A stearoyl-acyl carrier protein desaturase, NbSACPD-C, is critical for ovule development in Nicotiana benthamiana

Plant Journal

Volumn 80, Issue 3, 2014, Pages 489-502

  Zhang, Jiantao ^a   Li, Jianhui ^a   Garcia Ruiz, Hernan ^b   Bates, Philip D ^c   Mirkov, Theodore Erik ^d   Wang, Xiaofeng ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c The University of Southern Mississippi   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Fatty acids; Female sterility; Nicotiana benthamiana; Ovule development; Stearoyl acyl carrier protein desaturase

Indexed keywords

CELL DEATH; GENE EXPRESSION; GENES; LIPIDS; PLANTS (BOTANY); PROTEINS; RNA; SALICYLIC ACID; UNSATURATED FATTY ACIDS;

ACYL CARRIER PROTEINS; ARTIFICIAL MICRORNA; BIOTIC AND ABIOTIC STRESS; DESATURASE; FEMALE STERILITY; MEMBRANE LIPID COMPOSITION; NICOTIANA BENTHAMIANA; OVULE DEVELOPMENT;

FATTY ACIDS;

ARABIDOPSIS; NICOTIANA BENTHAMIANA;

ACYL COENZYME A DESATURASE; ACYL-(ACYL-CARRIER-PROTEIN)DESATURASE; FATTY ACID; MICRORNA; MIXED FUNCTION OXIDASE; SALICYLIC ACID;

AMINO ACID SEQUENCE; ENZYMOLOGY; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; OVULE; PHENOTYPE; PLANT LEAF; TOBACCO;

AMINO ACID SEQUENCE; FATTY ACID DESATURASES; FATTY ACIDS; GENE KNOCKDOWN TECHNIQUES; MICRORNAS; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OVULE; PHENOTYPE; PLANT LEAVES; SALICYLIC ACID; TOBACCO;

EID: 84926507138     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12649     Document Type: Article

References (67)

