, Volume 181, Issue 4, pp 1069–1082 | Cite as

Ultraviolet-B-induced DNA damage and ultraviolet-B tolerance mechanisms in species with different functional groups coexisting in subalpine moorlands

  • Qing-Wei Wang
  • Chiho Kamiyama
  • Jun Hidema
  • Kouki Hikosaka
Physiological ecology - original research


High doses of ultraviolet-B (UV-B; 280–315 nm) radiation can have detrimental effects on plants, and especially damage their DNA. Plants have DNA repair and protection mechanisms to prevent UV-B damage. However, it remains unclear how DNA damage and tolerance mechanisms vary among field species. We studied DNA damage and tolerance mechanisms in 26 species with different functional groups coexisting in two moorlands at two elevations. We collected current-year leaves in July and August, and determined accumulation of cyclobutane pyrimidine dimer (CPD) as UV-B damage and photorepair activity (PRA) and concentrations of UV-absorbing compounds (UACs) and carotenoids (CARs) as UV-B tolerance mechanisms. DNA damage was greater in dicot than in monocot species, and higher in herbaceous than in woody species. Evergreen species accumulated more CPDs than deciduous species. PRA was higher in Poaceae than in species of other families. UACs were significantly higher in woody than in herbaceous species. The CPD level was not explained by the mechanisms across species, but was significantly related to PRA and UACs when we ignored species with low CPD, PRA and UACs, implying the presence of another effective tolerance mechanism. UACs were correlated negatively with PRA and positively with CARs. Our results revealed that UV-induced DNA damage significantly varies among native species, and this variation is related to functional groups. DNA repair, rather than UV-B protection, dominates in UV-B tolerance in the field. Our findings also suggest that UV-B tolerance mechanisms vary among species under evolutionary trade-off and synergism.


Photorepair Ultraviolet-B protection Trade-off Interspecific variation Cyclobutane pyrimidine dimer 



We thank Drs Riichi Oguchi, Hiroshi Ozaki, Soichiro Nagano, and Michio Oguro for valuable comments. We are also grateful to Dr Mika Teranishi, Hiroko Yamaguchi, Nan Li, and Mami Kanbayashi for field and laboratory support. This study was supported by grants from MEXT, Japan (KAKENHI, nos. 21114009, 25291095, 25660113); the Global Environment Research Fund (F-092/D-0904) of the Ministry of the Environment, Japan; the Global COE Program the Center for Ecosystem Management Adapting to Global Change (J03) of MEXT, Japan; CREST, JST, Japan; and a research grant from the Mitsui Environment Fund.

Author contribution statement

KH and QWW conceived and designed the experiment. QWW, CK, and KH collected samples in the field. QWW and JH performed the biochemical analyses. QWW analyzed the data and wrote the manuscript. KH, CK, and JH provided comments.

Supplementary material

442_2016_3644_MOESM1_ESM.docx (223 kb)
Supplementary material 1 (DOCX 222 kb)


