PAG1, a cotton brassinosteroid catabolism gene, modulates fiber elongation

New Phytologist

Volumn 203, Issue 2, 2014, Pages 437-448

  Yang, Zuoren ^a   Zhang, Chaojun ^a   Yang, Xiaojie ^a   Liu, Kun ^a   Wu, Zhixia ^a   Zhang, Xueyan ^a   Zheng, Wu ^a   Xun, Qingqing ^b   Liu, Chuanliang ^a   Lu, Lili ^a   Yang, Zhaoen ^a   Qian, Yuyuan ^a   Xu, Zhenzhen ^a   Li, Changfeng ^a   Li, Jia ^b   Li, Fuguang ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b LANZHOU UNIVERSITY   (China)

Author keywords

Activation tagging; Brassinosteroid (BR); Cotton (Gossypium hirsutum); Fiber elongation; Transcriptome

Indexed keywords

CADMIUM; CATABOLISM; CELL ORGANELLE; COTTON; DEVELOPMENTAL BIOLOGY; ETHYLENE; FATTY ACID; GENE EXPRESSION; GENOME; MOLECULAR ANALYSIS;

BRASSINOLIDE; BRASSINOSTEROID; CYTOCHROME P450; ETHYLENE; ETHYLENE DERIVATIVE; HETEROCYCLIC STEROID; VEGETABLE PROTEIN;

ARABIDOPSIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GOSSYPIUM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; BRASSINOSTEROIDS; CYTOCHROME P-450 ENZYME SYSTEM; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GOSSYPIUM; MUTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; STEROIDS, HETEROCYCLIC;

EID: 84902481943     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12824     Document Type: Article

