MULTI-FLORET SPIKELET 4 (MFS4) Regulates Spikelet Development and Grain Size in Rice
#These authors contributed equally to this work
Received date: 2020-08-27
Accepted date: 2020-11-17
Online published: 2021-07-28
In rice, the spikelet is the basic unit of inflorescence, and its development is important for determining the grain yield and quality. We reported a rice spikelet mutant multi-floret spikelet 4 (mfs4) which resulted in the production of extra floral organs or a whole extra floret, and elongated sterile lemmas. The results suggested that the mutation of the MFS4 gene interfered with spikelet meristem determinacy and floral organ identity. In addition, the plant height and the grain length and width in the mfs4 mutant were all less than those in the wild type. Using the bulked segregant analysis method, the MFS4 gene was localized in a 557-kb region on the long arm of chromosome 1. Sequence analysis showed that there was a C-base deletion at the open reading frame of LOC_Os01g67430. Further tests indicated that a wild type copy of LOC_Os01g67430 was able to reverse the mfs4 defects, which indicated that LOC_Os01g67430 was the MFS4 gene. The MFS4 gene encodes a lipase located in the mitochondria and is expressed strongly in the young inflorescence. qRT-PCR results showed that the expression of some genes that were known to regulate spikelet meristem determinacy and grain size were decreased in the mfs4 mutant, which indicated that the MFS4 gene regulates spikelet meristem determinacy and grain size by modulating the expression of these genes.
Key words： rice; sterile lemma; multi-floret spikelet; meristem; grain size
Yan Wang, Xiaoqin Zeng, Lu Lu, Qinglan Cheng, Fayu Yang, Mingjiang Huang, Mao Xiong, Yunfeng Li . MULTI-FLORET SPIKELET 4 (MFS4) Regulates Spikelet Development and Grain Size in Rice[J]. Rice Science, 2021 , 28(4) : 344 -357 . DOI: 10.1016/j.rsci.2021.05.005
| [1] | Arora R, Agarwal P, Ray S, Singh A K, Singh V P, Tyagi A K, Kapoor S. 2007. MADS-box gene family in rice: Genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genom, 8(1): 242. |
| [2] | Ashikari M, Sakakibara H, Lin S Y, Yamamoto T, Takashi T, Nishimura A, Angeles E R, Qian Q, Kitano H, Matsuoka M. 2005. Cytokinin oxidase regulates rice grain production. Science, 309: 741?745. |
| [3] | Aya K, Hobo T, Sato-Izawa K, Ueguchi-Tanaka M, Kitano H, Matsuoka M. 2014. A novel AP2-type transcription factor, SMALL ORGAN SIZE1, controls organ size downstream of an auxin signaling pathway. Plant Cell Physiol, 55(5): 897-912. |
| [4] | Cai Q, Yuan Z, Chen M J, Yin C S, Luo Z J, Zhao X X, Liang W Q, Hu J P, Zhang D B. 2014. Jasmonic acid regulates spikelet development in rice. Nat Commun, 5: 3476. |
| [5] | Chuck G, Meeley R, Hake S. 2008. Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1. Development, 135(18): 3013-3019. |
| [6] | Deng Z Y, Liu L T, Li T, Yan S, Kuang B J, Huang S J, Yan C J, Wang T. 2015. OsKinesin-13A is an active microtubule depolymerase involved in glume length regulation via affecting cell elongation. Sci Rep, 5: 9457. |
| [7] | Dong N Q, Sun Y W, Guo T, Shi C L, Zhang Y M, Kan Y, Xiang Y H, Zhang H, Yang Y B, Li Y C, Zhao H Y, Yu H X, Lu Z Q, Wang Y, Ye W W, Shan J X, Lin H X. 2020. UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice. Nat Commun, 11(1): 2629. |
