Endopolyploidy is a common response to UV-B stress in natural plant populations, but its magnitude may be affected by chromosome type

Abstract

Background and Aims Ultraviolet-B radiation (UV-B) radiation damages the DNA, cells and photosynthetic apparatus of plants. Plants commonly prevent this damage by synthetizing UV-B-protective compounds. Recent laboratory experiments in Arabidopsis and cucumber have indicated that plants can also respond to UV-B stress with endopolyploidy. Here we test the generality of this response in natural plant populations, considering their monocentric or holocentric chromosomal structure. Methods We measured the endopolyploidy index (flow cytometry) and the concentration of UV-B-protective compounds in leaves of 12 herbaceous species (1007 individuals) from forest interiors and neighbouring clearings where they were exposed to increased UV-B radiation (103 forest + clearing populations). We then analysed the data using phylogenetic mixed models. Key Results The concentration of UV-B protectives increased with UV-B doses estimated from hemispheric photographs of the sky above sample collection sites, but the increase was more rapid in species with monocentric chromosomes. Endopolyploidy index increased with UV-B doses and with concentrations of UV-B-absorbing compounds only in species with monocentric chromosomes, while holocentric species responded negligibly. Conclusions Endopolyploidy seems to be a common response to increased UV-B in monocentric plants. Low sensitivity to UV-B in holocentric species might relate to their success in high-UV-stressed habitats and corroborates the hypothesized role of holocentric chromosomes in plant terrestrialization.

Holocentric plants are more competitive under higher UV‐B doses

“…Our results showed that the holocentric : monocentric cover ratio increased with the dose of UV-B radiation across Europe (Fig. 3; Table 1), suggesting that the previously reported ability of the holocentric chromosomes of cyperids to mitigate UV-B stress (Zedek et al, 2020(Zedek et al, , 2021 may, indeed, be turned into a competitive advantage. The dose of UV-B explained only 0.61% of the variability in the relative cover of cyperids and grasses (Table 1).…”

“…Endopolyploidy is one or multiple rounds of nuclear DNA replication without subsequent cell division and may be induced by various stress conditions, including UV-B and DNA lesions (Leitch & Dodsworth, 2017;Lang & Schnittger, 2020). We obtained results suggesting that holocentric plants might indeed be less stressed by abruptly increased UV-B doses than monocentric plants (Zedek et al, 2020). This was confirmed in the following study in which we compared endopolyploid stress responses to UV-B between two closely related clades, grasses (Poaceae) and cyperids (Cyperaceae and Luzula (Juncaceae)), along a broad altitudinal UV-B gradient and showed that the stress response of cyperids (holocentric graminoids) was milder than the response of grasses (monocentric graminoids; Zedek et al, 2021).…”

“…1 for details). Due to their structure, holocentric chromosomes could confer a selective advantage against factors causing chromosome fragmentation (clastogens), such as ionising radiation (Bakri et al, 2005;Carpenter et al, 2005;Zedek & Bureš, 2019), certain chemicals (Mandrioli & Manicardi, 2012 and also UV-B radiation Zedek et al, 2020Zedek et al, , 2021.…”

Changes in global DNA methylation under climatic stress in two related grasses suggest a possible role of epigenetics in the ecological success of polyploids

“…This is probably caused by the effect of UV radiation, which is harmful to living organisms, the increase in cell transpiration through the leaves, and the more noticeable drought. Recent research has shown that insolation is a key driver of short-term changes in DNA methylation, and thus the stress experienced by the plant, as well as their physiological changes and adaptation to harmful conditions 38 , 39 . However, it seems that there is no universal rule governing the DNA methylation response of plants to UV radiation: UV-B radiation elicited DNA demethylation in Artemisia annua 40 and UV-A/B irradiation resulted in minimal changes in DNA methylation in maize 41 .…”

Ploidy and local environment drive intraspecific variation in endoreduplication in Arabidopsis arenosa

“…In line with this expectation, an increasing number of studies showed the effects of various environmental factors on endoreduplication in plants. For instance, correlations between endoreduplication and soil water content (Cookson et al, 2006), salt adaptation (Ceccarelli et al, 2006), UV‐B radiation (Zedek et al, 2020), cold temperature (Jovtchev et al, 2007) (Pierre et al, 2014), and various biotic interactions (Wildermuth, 2010; de Almeida Engler and Gheysen, 2013) have all been reported.…”