References (72)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11: R106.
2. Ayliffe MA, Pallotta M, Langridge P, Pryor AJ. 2007. A barley activation tagging system. Plant Molecular Biology 64: 329-347.
3. Bai MY, Fan M, Oh E, Wang ZY. 2012. A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24: 4917-4929.
4. Bajguz A. 2007. Metabolism of brassinosteroids in plants. Plant Physiology and Biochemistry 45: 95-107.
5. Bancos S, Nomura T, Sato T, Molnar G, Bishop GJ, Koncz C, Yokota T, Nagy F, Szekeres M. 2002. Regulation of transcript levels of the Arabidopsis cytochrome p450 genes involved in brassinosteroid biosynthesis. Plant Physiology 130: 504-513.
6. Beasley C, Ting IP. 1973. The effects of plant growth substances on in vitro fiber development from fertilized cotton ovules. American Journal of Botany 60: 130-139.
7. Busov V, Yordanov Y, Gou JQ, Meilan R, Ma C, Regan S, Strauss S. 2011. Activation tagging is an effective gene tagging system in Populus. Tree Genetics & Genomes 7: 91-101.
8. Busov VB, Meilan R, Pearce DW, Ma CP, Rood SB, Strauss SH. 2003. Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiology 132: 1283-1291.
9. Choe S. 2006. Brassinosteroid biosynthesis and inactivation. Physiologia Plantarum 126: 539-548.
10. Clouse SD. 2002. Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Molecular Cell 10: 973-982.
11. Clouse SD, Sasse JM. 1998. Brassinosteroids: essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology 49: 427-451.
12. Coll-Garcia D, Mazuch J, Altmann T, Mussig C. 2004. EXORDIUM regulates brassinosteroid-responsive genes. Febs Letters 563: 82-86.
13. Davidonis G. 1993. A comparison of cotton ovule and cotton cell suspension cultures: response to gibberellic acid and 2-chloroethylphosphonic acid. Journal of Plant Physiology 141: 505-507.
14. Deng FL, Tu LL, Tan JF, Li Y, Nie YC, Zhang XL. 2012. GbPDF1 is involved in cotton fiber initiation via the core cis-element HDZIP2ATATHB2. Plant Physiology 158: 890-904.
15. 2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437: 741-745.
16. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S. 2002. Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiology 130: 1319-1334.
17. Grove MD, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen JD, Steffens GL, Flippen-Anderson JL, Cook JC. 1979. Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281: 216-217.
18. Gudesblat GE, Russinova E. 2011. Plants grow on brassinosteroids. Current Opinion in Plant Biology 14: 530-537.
19. Guo Z, Fujioka S, Blancaflor EB, Miao S, Gou X, Li J. 2010. TCP1 modulates brassinosteroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell 22: 1161-1173.
20. Hao J, Tu LL, Hu HY, Tan JF, Deng FL, Tang WX, Nie YC, Zhang XL. 2012. GbTCP, a cotton TCP transcription factor, confers fibre elongation and root hair development by a complex regulating system. Journal of Experimental Botany 63: 6267-6281.
21. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY. 2005. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307: 1634-1638.
22. He XC, Qin YM, Xu Y, Hu CY, Zhu YX. 2008. Molecular cloning, expression profiling, and yeast complementation of 19 β-tubulin cDNAs from developing cotton ovules. Journal of Experimental Botany 59: 2687-2695.
23. Huang GQ, Gong SY, Xu WL, Li W, Li P, Zhang CJ, Li DD, Zheng Y, Li FG, Li XB. 2013. A fasciclin-like arabinogalactan protein, GhFLA1, is involved in fiber initiation and elongation of cotton. Plant Physiology 161: 1278-1290.
24. Huang GQ, Xu WL, Gong SY, Li B, Wang XL, Xu D, Li XB. 2008a. Characterization of 19 novel cotton FLA genes and their expression profiling in fiber development and in response to phytohormones and salt stress. Physiologia Plantarum 134: 348-359.
25. Huang QS, Wang HY, Gao P, Wang GY, Xia GX. 2008b. Cloning and characterization of a calcium dependent protein kinase gene associated with cotton fiber development. Plant Cell Reports 27: 1869-1875.
26. Husar S, Berthiller F, Fujioka S, Rozhon W, Khan M, Kalaivanan F, Elias L, Higgins GS, Li Y, Schuhmacher R et al. 2011. Overexpression of the UGT73C6 alters brassinosteroid glucoside formation in Arabidopsis thaliana. BMC Plant Biology 11: 51.
27. Ichikawa T, Nakazawa M, Kawashima M, Muto S, Gohda K, Suzuki K, Ishikawa A, Kobayashi H, Yoshizumi T, Tsumoto Y et al. 2003. Sequence database of 1172 T-DNA insertion sites in Arabidopsis activation-tagging lines that showed phenotypes in T1 generation. Plant Journal 36: 421-429.
28. Ikeda M, Fujiwara S, Mitsuda N, Ohme-Takagi M. 2012. A triantagonistic basic helix-loop-helix system regulates cell elongation in Arabidopsis. Plant Cell 24: 4483-4497.
29. Jeong DH, An S, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim SR et al. 2006. Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant Journal 45: 123-132.
30. Ji SJ, Lu YC, Feng JX, Wei G, Li J, Shi YH, Fu Q, Liu D, Luo JC, Zhu YX. 2003. Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic Acids Research 31: 2534-2543.
31. Kim HB, Kwon M, Ryu H, Fujioka S, Takatsuto S, Yoshida S, An CS, Lee I, Hwang I, Choe S. 2006. The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiology 140: 548-557.
32. Kim HJ, Triplett BA. 2001. Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiology 127: 1361-1366.
33. Lee J, Burns TH, Light G, Sun Y, Fokar M, Kasukabe Y, Fujisawa K, Maekawa Y, Allen RD. 2010. Xyloglucan endotransglycosylase/hydrolase genes in cotton and their role in fiber elongation. Planta 232: 1191-1205.
34. Li DD, Ruan XM, Zhang J, Wu YJ, Wang XL, Li XB. 2013. Cotton plasma membrane intrinsic protein 2s (PIP2s) selectively interact to regulate their water channel activities and are required for fibre development. New Phytologist 199: 695-707.
35. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222.
36. Li L, Wang XL, Huang GQ, Li XB. 2007. Molecular characterization of cotton GhTUA9 gene specifically expressed in fibre and involved in cell elongation. Journal of Experimental Botany 58: 3227-3238.
37. Li XB, Fan XP, Wang XL, Cai L, Yang WC. 2005. The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17: 859-875.
