
SRG1, Encoding a Kinesin-4 Protein, Is an Important Factor for Determining Grain Shape in Rice
Received date: 2018-04-02
Accepted date: 2018-06-14
Online published: 2018-08-20
Grain shape is one of the important agronomic traits, which is closely related to the yield of rice. A new rice mutant, named small and round grain (srg1), was isolated from an indica cultivar Zhenong 34 by ethyl methane sulfonate (EMS) mutagenesis. The microscopic analysis showed that the cell length of spikelet in srg1 was decreased compared with that in wild type (WT), which caused the grain length short. Meanwhile, the grains of srg1 were wider than those of WT because of the increased cell layers in spikelet in the lateral direction. Therefore, the inhibition of cell expansion and increased cell proliferation collectively led to the small and round grain. By map-based cloning, the gene SRG1 was located on the short arm of chromosome 9, which encodes a kinesin-4 protein, represented by the gene LOC_Os09g02650. A single nucleotide polymorphism, occurred in the 16th exon of SRG1, led to premature translation stop in mutant. The cell cycle-related genes were up-regulated in srg1, which conferred that SRG1 controlled grain width through the cell proliferation. Since the role of SRG1 in regulating grain shape was not clarified well before, it is valuable to explore the mechanism of grain development. This study could, hence, provide a morphogenesis and molecular basis for elucidating the function of SRG1, as well as a new germplasm resource for the further study of grain development.
Key words: small and round grain; kinesin-4 protein; gene mapping; rice
Ran Qin, Akhter Delara, Chengcong Yang, Kumar Nath Ujjal, Eshag Jamal, Xiaoli Jin, Chunhai Shi . SRG1, Encoding a Kinesin-4 Protein, Is an Important Factor for Determining Grain Shape in Rice[J]. Rice Science, 2018 , 25(6) : 297 -307 . DOI: 10.1016/j.rsci.2018.06.008
| [1] | Abe Y, Mieda K, Ando T, Kono I, Yano M, Kitano H, Wasaki Y.2010. TheSMALL AND ROUND SEED1 (SRS1/DEP2) gene is involved in the regulation of seed size in rice. Genes Genet Syst, 85(5): 327-339. |
| [2] | Aohara T, Kotake T, Kaneko Y, Takatsuji H, Tsumuraya Y, Kawasaki S.2009. RiceBRITTLE CULM 5(BRITTLE NODE) is involved in secondary cell wall formation in the sclerenchyma tissue of nodes. Plant Cell Physiol, 50(11): 1886-1897. |
| [3] | Cobbe N, Heck M M S.2004. The evolution of SMC proteins: Phylogenetic analysis and structural implications. Mol Biol Evo, 21(2): 332-347. |
| [4] | Duan P G, Rao Y H, Zeng D L, Yang L Y, Xu R, Zhang B L, Dong G J, Qian Q, Li Y H.2014. SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J, 77(4): 547-557. |
| [5] | Fan C H, Xing Y Z, Mao H L, Lu T T, Han B, Xu C G, Li X H, Zhang Q F.2006. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet, 112(6): 1164-1171. |
| [6] | Hirano K, Kotake T, Kamihara K, Tsuna K, Aohara T, Kaneko Y, Takatsuji H, Tsumuraya Y, Kawasaki S.2010. Rice BRITTLE CULM 3 (BC3) encodes a classical dynamin OsDRP2B essential for proper secondary cell wall synthesis. Planta, 232(1): 95-108. |
| [7] | Hong Z, Ueguchi-Tanaka M, Shimizu-Sato S, Inukai Y, Fujioka S, Shimada Y, Takatsuto S, Agetsuma M, Yoshida S, Watanabe Y, Uozu S, Kitano H, Ashikari M, Matsuoka M.2002. Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem.Plant J, 32: 495-508. |
