UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants

Plant Journal

Volumn 96, Issue 3, 2018, Pages 503-517

  Clayton, William A ^a,b   Albert, Nick W ^a   Thrimawithana, Amali H ^a   McGhie, Tony K ^a   Deroles, Simon C ^a   Schwinn, Kathy E ^a   Warren, Ben A ^a   McLachlan, Andrew R G ^a   Bowman, John L ^c   Jordan, Brian R ^b   Davies, Kevin M ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b LINCOLN UNIVERSITY   (New Zealand)

^c MONASH UNIVERSITY   (Australia)

Author keywords

CRISPR Cas9; evolution; flavonoid; HY5; liverwort; Marchantia polymorpha; UVB; UVR8

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; CHEMICAL ANALYSIS; PLANTS (BOTANY);

CRISPR/CAS9; EVOLUTION; FLAVONOID; LIVERWORT; MARCHANTIA POLYMORPHA; UVR8;

FLAVONOIDS;

BIOCHEMISTRY; BIOSYNTHESIS; CHEMICAL ANALYSIS; EVOLUTION; FLAVONOIDS; LAND; PLANTS; TOLERANCE;

FLAVONOID; PLANT PROTEIN;

ANGIOSPERM; BIOSYNTHESIS; GENE EXPRESSION PROFILING; GENETICS; MARCHANTIA; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

BIOSYNTHETIC PATHWAYS; FLAVONOIDS; GENE EXPRESSION PROFILING; MAGNOLIOPSIDA; MARCHANTIA; PLANT PROTEINS; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS;

EID: 85052437945     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.14044     Document Type: Article

References (58)

