A bHLH transcription factor regulates bisbibenzyl biosynthesis in the liverwort plagiochasma appendiculatum

Plant and Cell Physiology

Volumn 59, Issue 6, 2018, Pages 1187-1199

  Wu, Yi Feng ^a   Zhao, Yu ^a   Liu, Xin Yan ^a   Gao, Shuai ^a   Cheng, Ai Xia ^a   Lou, Hong Xiang ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Activator; bHLH transcription factor; Bisbibenzyl; Plagiochasma appendiculatum; Subgroup IIIf

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BIBENZYL DERIVATIVE; FUSION PROTEIN; PLANT PROTEIN;

AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIVERWORT; METABOLISM; PHYLOGENY; REPORTER GENE; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIBENZYLS; BIOSYNTHETIC PATHWAYS; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HEPATOPHYTA; PHYLOGENY; PLANT PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTIONAL ACTIVATION;

EID: 85048034539     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcy053     Document Type: Article

References (54)

1. Asakawa, Y. (1990) Terpenoids and aromatic compounds with pharmacological activity from bryophytes. In Bryophytes: Their Chemistry and Chemical Taxonomy. Edited by Zinsmeister, H.D. and Mues, R. pp. 369-410. Oxford University Press, Oxford.
2. Asakawa, Y. (1994) Highlights in phytochemistry of hepaticae-biologically active terpenoids and aromatic compounds. Pure Appl. Chem. 66: 2193-2196.
3. Asakawa, Y. (1995) Chemical constituents of the bryophytes. In Progress in the Chemistry of Organic Natural Products. Edited by Herz, W., Grisebach, H. and Kirby, G.W. pp. 1-285. Springer, Vienna.
4. Asakawa, Y. (2007) Biologically active compounds from bryophytes. Pure Appl. Chem. 79: 557-580.
5. Asakawa, Y. and Ludwiczuk, A. (2012) Distribution of cyclic and acyclic bisbibenzyls in the marchantiophyta (liverworts), ferns and higher plants and their biological activities, biosynthesis, and total synthesis (Dedicated to Professor Dr. Ei-ichi Negishi on the occasion of his 77th birthday). Heterocycles 86: 891-917.
6. Asakawa, Y., Toyota, M., Tori, M. and Hashimoto, T. (2000) Chemical structures of macrocyclic bisbibenzyls isolated from liverworts (Hepaticae). J. Spectrosc. 14: 149-175.
7. Cheng, A., Sun, L., Wu, X. and Lou, H. (2009) The inhibitory effect of a macrocyclic bisbibenzyl riccardin D on the biofilms of Candida albicans. Biol. Pharm. Bull. 32: 1417-1421.
8. Cheng, A., Wang, L., Sun, Y. and Lou, H. (2013) Identification and expression analysis of key enzymes of the terpenoids biosynthesis pathway of a liverwort Plagiochasma appendiculatum by EST analysis. Acta Physiol. Plant. 35: 107-118.
9. Danzer, J., Mellott, E., Bui, A.Q., Le, B.H., Martin, P., Hashimoto, M., et al. (2015) Down-regulating the expression of 53 soybean transcription factor genes uncovers a role for SPEECHLESS in initiating stomatal cell lineages during embryo development. Plant Physiol. 168: 1025-1035.
10. Eckermann, C., Schröder, G., Eckermann, S., Strack, D., Schmidt, J., Schneider, B., et al. (2003) Stilbenecarboxylate biosynthesis: A new function in the family of chalcone synthase-related proteins. Phytochemistry 62: 271-286.
11. Feng, H.L., Ma, N.N., Meng, X., Zhang, S., Wang, J.R., Chai, S., et al. (2013) A novel tomato MYC-type ICE1-like transcription factor, SlICE1a, confers cold, osmotic and salt tolerance in transgenic tobacco. Plant Physiol. Biochem. 73: 309-320.
12. Friederich, S., Maier, U.H., Deus-Neumann, B., Asakawa, Y. and Zenk, M.H. (1999a) Biosynthesis of cyclic bisbibenzyls in Marchantia polymorpha. Phytochemistry 50: 589-598.
