Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha

Journal of Plant Research

Volumn 131, Issue 5, 2018, Pages 849-864

  Kubo, Hiroyoshi ^a   Nozawa, Shunsuke ^a   Hiwatashi, Takuma ^b   Kondou, Youichi ^c   Nakabayashi, Ryo ^d   Mori, Tetsuya ^d   Saito, Kazuki ^d,e   Takanashi, Kojiro ^a   Kohchi, Takayuki ^f   Ishizaki, Kimitsune ^b  

^a SHINSHU UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

^c KANTO GAKUIN UNIVERSITY   (Japan)

^d Elements Chemistry Laboratory   (Japan)

^e CHIBA UNIVERSITY   (Japan)

^f KYOTO UNIVERSITY   (Japan)

Author keywords

Anthocyanin; Marchantia polymorpha; Marchantin; Phenolic metabolism; R2R3 MYB

Indexed keywords

ANTHOCYANIN; PHENOL; PLANT PROTEIN; TRANSCRIPTION FACTOR;

DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; LIQUID CHROMATOGRAPHY; MARCHANTIA; METABOLISM; RADIATION RESPONSE; TANDEM MASS SPECTROMETRY; ULTRAVIOLET RADIATION; UPREGULATION;

ANTHOCYANINS; CHROMATOGRAPHY, LIQUID; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; MARCHANTIA; PHENOL; PLANT PROTEINS; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTORS; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 85047662271     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10265-018-1044-7     Document Type: Article

References (81)