  1. Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363CrossRefPubMedGoogle Scholar
  2. Ballaré CL, Caldwell MM, Flint SD, Robinson S, Bornman JF (2011) Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochem Photobiol SciGoogle Scholar
  3. Ballaré CL, Mazza CA, Austin AT, Pierik R (2012) Canopy light and plant health. J Plant Physiol 160:145–155CrossRefGoogle Scholar
  4. Ballaré CL et al (2001) Impacts of solar ultraviolet-B radiation on terrestrial ecosystems of Tierra del Fuego (southern Argentina). An overview of recent progress. J Photochem Photobiol B: Biol 62:67–77CrossRefGoogle Scholar
  5. Barnes PW, Flint SD, Caldwell MM (1990) Morphological responses of crop and weed species of different growth forms to ultraviolet-B radiation. Am J Bot:1354-1360Google Scholar
  6. Bassman JH, Edwards GE, Robberecht R (2002) Long-term exposure to enhanced UV-B radiation is not detrimental to growth and photosynthesis in Douglas-fir. New Phytol 154:107–120CrossRefGoogle Scholar
  7. Berli FJ, Alonso R, Bressan-Smith R, Bottini R (2013) UV-B impairs growth and gas exchange in grapevines grown in high altitude. Physiol Plant 149:127–140CrossRefPubMedGoogle Scholar
  8. Bilger W, Rolland M, Nybakken L (2007) UV screening in higher plants induced by low temperature in the absence of UV-B radiation. Photochem Photobiol Sci 6:190–195CrossRefPubMedGoogle Scholar
  9. Bornman JF, Barnes PW, Robinson SA, Ballare CL, Flint SD, Caldwell MM (2015) Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems. Photochem Photobiol Sci 14:88–107CrossRefPubMedGoogle Scholar
  10. Bray CM, West CE (2005) DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity. New Phytol 168:511–528CrossRefPubMedGoogle Scholar
  11. Britt AB (1996) DNA damage and repair in plants. Ann Rev Plant Biol 47:75–100CrossRefGoogle Scholar
  12. Britt AB (2004) Repair of DNA damage induced by solar UV. Photosynth Res 81:105–112CrossRefGoogle Scholar
  13. Britt AB, Chen JJ, Wykoff D, Mitchell D (1993) A UV-sensitive mutant of Arabidopsis defective in the repair of pyrimidine-pyrimidinone (6-4) dimers. Science 261:1571–1574CrossRefPubMedGoogle Scholar
  14. Casati P, Stapleton AE, Blum JE, Walbot V (2006) Genome-wide analysis of high-altitude maize and gene knockdown stocks implicates chromatin remodeling proteins in response to UV-B. Plant J 46:613–627CrossRefPubMedGoogle Scholar
  15. Chen JJ, Jiang CZ, Britt AB (1996) Little or no repair of cyclobutyl pyrimidine dimers is observed in the organellar genomes of the young Arabidopsis seedling. Plant Physiol 111:19–25PubMedPubMedCentralGoogle Scholar
  16. Day TA (1993) Relating UV-B radiation screening effectiveness of foliage to absorbing-compound concentration and anatomical characteristics in a diverse group of plants. Oecologia 95:542–550CrossRefGoogle Scholar
  17. Day TA, Vogelmann TC, DeLucia EH (1992) Are some plant life forms more effective than others in screening out ultraviolet-B radiation? Oecologia 92:513–519CrossRefGoogle Scholar
  18. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95:14863–14868CrossRefPubMedPubMedCentralGoogle Scholar
  19. Freeman SE, Blackett AD, Monteleone DC, Setlow RB, Sutherland BM, Sutherland JC (1986) Quantitation of radiation-, chemical-, or enzyme-induced single strand breaks in nonradioactive DNA by alkaline gel electrophoresis: application to pyrimidine dimers. Analytical biochemistry 158:119–129CrossRefPubMedGoogle Scholar
  20. Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y, Yamamoto KT (2004) A methyl viologenresistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134:275–285CrossRefPubMedPubMedCentralGoogle Scholar
  21. Giordano CV, Mori T, Sala OE, Scopel AL, Caldwell MM, Ballare CL (2003) Functional acclimation to solar UV-B radiation in Gunnera magellanica, a native plant species of southernmost Patagonia. Plant Cell and Environment 26:2027–2036CrossRefGoogle Scholar