13. Friederich, S., Rueffer, M., Asakawa, Y. and Zenk, M.H. (1999b) Cytochromes P-450 catalyze the formation of marchantins A and C in Marchantia polymorpha. Phytochemistry 52: 1195-1202.
14. Gao, S., Yu, H.N., Xu, R.X., Cheng, A.X. and Lou, H.X. (2015) Cloning and functional characterization of a 4-coumarate CoA ligase from liverwort Plagiochasma appendiculatum. Phytochemistry 111: 48-58.
15. Gong, Z.Z., Yamagishi, E., Yamazaki, M. and Saito, K. (1999) A constitutively expressed Myc-like gene involved in anthocyanin biosynthesis from Perilla frutescens: Molecular characterization, heterologous expression in transgenic plants and transactivation in yeast cells. Plant Mol. Biol. 41: 33-44.
16. Groszmann, M., Paicu, T. and Smyth, D.R. (2008) Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis. Plant J. 55: 40-52.
17. He, Y., Li, W., Lv, J., Jia, Y., Wang, M. and Xia, G. (2011) Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. J. Exp. Bot. 63: 1511-1522.
18. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B. and Bailey, P.C. (2003) The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20: 735-747.
19. Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S. and Lauvergeat, V. (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 62: 2465-2483.
20. Hichri, I., Heppel, S.C., Pillet, J., Léon, C., Czemmel, S., Delrot, S., et al. (2010) The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Mol. Plant 3: 509-523.
21. Huang, X.S., Wang, W., Zhang, Q. and Liu, J.H. (2013) A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol. 162: 1178-1194.
22. Ishizaki, K., Chiyoda, S., Yamato, K.T. and Kohchi, T. (2008) Agrobacteriummediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant Cell Physiol. 49: 1084-1091.
23. Jones, S. (2004) An overview of the basic helix-loop-helix proteins. Genome Biol. 5: 226.
24. Kaiser, B.N., Finnegan, P.M., Tyerman, S.D., Whitehead, L.F., Bergersen, F.J., Day, D.A., et al. (1998) Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science 281: 1202-1206.
25. Kennck, P. and Crane, P. (1997) The Origin and Early Diversification of Land Plants. Smithsonian Institution, Washington, DC.
26. Keserü, G. and Nogradi, M. (1995) The chemistry of macrocyclic bisbibenzyls. Nat. Prod. Rep. 12: 69-75.
27. Koes, R., Verweij, W. and Quattrocchio, F. (2005) Flavonoids: A colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10: 236-242.
28. Littlewood, T.D. and Evan, G.I. (1995) Transcription factors 2: Helix-loop-helix. Protein Profile 2: 621.
29. Liu, Y., Li, X., Li, K., Liu, H. and Lin, C. (2013) Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis. PLoS Genet. 9: E1003861.
30. Lou, H.X., Li, G.Y. and Wang, F.Q. (2002) A cytotoxic diterpenoid and antifungal phenolic compounds from Frullania muscicola Steph. J. Asian Nat. Prod. Res. 4: 87-94.
31. Matus, J., Poupin, M., Cañón, P., Bordeu, E., Alcalde, J. and Arce-Johnson, P. (2010) Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.). Plant Mol. Biol. 72: 607-620.
32. Muir, S.R., Collins, G.J., Robinson, S., Hughes, S., Bovy, A., De Vos, C.R., et al. (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat. Biotechnol. 19: 470-474.
33. Mullen, M.A., Wang, H., Wilcox, K. and Herman, T. (1994) Characterization of a Max:DNA complex by cross-linking to photoactive oligonucleotides. DNA Cell Biol. 13: 521-530.
34. Nesi, N., Debeaujon, I., Jond, C., Pelletier, G., Caboche, M. and Lepiniec, L. (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12: 1863-1878.
