Overexpression of Arabidopsis MYB96 confers drought resistance in Camelina sativa via cuticular wax accumulation

Plant Cell Reports

Volumn 33, Issue 9, 2014, Pages 1535-1546

  Lee, Saet Buyl ^a   Kim, Hyojin ^a   Kim, Ryeo Jin ^a   Suh, Mi Chung ^a  

^a Chonnam National University   (South Korea)

Author keywords

Camelina sativa; Cuticular wax; Drought resistance; MYB96; Transcription factor; Transformation

Indexed keywords

ARABIDOPSIS; CAMELINA; CAMELINA SATIVA; EMBRYOPHYTA;

ARABIDOPSIS PROTEIN; CHLOROPHYLL; MYB96 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; WATER; WAX;

AMINO ACID SEQUENCE; ARABIDOPSIS; BRASSICACEAE; DROUGHT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT EPIDERMIS; PLANT LEAF; PLANT STOMA; PROMOTER REGION; TRANSGENIC PLANT; UPREGULATION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BRASSICACEAE; CHLOROPHYLL; DROUGHTS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; PLANT EPIDERMIS; PLANT LEAVES; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; UP-REGULATION; WATER; WAXES;

EID: 84906222231     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-014-1636-1     Document Type: Article

References (72)

1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15: 63-78.
2. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480.
3. Ashraf M (2010) Inducing drought tolerance in plants: recent advances. Biotechnol Adv 28: 169-183.
4. Bengtson C, Larsson S, Liljenberg C (1978) Effects of water stress on cuticular transpiration rate and amount and composition of epicuticular wax in seedlings of six oat varieties. Physiol Plant 44: 319-324.
5. Bernard A, Joubès J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Prog Lipid Res 52: 110-129.
6. Bernard A, Domergue F, Pascal S, Jetter R, Renne C, Faure JD, Haslam RP, Napier JA, Lessire R, Joubès J (2012) Reconstitution of plant alkane biosynthesis in yeast demonstrates that Arabidopsis ECERIFERUM1 and ECERIFERUM3 are core components of a very-longchain-alkane synthesis complex. Plant Cell 24: 3106-3118.
7. Bondada BR, Oosterhuis DM, Murphy JB, Kim KS (1996) Effect of water stress on the epicuticular wax composition and ultrastructure of cotton (Gossypium hirsutum L.) leaf, bract, and boll. Environ Exp Bot 36: 61-67.
8. Bourdenx B, Bernard A, Domergue F, Pascal S, Léger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Joubès J (2011) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol 156: 29-45.
9. Broun P, Poindexter P, Osborne E, Jiang C-Z, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101: 4706-4711.
10. Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140: 176-183.
11. Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15: 1170-1185.
12. Chen X, Truksa M, Snyder CL, El-Mezawy A, Shah S, Weselake RJ (2011) Three homologous genes encoding sn-glycerol-3-phosphate acyltransferase 4 exhibit different expression patterns and functional divergence in Brassica napus. Plant Physiol 155: 851-865.
13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
14. Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 53: 53-64.
15. De Ronde JA, Cress WA, Kruger GHJ, Strasser RJ, van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene during heat and drought stress. J Plant Physiol 161: 1211-1224.
16. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573-581.
17. Dyer J, Stymne S, Green A, Carlsson A (2008) High value oils from plants. Plant J 54: 640-654.
18. Enjalbert J-N, Zheng S, Johnson JJ, Mullen JL, Byrne PF, McKay JK (2013) Brassicaceae germplasm diversity for agronomic and seed quality traits under drought stress. Ind Crops Prod 47: 176-185.
19. Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, Hetherington AM (2000) The HIC signaling pathway links CO2 perception to stomatal development. Nature 408: 713-716.
20. Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L, Jetter R (2007) The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol 145: 653-667.
21. Hansen JD, Pyee J, Xia Y, Wen TJ, Robertson DS, Kolattukudy PE, Nikolau BJ, Schnable PS (1997) The glossy1 locus of maize and an epidermis-specific cDNA from Kleinia odora define a class of receptor-like proteins required for the normal accumulation of cuticular waxes. Plant Physiol 113: 1091-1100.
