Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Sahni, Sangita ^a   Prasad, Bishun D ^a   Liu, Qing ^b   Grbic, Vojislava ^a   Sharpe, Andrew ^c   Singh, Surinder P ^b   Krishna, Priti ^a,d  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CSIRO   (Australia)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINOSTEROID; CYTOCHROME P450; DWF4 PROTEIN, ARABIDOPSIS; TRANSCRIPTOME; VEGETABLE OIL;

ADAPTATION; ARABIDOPSIS; ASCOMYCETES; BIOSYNTHESIS; DEHYDRATION; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETIC ENHANCEMENT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT ROOT; PLANT SEED; RAPESEED; SHOOT;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; BIOSYNTHETIC PATHWAYS; BRASSICA NAPUS; BRASSINOSTEROIDS; CYTOCHROME P-450 ENZYME SYSTEM; DEHYDRATION; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ENHANCEMENT; PLANT DISEASES; PLANT OILS; PLANT ROOTS; PLANT SHOOTS; SEEDS; TRANSCRIPTOME;

EID: 84975862360     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28298     Document Type: Article

References (60)

1. Belkhadir, Y. & Jaillais, Y. The molecular circuitry of brassinosteroid signalling. New Phytol. 206, 522-540 (2015).
2. Coll, Y. et al. Brassinosteroids roles and applications: an up-date. Biologia. 70, 726-732 (2016).
3. Krishna, P. Brassinosteroid-mediated stress responses. J. Plant Growth Regul. 22, 289-297 (2003).
4. Divi, U. K. & Krishna, P. Brassinosteroids confer stress tolerance. In: Hirt, H. Ed. Plant Stress Biology: from Genomics to System Biology. 119-135 (Wiley-VCH, 2010a).
5. Sun, Y. et al. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 765-777 (2010).
6. Yu, X. et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634-646 (2011).
7. Choe, S. et al. Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J. 26, 573-582 (2001).
8. Liu, T. et al. Expression and functional analysis of ZmDWF4, an ortholog of Arabidopsis DWF4 from maize (Zea mays L.). Plant Cell Rep. 26, 2091-2099 (2007).
9. Wu, C. Y. et al. Brassinosteroids regulate grain filling in rice. Plant Cell. 20, 2130-2145 (2008).
10. Vriet, C., Russinova, E. & Reuzeau, C. From squalene to brassinolide: the steroid metabolic and signaling pathways across the plant kingdom. Mol. Plant 6, 1738-1757 (2013).
11. Koh, S. et al. T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol. Biol. 65, 453-466 (2007).
12. Nakashita, H. et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33, 887-898 (2003).
13. Ali, S. S. et al. Brassinosteroid enhances resistance to fusarium diseases of barley. Phytopathology 103, 1260-1267 (2013).
14. Albrecht, C. et al. Brassinosteroids inhibit pathogen-Associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc. Natl Acad. Sci. USA 109, 303-308 (2012).
15. Belkhadir, Y. et al. Brassinosteroids modulate the efficiency of plant immune responses to microbe-Associated molecular patterns. Proc. Natl. Acad. Sci. USA 109, 297-302 (2012).
16. De Vleesschauwer, D. et al. Brassinosteroids antagonize gibberellin-And salicylate-mediated root immunity in rice. Plant Physiol. 158, 1833-1846 (2012).
17. Divi, U. K. & Krishna, P. Overexpression of the brassinosteroid biosynthetic gene AtDWF4 in Arabidopsis seeds overcomes abscisic acid-induced inhibition of germination and increases cold tolerance in transgenic seedlings. J. Plant Growth Regul. 29, 385-393(2010b).
18. Kagale, S. et al. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225, 353-364 (2007).
19. Shinozaki, K. & Yamaguchi-Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781-803 (2006).
20. Janeczko, A. et al. Physiological and biochemical characterisation of watered and drought-stressed barley mutants in the HvDWARF gene encoding C6-oxidase involved in brassinosteroid biosynthesis. Plant Physiol Biochem. 99, 126-41 (2016).
21. Angadi, S. V. et al. Response of three Brassica species to high temperature injury during reproductive growth. Can. J. Plant Sci. 80, 693-710 (2000).
22. Dhaubhadel, S. et al. Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Mol. Biol. 40, 333-342 (1999).
23. Dhaubhadel, S. et al. Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. Plant J. 29, 681-691 (2002).
24. Rouxel, T. & Balesdent, M. H. The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol. Plant Pathol. 6, 225-241 (2005).
25. Hegedus, D. D. & Rimmer, S. R. Sclerotinia sclerotiorum: when "to be or not to be" a pathogen? FEMS Microbiol. Lett. 251, 177-184 (2005).
26. Howe, G. A. & Jander, G. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59, 41-66 (2008).
27. Robert-Seilaniantz, A., Grant, M. & Jones, J. D. G. Hormone crosstalk in plant disease and defense: more than just JASMONATESALICYLATE antagonism. Annu. Rev. Phytopathol. 49, 317-343 (2011).