  22. He J, Huang LK, Chow WS, Whitecross MI, Anderson JM (1993) Effects of supplementary ultraviolet-B radiation on rice and pea plants. Functional Plant Biology 20:129–142Google Scholar
  23. Heijde M, Ulm R (2012) UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci 17:230–237CrossRefPubMedGoogle Scholar
  24. Hideg E, Jansen MA, Strid A (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18:107–115CrossRefPubMedGoogle Scholar
  25. Hidema J, Kumagai T (1998) UVB-induced cyclobutyl pyrimidine dimer and photorepair with progress of growth and leaf age in rice. Journal of Photochemistry and Photobiology B: Biology 43:121–127CrossRefGoogle Scholar
  26. Hidema J, Kumagai T, Sutherland BM (2000) UV radiation-sensitive Norin 1 rice contains defective cyclobutane pyrimidine dimer photolyase. The Plant Cell 12:1569–1578CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hidema J, Kumagai T, Sutherland JC, Sutherland BM (1997) Ultraviolet B-sensitive rice cultivar deficient in cyclobutyl pyrimidine dimer repair. Plant Physiol 113:39–44PubMedPubMedCentralGoogle Scholar
  28. Hidema J, Taguchi T, Ono T, Teranishi M, Yamamoto K, Kumagai T (2007) Increase in CPD photolyase activity functions effectively to prevent growth inhibition caused by UVB radiation. The Plant Journal 50:70–79CrossRefPubMedGoogle Scholar
  29. Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411:366–374CrossRefPubMedGoogle Scholar
  30. Iyer RR, Pluciennik A, Burdett V, Modrich PL (2006) DNA mismatch repair: functions and mechanisms. Chemical reviews 106:302–323CrossRefPubMedGoogle Scholar
  31. Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annual review of plant biology 60:407–431CrossRefPubMedGoogle Scholar
  32. Johanson U, Gehrke C, Bjorn LO, Callaghan TV (1995) The effects of enhanced UV-B radiation on the growth of dwarf shrubs in a subarctic heathland. Functional Ecology :713-719Google Scholar
  33. Julkunen-Tiitto R, Haggman H, Aphalo PJ, Lavola A, Tegelberg R, Veteli T (2005) Growth and defense in deciduous trees and shrubs under UV-B. Environ Pollut 137:404–414CrossRefPubMedGoogle Scholar
  34. Kalbina I, Strid A (2006) Supplementary ultraviolet-B irradiation reveals differences in stress responses between Arabidopsis thaliana ecotypes. Plant Cell and Environment 29:754–763CrossRefGoogle Scholar
  35. Kamiyama C, Oikawa S, Hikosaka K (2014) Seasonal change in light partitioning among coexisting species of different functional groups along elevation gradient in subalpine moorlands. New Phytol 204:913–923CrossRefPubMedGoogle Scholar
  36. Kamiyama C, Oikawa S, Kubo T, Hikosaka K (2010) Light interception in species with different functional groups coexisting in moorland plant communities. Oecologia 164:591–599CrossRefPubMedGoogle Scholar
  37. Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2nd, ed edn. Springer, Berlin Heidelberg New YorkCrossRefGoogle Scholar
  38. Laakso K, Huttunen S (1998) Effects of the ultraviolet-B radiation (UV-B) on conifers: a review. Environmental Pollution 99:319–328CrossRefPubMedGoogle Scholar
  39. Lario LD, Ramirez-Parra E, Gutierrez C, Casati P, Spampinato CP (2011) Regulation of plant MSH2 and MSH6 genes in the UV-B-induced DNA damage response. Journal of Experimental Botany 62:2925–2937CrossRefPubMedGoogle Scholar
  40. Li FR, Peng SL, Chen BM, Hou YP (2010) A meta-analysis of the responses of woody and herbaceous plants to elevated ultraviolet-B radiation. Acta Oecologica 36:1–9CrossRefGoogle Scholar
  41. Liu Q, Yao XQ, Zhao CZ, Cheng XY (2011) Effects of enhanced UV-B radiation on growth and photosynthetic responses of four species of seedlings in subalpine forests of the Eastern Tibet Plateau. Environmental and Experimental Botany 74:151–156CrossRefGoogle Scholar