22. Haslam TM, Kunst L (2013) Extending the story of very-long-chain fatty acid elongation. Plant Sci 210: 93-107.
23. Hutcheon C, Ditt RF, Beilstein M, Comai L, Schroeder J, Goldstein E, Shewmaker CK, Nguyen T, De Rocher J, Kiser J (2010) Polyploid genome of Camelina sativa revealed by isolation of fatty acid synthesis genes. BMC Plant Biol 10: 233-247.
24. Islam MA, Du H, Ning J, Ye H, Xiong L (2009) Characterization of Glossy1-homologous genes in rice involved in leaf wax accumulation and drought resistance. Plant Mol Biol 70: 443-456.
25. Jefferson PG, Johnson DA, Rumbaugh MD, Asay KH (1989) Water stress and genotypic effects on epicuticular wax production of alfalfa and crested wheatgrass in relation to yield and excised leaf water loss rate. Can J Plant Sci 69: 481-490.
26. Jeong JS, Kim YS, Redillas MC, Jang G, Jung H, Bang SW, Choi YD, Ha SH, Reuzeau C, Kim JK (2013) OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol J 11: 101-114.
27. Jetter R, Kunst L (2008) Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J 54: 670-683.
28. Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18: 3015-3032.
29. Kagale S, Koh C, Nixon J, Bollina V, Clarke WE, Tuteja R, Spillane C, Robinson SJ, Links MG, Clarke C, Higgins EE, Huebert T, Sharpe AG, Parkin IAP (2014) The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat Commun 5: 3706. doi: 10. 1038/ncomms4706.
30. Kang J, Snapp AR, Lu C (2011) Identification of three genes encoding microsomal oleate desaturases (FAD2) from the oilseed crop Camelina sativa. Plant Physiol Biochem 49: 223-229.
31. Kim KS, Park SH, Jenks MA (2007) Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. J Plant Physiol 164: 1134-1143.
32. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lü S, Joubès J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151: 1918-1929.
33. Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12: 721-727.
34. Lee SB, Suh MC (2013) Recent advances in cuticular wax biosynthesis and its regulation in Arabidopsis. Mol Plant 6: 246-249.
35. Leide J, Hildebrandt U, Reussing K, Riederer M, Vogg G (2007) The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a β-ketoacyl-coenzyme A synthase (LeCER6). Plant Physiol 144: 1667-1679.
36. Li Y, Beisson F, Koo AJ, Molina I, Pollard M, Ohlrogge J (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104: 18339-18344.
37. Li F, Wu X, Lam P, Bird D, Zheng H, Samuels L, Jetter R, Kunst L (2008) Identification of the wax ester synthase/acyl-coenzyme A: diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol 148: 97-107.
38. Li Y, Zhang J, Zhang J, Hao L, Hua J, Duan L, Zhang M, Li Z (2013) Expression of an Arabidopsis molybdenum cofactor sulphurase gene in soybean enhances drought tolerance and increases yield under field conditions. Plant Biotechnol J 11: 747-758.
39. Li-Beisson Y, Shorrosh B, Beisson F, Andersson M, Arondel V, Bates P, Baud S, Bird D, DeBono A, Durrett T, Franke R, Graham I, Katayama K, Kelly A, Larson T, Markham J, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid K, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2013) Acyl-lipid metabolism. Arabidopsis Book 11: e0161. doi: 10. 1199/tab. 0161.
40. Liu X, Brost J, Hutcheon C, Guilfoil R, Wilson AK, Leung S, Shewmaker CK, Rooke S, Nguyen T, Kiser J, De Rocher J (2012) Transformation of the oilseed crop Camelina sativa by Agrobacterium-mediated floral dip and simple large-scale screening of transformants. In Vitro Cell Dev Biol Plant 48: 462-468.
41. Lolle SJ, Hsu W, Pruitt RE (1998) Genetic analysis of organ fusion in Arabidopsis thaliana. Genetics 149: 607-619.
42. Lu C, Kang J (2008) Generation of transgenic plants of a potential oilseed crop Camelina sativa by Agrobacterium-mediated transformation. Plant Cell Rep 27: 273-278.
43. Mao B, Cheng Z, Lei C, Xu F, Gao S, Ren Y, Wang J, Zhang X, Wang J, Wu F, Guo X, Liu X, Wu C, Wang H, Wan J (2012) Wax crystal-sparse leaf2, a rice homologue of WAX2/GL1, is involved in synthesis of leaf cuticular wax. Planta 235: 39-52.