38. Lisso J, Steinhauser D, Altmann T, Kopka J, Mussig C. 2005. Identification of brassinosteroid-related genes by means of transcript co-response analyses. Nucleic Acids Research 33: 2685-2696.
39. Luo M, Xiao Y, Li X, Lu X, Deng W, Li D, Hou L, Hu M, Li Y, Pei Y. 2007. GhDET2, a steroid 5α-reductase, plays an important role in cotton fiber cell initiation and elongation. Plant Journal 51: 419-430.
40. Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightner J et al. 2003. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15: 1689-1703.
41. Mathur J, Molnar G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, Adam G, Voigt B, Nagy F, Maas C et al. 1998. Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant Journal 14: 593-602.
42. Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, Sugimoto K, Okabe K, Kajiwara H, Satoh K, Yamamoto K et al. 2002. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiology 130: 1152-1161.
43. Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S et al. 1999. BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proceedings of the National Academy of Sciences, USA 96: 15 316-15 323.
44. Ohnishi T, Nomura T, Watanabe B, Ohta D, Yokota T, Miyagawa H, Sakata K, Mizutani M. 2006. Tomato cytochrome P450 CYP734A7 functions in brassinosteroid catabolism. Phytochemistry 67: 1895-1906.
45. Poppenberger B, Fujioka S, Soeno K, George GL, Vaistij FE, Hiranuma S, Seto H, Takatsuto S, Adam G, Yoshida S et al. 2005. The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. Proceedings of the National Academy of Sciences, USA 102: 15 253-15 258.
46. Qin YM, Hu CY, Pang Y, Kastaniotis AJ, Hiltunen JK, Zhu YX. 2007a. Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell 19: 3692-3704.
47. Qin YM, Pujol FM, Hu CY, Feng JX, Kastaniotis AJ, Hiltunen JK, Zhu YX. 2007b. Genetic and biochemical studies in yeast reveal that the cotton fibre-specific GhCER6 gene functions in fatty acid elongation. Journal of Experimental Botany 58: 473-481.
48. Qin YM, Zhu YX. 2011. How cotton fibers elongate: a tale of linear cell-growth mode. Current Opinion in Plant Biology 14: 106-111.
49. Rouleau M, Marsolais F, Richard M, Nicolle L, Voigt B, Adam G, Varin L. 1999. Inactivation of brassinosteroid biological activity by a salicylate-inducible steroid sulfotransferase from Brassica napus. Journal of Biological Chemistry 274: 20 925-20 930.
50. Sakamoto T, Kawabe A, Tokida-Segawa A, Shimizu B, Takatsuto S, Shimada Y, Fujioka S, Mizutani M. 2011. Rice CYP734As function as multisubstrate and multifunctional enzymes in brassinosteroid catabolism. Plant Journal 67: 1-12.
51. Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX. 2006. Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18: 651-664.
52. Sun Y, Fan XY, Cao DM, Tang WQ, He K, Zhu JY, He JX, Bai MY, Zhu SW, Oh E et al. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19: 765-777.
53. Sun Y, Fokar M, Asami T, Yoshida S, Allen RD. 2004. Characterization of the Brassinosteroid insensitive 1 genes of cotton. Plant Molecular Biology 54: 221-232.
54. Sun Y, Veerabomma S, Abdel-Mageed HA, Fokar M, Asami T, Yoshida S, Allen RD. 2005. Brassinosteroid regulates fiber development on cultured cotton ovules. Plant and Cell Physiology 46: 1384-1391.
55. Symons GM, Reid JB. 2004. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiology 135: 2196-2206.
56. Symons GM, Ross JJ, Jager CE, Reid JB. 2008. Brassinosteroid transport. Journal of Experimental Botany 59: 17-24.
57. Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei GP, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171-182.
58. Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S. 2005. Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiology 138: 1117-1125.
59. Thornton LE, Peng H, Neff MM. 2011. Rice CYP734A cytochrome P450s inactivate brassinosteroids in Arabidopsis. Planta 234: 1151-1162.
60. Tiwari SC, Wilkins TA. 1995. Cotton (Gossypium hirsutum) seed trichomes expand via diffuse growing mechanism. Canadian Journal of Botany 73: 746-757.
61. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
62. Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Denzel MA, Torres QI, Neff MM. 2003. CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiology 133: 1643-1653.
63. Wan SY, Wu JX, Zhang ZG, Sun XH, Lv Y, Gao C, Ning YD, Ma J, Guo YP, Zhang Q et al. 2009. Activation tagging, an efficient tool for functional analysis of the rice genome. Plant Molecular Biology 69: 69-80.
64. Xu B, Gou J-Y, Li F-G, Shangguan X-X, Zhao B, Yang C-Q, Wang L-J, Yuan S, Liu C-J, Chen X-Y. 2013. A cotton BURP domain protein interacts with α-expansin and their co-expression promotes plant growth and fruit production. Molecular Plant 6: 945-958.
65. Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL. 2011. The mechanisms of brassinosteroids' action: from signal transduction to plant development. Molecular Plant 4: 588-600.
66. Yao D, Zhang X, Zhao X, Liu C, Wang C, Zhang Z, Zhang C, Wei Q, Wang Q, Yan H et al. 2011. Transcriptome analysis reveals salt-stress-regulated biological processes and key pathways in roots of cotton (Gossypium hirsutum L.). Genomics 98: 47-55.
67. Yi X, Du Z, Su Z. 2013. PlantGSEA: a gene set enrichment analysis toolkit for plant community. Nucleic Acids Research 41: W98-W103.
68. Yuan T, Fujioka S, Takatsuto S, Matsumoto S, Gou X, He K, Russell SD, Li J. 2007. BEN1, a gene encoding a dihydroflavonol 4-reductase (DFR)-like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. Plant Journal 51: 220-233.
69. Zhang C, Yu S, Fan S, Zhang J, Li F. 2011. Inheritance of somatic embryogenesis using leaf petioles as explants in upland cotton. Euphytica 181: 1-9.
70. Zhang XR, Henriques R, Lin SS, Niu QW, Chua NH. 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1: 641-646.
71. Zhao B, Li J. 2012. Regulation of brassinosteroid biosynthesis and inactivation. Journal of Integrative Plant Biology 54: 746-759.
72. 2+ elevation involvement in plant brassinosteroid signal transduction cascades. Plant Physiology 163: 555-565.