1. Allen, E., Xie, Z., Gustafson, A. M. and Carrington, J. C. (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 121, 207-221.
2. Bates, P. D., Stymne, S. and Ohlrogge, J. (2013) Biochemical pathways in seed oil synthesis. Curr. Opin. Plant Biol. 16, 358-364.
3. Baud, S., Guyon, V., Kronenberger, J., Wuilleme, S., Miquel, M., Caboche, M., Lepiniec, L. and Rochat, C. (2003) Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant J. 33, 75-86.
4. Benning, C. (2008) A role for lipid trafficking in chloroplast biogenesis. Prog. Lipid Res. 47, 381-389.
5. Boersma, J. G., Gillman, J. D., Bilyeu, K. D., Ablett, G. R., Grainger, C. and Rajcan, I. (2012) New mutations in a delta-9-stearoyl-acyl carrier protein desaturase gene associated with enhanced stearic acid levels in soybean seed. Crop Sci. 52, 1736-1742.
6. Byfield, G. E., Xue, H. and Upchurch, R. G. (2006) Two genes from soybean encoding soluble A9 stearoyl-ACP desaturases. Crop Sci. 46, 840-846.
7. Cahoon, E. B., Mills, L. A. and Shanklin, J. (1996) Modification of the fatty acid composition of Escherichia coli by coexpression of a plant acyl-acyl carrier protein desaturase and ferredoxin. J. Bacteriol. 178, 936-939.
8. Cahoon, E. B., Shah, S., Shanklin, J. and Browse, J. (1998) A determinant of substrate specificity predicted from the acyl-acyl carrier protein desaturase of developing cat's claw seed. Plant Physiol. 117, 593-598.
9. Carbonell, A., Takeda, A., Fahlgren, N., Johnson, S. C., Cuperus, J. T. and Carrington, J. C. (2014) New generation of artificial microRNA and synthetic trans-acting small interfering RNA vectors for efficient gene silencing in Arabidopsis. Plant Physiol. 165, 15-29.
10. Chen, Q.-F., Xiao, S., Qi, W., Mishra, G., Ma, J., Wang, M. and Chye, M.-L. (2010) The Arabidopsis acbp1acbp2 double mutant lacking acyl-CoA-binding proteins ACBP1 and ACBP2 is embryo lethal. New Phytol. 186, 843-855.
11. Christensen, C. A., King, E. J. and Jordan, J. R. (1997) Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 10, 49-64.
12. Cuperus, J. T., Carbonell, A. and Fahlgren, N. (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17, 997-1003.
13. Emanuelsson, O., Brunak, S., Von Heijne, G. and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971.
14. Feys, B., Benedetti, C. E., Penfold, C. N. and Turner, J. G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 6, 751-759.
15. Hicks, G. R., Rojo, E., Hong, S., Carter, D. G. and Raikhel, N. V. (2004) Geminating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol. 134, 1227-1239.
16. Jefferson, R. A., Kavanagh, T. A. and Bevan, M. W. (1987) GUS Fusion: beta glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
17. Jiang, C.-J., Shimono, M., Maeda, S., Inoue, H., Mori, M., Hasegawa, M., Sugano, S. and Takatsuji, H. (2009) Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol. Plant Microbe Interact. 22, 820-829.
18. Johansen, L. K. and Carrington, J. C. (2001) Silencing on the spot: induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 126, 930-938.
19. Kachroo, A. and Kachroo, P. (2009) Fatty acid-derived signals in plant defense. Annu. Rev. Phytopathol. 47, 153-176.
20. Kachroo, P., Shanklin, J., Shah, J., Whittle, E. J. and Klessig, D. F. (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc. Natl Acad. Sci. USA, 98, 9448-9453.
21. Kachroo, A., Lapchyk, L., Fukushige, H., Hildebrand, D., Klessig, D. and Kachroo, P. (2003a) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell, 15, 2952-2965.
22. Kachroo, P., Kachroo, A., Lapchyk, L., Hildebrand, D. and Klessig, D. F. (2003b) Restoration of defective cross talk in ssi2 mutants: role of salicylic acid, jasmonic acid, and fatty acids in SSI2-mediated signaling. Mol. Plant Microbe Interact. 16, 1022-1029.
23. Kachroo, A., Venugopal, S. C., Lapchyk, L., Falcone, D., Hildebrand, D. and Kachroo, P. (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl Acad. Sci. USA, 101, 5152-5157.
