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.

Department of Botany and Zoology Masaryk University Brno Czech Republic

Zobrazit více v PubMed

Barow M. 2006. Endopolyploidy in seed plants. BioEssays  28: 271–281. PubMed

Barow M, Meister A. 2003. Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant, Cell & Environment  26: 571–584.

Beckmann M, Václavík T, Manceur AM, . et al 2014. glUV: a global UV-B radiation data set for macroecological studies. Methods in Ecology and Evolution  5: 372–383

Bieza K, Lois R. 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiology  126: 1105–1115. PubMed PMC

Bouchenak-Khelladi Y, Muasya AM, Linder HP. 2014. A revised evolutionary history of Poales: origins and diversification. Botanical Journal of the Linnean Society  175: 4–16.

Bureš P.  Zedek F, Marková M. 2013. Holocentric chromosomes. In: Leitch IJ, Greilhuber J, Doležel J, Wendel J, eds. Plant genome diversity, Vol. 2 Heidelberg: Springer, 187–208.

Caldwell MM. 1968. Solar ultraviolet radiation as an ecological factor for alpine plants. Ecological Monographs  38: 243–268.

Cuacos M, Franklin FCH, Heckmann S. 2015. Atypical centromeres in plants – what they can tell us. Frontiers in Plant Science  6: 913. PubMed PMC

de Villemereuil P, Nakagawa S. 2014. General quantitative genetic methods for comparative biology. In: Garamszegi L, eds. Modern phylogenetic comparative methods and their application in evolutionary biology. Heidelberg: Springer, 287–303.

Escudero M, Márquez-Corro JI, Hipp AL. 2016. The phylogenetic origins and evolutionary history of holocentric chromosomes. Systematic Botany  41: 580–585.

Frazer GW, Canham CD, Lertzman KP. 1999. Gap Light Analyzer (GLA), Version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, user’s manual and program documentation. Copyright © 1999: Simon Fraser University, Burnaby, British Columbia, and the Institute of Ecosystem Studies, Millbrook, New York.

Gegas VC, Wargent JJ, Pesquet E, Granqvist E, Paul ND, Doonan JH. 2014. Endopolyploidy as a potential alternative adaptive strategy for Arabidopsis leaf size variation in response to UV-B. Journal of Experimental Botany  65: 2757–2766. PubMed PMC

Gill SS, Anjum NA, Gill R, Jha M, Tuteja N. 2015. DNA damage and repair in plants under ultraviolet and ionizing radiations. The Scientific World Journal  2015: 250158. PubMed PMC

Gonzalez R, Paul ND, Percy K, et al.  1996. Responses to ultraviolet‐B radiation (280–315 nm) of pea (Pisum sativum) lines differing in leaf surface wax. Physiologia Plantarum  98: 852–860.

Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software  33: 1–22. PubMed PMC

Hadfield JD, Nakagawa S. 2010. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. Journal of Evolutionary Biology  23: 494–508. PubMed

Hase Y, Trung KH, Matsunaga T, Tanaka A. 2006. A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. The Plant Journal: for Cell and Molecular Biology  46: 317–326. PubMed

Hopkins L, Bond MA, Tobin AK. 2002. Ultraviolet-B radiation reduces the rates of cell division and elongation in the primary leaf of wheat (Triticum aestivum L. cv Maris Huntsman). Plant, Cell & Environment  25: 617–624.

Jankowska M, Fuchs J, Klocke E, et al.  2015. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma  124: 519–528. PubMed

Jansen MA, Gaba V, Greenberg BM. 1998. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends in Plant Science  3: 131–135.

Klančnik K, Vogel-Mikuš K, Gaberščik A. 2014. Silicified structures affect leaf optical properties in grasses and sedge. Journal of Photochemistry and Photobiology B  130: 1–10. PubMed

Kolodin P, Cempírková H, Bureš P, et al.  2018. Holocentric chromosomes may be an apomorphy of Droseraceae. Plant Systematics and Evolution  304: 1289–1296.

Körner C. 2003. Alpine plant life: functional plant ecology of high mountain ecosystems. Berlin: Springer.

Král J, Forman M, Kořínková T, et al.  2019. Insights into the karyotype and genome evolution of haplogyne spiders indicate a polyploid origin of lineage with holokinetic chromosomes. Scientific Reports  9: 3001. PubMed PMC

Kumar S, Stecher G, Suleski M, Blair Hedges S. 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Molecular Biology and Evolution  32: 835–845. PubMed

Lavola A. 1998. Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiology  18: 53–58. PubMed

Leitch IJ, Dodsworth S. 2017. Endopolyploidy in plants. In: Hetherington AM. ed. Encyclopedia of life sciences. Chichester, UK: John Wiley & Sons, 1–10.

Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL. 1993. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. The Plant Cell  5: 171–179. PubMed PMC

Linder HP, Rudall PJ. 2005. Evolutionary history of Poales. Annual Review of Ecology, Evolution, and Systematics  36: 107–124.

Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL. 2000. Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiology  122: 117–126. PubMed PMC

Mehra PN, Sharma OP. 1965. Epidermal silica cells in the Cyperaceae. Botanical Gazette  126: 53–58.