| [8] | Hong Z, Ueguchi-Tanaka M, Fujioka S, Takatsuto S, Yoshida S, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M.2005. The rice brassinosteroid-deficient dwarf2 mutant, defective in the rice homolog of Arabidopsis DIMINUTO/DWARF1, is rescued by the endogenously accumulated alternative bioactive brassinosteroid, dolichosterone. Plant Cell, 17(8): 2243-2254. |
| [9] | Hu J, Wang Y X, Fang Y X, Zeng L J, Xu J, Yu H P, Shi Z Y, Pan J J, Zhang D, Kang S J, Zhu L, Dong G J, Guo L B, Zeng D L, Zhang G H, Xie L H, Xiong G S, Li J Y, Qian Q.2015. A rare allele of GS2 enhances grain size and grain yield in rice. Mol Plant, 8(6): 1455-1465. |
| [10] | Huang K, Wang D K, Duan P G, Zhang B L, Xu R, Li N, Li Y H.2017. WIDE AND THICK GRAIN 1, which encodes an otubain-like protease with deubiquitination activity, influences grain size and shape in rice. Plant J, 91: 849-860. |
| [11] | Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B, Onishi A, Miyagawa H, Katoh E.2013. Loss of function of the IAA-glucose hydrolase geneTGW6 enhances rice grain weight and increases yield. Nat Genet, 45(6): 707-712. |
| [12] | Jiang Y H, Bao L, Jeong S Y, Kim S K, Xu C G, Li X H, Zhang Q F.2012. XIAO is involved in the control of organ size by contributing to the regulation of signaling and homeostasis of brassinosteroids and cell cycling in rice. Plant J, 70(3): 398-408. |
| [13] | Kitagawa K, Kurinami S, Oki K, Abe Y, Ando T, Kono I, Yano M, Kitano H, Iwasaki Y.2010. A novel kinesin 13 protein regulating rice seed length. Plant Cell Physiol, 51(8): 1315-1329. |
| [14] | Kotake T, Aohara T, Hirano K, Sato A, Kaneko Y, Tsumuraya Y, Takatsuji H, Kawasaki S.2011. Rice Brittle culm 6 encodes a dominant-negative form of CesA protein that perturbs cellulose synthesis in secondary cell walls. J Exp Bot, 62(6): 2053-2062. |
| [15] | Li J, Jiang J F, Qian Q, Xu Y Y, Zhang C, Xiao J, Du C, Luo W, Zou G X, Chen M L, Huang Y Q, Feng Y Q, Cheng Z K, Yuan M, Chong K.2011. Mutation of riceBC12/GDD1, which encodes a kinesin-like protein that binds to a GA biosynthesis gene promoter, leads to dwarfism with impaired cell elongation. Plant Cell, 23(2): 628-640. |
| [16] | Li J, Xu Y Y, Chong K.2012. The novel functions of kinesin motor proteins in plants. Protoplasma, 249(2): 95-100. |
| [17] | Li Y H, Qian Q, Zhou Y H, Yan M X, Sun L, Zhang M, Fu Z M, Wang Y H, Han B, Pang X M, Chen M S, Li J Y.2003. BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell, 15(9): 2020-2031. |
| [18] | Nakagawa H, Tanaka A, Tanabata T, Ohtake M, Fujioka S, Nakamura H, Ichikawa H, Mori M.2012. SHORT GRAIN1 decreases organ elongation and brassinosteroid response in rice. Plant Physiol, 158(3): 1208-1219. |
| [19] | Persson S, Caffall K H, Freshour G, Hilley M T, Bauer S, Poindexter P, Hahn M G, Mohnen D, Somerville C.2007. TheArabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell, 19(1): 237-255. |
| [20] | Preuss M L, Kovar D R, Lee Y R J, Staiger C J, Delmer D P, Liu B.2004. A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol, 136(4): 3945-3955. |
| [21] | Reddy V S, Reddy A S N.2002. The calmodulin-binding domain from a plant kinesin functions as a modular domain in conferring Ca2+-calmodulin regulation to animal plus- and minus-end kinesins. J Biol Chem, 277: 48058-48065. |
| [22] | Schmittgen T D, Livak K J.2008. Analyzing real-time PCR data by the comparative C-T method. Nat Prot, 3(6): 1101-1108. |
| [23] | Segami S, Kono I, Ando T, Yano M, Kitano H, Miura K, Iwasaki Y.2012. Small and round seed 5 gene encodes alpha-tubulin regulating seed cell elongation in rice. Rice, 5(1): 4. |