24. Kachroo, P., Venugopal, S. C., Navarre, D. A., Lapchyk, L. and Kachroo, A. (2005) Role of salicylic acid and fatty acid desaturation pathways in ssi2-mediated signaling. Plant Physiol. 139, 1717-1735.
25. Kachroo, A., Shanklin, J., Whittle, E., Lapchyk, L., Hildebrand, D. and Kachroo, P. (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol. Biol. 63, 257-271.
26. Kachroo, A., Fu, D.-Q., Havens, W., Navarre, D., Kachroo, P. and Ghabrial, S. A. (2008) An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Mol. Plant Microbe Interact. 21, 564-575.
27. Khodakovskaya, M., McAvoy, R., Peters, J., Wu, H. and Li, Y. (2006) Enhanced cold tolerance in transgenic tobacco expressing a chloroplast omega-3 fatty acid desaturase gene under the control of a cold-inducible promoter. Planta, 223, 1090-1100.
28. Kim, H. U. and Huang, A. H. C. (2004) Plastid lysophosphatidyl acyltransferase is essential for embryo development in Arabidopsis. Plant Physiol. 134, 1206-1216.
29. Kim, H. U., Li, Y. and Huang, A. H. C. (2005) Ubiquitous and endoplasmic reticulum-located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell, 17, 1073-1089.
30. Knutzon, D. S., Thompson, G. A., Radke, S. E., Johnson, W. B., Knauf, V. C. and Kridl, J. C. (1992) Modification of Brassica seed oil by antisense expression of a stearoyl-acyl carrier protein desaturase gene. Proc. Natl Acad. Sci. USA, 89, 2624-2628.
31. Kodama, H., Hamada, T., Horiguchi, G., Nishimura, M. and Iba, K. (1994) Genetic enhancement of cold tolerance by expression of a gene for chloroplast x-3 fatty acid desaturase in transgenic tobacco. Plant Physiol. 105, 601-605.
32. Köhrer, K. and Domdey, H. (1991) Preparation of high molecular weight RNA. Methods Enzymol. 194, 398-405.
33. Li, L., Li, C. and Howe, G. A. (2001) Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiol. 127, 1414-1417.
34. Li, L., Zhao, Y., McCaig, B. C., Wingerd, B. A., Wang, J., Whalon, M. E., Pichersky, E. and Howe, G. A. (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell, 16, 126-143.
35. Li, X.-C., Zhu, J., Yang, J., Zhang, G.-R., Xing, W.-F., Zhang, S. and Yang, Z.-N. (2012) Glycerol-3-phosphate acyltransferase 6 (GPAT6) is important for tapetum development in Arabidopsis and plays multiple roles in plant fertility. Mol. Plant, 5, 131-142.
36. Li-Beisson, Y., Shorrosh, B., Beisson, F. et al. (2013) Acyl-lipid metabolism. Arabidopsis Book, 11, e0161.
37. Lightner, J., James, D. W., Dooner, H. K. and Browse, J. (1994a) Altered body morphology is caused by increased stearate levels in a mutant of Arabidopsis. Plant J. 6, 401-412.
38. Lightner, J., Wu, J. and Browse, J. (1994b) A mutant of Arabidopsis with increased levels of stearic acid. Plant Physiol. 106, 1443-1451.
39. Lindqvist, Y., Huang, W., Schneider, G. and Shanklin, J. (1996) Crystal structure of D9 stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins. EMBO J. 15, 4081-4092.
40. Liu, C. M. and Meinke, D. W. (1998) The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. Plant J. 16, 21-31.
41. Liu, Y., Schiff, M., Marathe, R. and Dinesh Kumar, S. P. (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30, 415-429.
42. Mandal, M. K., Chandra-Shekara, A. C., Jeong, R.-D., Yu, K., Zhu, S., Chanda, B., Navarre, D., Kachroo, A. and Kachroo, P. (2012) Oleic acid-dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide-mediated defense signaling in Arabidopsis. Plant Cell, 24, 1654-1674.
43. McConn, M. and Browse, J. (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell, 8, 403-416.
44. Mikami, K. and Murata, N. (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog. Lipid Res. 42, 527-543.
45. Miquel, M., James, D., Dooner, H. and Browse, J. (1993) Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc. Natl Acad. Sci. USA, 90, 6208-6212.
46. Murakami, Y., Tsuyama, M., Kobayashi, Y., Kodama, H. and Iba, K. (2000) Trienoic fatty acids and plant tolerance of high temperature. Science, 287, 476-479.
