Chinese Journal OF Rice Science >
Tryptophanyl-tRNA Synthetase Gene WRS1 Regulates Rice Seed Development
Received date: 2020-03-01
Revised date: 2020-03-18
Online published: 2020-09-10
【Objective】 Aminoacyl-tRNA synthetases (aaRSs) are closely related to the transmission of genetic information. Besides translation, aaRSs in plants participate in gametogenesis and embryo development, early plastid development, immune signal perception and disease defense. In this study, we used a rice endosperm defective mutant to analyze the function of tryptophanyl-tRNA synthase (WRS1) during seed development, proving that WRS1 gene encodes a key factor affecting rice endosperm development. 【Method】 In this study, a stably-inherited rice floury endosperm mutant (wrs1) was screened from the mutant library of indica cultivar N22 (Oryza sativa subsp. indica) induced by ethyl methane sulfonate (EMS). Map-based cloning and complementation test identified the target gene. Morphological observation and starch physicochemical properties of wrs1 mature seeds were analyzed. Semi-thin sections were prepared to observe the developing endosperm structure with a scanning electron microscope. qRT-PCR and GUS staining were performed to analyze the expression of WRS1. The expression of starch synthesis related genes in the endosperm at 12 days after flowering was determined by qRT-PCR, and these protein expression levels in mature seed were detected by immunoblotting. The free amino acid contents of mature seeds were measured with a fully automatic amino acid analyzer. 【Result】 The seedlings of wrs1 were featured by obvious delay in development and finally withered and died. The floury grains isolated from the heterozygous mutant (WRS1wrs1) showed shrunken belly, decreased grain thickness and thousand-grain weight. Total starch contents, the peak viscosity and breakdown viscosity of pasting starch were lower in wrs1. The compound starch granules in developing endosperm of wrs1 were smaller and loosely arranged. WRS1 was restricted to the 183 kb region of the long arm of chromosome 12. Sequencing revealed a single base substitution in exon 6 of the tryptophanyl-tRNA synthetase gene (WRS1), resulting in a substitution of methionine. The expression of most starch synthesis-related genes in wrs1 was down-regulated, while these proteins showed different accumulation levels. The contents of proteins in wrs1 grains were decreased, while free amino acids contents were significantly increased. 【Conclusion】 WRS1 encodes tryptophanyl-tRNA synthase. Mutation of this gene affects amino acid homeostasis and protein synthesis in rice endosperm, resulting in abnormal expression of the genes in starch synthesis pathway which affects starch synthesis and accumulation, and eventually lead to seed development defects.
Xiaohan TANG, Shijia LIU, Xi LIU, Yunlu TIAN, Yunlong WANG, Xuan TENG, Erchao DUAN, Yuanyan ZHANG, Ling JIANG, Wenwei ZHANG, Yihua WANG, Jianmin WAN . Tryptophanyl-tRNA Synthetase Gene WRS1 Regulates Rice Seed Development[J]. Chinese Journal OF Rice Science, 2020 , 34(5) : 383 -396 . DOI: 10.16819/j.1001-7216.2020.0302