35. Ohno, S., Hosokawa, M., Hoshino, A., Kitamura, Y., Morita, Y., Park, K., et al. (2011) A bHLH transcription factor, DvIVS, is involved in regulation of anthocyanin synthesis in dahlia (Dahlia variabilis). J. Exp. Bot. 62: 5105-5116.
36. Park, K.I., Choi, J.D., Hoshino, A., Morita, Y. and Iida, S. (2004) An intragenic tandem duplication in a transcriptional regulatory gene for anthocyanin biosynthesis confers pale-colored flowers and seeds with fine spots in Ipomoea tricolor. Plant J. 38: 840-849.
37. Park, K.I., Ishikawa, N., Morita, Y., Choi, J.D., Hoshino, A. and Iida, S. (2007) A bHLH regulatory gene in the common morning glory, Ipomoea purpurea, controls anthocyanin biosynthesis in flowers, proanthocyanidin and phytomelanin pigmentation in seeds, and seed trichome formation. Plant J. 49: 641-654.
38. Pires, N. and Dolan, L. (2010) Early evolution of bHLH proteins in plants. Plant Signal. Behav. 5: 911-912.
39. Porebski, S., Bailey, L.G. and Baum, B.R. (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol. Biol. Rep. 15: 8-15.
40. Quattrocchio, F., Wing, J.F., Leppen, H.T., Mol, J.N. and Koes, R.E. (1993) Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5: 1497-1512.
41. Seo, P.J., Hong, S.Y., Kim, S.G. and Park, C.-M. (2011) Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci. 16: 541-549.
42. Shimizu, T., Miyamoto, K., Minami, E., Nishizawa, Y., Iino, M., Nojiri, H., et al. (2013) OsJAR1 contributes mainly to biosynthesis of the stressinduced jasmonoyl-isoleucine involved in defense responses in rice. Biosci. Biotechnol. Biochem. 77: 1556-1564.
43. Singh, M., Govindarajan, R., Nath, V., Rawat, A.K.S. and Mehrotra, S. (2006) Antimicrobial, wound healing and antioxidant activity of Plagiochasma appendiculatum Lehm. et Lind. J. Ethnopharmacol. 107: 67-72.
44. Spelt, C., Quattrocchio, F., Mol, J.N. and Koes, R. (2000) anthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12: 1619-1631.
45. Taira, Z., Takei, M., Endo, K., Hashimoto, T., Sakiya, Y. and Asakawa, Y. (1994) Marchantin A trimethyl ether: Its molecular structure and tubocurarinelike skeletal muscle relaxation activity. Chem. Pharm. Bull. 42: 52-56.
46. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
47. Toledo-Ortiz, G., Huq, E. and Quail, P.H. (2003) The Arabidopsis basic/ helix-loop-helix transcription factor family. Plant Cell 15: 1749-1770.
48. Wang, F., Zhu, H., Chen, D., Li, Z., Peng, R. and Yao, Q. (2016) A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell Tissue Organ Cult. 125: 387-398.
49. Wu, X.Z., Chang, W.Q., Cheng, A.X., Sun, L.M. and Lou, H.X. (2010) Plagiochin E, an antifungal active macrocyclic bisbibenzyl, induced apoptosis in Candida albicans through a metacaspase-dependent apoptotic pathway. Biochim. Biophys. Acta 1800: 439-447.
50. Xie, C.F., Qu, J.B., Wu, X.Z., Liu, N., Ji, M. and Lou, H.X. (2010) Antifungal macrocyclic bisbibenzyls from the Chinese liverwort Ptagiochasm intermedlum L. Nat. Prod. Res. 24: 515-520.
51. Yamaguchi-Shinozaki, K. and Shinozaki, K. (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57: 781-803.
52. Yu, H.N., Liu, X.Y., Gao, S., Han, X.J., Cheng, A.X. and Lou, H.X. (2014) Molecular cloning and functional characterization of a phenylalanine ammonia-lyase from liverwort Plagiochasma appendiculatum. Plant Cell Tissue Organ Cult. 117: 265-277.
53. Yu, H.N., Wang, L., Sun, B., Gao, S., Cheng, A.X. and Lou, H.X. (2015) Functional characterization of a chalcone synthase from the liverwort Plagiochasma appendiculatum. Plant Cell Rep. 34: 233-245.
54. Zhu, Z., Shi, J., Cao, J., He, M. and Wang, Y. (2012) VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata. Plant Cell Rep. 31: 2109-2120.