47. Rotenberg, D., Thompson, T. S. and German, T. L. (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J. Virol. Methods, 138, 49-59.
48. Ruddle, P., Whetten, R., Cardinal, A., Upchurch, R. G. and Miranda, L. (2013) Effect of a novel mutation in a D9-stearoyl-ACP-desaturase on soybean seed oil composition. Theor. Appl. Genet. 126, 241-249.
49. Ruddle, P., Whetten, R., Cardinal, A., Upchurch, R. G. and Miranda, L. (2014) Effect of D9-stearoyl-ACP-desaturase-C mutants in a high oleic background on soybean seed oil composition. Theor. Appl. Genet. 127, 349-358.
50. Sekine, K.-T., Nandi, A., Ishihara, T., Hase, S., Ikegami, M., Shah, J. and Takahashi, H. (2004) Enhanced resistance to Cucumber mosaic virus in the Arabidopsis thaliana ssi2 mutant is mediated via an SA-independent mechanism. Mol. Plant Microbe Interact. 17, 623-632.
51. Senthil-Kumar, M. and Mysore, K. S. (2011) New dimensions for VIGS in plant functional genomics. Trends Plant Sci. 16, 656-665.
52. Shah, J., Kachroo, P., Nandi, A. and Klessig, D. F. (2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 25, 563-574.
53. Shanklin, J. and Somerville, C. (1991) Stearoyl-acyl-carrier-protein desaturase from higher plants is structurally unrelated to the animal and fungal homologs. Proc. Natl Acad. Sci. USA, 88, 2510-2514.
54. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
55. Tasseva, G., De Virville, J. D., Cantrel, C., Moreau, F. and Zachowski, A. (2004) Changes in the endoplasmic reticulum lipid properties in response to low temperature in Brassica napus. Plant Physiol. Biochem. 42, 811-822.
56. Thompson, G. A., Scherer, D. E., Foxall-Van Aken, S., Kenny, J. W., Young, H. L., Shintani, D. K., Kridl, J. C. and Knauf, V. C. (1991) Primary structures of the precursor and mature forms of stearoyl-acyl carrier protein desaturase from safflower embryos and requirement of ferredoxin for enzyme activity. Proc. Natl Acad. Sci. USA, 88, 2578-2582.
57. Tong, L., Shu-Ming, P., Wu-Yuan, D., Dan-Wei, M., Ying, X., Meng, X. and Fang, C. (2006) Characterization of a new stearoyl-acyl carrier protein desaturase gene from Jatropha curcas. Biotechnol. Lett. 28, 657-662.
58. Upchurch, R. G. (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol. Lett. 30, 967-977.
59. Vega, S. E., Alfonso, H., Bamberg, J. B. and Palta, J. P. (2004) Evidence for the up-regulation of stearoyl-ACP (D9) desaturase gene expression during cold acclimation. Am. J. Potato Res. 81, 125-135.
60. Wallis, J. G. and Browse, J. (2002) Mutants of Arabidopsis reveal many roles for membrane lipids. Prog. Lipid Res. 41, 254-278.
61. Wendehenne, D. and Hancock, J. T. (2011) New frontiers in nitric oxide biology in plant. Plant Sci. 181, 507-508.
62. Whittle, E., Cahoon, E. B., Subrahmanyam, S. and Shanklin, J. (2005) A multifunctional acyl-acyl carrier protein desaturase from Hedera helix L. (English ivy) can synthesize 16- and 18-carbon monoene and diene products. J. Biol. Chem. 280, 28169-28176.
63. Yang, L., Tang, R., Zhu, J., Liu, H., Mueller-Roeber, B., Xia, H. and Zhang, H. (2008) Enhancement of stress tolerance in transgenic tobacco plants constitutively expressing AtIpk2beta, an inositol polyphosphate 6-/3-kinase from Arabidopsis thaliana. Plant Mol. Biol. 66, 329-343.
64. Yu, B., Wakao, S., Fan, J. and Benning, C. (2004) Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol. 45, 503-510.
65. Zhang, P., Burton, J. W., Upchurch, R. G., Whittle, E., Shanklin, J. and Dewey, R. E. (2008) Mutations in a D9-stearoyl-ACP-desaturase gene are associated with enhanced stearic acid levels in soybean seeds. Crop Sci. 48, 2305.
66. Zhang, J., Liu, H., Sun, J., Li, B., Zhu, Q., Chen, S. and Zhang, H. (2012) Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PLoS One, 7, e30355.
67. Zheng, Z., Xia, Q., Dauk, M., Shen, W., Selvaraj, G. and Zou, J. (2003) Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell, 15, 1872-1887.