Melters DP, Paliulis LV, Korf IF, Chan SW. 2012. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Research: An International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology  20: 579–593. PubMed

Nelissen H, Gonzalez N, Inzé D. 2016. Leaf growth in dicots and monocots: so different yet so alike. Current Opinion in Plant Biology  33: 72–76. PubMed

Oliveira L, Neumann P, Jang TS, et al.  2020. Mitotic spindle attachment to the holocentric chromosomes of Cuscuta europaea does not correlate with the distribution of CENH3 chromatin. Frontiers in Plant Science  10: 1799. PubMed PMC

Orr-Weaver TL. 2015. When bigger is better: the role of polyploidy in organogenesis. Trends in Genetics: TIG  31: 307–315. PubMed PMC

Prychid CJ, Rudall PJ, Gregory M. 2003. Systematics and biology of silica bodies in Monocotyledons. Botanical Review  69: 377–440.

R Core Team 2018. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; http://www.R-project.org/.

Radziejwoski A, Vlieghe K, Lammens T, et al.  2011. Atypical E2F activity coordinates PHR1 photolyase gene transcription with endoreduplication onset. The EMBO Journal  30: 355–363. PubMed PMC

Rastogi RP, Richa Kumar A, Tyagi MB, Sinha RP. 2010. Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. Journal of Nucleic Acids  2010: 592980. PubMed PMC

Robson TM, Klem K, Urban O, Jansen MA. 2015. Re-interpreting plant morphological responses to UV-B radiation. Plant, Cell & Environment  38: 856–866. PubMed

Rozema J, Björn LO, Bornman JF, et al.  2002. The role of UV-B radiation in aquatic and terrestrial ecosystems – an experimental and functional analysis of the evolution of UV-absorbing compounds. Journal of Photochemistry and Photobiology. B, Biology  66: 2–12. PubMed

Rozema J, van de Staaij J, Björn LO, Caldwell M. 1997. UV-B as an environmental factor in plant life: stress and regulation. Trends in Ecology & Evolution  12: 22–28. PubMed

Santos I, Fidalgo F, Almeida JM, Salema R. 2004. Biochemical and ultrastructural changes in leaves of potato plants grown under supplementary UV-B radiation. Plant Science  167: 925–935.

Schaller J, Brackhage C, Bäucker E, Dudel EG. 2013. UV-screening of grasses by plant silica layer?  Journal of Biosciences  38: 413–416. PubMed

Scholes DR, Paige KN. 2015. Plasticity in ploidy: a generalized response to stress. Trends in Plant Science  20: 165–175. PubMed

Sheikh SA, Kondo K, Hoshi Y. 1995. Study of diffused centromeric nature of Drosera chromosomes. Cytologia  60: 43–47.

Šmarda P, Bureš P, Šmerda J, Horová L. 2012. Measurements of genomic GC content in plant genomes with flow cytometry: a test for reliability. New Phytologist  193: 513–521. PubMed

Stapleton AE, Walbot V. 1994. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiology  105: 881–889. PubMed PMC

Tanaka N. 2020. High stability in chromosomal traits of Chamaelirium japonicum and C. koidzuminum (Melanthiaceae) with holocentric chromosomes. Cytologia  85: 33–40.

Wargent JJ, Moore JP, Roland Ennos A, Paul ND. 2009. Ultraviolet radiation as a limiting factor in leaf expansion and development. Photochemistry and Photobiology  85: 279–286. PubMed

Willis KJ, Bennett KD, Birks HJB. 2009. Variability in thermal and UV-B energy fluxes through time and their influence on plant diversity and speciation. Journal of Biogeography  36: 1630–1644.

Yamasaki S, Shigeto H, Ashihara Y, Noguchi N. 2014. Continuous long-term UV-B irradiation reduces division and expansion of epidermal cells in true leaves, but accelerates developmental stages such as true leaf unfolding and male flower bud production in cucumber (Cucumis sativus L.) seedlings. Environmental Control in Biology  52: 13–19.

Yamasaki S, Shimada E, Kuwano T, Kawano T, Noguchi N. 2010. Continuous UV-B irradiation induces endoreduplication and peroxidase activity in epidermal cells surrounding trichomes on cucumber cotyledons. Journal of Radiation Research  51: 187–196. PubMed

Zedek F, Bureš P. 2016. Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Annals of Botany  118: 1347–1352. PubMed PMC

Zedek F, Bureš P. 2018. Holocentric chromosomes: from tolerance to fragmentation to colonization of the land. Annals of Botany  121: 9–16. PubMed PMC

Zedek F, Bureš P. 2019. Pest arthropods with holocentric chromosomes are more resistant to sterilizing ionizing radiation. Radiation Research  191: 255–261. PubMed

Zedek F, Šmerda J, Veselý P, Horová L, Kocmanová J, Bureš P. 2020. Elevation-dependent endopolyploid response suggests that plants with holocentric chromosomes are less stressed by UV-B. Botanical Journal of the Linnean Society, doi: 10.1093/botlinnean/boaa054. DOI

Zedek F, Veselý P, Horová L, Bureš P. 2016. Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants. Scientific Reports  6: 27161. PubMed PMC