  42. Miazek K, Ledakowicz S (2013) Chlorophyll extraction from leaves, needles and microalgae: A kinetic approach. International Journal of Agricultural & Biological Engineering 6:107–115Google Scholar
  43. Muraoka H, Takakura S (1988) Explanatory text of the geological map of the Hakkoda Geother-mal area (in Japanese). Geol Surv Japan, TsukubaGoogle Scholar
  44. Musil CF (1995) Differential effects of elevated ultraviolet-B radiation on the photochemical and reproductive performances of dicotyledonous and monocotyledonous arid-environment ephemerals. Plant, Cell & Environment 18:844-854 %Google Scholar
  45. Neugart S, Zietz M, Schreiner M, Rohn S, Kroh LW, Krumbein A (2012) Structurally different flavonol glycosides and hydroxycinnamic acid derivatives respond differently to moderate UV-B radiation exposure. Physiol Plant 145:582–593CrossRefPubMedGoogle Scholar
  46. Pal M, Sharma A, Abrol YP, Sengupta UK (1997) Exclusion of UV-B radiation from normal solar spectrum on the growth of mung bean and maize. Agriculture, ecosystems & environment 61:29–34CrossRefGoogle Scholar
  47. Pal M, Zaidi PH, Voleti SR, Raj A (2006) Solar UV-B exclusion effects on growth and photosynthetic characteristics of wheat and pea. Journal of New Seeds 8:19–34CrossRefGoogle Scholar
  48. Phoenix GK, Gwynn-Jones D, Callaghan TV, Sleep D, Lee JA (2001) Effects of global change on a sub-Arctic heath: effects of enhanced UV-B radiation and increased summer precipitation. Journal of Ecology 89:256–267CrossRefGoogle Scholar
  49. Quaite FE, Takayanagi S, Ruffini J, Sutherland JC, Sutherland BM (1994) DNA damage levels determine cyclobutyl pyrimidine dimer repair mechanisms in alfalfa seedlings. The Plant Cell Online 6:1635–1641CrossRefGoogle Scholar
  50. Rau W, Hofmann H (1996) Sensitivity to UV-B of plants growing in different altitudes in the Alps. J Plant Physiol 148:21–25CrossRefGoogle Scholar
  51. Ries G, Heller W, Puchta H, Sandermann H, Seidlitz HK, Hohn B (2000) Elevated UV-B radiation reduces genome stability in plants. Nature 406:98–101CrossRefPubMedGoogle Scholar
  52. Rozema J et al (2006) Stratospheric ozone depletion: high arctic tundra plant growth on Svalbard is not affected by enhanced UV-B after 7 years of UV-B supplementation in the field. Plant Ecology 182:121–135CrossRefGoogle Scholar
  53. Ruhland CT, Dyslin MJ, Krenz JD (2013) Wyoming big sagebrush screens ultraviolet radiation more effectively at higher elevations. Journal of Arid Environments 96:19–22CrossRefGoogle Scholar
  54. Saito N, Werbin H (1969) Evidence for a DNA-photoreactivating enzyme in higher plants. Photochemistry and photobiology 9:389–393CrossRefPubMedGoogle Scholar
  55. Sasaki T, Katabuchi M, Kamiyama C, Shimazaki M, Nakashizuka T, Hikosaka K (2012) Diversity partitioning of moorland plant communities across hierarchical spatial scales. Biodiversity and Conservation 21:1577–1588CrossRefGoogle Scholar
  56. Sasaki T, Katabuchi M, Kamiyama C, Shimazaki M, Nakashizuka T, Hikosaka K (2013) Variations in species composition of moorland plant communities along environmental gradients within a subalpine zone in northern Japan. Wetlands 33:269–277CrossRefGoogle Scholar
  57. Schofield MJ, Hsieh P (2003) DNA mismatch repair: molecular mechanisms and biological function. Annual Reviews in Microbiology 57:579–608CrossRefGoogle Scholar
  58. Solovchenko AE, Merzlyak MN (2008) Screening of visible and UV radiation as a photoprotective mechanism in plants. Russian Journal of Plant Physiol 55:719–737CrossRefGoogle Scholar
  59. Stapleton AE, Thornber CS, Walbot V (1997) UV-B component of sunlight causes measurable damage in field-grown maize (Zea mays L): developmental and cellular heterogeneity of damage and repair. Plant Cell and Environment 20:279–290CrossRefGoogle Scholar
  60. Sullivan JH (2005) Possible impacts of changes in UV-B radiation on North American trees and forests. Environ Pollut 137:380–389CrossRefPubMedGoogle Scholar