| [8] | Duan P G, Ni S, Wang J M, Zhang B L, Xu R, Wang Y X, Chen H Q, Zhu X D, Li Y H. 2016. Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat Plants, 2(1): 1-5. |
| [9] | Feng Z M, Wu C Y, Wang C M, Roh J, Zhang L, Chen J, Zhang S Z, Zhang H, Yang C Y, Hu J L, You Xi M, Liu X, Yang X M, Guo X P, Zhang X, Wu F Q, Terzaghi W, Kim S K, Jiang L, Wan J M. 2016. SLG controls grain size and leaf angle by modulating brassinosteroid homeostasis in rice. J Exp Bot, 67(14): 4241-4253. |
| [10] | Guo T, Lu Z Q, Shan J X, Ye W W, Dong N Q, Lin H X. 2020. ERECTA1 acts upstream of the OsMKKK10-OsMKK4- OsMPK6 cascade to control spikelet number by regulating cytokinin metabolism in rice. Plant Cell, 32(9): 2763-2779. |
| [11] | Heang D, Sassa H. 2012a. Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice. PLoS One, 7(2): e31325. |
| [12] | Heang D, Sassa H. 2012b. An atypical bHLH protein encoded by POSITIVE REGULATOR OF GRAIN LENGTH 2 is involved in controlling grain length and weight of rice through interaction with a typical bHLH protein APG. Breeding Sci, 62(2): 133-141. |
| [13] | 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(10): 1455-1465. |
| [14] | 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(5): 849-860. |
| [15] | Huang X Z, Qian Q, Liu Z B, Sun H Y, He S Y, Luo D, Xia G M, Chu C C, Li J Y, Fu X D. 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet, 41(4): 494-497. |
| [16] | Ikeda K, Sunohara H, Nagato Y. 2004. Developmental course of inflorescence and spikelet in rice. Breeding Sci, 54(2): 147-156. |
| [17] | 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 gene TGW6 enhances rice grain weight and increases yield. Nat Genet, 45(6): 707-713. |
| [18] | Jeon J S, Jang S, Lee S, Nam J, Kim C, Lee S H, Chung Y Y, Kim S R, Lee Y H, Cho Y G, An G. 2000. leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell, 12(6): 871-884. |
| [19] | Jin Y, Luo Q, Tong H N, Wang A J, Cheng Z J, Tang J F, Li D Y, Zhao X F, Li X B, Wan J M, Jiao Y L, Chu C C, Zhu L H. 2011. An AT-hook gene is required for palea formation and floral organ number control in rice. Develop Biol, 359(2): 277-288. |
| [20] | 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. |
| [21] | La H G, Li J, Ji Z D, Cheng Y J, Li X L, Jiang S Y, Venkatesh P N, Ramachandran S. 2006. Genome-wide analysis of cyclin family in rice (Oryza sativa L.). Mol Genet Genom, 275(4): 374-386. |
| [22] | Lee D Y, An G. 2012. Two AP2 family genes, SUPERNUMERARY BRACT (SNB) and OsINDETERMINATE SPIKELET 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J, 69(3): 445-461. |
| [23] | Lee D Y, Lee J, Moon S, Park S Y, An G. 2007. The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J, 49(1): 64-78. |
| [24] | Li H F, Liang W Q, Jia R D, Yin C S, Zong J, Kong H Z, Zhang D B. 2010. The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Res, 20(3): 299-313. |
| [25] | Li H G, Xue D W, Gao Z Y, Yan M X, Xu W Y, Xing Z, Huang D N, Qian Q, Xue Y B. 2009. A putative lipase gene EXTRA GLUME1 regulates both empty-glume fate and spikelet development in rice. Plant J, 57(4): 593-605. |
