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.

Keywords: Endopolyploidy; UV-B-absorbing compounds; endoreduplication index; flow cytometry; holocentric chromosomes; monocentric chromosomes; natural population; ultraviolet radiation.

Fig. 1.

Sampling and sample processing design. (A) Maps of the Czech Republic (source: mapy.cz© Seznam.cz, a.s.) with sampled areas and localities (one locality comprises 1–13 studied populations). (B) Design of sampling in studied natural experiment using the example of one of 103 studied populations, each represented by five samples from the forest interior and five from a neighbouring clearing. (C) Sample processing depending on the type of studied herbaceous species (forb or graminoid).

Fig. 2.

The fits of phylogenetic mixed models performed in MCMCglmm. (A) The concentration of UV-B-absorbing compounds increases with the dose of direct light transmitted by the canopy, but the increase is more rapid in plants with monocentric chromosomes (β _monocentric = 0.061, vs. β _holocentric = 0.036, P_MCMC < 0.0002). (B) Endopolyploidy index increases with the dose of direct light transmitted by the canopy, but only in species with monocentric chromosomes (β _monocentric = 0.025, P_MCMC = 0.002 vs. β _holocentric = 0.008, P_MCMC = 0.105). (C) Endopolyploidy index increases with the concentration of UV-B-absorbing compounds only in species with monocentric chromosomes (β _monocentric = 0.255, P_MCMC = 0.004 vs. β _holocentric = 0.049, P_MCMC = 0.487).