| [1] | Fitzgerald M A, McCouch S R, Hall R D. Not just a grain of rice: The quest for quality[J]. Trends in Plant Science, 2009, 14(3): 133-139. |
| [2] | Crofts N, Nakamura Y, Fujita N.Critical and speculative review of the roles of multi-protein complexes in starch biosynthesis in cereals[J]. Plant Science, 2017, 262: 1-8. |
| [3] | Feike D, Seung D, Graf A, Bischof S, Ellick T, Coiro M, Soyk S, Eicke S, Mettler-Altmann T, Lu K J, Trick M, Zeeman S C, Smith A M.The starch granule-associated protein EARLY STARVATION1 is required for the control of starch degradation in Arabidopsis thaliana leaves[J]. Plant Cell, 2016, 28(6): 1472-1489. |
| [4] | Silver D M, Kotting O, Moorhead G B.Phosphoglucan phosphatase function sheds light on starch degradation[J]. Trends in Plant Science, 2014, 19(7): 471-478. |
| [5] | Hejazi M, Mahlow S, Fettke J.The glucan phosphorylation mediated by α-glucan, water dikinase (GWD) is also essential in the light phase for a functional transitory starch turn-over[J/OL].Plant Signaling & Behavior, 2014, 9(7): e28892. |
| [6] | Hwang S K, Nishi A, Satoh H, Okita T W.Rice endosperm-specific plastidial alpha-glucan phosphorylase is important for synthesis of short-chain malto- oligosaccharides[J]. Archives of Biochemistry and Biophysics, 2010, 495(1): 82-92. |
| [7] | Higgins J E, Kosar-Hashemi B, Li Z, Howitt C A, Larroque O, Flanagan B, Morell M K, Rahman S.Characterization of starch phosphorylases in barley grains[J]. Journal of the Science of Food and Agriculture, 2013, 93(9): 2137-2145. |
| [8] | Peng C, Wang Y, Liu F, Ren Y, Zhou K, Lv J, Zheng M, Zhao S, Zhang L, Wang C, Jiang L, Zhang X, Guo X, Bao Y, Wan J.FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm[J]. Plant Journal, 2014, 77(6): 917-930. |
| [9] | Seung D, Soyk S, Coiro M, Maier B A, Eicke S, Zeeman S C.PROTEIN TARGETING TO STARCH is required for localizing GRANULE-BOUND STARCH SYNTHASE to starch granules and for normal amylose synthesis in Arabidopsis[J/OL].PLoS Biology, 2015, 13(2): e1002080. |
| [10] | Pfister B, Zeeman S C.Formation of starch in plant cells[J]. Cellular and Molecular Life Sciences, 2016, 73(14): 2781-2807. |
| [11] | Hunter B G, Beatty M K, Singletary G W, Hamaker B R, Dilkes B P, Larkins B A, Jung R.Maize opaque endosperm mutations create extensive changes in patterns of gene expression[J]. Plant Cell, 2002, 14(10): 2591-2612. |
| [12] | Wakasa Y, Yasuda H, Oono Y, Kawakatsu T, Hirose S, Takahashi H, Hayashi S, Yang L, Takaiwa F.Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm[J]. Plant Journal, 2011, 65(5): 675-689. |
| [13] | Han X, Wang Y, Liu X, Jiang L, Ren Y, Liu F, Peng C, Li J, Jin X, Wu F, Wang J, Guo X, Zhang X, Cheng Z, Wan J.The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice[J]. Journal of Experiment Botany, 2012, 63(1): 121-130. |
| [14] | Wang Y, Ren Y, Liu X, Jiang L, Chen L, Han X, Jin M, Liu S, Liu F, Lv J, Zhou K, Su N, Bao Y, Wan J.OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells[J]. Plant Journal, 2010, 64(5): 812-824. |
| [15] | Liu F, Ren Y, Wang Y, Peng C, Zhou K, Lv J, Guo X, Zhang X, Zhong M, Zhao S, Jiang L, Wang H, Bao Y, Wan J.OsVPS9A functions cooperatively with OsRAB5A to regulate post-Golgi dense vesicle-mediated storage protein trafficking to the protein storage vacuole in rice endosperm cells[J]. Molecular Plant, 2013, 6(6): 1918-1932. |
