Special Issue:
植物抗病遗传合辑Plant Disease-resistance Genetics
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Multi-functional roles of TaSSI2 involved in Fusarium head blight and powdery mildew resistance and drought tolerance
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HU Li-qin1*, MU Jing-jing2*, SU Pei-sen1, WU Hong-yan3, YU Guang-hui4, WANG Gui-ping1, WANG Liang1, MA Xin1, LI An-fei1, WANG Hong-wei1, ZHAO Lan-fei1, KONG Ling-rang1 |
1 State Key Laboratory of Crop Biology/Shandong Key Laboratory of Crop Biology/College of Agronomy, Shandong Agricultural University, Tai’an 271018, P.R.China
2 Agriculture Bureau of Rushan, Rushan 264500, P.R.China
3 Shandong Agricultural University Fertilizer Science Technology Co., Ltd., Feicheng 271600, P.R.China
4 College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, P.R.China |
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Abstract The mutation of the gene encoding a stearoyl-acyl carrier protein fatty acid desaturase (ssi2) has been proved to enhance pathogen resistance in several plants, while it’s potential to regulate biotic and abiotic stresses in wheat is still unclear. In this study, we cloned TaSSI2 gene in wheat and provided several evidences of its involvement in multiple biological functions. By using barley stripe mosaic virus (BSMV)-induced gene silencing (VIGS) in wheat, it was found that TaSSI2 negatively regulated both powdery mildew and Fusarium head blight (FHB) resistance, which was consistent with the phenotype observed in knock-out mutants of Kronos. The expression of TaSSI2 was down-regulated by in vitro treatments of methyl jasmonate (MeJA), but positively regulated by salicylic acid (SA) and abscisic acid (ABA), implying the cross-talk between different hormone signaling pathways involved in wheat to regulate biotic stresses is still to be elucidated. Furthermore, the up-regulated expression of PR4 and PR5 indicated that TaSSI2 probably regulated FHB resistance by depressing the SA signaling pathway in wheat. In addition, the over-expression of TaSSI2 increased the content of linolenic acid (18:3) and subsequently enhanced drought tolerance of transgenic Brachypodium. This phenomenon might be associated with its subcellular localization in the whole cytosol, partly overlapping with Golgi apparatus and the secreted vesicles. As a stearoyl-acyl carrier protein fatty acid desaturase, TaSSI2 was proposed to be involved in cell lipid metabolism and carried targets out of the cell from membrane or wax synthesis, resulting in enhanced drought tolerance in plant.
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Received: 08 March 2017
Accepted:
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Fund: This work was supported by the National Natural Science Foundation of China (3315203911, 31471488), the National Key Research and Development Program of China (2016YFD0100602), the Transgenic Special Item, China (2016ZX08002003-002 and 2016ZX08009-003). |
Corresponding Authors:
Correspondence KONG Ling-rang, Tel: +86-538-8249278, Fax: +86-538-8242226, E-mail: lkong@sdau.edu.cn; ZHAO Lan-fei, E-mail: skyfly231@163.com
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About author: HU Li-qin, E-mail: lqhu926@126.com; MU Jing-jing, E-mail: mjj.8989@163.com;* These authors contributed equally to this study. |
Cite this article:
HU Li-qin, MU Jing-jing, SU Pei-sen, WU Hong-yan, YU Guang-hui, WANG Gui-ping, WANG Liang, MA Xin, LI An-fei, WANG Hong-wei, ZHAO Lan-fei, KONG Ling-rang .
2018.
Multi-functional roles of TaSSI2 involved in Fusarium head blight and powdery mildew resistance and drought tolerance
. Journal of Integrative Agriculture, 17(2): 368-380.