44. Mitra J (2001) Genetics and genetic improvement of drought resistance in crop plants. Curr Sci 80: 758-763.
45. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Krolikowski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA 104: 16450-16455.
46. Nguyen HT, Silva JE, Podicheti R, Macrander J, Yang W, Nazarenus TJ, Nam JW, Jaworski JG, Lu C, Scheffler BE, Mockaitis K, Cahoon EB (2013) Camelina seed transcriptome: a tool for meal and oil improvement and translational research. Plant Biotechnol J 11: 759-769.
47. Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150: 1368-1379.
48. Oshima Y, Shikata M, Koyama T, Ohtsubo N, Mitsuda N, Ohme-Takagi M (2013) MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25: 1609-1624.
49. Putnam D, Budin J, Field L, Breene W (1993) Camelina: a promising low-input oilseed. In: Janick J, Simon JE (eds) New crops. Wiley, New York, pp 314-322.
50. Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol J 2: 477-486.
51. Raffaele S, Vailleau F, Léger A, Joubès J, Miersch O, Huard C, Blée E, Mongrand S, Domergue F, Roby D (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20: 752-767.
52. Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142: 866-877.
53. Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151: 275-289.
54. Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23: 1138-1152.
55. Specht JE, Hume DJ, Kumudini SV (1999) Soybean yield potential-a genetic and physiological perspective. Crop Sci 39: 1560-1570.
56. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447-456.
57. Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5: 1529-1539.
58. Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA, Riederer M (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid β-ketoacyl-CoA synthase. J Exp Bot 55: 1401-1410.
59. Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C, Uchacz T, Sarvas C, Wan J, Dennis DT, McCourt P, Huang Y (2005) Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J 43: 413-424.
60. Wang Y, Wan L, Zhang L, Zhang Z, Zhang H, Quan R, Zhou S, Huang R (2012) An ethylene response factor OsWR1 responsible to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 8: 275-288.
61. Wright PR, Morgan JM, Jessop RS, Cass A (1995) Comparative adaptation of canola (Brassica napus) and Indian mustard (B. juncea) to soil water deficits: yield and yield components. Field Crops Res 42: 1-13.
62. Xu X, Dietrich CR, Delledonne M, Xia Y, Wen TJ, Robertson DS, Nikolau BJ, Schnable PS (1997) Sequence analysis of the cloned glossy8 gene of maize suggests that it may code for a β-ketoacyl reductase required for the biosynthesis of cuticular waxes. Plant Physiol 115: 501-510.
63. Yang J, Isabel Ordiz M, Jaworski JG, Beachy RN (2011a) Induced accumulation of cuticular waxes enhances drought tolerance in Arabidopsis by changes in development of stomata. Plant Physiol Biochem 49: 1448-1455.
64. Yang M, Yang Q, Fu T, Zhou Y (2011b) Overexpression of the Brassica napus BnLAS gene in Arabidopsis affects plant development and increases drought tolerance. Plant Cell Rep 30: 373-388.
65. Yu D, Ranathunge K, Huang H, Pei Z, Franke R, Schreiber L, He C (2008) Wax Crystal-Sparse Leaf1 encodes a β-ketoacyl CoA synthase involved in biosynthesis of cuticular waxes on rice leaf. Planta 228: 675-685.
66. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42: 689-707.
67. Zhang X, Henriques R, Lin S-S, Niu Q-W, Chua N-H (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1: 641-646.
68. Zhang JY, Broeckling CD, Sumner LW, Wang ZY (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64: 265-278.
69. Zhang ZJ, Li F, Li DJ, Zhang HW, Huang RF (2010) Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232: 765-774.
70. Zhu X, Xiong L (2013) Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice. Proc Natl Acad Sci USA 110: 17790-17795.
71. Zingaretti SM, Inácio MC, de Matos Pereira L, Paz TA, de Castro França S (2013) Water Stress and Agriculture. In: Sener A (ed) Responses of organisms to water stress. InTech, doi: 10. 5772/53877. ISBN: 978-953-51-0933-4.
72. Zubr J (1997) Oil-seed crop: Camelina sativa. Ind Crops Prod 6: 113-119.