| [24] | Shomura A, Izawa T, Ebana K, Ebitani T, Kanegae H, Konishi S, Yano M.2008. Deletion in a gene associated with grain size increased yields during rice domestication.Nat Genet, 40(8): 1023-1028. |
| [25] | Song X J, Huang W, Shi M, Zhu M Z, Lin H X.2007. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet, 39(5): 623-630. |
| [26] | Tanabe S, Ashikari M, Fujioka S, Takatsuto S, Yoshida S, Yano M, Yoshimura A, Kitano H, Matsuoka M, Fujisawa Y, Kato H, Iwasaki Y.2005. A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant,dwarf11, with reduced seed length. Plant Cell, 17(3): 776-790. |
| [27] | Ueguchi-Tanaka M, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M.2000. Rice dwarf mutantd1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA, 97(21): 11638-11643. |
| [28] | van Soest P J, Robertson J B, Lewis B A.1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.J Dairy Sci, 74(10): 3583-3597. |
| [29] | Vert G, Chory J.2006. Downstream nuclear events in brassinosteroid signalling. Nature, 441: 96-100. |
| [30] | Wang L, Xu Y Y, Ma Q B, Li D, Xu Z H, Chong K.2006. Heterotrimeric G protein alpha subunit is involved in rice brassinosteroid response. Cell Res, 16(12): 916-922. |
| [31] | Wang S K, Wu K, Yuan Q B, Liu X Y, Liu Z B, Lin X Y, Zeng R Z, Zhu H T, Dong G J, Qian Q, Zhang G Q, Fu X D.2012. Control of grain size, shape and quality byOsSPL16 in rice. Nat Genet, 44(8): 950-954. |
| [32] | Wang S K, Li S, Liu Q, Wu K, Zhang J Q, Wang S S, Wang Y, Chen X B, Zhang Y, Gao C X, Wang F, Huang H X, Fu X D.2015. TheOsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet, 47(8): 949-956. |
| [33] | Wang Y X, Xiong G S, Hu J, Jiang L, Yu H, Xu J, Fang Y X, Zeng L J, Xu E B, Xu J, Ye W J, Meng X B, Liu R F, Chen H Q, Jing Y H, Wang Y H, Zhu X D, Li J Y, Qian Q.2015. Copy number variation at theGL7 locus contributes to grain size diversity in rice. Nat Genet, 47(8): 944-948. |
| [34] | Wu Y Z, Fu Y C, Zhao S S, Gu P, Zhu Z F, Sun C Q, Tan L B.2016. CLUSTERED PRIMARY BRANCH 1, a new allele of DWARF11, controls panicle architecture and seed size in rice. Plant Biotech J, 14(1): 377-386. |
| [35] | Xing Y Z, Zhang Q F.2010. Genetic and molecular bases of rice yield. Annu Rev Plant Biol, 61: 421-442. |
| [36] | Xu J D, Zhang Q G, Zhang T, Zhang H Y, Xu P Z, Wang X D, Wu X J.2008. Phenotypic characterization, genetic analysis and gene-mapping for a brittle mutant in rice. J Integr Plant Biol, 50(3): 319-328. |
| [37] | Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M.2000. Loss of function of a ricebrassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell, 12(9): 1591-1605. |
| [38] | Yu H P, Ren D Y, Zhu Y Z, Xu J M, Wang Y X, Liu R F, Fang Y X, Shi Z Y, Pan J J, Lu M, Ma B J, Hu J, Rao Y C.2016. Multi-tillering dwarf1, a new allele of brittle culm 12, affects plant height and tiller in rice. Sci Bull, 61(23): 1810-1817. |
| [39] | Zhang B C, Liu X L, Qian Q, Liu L F, Dong G J, Xiong G Y, Zeng D L, Zhou Y H.2011. Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice.Proc Natl Acad Sci USA, 108(12): 5110-5115. |
| [40] | Zhang M, Zhang B C, Qian Q, Yu Y C, Li R, Zhang J W, Liu X L, Zeng D L, Li J Y, Zhou Y H.2010. Brittle Culm 12, a dual-targeting kinesin-4 protein, controls cell-cycle progression and wall properties in rice. Plant J, 63(2): 312-328. |
| [41] | Zhang Q, Shen B Z, Dai X K, Mei M H, Saghai Maroof M A, Li Z B.1994. Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice.Proc Natl Acad Sci USA, 91(18): 8675-8679. |
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