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Bai G, Shaner G. 1994. Scab of wheat: Prospects for control. Plant Disease, 78, 760–766.Bollina V, Kumaraswamy G K, Kushalappa A C, Choo T M, Dion Y, Rioux S, Faubert D, Hamzehzarghani H. 2010. Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Molecular Plant Pathology, 11, 769–782.Bragg J N, Wu J, Gordon S P, Guttman M E, Thilmony R, Lazo G R, Gu Y Q, Vogel J P. 2012. Generation and characterization of the Western Regional Research Center Brachypodium T-DNA insertional mutant collection. PLoS ONE, 7, e41916.Cahoon E, Shanklin J. 1997. Approaches to the design of acyl-ACP desaturases with altered fatty acid chain-length and double bond positional specificities. In: Williams J, Khan M, Lem N, eds., Physiology, Biochemistry and Molecular Biology of Plant Lipids. Springer, the Netherlands. pp. 374–376.Chen X, Steed A, Travella S, Keller B, Nicholson P. 2009. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytologist, 182, 975–983.Das P, Ito T, Wellmer F, Vernoux T, Dedieu A, Traas J, Meyerowitz E M. 2009. Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development, 136, 1605–1611.Ding L, Xu H, Yi H, Yang L, Kong Z, Zhang L, Xue S, Jia H, Ma Z. 2011. Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS One, 6, e19008.Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology, 300, 1005–1016.Ferrari S, Sella L, Janni M, De Lorenzo G, Favaron F, D’Ovidio R. 2012. Transgenic expression of polygalacturonase-inhibiting proteins in Arabidopsis and wheat increases resistance to the flower pathogen Fusarium graminearum. Plant Biology, 14, 31–38.Gao C S, Kou X J, Li H P, Zhang J B, Saad A S I, Liao Y C. 2013. Inverse effects of Arabidopsis NPR1 gene on fusarium seedling blight and fusarium head blight in transgenic wheat. Plant Pathology, 62, 383–392.Gigon A, Matos A R, Laffray D, Zuily-Fodil Y, Pham-Thi A T. 2004. Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Annals of Botany, 94, 345–351.Hou W, Mu J, Li A, Wang H, Kong L. 2015. Identification of a wheat polygalacturonase-inhibiting protein involved in Fusarium head blight resistance. European Journal of Plant Pathology, 141, 731–745.Jansen C, von Wettstein D, Schafer W, Kogel K H, Felk A, Maier F J. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America, 102, 16892–16897.Jiang C J, Shimono M, Maeda S, Inoue H, Mori M, Hasegawa M, Sugano S, Takatsuji H. 2009. Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Molecular Plant-Microbe Interactions, 22, 820–829.Kachroo A, Fu D Q, Havens W, Navarre D, Kachroo P, Ghabrial S A. 2008. An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Molecular Plant-Microbe Interactions, 21, 564–575.Kachroo A, Kachroo P. 2009. Fatty acid-derived signals in plant defense. Annual Review of Phytopathology, 47, 153–176.Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P. 2003. Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. The Plant Cell, 15, 2952–2965.Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D, Kachroo P. 2007. The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Molecular Biology, 63, 257–271.Kachroo A, Venugopal S C, Lapchyk L, Falcone D, Hildebrand D, Kachroo P. 2004. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 101, 5152–5157.Kachroo P, Shanklin J, Shah J, Whittle E J, Klessig D F. 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proceedings of the National Academy of Sciences of the United States of America, 98, 9448–9453.Kazan K, Gardiner D M, Manners J M. 2012. On the trail of a cereal killer: Recent advances in Fusarium graminearum pathogenomics and host resistance. Molecular Plant Pathology, 13, 399–413.Klinkenberg J, Faist H, Saupe S, Lambertz S, Krischke M, Stingl N, Fekete A, Mueller M J, Feussner I, Hedrich R, Deeken R. 2014. Two fatty acid desaturases, STEAROYL-ACYL CARRIER PROTEIN Delta9-DESATURASE6 and FATTY ACID DESATURASE3, are involved in drought and hypoxia stress signaling in Arabidopsis crown galls. Plant Physiology, 164, 570–583.Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu J K. 2001. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes & Development, 15, 912–924.Li G, Yen Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Science, 48, 1888–1896.Liu Z, Sun Q, Ni Z, Nevo E, Yang T. 2002. Molecular characterization of a novel powdery mildew resistance gene Pm30 in wheat originating from wild emmer. Euphytica, 123, 21–29.Ma X, Du X Y, Liu G J, Yang Z D, Hou W Q, Wang H W, Feng D S, Li A F, Kong L R. 2015. Cloning and characterization of a novel UDP-glycosyltransferase gene induced by DON from wheat. Journal of Integrative Agriculture, 14, 830–838.Makandar R, Essig J S, Schapaugh M A, Trick H N, Shah J. 2006. Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Molecular Plant-Microbe Interactions, 19, 123–129.Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks A A, Shah J. 2010. Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Molecular Plant-Microbe Interactions, 23, 861–870.Makandar R, Nalam V J, Lee H, Trick H N, Dong Y, Shah J. 2012. Salicylic acid regulates basal resistance to Fusarium head blight in wheat. Molecular Plant-Microbe Interactions, 25, 431–439.Maldonado A M, Doerner P, Dixon R A, Lamb C J, Cameron R K. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature, 419, 399–403.Mandal M K, Chandra-Shekara A C, Jeong R D, Yu K, Zhu S, Chanda B, Navarre D, Kachroo A, Kachroo P. 2012. Oleic acid-dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide-mediated defense signaling in Arabidopsis. The Plant Cell, 24, 1654–1674.McMullen M, Jones R, Gallenberg D. 1997. Scab of wheat and barley: A re-emerging disease of devastating impact. Plant Disease, 81, 1340–1348.Nelson B K, Cai X, Nebenführ A. 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. The Plant Journal, 51, 1126–1136.Okazaki Y, Saito K. 2014. Roles of lipids as signaling molecules and mitigators during stress response in plants. The Plant Journal, 79, 584–596.Peraldi A, Beccari G, Steed A, Nicholson P. 2011. Brachypodium distachyon: A new pathosystem to study Fusarium head blight and other Fusarium diseases of wheat. BMC Plant Biology, 11, 100.Pestka J J, Zhou H R, Moon Y, Chung Y J. 2004. Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: Unraveling a paradox. Toxicology Letters, 153, 61–73.Qi P F, Balcerzak M, Rocheleau H, Leung W, Wei Y M, Zheng Y L, Ouellet T. 2016. Jasmonic acid and abscisic acid play important roles in host-pathogen interaction between Fusarium graminearum and wheat during the early stages of Fusarium head blight. Physiological and Molecular Plant Pathology, 93, 39–48.Qin Y, Ma X, Yu G, Wang Q, Wang L, Kong L, Kim W, Wang H W. 2014. Evolutionary history of trihelix family and their functional diversification. DNA Research, 21, 499–510.Rawat N, Pumphrey M O, Liu S, Zhang X, Tiwari V K, Ando K, Trick H N, Bockus W W, Akhunov E, Anderson J A, Gill B S. 2016. Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nature Genetics, 48, 1576–1580.Rocha O, Ansari K, Doohan F M. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: A review. Food Additives & Contaminants, 22, 369–378.Rudd J C, Horsley R D, McKendry A L, Elias E M. 2001. Host plant resistance genes for Fusarium head blight: Sources, mechanisms, and utility in conventional breeding systems. Crop Science, 41, 620–627.Sekine K T, Nandi A, Ishihara T, Hase S, Ikegami M, Shah J, Takahashi H. 2004. Enhanced resistance to Cucumber mosaic virus in the Arabidopsis thalianassi2 mutant is mediated via an SA-independent mechanism. Molecular Plant-Microbe Interactions, 17, 623–632.Shah J, Kachroo P, Nandi A, 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. The Plant Journal, 25, 563–574.Shanklin J, Somerville C. 1991. Stearoyl-acyl-carrier-protein desaturase from higher plants is structurally unrelated to the animal and fungal homologs. Proceedings of the National Academy of Sciencesof the United States of America, 88, 2510–2514.Shen X, Kong L, Ohm H. 2004. Fusarium head blight resistance in hexaploid wheat (Triticum aestivum)-Lophopyrum genetic lines and tagging of the alien chromatin by PCR markers. Theoretical and Applied Genetics, 108, 808–813.Song N, Hu Z, Li Y, Li C, Peng F, Yao Y, Peng H, Ni Z, Xie C, Sun Q. 2013. Overexpression of a wheat stearoyl-ACP desaturase (SACPD) gene TaSSI2 in Arabidopsis ssi2 mutant compromise its resistance to powdery mildew. Gene, 524, 220–227.Sorahinobar M, Niknam V, Ebrahimzadeh H, Soltanloo H, Behmanesh M, Enferadi S T. 2015. Central role of salicylic acid in resistance of wheat against Fusarium graminearum. Journal of Plant Growth Regulation, 35, 477–491.Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.Torres-Franklin M L, Repellin A, Huynh V B, d’Arcy-Lameta A, Zuily-Fodil Y, Pham-Thi A T. 2009. Omega-3 fatty acid desaturase (FAD3, FAD7, FAD8) gene expression and linolenic acid content in cowpea leaves submitted to drought and after rehydration. Environmental and Experimental Botany, 65, 162–169.Toyooka K, Goto Y, Asatsuma S, Koizumi M, Mitsui T, Matsuoka K. 2009. A mobile secretory vesicle cluster involved in mass transport from the Golgi to the plant cell exterior. The Plant Cell, 21, 1212–1229.Xiang Y, Song M, Wei Z, Tong J, Zhang L, Xiao L, Ma Z, Wang Y. 2011. A jacalin-related lectin-like gene in wheat is a component of the plant defence system. Journal of Experimental Botany, 62, 5471–5483.Xiao J, Jin X, Jia X, Wang H, Cao A, Zhao W, Pei H, Xue Z, He L, Chen Q, Wang X. 2013. Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics, 14, 197.Yu G, Hou W, Du X, Wang L, Wu H, Zhao L, Kong L, Wang H. 2014. Identification of wheat non-specific lipid transfer proteins involved in chilling tolerance. Plant Cell Reports, 33, 1757–1766.Yuan C, Li C, Yan L, Jackson A O, Liu Z, Han C, Yu J, Li D. 2011. A high throughput Barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLoS ONE, 6, e26468.Zhang X L, Shen X R, Hao Y F, Cai J J, Ohm H, Kong L R. 2011. A genetic map of Lophopyrum ponticum chromosome 7E, harboring resistance genes to Fusarium head blight and leaf rust. Theoretical and Applied Genetics, 122, 263–270. |
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