| [16] | Ren Y, Wang Y, Liu F, Zhou K, Ding Y, Zhou F, Wang Y, Liu K, Gan L, Ma W, Han X, Zhang X, Guo X, Wu F, Cheng Z, Wang J, Lei C, Lin Q, Jiang L, Wu C, Bao Y, Wang H, Wan J.GLUTELIN PRECURSOR ACCUMULATION3 encodes a regulator of post-Golgi vesicular traffic essential for vacuolar protein sorting in rice endosperm[J]. Plant Cell, 2014, 26(1): 410-425. |
| [17] | Wang Y, Liu F, Ren Y, Wang Y, Liu X, Long W, Wang D, Zhu J, Zhu X, Jing R, Wu M, Hao Y, Jiang L, Wang C, Wang H, Bao Y, Wan J.GOLGI TRANSPORT 1B regulates protein export from the endoplasmic reticulum in rice endosperm cells[J]. Plant Cell, 2016, 28(11): 2850-2865. |
| [18] | Zhu J, Ren Y, Wang Y, Liu F, Teng X, Zhang Y, Duan E, Wu M, Zhong M, Hao Y, Zhu X, Lei J, Wang Y, Yu Y, Pan T, Bao Y, Wang Y, Wan J.OsNHX5-mediated pH homeostasis is required for post-Golgi trafficking of seed storage proteins in rice endosperm cells[J/OL].BMC Plant Biology, 2019, 19(1): 295. |
| [19] | Perona J J, Gruic-Sovulj I.Synthetic and Editing Mechanisms of Aminoacyl-tRNA Synthetases[M]//Kim S. Topics in Current Chemistry-Series, 2014: 1-41. |
| [20] | Guo M, Yang X L, Schimmel P.New functions of aminoacyl-tRNA synthetases beyond translation[J]. Nature Reviews Molecular Cell Biology, 2010, 11(9): 668-674. |
| [21] | Park S G, Ewalt K L, Kim S.Functional expansion of aminoacyl-tRNA synthetases and their interacting factors: New perspectives on housekeepers[J]. Trends in Biochemical Sciences, 2005, 30(10): 569-574. |
| [22] | Duchêne A, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters N M, Zaepfel M, Maréchal-Drouard L, Small I D.Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(45): 16484-16489. |
| [23] | Steiner R E, Ibba M. Regulation of tRNA-dependent translational quality control[J/OL]. IUBMB Life, 2019, 69: DOI: 10.1002/iub.2080. |
| [24] | Jin M. Unique roles of tryptophanyl-tRNA synthetase in immune control and its therapeutic implications[J].Experimental & Molecular Medicine, 2019, 51(1): . |
| [25] | Yakobov N, Debard S, Fischer F, Senger B, Becker H D.Cytosolic aminoacyl-tRNA synthetases: Unanticipated relocations for unexpected functions[J]. Biochimica et Biophysica Acta, 2018, 1861(4): 387-400. |
| [26] | Ray P, Arif A, Fox P.Macromolecular complexes as depots for releasable regulatory proteins[J]. Trends in Biochemical Sciences, 2007, 32(4): 158-164. |
| [27] | Berg M, Rogers R, Muralla R, Meinke D.Requirement of aminoacyl-tRNA synthetases for gametogenesis and embryo development in Arabidopsis[J]. Plant Journal, 2005, 44(5): 866-878. |
| [28] | Yang X, Li G, Tian Y, Song Y, Liang W, Zhang D.A rice glutamyl-tRNA synthetase modulates early anther cell division and patterning[J]. Plant Physiology, 2018, 177(2): 728-744. |
| [29] | Kagi C, Baumann N, Nielsen N, Stierhof Y D, Gross-Hardt R.The gametic central cell of Arabidopsis determines the lifespan of adjacent accessory cells[J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(51): 22 350-22 355. |