| [26] | Li X J, Sun L J, Tan L B, Liu F, Zhu Z F, Fu Y C, Sun X Y, Sun X W, Xie D X, Sun C Q. 2012. TH1, a DUF640 domain-like gene controls lemma and palea development in rice. Plant Mol Biol, 78(4/5): 351-359. |
| [27] | Li Y B, Fan C C, Xing Y Z, Jiang Y H, Luo L J, Sun L, Shao D, Xu C J, Li X H, Xiao J H, He Y Q, Zhang Q F. 2011. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet, 43(12): 1266-1270. |
| [28] | Li Y F, Zeng X Q, Li Y, Wang L, Zhuang H, Wang Y, Tang J, Wang H L, Xiong M, Yang F Y, Yuan X Z, He G H. 2020. MULTI-FLORET SPIKELET 2, a MYB transcription factor, determines spikelet meristem fate and floral organ identity in rice. Plant Physiol, 184: 988?1003. |
| [29] | Ma X D, Cheng Z J, Wu F Q, Jin M G, Zhang L G, Zhou F, Wang J L, Zhou K N, Ma J, Lin Q B, Lei C L, Wan J M. 2013. BEAK LIKE SPIKELET1 is required for lateral development of lemma and palea in rice. Plant Mol Biol Rep, 31(1): 98-108. |
| [30] | Malcomber S T, Preston J C, Reinheimer R, Kossuth J, Kellogg E A. 2006. Developmental gene evolution and the origin of grass inflorescence diversity. Adv Bot Res, 44: 425?481. |
| [31] | Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y. 2003. SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development, 130(4): 705-718. |
| [32] | Ren D Y, Li Y F, Zhao F M, Sang X C, Shi J Q, Wang N, Guo S, Ling Y H, Zhang C W, Yang Z L, He G H. 2013. MULTI- FLORET SPIKELET1, which encodes an AP2/ERF protein, determines spikelet meristem fate and sterile lemma identity in rice. Plant Physiol, 162(2): 872-884. |
| [33] | Ren D Y, Rao Y C, Wu L W, Xu Q K, Li Z Z, Yu H P, Zhang Y, Leng Y J, Hu J, Zhu L, Gao Z Y, Dong G J, Zhang G H, Guo L B, Zeng D L, Qian Q. 2016. The pleiotropic ABNORMAL FLOWER AND DWARF1 affects plant height, floral development and grain yield in rice. J Integr Plant Biol, 58(6): 529-539. |
| [34] | Ren D Y, Hu J, Xu Q K, Cui Y J, Zhang Y, Zhou T T, Rao Y C, Xue D W, Zeng D L, Zhang G H, Gao Z Y, Zhu L, Shen L, Chen G, Guo L B, Qian Q. 2018a. FZP determines grain size and sterile lemma fate in rice. J Exp Bot, 69(20): 4853-4866. |
| [35] | Ren D Y, Yu H P, Rao Y C, Xu Q K, Zhou T T, Hu J, Zhang Y, Zhang G H, Zhu L, Gao Z Y, Chen G, Guo L B, Zeng D L, Qian Q. 2018b. ‘Two-floret spikelet’ as a novel resource has the potential to increase rice yield. Plant Biotechnol J, 16(2): 351-353. |
| [36] | Ren D Y, Rao Y C, Yu H P, Xu Q K, Cui Y J, Xia S S, Yu X Q, Liu H, Hu H T, Xue D W, Zeng D L, Hu J, Zhang G H, Gao Z Y, Zhu L, Zhang Q, Shen L, Guo L B, Qian Q. 2020. MORE FLORET 1 encodes a MYB transcription factor that regulates spikelet development in rice. Plant Physiol, 184(1): 251-265. |
| [37] | Ruan B P, Shang L G, Zhang B, Hu J, Wang Y X, Lin H, Zhang A P, Liu C L, Peng Y L, Zhu L, Ren D Y, Shen L, Dong G J, Zhang G H, Zeng D L, Guo L B, Qian Q, Gao Z Y. 2020. Natural variation in the promoter of TGW2 determines grain width and weight in rice. New Phytol, 227(2): 629-640. |
| [38] | 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: 4. |
| [39] | 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. |
| [40] | Su’udi M, Cha J Y, Ahn I P, Kwak Y S, Woo Y M, Son D Y. 2012. Functional characterization of a B-type cell cycle switch 52 in rice (OsCCS52B). Plant Cell Tissue Organ Cult, 111(1): 101-111. |