1. Afendi FM, Okada T, Yamazaki M, Hirai-Morita A, Nakamura Y, Nakamura K, Ikeda S, Takahashi H, Altaf-Ul-Amin M, Darusman LK, Saito K, Kanaya S (2012) KNApSAcK family databases: integrated metabolite-plant species databases for multifaceted plant research. Plant Cell Physiol 53:e1
2. A-H-Mackerness S (2000) Plant responses to ultraviolet-B (UV-B: 280–320 nm) stress: what are the key regulators? Plant Growth Regul 32:27–39
3. Albert N, Thrimawithana A, McGhie T, Clayton W, Deroles S, Schwinn K, Bowman J, Jordan B, Davies K (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. 10.1111/nph.15002
4. Aoyama T, Chua NH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11:605–612
5. Asakawa Y, Ludwiczuk A, Nagashima F (2012) Chemical constituents of marchantiophyta. Chemical constituents of bryophytes: Bio- and chemical diversity, biological activity, and chemosystematics. In: Kinghorn AD, Falk H, Kobayashi J (eds) Progress in the chemistry of organic natural products. Springer, Wien, pp 25–562
6. Asakawa Y, Ludwiczuk A, Nagashima F (2013) Phytochemical and biological studies of bryophytes. Phytochemistry 91:52–80
7. Aya K, Hiwatashi Y, Kojima M, Sakakibara H, Ueguchi-Tanaka M, Hasebe M, Matsuoka M (2011) The Gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution. Nat Commun 2:544
8. Bendz G, Mårtensson O, Terenius L (1962) Moss pigments I. The anthocyanins of Bryum cryophilum O. Mårt. Acta Chem Scand 16:1183–1190
9. Böttcher C, Krähmer A, Stürtz M, Widder S, Schulz H (2017) Comprehensive metabolite profiling of onion bulbs (Allium cepa) using liquid chromatography coupled with electrospray ionization quadrupole time-of-flight mass spectrometry. Metabolomics 13:35
10. Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304
11. Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5:e1000430
12. Burda S, Oleszek W (2001) Antioxidant and antiradical activities of flavonoids. J Agric Food Chem 49:2774–2779
13. Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, Tonelli C (2008) Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana. J Plant Physiol 165:886–894
14. Couée I, Sulmon C, Gouesbet G, Amrani AEI (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
15. Davin LB, Wang HB, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275:362–366
16. De Vos M, Denekamp M, Dicke M, Vuylsteke M, Van Loon LC, Smeekens SCM, Pieterse CMJ (2006) The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal Behav 1:305–311
17. Douglas CJ (1996) Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends Plant Sci 1:171–178
18. Du H, Liang Z, Zhao S, Nan MG, Tran LSP, Lu K, Huang YB, Li JN (2015) The evolutionary history of R2R3-MYB proteins across 50 eukaryotes: new insights into subfamily classification and expansion. Sci Rep 5:11037
19. Dubos C, Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Routabou JM, Alboresi A, Weisshaar B, Lepiniec L (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J 55:940–953
20. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581
21. Dunwell JM, Purvis A, Khuri S (2004) Cupins: the most functionally diverse protein superfamily? Phytochemistry 65:7–17
22. Friederich S, Rueffer M, Asakawa Y, Zenk MH (1999) Cytochromes P-450 catalyze the formation of marchantins A and C in Marchantia polymorpha. Phytochemistry 52:1195–1202
23. Gao C, Xing D, Li L, Zhang L (2008) Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227:755–767
24. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53:814–827
25. Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 7:1879–1891
26. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
27. Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Müller I, Voß U, Jürgens G, Ito M (2007) R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 134:1101–1110
28. Hatier J-HB, Gould KS (2009) Anthocyanin function in vegetative organs. In: Gould K, Davies K, Winefield C (eds) Anthocyanin: biosynthesis, functions, and applications. Springer Science + Business Media, LLC, New York, pp 1–19
29. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282
30. Hsiao G, Teng CM, Wu CL, Ko FN (1996) Marchantin H as a natural antioxidant and free radical scavenger. Arch Biochem Biophys 334:18–26
31. Ishizaki K (2017) Evolution of land plants: insights from molecular studies on basal lineages. Biosci Biotechnol Biochem 81:73–80
32. Ishizaki K, Chiyoda S, Yamato KT, Kohchi T (2008) Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L. an emerging model for plant biology. Plant Cell Physiol 49:1084–1091
33. Ishizaki K, Kohchi T, Yamato KT (2016) Molecular genetic tools and techniques for Marchantia polymorpha research. Plant Cell Physiol 57:262–270
34. Ito M (2005) Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res 118:61–69
35. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161
36. Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045
37. Kageyama A, Ishizaki K, Kohchi T, Matsuura H, Takahashi K (2015) Abscisic acid induces biosynthesis of bisbibenzyls and tolerance to UV-C in the liverwort Marchantia polymorpha. Phytochemistry 117:547–553
38. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:36
39. Kobayashi K, Suzuki T, Iwata E, Magyar Z, Bögre L, Ito M (2015) MYB3Rs, plant homologs of Myb oncoproteins, control cell cycle-regulated transcription and form DREAM-like complexes. Transcription 6:106–111
40. Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263–276
41. Kunz S, Burkhardt G, Becker H (1994) Riccionidins a and b, anthocyanidins from the cell walls of the liverwort Ricciocarpos natans. Phytochemistry 35:233–235
42. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948
43. Lea U, Slimestad R, Smedvig P, Lillo C (2007) Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway. Planta 225:1245–1253
44. Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99:473–483
45. Lippold F, Sanchez DH, Musialak M, Schlereth A, Scheible WR, Hincha DK, Udvardi MK (2009) AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. Plant Physiol 149:1761–1772
46. Liu JJ, Sturrock R, Ekramoddoullah AKM (2010) The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep 29:419–436
47. Lloyd AM, Schena M, Walbot V, Davis RW (1994) Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid-inducible regulator. Science 266:436–439
48. Lotkowska ME, Tohge T, Fernie AR, Xue GP, Balazadeh S, Mueller-Roeber B (2015) The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiol 169:1862–1880
49. Magallón S, Hilu KW, Quandt D (2013) Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. Am J Bot 100:556–573
50. Markham KR, Porter IJ (1974) Flavonoids of the liverwort Marchantia polymorpha. Phytochemistry 13:1937–1942
51. McClure JW (1975) Physiology and functions of flavonoids. In: Harborne JB, Mabry TJ, Mabry H (eds) The flavonoids. Academic Press, San Francisco, pp 990–1055
52. Mu L, Cao YR, Liu YF, Lei G, Zou HF, Liao Y, Wang HW, Zhang WK, Ma B, Du JZ, Yuan M, Zhang JS, Chen SY (2009) An R2R3-type transcription factor gene AtMYB59 regulates root growth and cell cycle progression in Arabidopsis. Cell Res 19:1291–1304
53. Müller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18:586–597
54. Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 13:2099–2114
55. Newman LJ, Perazza DE, Juda L, Campbell MM (2004) Involvement of the R2R3-MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. Plant J 37:239–250
56. Oh JE, Kim YH, Kim JH, Kwon YR, Lee H (2011) Enhanced level of anthocyanin leads to increased salt tolerance in Arabidopsis PAP1-D plants upon sucrose treatment. J Korean Soc Appl Biol Chem 54:79–88
57. Ohta Y, Abe S, Komura H, Kobayashi M (1983) Prelunularic acid, a probable immediate precursor of lunularic acid. First example of a “prearomatic” intermediate in the phenylpropanoid-poly malonate pathway. J Am Chem Soc 105:4480–4481
58. Perrière G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369
59. Quattrocchio F, Baudry A, Lepiniec L, Grothwold E (2006) The regulation of flavonoid biosynthesis. In: Grotewold E (ed) The science of flavonoids. Springer, New York, pp 97–122
60. Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
61. Rosinski JA, Atchley WR (1998) Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. J Mol Evol 46:74–83
62. Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248
63. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jurgens G, Hülskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046
64. Schena M, Lloyd AM, Davis RW (1991) A steroid-inducible gene expression system for plant cells. Proc Natl Acad Sci USA 88:10421–10425
65. Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357
66. Stracke R, Werber M, Weisshaar B (2001) The R2R3-Myb gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456
67. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677
68. Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T (2014) CRISPR/Cas9-mediated target mutagenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol 55:475–481
69. Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139:1840–1852
70. Tohge T, Nishiyama Y, Yokota-Hirai M, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42:218–235
71. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-sEq. Nat Biotechnol 31:46–53
72. Uchida K, Akashi T, Aoki T (2017) The missing link in leguminous pterocarpan biosynthesis is a dirigent domain-containing protein with isoflavanol dehydratase activity. Plant Cell Physiol 58:398–408
73. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116
74. Weston K, Bishop JM (1989) Transcriptional activation by the v-myb oncogene and its cellular progenitor, c-myb. Cell 58:85–93
75. Williams CE, Grotewold E (1997) Differences between plant and animal Myb domains are fundamental for DNA binding activity, and chimeric Myb domains have novel DNA binding specificities. J Biol Chem 272:563–571
76. Xiao A, Cheng Z, Kong L, Zhu Z, Lin S, Gao G, Zhang B (2014) CasOT: a genome-wide Cas9/gRNA off-target searching tool. Bioinformatics 30:1180–1182
77. Xing J, Xie C, Qu J, Guo H, Lv B, Lou H (2007) Rapid screening for bisbibenzyls in bryophyte crude extracts using liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 21:2467–2476
78. Yamaguchi T, Takamura H, Matoba T, Terao J (1998) HPLC method for evaluation of the free radical-scavenging activity of foods by using 1,1-diphenyl-2-picrylhydrazyl. Biosci Biotechnol Biochem 62:1201–1204
79. Zhang Y, Zhang X, Liu B, Wang W, Liu X, Chen C, Liu X, Yang S, Ren H (2014) A GAMYB homologue CsGAMYB1 regulates sex expression of cucumber via an ethylene-independent pathway. J Exp Bot 65:3201–3213
80. Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266
81. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71