  61. Sullivan JH, Howells BW, Ruhland CT, Day TA (1996) Changes in leaf expansion and epidermal screening effectiveness in Liquidambar styraciflua and Pinus taeda in response to UV-B radiation. Physiologia Plantarum 98:349–357CrossRefGoogle Scholar
  62. Sullivan JH et al (2010) Assessment of DNA damage as a tool to measure UV-B tolerance in soybean lines differing in foliar flavonoid composition. UV Radiation in Global Climate Change. Springer, Berlin Heidelberg New York, pp 437–457Google Scholar
  63. Sullivan JH, Teramura AH, Ziska LH (1992) Variation in UV-B sensitivity in plants from a 3,000-m elevational gradient in Hawaii. American Journal of Botany:737-743Google Scholar
  64. Tattini M et al (2006) Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. New Phytol 170:779–794CrossRefPubMedGoogle Scholar
  65. Taulavuori E et al (1998) Long-term exposure to enhanced ultraviolet-B radiation in the sub-arctic does not cause oxidative stress in Vaccinium myrtillus. New Phytol 140:691–697CrossRefGoogle Scholar
  66. Taylor RM, Nikaido O, Jordan BR, Rosamond J, Bray CM, Tobin AK (1996) Ultraviolet-B-induced DNA lesions and their removal in wheat (Triticum aestivum L.) leaves. Plant Cell and Environment 19:171–181CrossRefGoogle Scholar
  67. Tegelberg R, Julkunen-Tiitto R, Aphalo PJ (2001) The effects of long-term elevated UV-B on the growth and phenolics of field-grown silver birch (Betula pendula). Global Change Biology 7:839–848CrossRefGoogle Scholar
  68. Teranishi M, Fujino T, Hidema J, Hirouchi T, Yamamoto K, Kumagai T (2002) Relationship between the UV-sensitivity of rice and structural alteration of CPD photolyase. Plant and Cell Physiology 43:S160–S160Google Scholar
  69. Teranishi M, Iwamatsu Y, Hidema J, Kumagai T (2004) Ultraviolet-B sensitivities in Japanese lowland rice cultivars: cyclobutane pyrimidine dimer photolyase activity and gene mutation. Plant and Cell Physiology 45:1848–1856CrossRefPubMedGoogle Scholar
  70. Tsuyuzaki S, Haraguchi A, Kanda F (2004) Effects of scale-dependent factors on herbaceous vegetation patterns in a wetland, northern Japan. Ecological Research 19:349-355 %@ 1440-1703Google Scholar
  71. Turnbull JD, Robinson SA (2009) Accumulation of DNA damage in Antarctic mosses: correlations with ultraviolet-B radiation, temperature and turf water content vary among species. Global Change Biology 15:319–329CrossRefGoogle Scholar
  72. Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutation Research/Reviews in Mutation Research 681:134–149CrossRefGoogle Scholar
  73. Wang Q-W, Hidema J, Hikosaka K (2014) Is UV-induced DNA damage greater at higher elevation? American Journal of Botany 101:796–802CrossRefPubMedGoogle Scholar
  74. Wargent JJ, Jordan BR (2013) From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production. New Phytol 197:1058–1076CrossRefPubMedGoogle Scholar
  75. Williamson CE et al (2014) Solar ultraviolet radiation in a changing climate. Nature Climate Change 4:434–441CrossRefGoogle Scholar
  76. Wolf L, Rizzini L, Stracke R, Ulm R, Rensing SA (2010) The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant physiology 153:1123–1134CrossRefPubMedPubMedCentralGoogle Scholar
  77. Xu CP, Sullivan JH (2010) Reviewing the technical designs for experiments with ultraviolet-B radiation and impact on photosynthesis, DNA and secondary metabolism. Journal of Integrative Plant Biology 52:377–387CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Qing-Wei Wang
    • 1
  • Chiho Kamiyama
    • 2
  • Jun Hidema
    • 1
  • Kouki Hikosaka
    • 1
    • 3
  1. 1.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  2. 2.Institute for the Advanced Study of SustainabilityUnited Nations UniversityTokyoJapan
  3. 3.CRESTJapan Science and Technology Agency (JST)Chiyoda, TokyoJapan

Personalised recommendations