| [30] | Kim Y K, Lee J Y, Cho H S, Lee S S, Ha H J, Kim S, Choi D, Pai H S.Inactivation of organellar glutamyl- and seryl-tRNA synthetases leads to developmental arrest of chloroplasts and mitochondria in higher plants[J]. Journal of Biological Chemistry, 2005, 280(44): 37098-37106. |
| [31] | Wang Y, Wang C, Zheng M, Lyu J, Xu Y, Li X, Niu M, Long W, Wang D, Wang H, Terzaghi W, Wang Y, Wan J.WHITE PANICLE1, a val-tRNA synthetase regulating chloroplast ribosome biogenesis in rice, is essential for early chloroplast development[J]. Plant Physiology, 2016, 170(4): 2110-2123. |
| [32] | Zhang Y, Hao Y, Wang Y, Wang C, Wang Y, Long W, Wang D, Liu X, Jiang L, Wan J.Lethal albinic seedling, encoding a threonyl-tRNA synthetase, is involved in development of plastid protein synthesis system in rice[J]. Plant Cell Reports, 2017, 36(7): 1053-1064. |
| [33] | Kitagawa M, Balkunde R, Bui H, Jackson D.An aminoacyl tRNA Synthetase, OKI1, is required for proper shoot meristem size in Arabidopsis[J]. Plant Cell Physiology, 2019, 60(11): 2597-2608. |
| [34] | Zuo D, Yi S, Liu R, Qu B, Huang T, He W, Li C, Li H, Liao Y.A deoxynivalenol-activated methionyl-tRNA synthetase gene from wheat encodes a nuclear localized protein and protects plants against fusarium pathogens and mycotoxins[J]. Phytopathology, 2016, 106(6): 614-623. |
| [35] | Luna E, van Hulten M, Zhang Y, Berkowitz O, López A, Pétriacq P, Sellwood M A, Chen B, Burrell M, van de Meene A, Pieterse C M J, Flors V, Ton J. Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase[J]. Nature Chemical Biology, 2014, 10(6): 450-456. |
| [36] | Long W, Wang Y, Zhu S, Jing W, Wang Y, Ren Y, Tian Y, Liu S, Liu X, Chen L, Wang D, Zhong M, Zhang Y, Hu T, Zhu J, Hao Y, Zhu X, Zhang W, Wang C, Zhang W, Wan J.FLOURY SHRUNKEN ENDOSPERM1 connects phospholipid metabolism and amyloplast development in rice[J]. Plant Physiology, 2018, 177(2): 698-712. |
| [37] | Robert X, Gouet P.Deciphering key features in protein structures with the new ENDscript server[J]. Nucleic Acids Research, 2014, 42: W320-W324. |
| [38] | Ries F, Herkt C, Willmund F.Co-translational protein folding and sorting in chloroplasts[J]. Plants (Basel), 2020, 9(2): 214. doi: 10.3390/plants9020214. |
| [39] | Zheng M, Wang Y, Liu X, Sun J, Wang Y, Xu Y, Lv J, Long W, Zhu X, Guo X, Jiang L, Wang C, Wan J.The RICE MINUTE-LIKE1 (RML1) gene, encoding a ribosomal large subunit protein L3B, regulates leaf morphology and plant architecture in rice[J]. Journal of Experimental Botany, 2016, 67(11): 3457-3469. |
| [40] | Wang S, Lei C, Wang J, Ma J, Tang S, Wang C, Zhao K, Tian P, Zhang H, Qi C, Cheng Z, Zhang X, Guo X, Liu L, Wu C, Wan J.SPL33, encoding an eEF1A-like protein, negatively regulates cell death and defense responses in rice[J]. Journal of Experimental Botany, 2017, 68(5): 899-913. |
| [41] | Jia J, Arif A, Ray P S, Fox P L.WHEP domains direct noncanonical function of glutamyl-prolyl tRNA synthetase in translational control of gene expression[J]. Molecular Cell, 2008, 29(6): 679-690. |
| [42] | Sajish M, Zhou Q, Kishi S, Valdez D J, Kapoor M, Guo M, Lee S, Kim S, Yang X L, Schimmel P.Trp-tRNA synthetase bridges DNA-PKcs to PARP-1 to link IFN-gamma and p53 signaling[J]. Nature Chemical Biology, 2012, 8(6): 547-554. |
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