1. Agati, G. and Tattini, M. (2010) Multiple functional roles of flavonoids in photoprotection. New Phytol. 186, 786–793.
2. Agati, G., Azzarello, E., Pollastri, S. and Tattini, M. (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci. 196, 67–76.
3. Aigner, S., Remias, D., Karsten, U. and Holzinger, A. (2013) Unusual phenolic compounds contribute to the ecophysiological performance in the purple- colored green alga Zygogonium ericetorum (Zygnematophyceae, Streptophyta) from a high-alpine habitat. J. Phycol. 49, 648–660.
4. Albert, N.W., Thirmawithana, H., McGhie, T.K., Clayton, W., Deroles, S.C., Schwinn, K.E., Bowman, J.L., Jordan, B.R. and Davies, K.M. (2018) Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. New Phytol. 218, 554–566.
5. Allorent, G., Lefebvre-Legendre, L., Chappuis, R., Kuntz, M., Truong, T.B., Niyogi, K.K., Ulm, R. and Goldschmidt-Clermont, M. (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 113, 14 864–14 869.
6. Asakawa, Y., Ludwiczuk, A. and Nagashima, F. (2013) Chemical constituents of bryophytes; bio- and chemical diversity, biological activity, and chemosystematics. In Progress in the Chemistry of Organic Natural Products (Kinghorn, A.D., Falk, H. and Kobayashi, J., eds). Vienna: Springer, Vol. 95, pp. 1–796.
7. Barnes, P.W., Tobler, M.A., Keefover-Ring, K., Flint, S.D., Barkley, E., Ryel, R.J. and Lindroth, R.L. (2016) Rapid modulation of ultraviolet shielding in plants is influenced by solar ultraviolet radiation and linked to alterations in flavonoids. Plant, Cell Environ. 39, 222–230.
8. Binkert, M., Kozma-Bognár, L., Terecskei, K., De Veylder, L., Nagy, F. and Ulm, R. (2014) UV-B-Responsive association of the Arabidopsis bZIP transcription factor ELONGATED HYPOCOTYL5 with target genes, including its own promoter. Plant Cell 26, 4200–4213.
9. Björn, L., Widell, S. and Wang, T. (2002) Evolution of UV-B regulation and protection in plants. Adv. Space Res. 30, 1557–1562.
10. Bowman, J.L., Araki, T. and Kohchi, T. (2016a) Marchantia: past, present and future. Plant Cell Physiol. 57, 205–209.
11. Bowman, J.L., Araki, T., Arteaga-Vazquez, M.A. et al. (2016b) The naming of names: guidelines for gene nomenclature in marchantia. Plant Cell Physiol. 57, 257–261.
12. Bowman, J.L., Kohchi, T., Yamato, K.T. et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171, 287–304.
13. Brown, B.A. and Jenkins, G.I. (2008) UV-B signalling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiol. 146, 576–588.
14. Buer, C.S., Muday, G.K. and Djordjevic, M.A. (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol. 145, 478–490.
15. Cheng, X., Zhang, X., Han, X.J., Zhang, Y.Y., Gao, S., Liu, C.J. and Lou, H.X. (2017) Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclisation activity for synthesis of flavonoids. New Phytol. 217, 909–924.
16. Cheynier, V., Comte, G., Davies, K.M., Lattanzio, V. and Martens, S. (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol. Biochem. 72, 1–20.
17. Christie, J.M., Arvai, S., Baxter, K.J. et al. (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335, 1492–1496.
18. Clarke, L.J. and Robinson, S.A. (2008) Cell wall-bound ultraviolet-screening compounds explain the high ultraviolet tolerance of the Antarctic moss, Ceratodon purpureus. New Phytol. 179, 776–783.
19. Cockell, C.S. and Knowland, J. (1999) Ultraviolet radiation screening compounds. Biol. Rev. 74, 311–345.
20. Davies, K.M., Albert, N.W., Zhou, Y. and Schwinn, K.E. (2018) Functions of flavonoid and betalain pigments in abiotic stress tolerance in plants. Ann. Plant Rev. Online 1, 1–41.
21. Favory, J.J., Stec, A., Gruber, H. et al. (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 28, 591–601.
22. Fernández, M.B., Tossi, V., Lamattina, L. and Cassia, R. (2016) A comprehensive phylogeny reveals functional conservation of the UV-B photoreceptor UVR8 from green algae to higher plants. Front. Plant Sci. 7, 1698.
23. Fernández-Calvo, P., Chini, A., Fernández-Barbero, G. et al. (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23, 701–715.
24. Gruber, H., Heijde, M., Heller, W., Albert, A., Seidlitz, H.K. and Ulm, R. (2010) Negative feedback regulation of UV-B–induced photomorphogenesis and stress acclimation in Arabidopsis. Proc. Natl Acad. Sci. USA 107, 20 132–20 137.
25. Gururani, M.A., Venkatesh, J. and Tran, L.S.P. (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol. Plant 8, 1304–1320.
26. Harholt, J., Moestrup, Ø. and Ulvskov, P. (2015) Why plants were terrestrial from the beginning. Trends Plant Sci. 21, 96–101.
27. Heijde, M. and Ulm, R. (2012) UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci. 17, 230–237.
28. Hideg, E., Jansen, M.A. and Strid, A. (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci. 18, 107–115.
29. Holzinger, A. and Pichrtová, M. (2016) Abiotic stress tolerance of charophyte green algae: new challenges for omics techniques. Front. Plant Sci. 7, 678.
30. Huang, X., Ouyang, X., Yang, P., Lau, O.S., Chen, L., Wei, N. and Deng, X.W. (2013) Conversion from CUL4-based COP1-SPA E3 apparatus to UVR8-COP1-SPA complexes underlies a distinct biochemical function of COP1 under UV-B. Proc. Natl Acad. Sci. USA 110, 16 669–16 674.