28. Müssig, C. et al. Molecular analysis of brassinosteroid action. Plant Biol. Stuttg. 8, 291-296 (2006).
29. Divi, U. K., Rahman, T. & Krishna P. Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. Plant Biotechnol. J. 14, 419-432 (2016).
30. Stasolla, C. et al. Buthionine sulfoximine (BSO)-mediated improvement in cultured embryo quality in vitro entails changes in ascorbate metabolism, meristem development and embryo maturation. Planta. 228, 255-272 (2008).
31. Vert, G. et al. Molecular mechanisms of steroid hormone signaling in plants. Annu. Rev. Cell Dev. Biol. 21, 177-201 (2005).
32. Thimm, O. et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939 (2004).
33. Deng, Z. et al. A proteomic study of brassinosteroid response in Arabidopsis. Mol. Cell Proteomics. 6, 2058-2071 (2007).
34. Le Gall, H. et al. Cell wall metabolism in response to abiotic stress. Plants 4, 112-166 (2015).
35. Chung, H. S. et al. Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol. 146, 952-964 (2008).
36. Divi, U. K., Rahman, T. & Krishna P. Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 10, 151 (2010).
37. Rushton, P. J. et al. WRKY transcription factors. Trends Plant Sci. 15, 247-258 (2010).
38. Saha, G. et al. Molecular characterization of BZR transcription factor family and abiotic stress induced expression profiling in Brassica rapa. Plant Physiol Biochem. 92, 92-104 (2015).
39. Trewavas, A. J. & Jones, H. G. An assessment of the role of ABA in plant development. In Abscisic acid: Physiology and Biochemistry, (eds. Davies, W. J. & Jones, H. G.), 169-188 (Oxford, UK: BIOS Scientific,1991).
40. Heinrich, M. et al. High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J. 73, 591-606 (2013).
41. Abreu, M. E. & Munné-Bosch, S. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J. Exp. Bot. 60, 1261-1271 (2009).
42. Wolf, S. et al. Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr. Biol. 22, 1732-1737 (2012).
43. Caño-Delgado, A. et al. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development, 131, 5341-5351 (2004).
44. Kim, S. Y., Kim, B. H. & Nam, K. H. Reduced expression of the genes encoding chloroplast-localized proteins in a cold-resistant bri1 (brassinosteroid-insensitive 1) mutant. Plant Signal Behav. 5, 458-463 (2010).
45. Li, X.-J. et al. Overexpression of a brassinosteroid biosynthetic gene Dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato. BMC Plant Biol. 16, 33 (2016).
46. Esposito, D. Anabolic effect of plant brassinosteroid. FASEB J. 25, 3708-3719 (2011).
47. Delourme, R. et al. A cluster of major specific resistance genes to Leptosphaeria maculans In Brassica napus. Phytopathology 94, 578-583 (2004).
48. Brun, H. et al. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans In Brassica napus. New Phytol. 185, 285-299 (2010).
49. Persson, M. et al. Layers of defense responses to Leptosphaeria maculans below the RLM1-And camalexin-dependent resistances. New Phytol. 182, 470-482 (2009).
50. Eynck, C. et al. Monolignol biosynthesis is associated with resistance to Sclerotinia sclerotiorum In Camelina sativa. Mol. Plant Pathol. 13, 887-899 (2012).
51. Garg, H. et al. The infection processes of Sclerotinia sclerotiorum in cotyledon tissue of a resistant and a susceptible genotype of Brassica napus. Ann. Bot. 106, 897-908 (2010).
52. Wolf, S. et al. A receptor-like protein mediates the response to pectin modification by activating brassinosteroid signaling. Proc. Natl Acad. Sci. USA 111, 15261-15266 (2014).
53. Xia, X. J. et al. Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol. 191, 706-720 (2011).
54. Zhang, A. et al. ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H2O2 in brassinosteroidinduced antioxidant defence in leaves of maize. J. Exp. Bot. 6, 4399-4411 (2010).
55. Nafisi, M., Fimognari, L. & Sakuragi, Y. Interplays between the cell wall and phytohormones in interaction between plants and necrotrophic pathogens. Phytochem. 112, 63-71 (2015).
56. Narsai, R. et al. Antagonistic, overlapping and distinct responses to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genomics 12, 14-93 (2013).
57. Moloney, M. M., Walker, J. M. & Sharma, K. K. High efficiency transformation of Brassica napus using Agrobacterium vectors. Plant Cell Rep. 8, 238-242 (1989).
58. Hoagland, D. R. & Arnon, D. I. The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347, 1-32 (1950).
59. Mengistu, A., Rimmer, R. & Williams, P. H. Protocols for in vitro sporulation, ascospore release, sexual mating, and fertility in crosses of Leptosphaeria maculans. Plant Dis. 77, 538-40 (1993).
60. Zhurov, V. et al. Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite. Plant Physiol. 164, 384-99 (2014).