| [41] | Wan X Y, Weng J F, Zhai H Q, Wang J K, Lei C L, Liu X L, Guo T, Jiang L, Su N, Wan J M. 2008. Quantitative trait loci (QTL) analysis for rice grain width and fine mapping of an identified QTL allele gw-5 in a recombination hotspot region on chromosome 5. Genetics, 179(4): 2239-2252. |
| [42] | Wang K J, Tang D, Hong L L, Xu W Y, Huang J, Li M, Gu M H, Xue Y B, Cheng Z K. 2010. DEP and AFO regulate reproductive habit in rice. PLoS Genet, 6(1): e1000818. |
| [43] | 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 by OsSPL16 in rice. Nat Genet, 44(8): 1-6. |
| [44] | Wu T, Shen Y Y, Zheng M, Yang C Y, Chen Y L, Feng Z M, Liu X, Liu S J, Chen Z J, Lei C L, Wang J L, Jiang L, Wan J M. 2014. Gene SGL, encoding a kinesin-like protein with transactivation activity, is involved in grain length and plant height in rice. Plant Cell Rep, 33(2): 235-244. |
| [45] | Xia D, Zhou H, Liu R J, Dan W H, Li P B, Wu B, Chen J X, Wang L Q, Gao G J, Zhang Q L, He Y Q. 2018. GL3.3, a novel QTL encoding a GSK3/SHAGGY-like kinase, epistatically interacts with GS3 to produce extra-long grains in rice. Mol Plant, 11(5): 754-756. |
| [46] | Xiong H Y, Yu J P, Miao J L, Li J J, Zhang H L, Wang X, Liu P L, Zhao Y, Jiang C H, Yin Z G, Li Y, Guo Y, Fu B Y, Wang W S, Li Z K, Ali J, Li Z C. 2018. Natural variation in OsLG3 increases drought tolerance in rice by inducing ROS scavenging. Plant Physiol, 178(1): 451-467. |
| [47] | Xue W Y, Xing Y Z, Weng X Y, Zhao Y, Tang W J, Wang L, Zhou H J, Yu S B, Xu C G, Li X H, Zhang Q F. 2008. Natural variation inGhd7 is an important regulator of heading date and yield potential in rice. Nat Genet, 40: 761. |
| [48] | Yan S, Zou G H, Li S J, Wang H, Liu H Q, Zhai G W, Guo P, Song H M, Yan C J, Tao Y Z. 2011. Seed size is determined by the combinations of the genes controlling different seed characteristics in rice. Theor Appl Genet, 123(7): 1173-1181. |
| [49] | Ying J Z, Ma M, Bai C, Huang X H, Liu J L, Fan Y Y, Song X J. 2018. TGW3, a major QTL that negatively modulates grain length and weight in rice. Mol Plant, 11(5): 750-753. |
| [50] | Yoshida A, Suzaki T, Tanaka W, Hirano H Y. 2009. The homeotic gene long sterile lemma (G1) specifies sterile lemma identity in the rice spikelet. Proc Natl Acad Sci USA, 106(47): 20103-20108. |
| [51] | Zhang B Y, Wu S H, Zhang Y E, Xu T, Guo F F, Tang H S, Li X, Wang P F, Qian W F, Xue Y B. 2016. A high temperature- dependent mitochondrial lipase EXTRA GLUME1 promotes floral phenotypic robustness against temperature fluctuation in rice (Oryza sativa L.). PLoS Genet, 12(7): e1006152. |
| [52] | Zhang L, Yu H, Ma B, Liu G F, Wang J J, Wang J M, Gao R C, Li J J, Liu J Y, Xu J, Zhang Y Y, Li Q, Huang X H, Xu J L, Li J M, Qian Q, Han B, He Z H, Li J Y. 2017. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun, 8(1): 14789. |
| [53] | Zheng H, Zhang J, Zhuang H, Zeng X Q, Tang J, Wang H L, Chen H, Li Y, Ling Y H, He G H, Li Y F. 2019. Gene mapping and candidate gene analysis of multi-floret spikelet 3 (mfs3) in rice (Oryza sativa L.). J Integr Agric, 18(12): 2673-2681. |
| [54] | Zhu Q H, Upadhyaya N M, Gubler F, Helliwell C A. 2009. Over- expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol, 9: 149. |
/
| 〈 |
|
〉 |