31. Jenkins, G.I. (2017) Photomorphogenic responses to ultraviolet-B light. Plant, Cell Environ. 40, 2544–2557.
32. Jiang, W., Yin, Q., Wu, R., Zheng, G., Liu, J., Dixon, R.A. and Pang, Y. (2015) Role of a chalcone isomerase-like protein in flavonoid biosynthesis in Arabidopsis thaliana. J. Exp. Bot. 66, 7165–7179.
33. Karsten, U. and Holzinger, A. (2014) Green algae in alpine biological soil crust communities: acclimation strategies against ultraviolet radiation and dehydration. Biodivers. Conserv. 23, 1845–1858.
34. Kliebenstein, D.J., Lim, J.E., Landry, L.G. and Last, R.L. (2002) Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human Regulator of Chromatin Condensation 1. Plant Physiol. 130, 234–243.
35. Love, M.I., Huber, W. and Anders, S. (2014) Moderated estimation of fold change and dispersion of RNA-seq data with DESeq2. Genome Biol. 15, 550.
36. Markham, K.R. and Porter, I.J. (1974) Flavonoids of the liverwort Marchantia polymorpha. Phytochemistry 13, 1937–1942.
37. Morales, L.O., Brosché, M., Vainonen, J., Jenkins, G.I., Wargent, J.J., Sipari, N., Strid, Å., Lindfors, V., Tegelberg, R. and Aphalo, P.J. (2013) Multiple roles for UV RESISTANCE LOCUS8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar ultraviolet radiation. Plant Physiol. 161, 744–759.
38. Morita, Y., Takagi, K., Fukuchi-Mizutani, M. et al. (2014) A chalcone isomerase-like protein enhances flavonoid production and flower pigmentation. Plant J. 78, 294–304.
39. Newsham, K.K. and Robinson, S.A. (2009) Responses of plants in polar regions to UVB exposure: a meta-analysis. Glob. Change Biol. 15, 2574–2589.
40. Niemi, R., Martikainen, P.J., Silvola, J., Sonninen, E., Wulff, A. and Holopainen, T. (2002) Responses of two Sphagnum moss species and Eriophorum vaginatum to enhanced UV-B in a summer of low UV intensity. New Phytol. 156, 509–515.
41. Rizzini, L., Favory, J.J., Cloix, C. et al. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103–106.
42. Rozema, J., Björn, L.O., Bornman, J.F. 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. J. Photochem. Photobiol. B 66, 2–12.
43. Rozema, J., Blokker, P., Mayoral Fuertes, M.A. and Broekman, R. (2009) UV-B absorbing compounds in present-day and fossil pollen, spores, cuticles, seed coats and wood: evaluation of a proxy for solar UV radiation. Photochem. Photobiol. Sci. 8, 1233–1243.
44. Searles, P.S., Flint, S.D. and Caldwell, M.M. (2001) A meta-analysis of plant field studies simulating stratospheric ozone depletion. Oecologia 127, 1–10.
45. Snell, K.R.S., Kokubun, T., Griffiths, H., Convey, P., Hodgson, D.A. and Newsham, K.K. (2009) Quantifying the metabolic cost to an Antarctic liverwort of responding to an abrupt increase in UVB radiation exposure. Glob. Change Biol. 15, 2563–2573.
46. Soriano, G., Cloix, C., Heilmann, M., Nunez-Olivera, E., Martinez-Abaigar, J. and Jenkins, G.I. (2018) Evolutionary conservation of structure and function of the UVR8 photoreceptor from the liverwort Marchantia polymorpha and the moss Physcomitrella patens. New Phytol. 217, 151–162.
47. Stracke, R., Favory, J.J., Gruber, H., Bartelniewoehner, L., Bartels, S., Binkert, M., Funk, M., Weisshaar, B. and Ulm, R. (2010) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant, Cell Environ. 33, 88–103.
48. Sumanta, N., Haque, C.I., Nishika, J. and Suprakash, R. (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res. J. Chem. Sci. 4, 63–69.
49. Tilbrook, K., Dubois, M., Crocco, C.D., Yin, R., Chappuis, R., Allorent, G., Schmid-Siegert, E., Goldschmidt-Clermont, M. and Ulm, R. (2016) UV-B Perception and acclimation in Chlamydomonas reinhardtii. Plant Cell 28, 966–983.
50. Ulm, R., Baumann, A., Oravecz, A., Máté, Z., Adám, E., Oakeley, E.J., Schäfer, E. and Nagy, F. (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc. Natl Acad. Sci. USA 101, 1397–1402.
51. de Vries, J. and Archibald, J.M. (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytol. 217, 1428–1434.
52. de Vries, J., de Vries, S., Slamovits, C.H., Rose, L.E. and Archibald, J.M. (2017) How embryophytic is the biosynthesis of phenylpropanoids and their derivatives in streptophyte algae? Plant Cell Physiol. 58, 934–945.
53. Wargent, J.J. and Jordan, B.R. (2013) From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production. New Phytol. 197, 1058–1076.
54. Winkel-Shirley, B. (2002) Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5, 218–223.
55. Wolf, L., Rizzini, L., Stracke, R., Ulm, R. and Rensing, S.A. (2010) The molecular and physiological responses of Physcomitrella patens to Ultraviolet-B radiation. Plant Physiol. 153, 1123–1134.
56. Wu, D., Hu, Q., Yan, Z. et al. (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484, 214–219.
57. Yin, R. and Ulm, R. (2017) How plants cope with UV-B: from perception to response. Curr. Opin. Plant Biol. 37, 42–48.
58. Yin, R., Skvortsova, M.Y., Loubéry, S. and Ulm, R. (2016) COP1 is required for UV-B-induced nuclear accumulation of the UVR8 photoreceptor. Proc. Natl Acad. Sci. USA 113, 4415–4422.