (C) Tetraploid (left) and diploid (right) apple (Malus × domestica cultivar G58) response to infection by the ascomycete fungus Venturia inaequalis causing apple scab disease (Hias et al., 2018). Visual symptoms and PCR quantification of V. inaequalis decreased in the neotetraploid relative to its diploid progenitor. (D) Tetraploid (left) and diploid (right) poker alumroot (Heuchera cylindrica) roots colonized by mycorrhizae fungal arbuscules (the nutritional-exchange structures; Anneberg and Segraves, 2019). Tetraploids show higher colonization rates, as measured by total arbuscules (arrows pointing to arbuscules in each image) than diploids. 200× magnification. Photo credits: (A and B) N. Forrester, (C) N. Hias, and (D) T.J. Anneberg.