Research Progress in Biological Functions of SPL Family Transcription Factors in Rice

doi:10.16819/j.1001-7216.2024.230308

Abstract

Abstract:

SPL (Squamosa Promoter-binding protein-like) family proteins are plant specific multifunctional transcription factors. There are 19 OsSPL genes in rice, all of which contain a highly conserved SBP domain, which is responsible for binding to the core motif GTAC of the downstream target gene to regulate the target gene expression. The expression of OsSPL is regulated by OsmiR156/529/535 and various factors. Studies have shown that OsSPL plays important roles in many biological processes of rice, including root development, ligule and auricles development, the formation of plant architecture and panicle morphology, grain development and stress response, and is a regulatory hub for rice growth and development. In this review, we summarized the research progress of the OsSPL family in rice, including its phylogenetic evolution, structural characteristics, expression regulation and biological functions, and the research prospects were also discussed.

Key words: OsSPL, transcription factor, OsmiR156, expression regulation, biological function

摘要：

SPL (SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE)家族蛋白是植物特有的一类多功能转录因子。水稻中有19个OsSPL基因，所编码蛋白均含有一个高度保守的SBP结构域，该结构域负责与下游靶基因的核心基序GTAC结合，调控靶基因表达。OsSPL的表达会受到OsmiR156/529/535和多种因子调控。研究表明OsSPL在水稻根系发育、叶舌叶耳发育、株型和穗型形成、籽粒发育和胁迫响应等多个生物学过程中发挥重要作用，是水稻生长发育的调控枢纽。本文综述了水稻OsSPL家族的系统进化与结构特征、表达调控及生物学功能研究进展，并对其研究前景进行了展望。

关键词: OsSPL, 转录因子, OsmiR156, 表达调控, 生物学功能

HU Li, YANG Fanmin, CHEN Weilan, YUAN Hua. Research Progress in Biological Functions of SPL Family Transcription Factors in Rice[J]. Chinese Journal OF Rice Science, 2024, 38(3): 223-232.

胡丽, 杨范敏, 陈薇兰, 袁华. 水稻SPL家族转录因子的生物学功能研究进展[J]. 中国水稻科学, 2024, 38(3): 223-232.

Figures/Tables 4

References 67

[1]	Klein J, Saedler H, Huijser P. A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA[J]. Molecular and General Genetics, 1996, 250(1): 7-16.
[2]	陈婉冰, 周波. SPL调控因子在植物生长调控的研究进展[J]. 分子植物育种, 2020, 18(5): 1505-1512.
	Chen W B, Zhou B. Research progress on SPL regulatory factor in plant growth regulation[J]. Molecular Plant Breeding, 2020, 18(5): 1505-1512. (in Chinese with English abstract)
[3]	Xie K, Wu C, Xiong L. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice[J]. Plant Physiology, 2006, 142(1): 280-293.
[4]	Jiang M, He Y, Chen X, Zhang X, Guo Y, Yang S, Huang J, Traw M B. CRISPR-based assessment of genomic structure in the conserved SQUAMOSA promoter-binding-like gene clusters in rice[J]. Plant Journal, 2020, 104(5): 1301-1314.
[5]	陈广龙. 水稻PPR和SPL基因家族及OsSPL4基因的功能分析[D]. 武汉: 武汉大学, 2019.
	Chen G L. Function analyses of the PPR and SPL gene family and OsSPL4 gene in rice[D]. Wuhan: Wuhan University, 2019. (in Chinese with English abstract)
[6]	Wang H, Wang H. The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits[J]. Molecular plant, 2015, 8(5): 677-688.
[7]	Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E, Ishizuka Y, Terada T, Shirouzu M, Osanai T, Tanaka A, Seki M, Shinozaki K, Yokoyama S. A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors[J]. Journal of Molecular Biology, 2004, 337(1): 49-63.
[8]	李明, 李长生, 赵传志, 李爱芹, 王兴军. 植物SPL转录因子研究进展[J]. 植物学报, 2013, 48(1): 107-116.
	Li M, Li C S, Zhao C Z, Li A Q, Wang X J. Research advances in plant SPL transcription factors[J]. Chinese Bulletin of Botany, 2013, 48(1): 107-116. (in Chinese with English abstract)
[9]	Birkenbihl R P, Jach G, Saedler H, Huijser P. Functional dissection of the plant-specific SBP-domain: Overlap of the DNA-binding and nuclear localization domains[J]. Journal of Molecular Biology, 2005, 352(3): 585-596.
[10]	Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C. Comparative study of SBP-box gene family in Arabidopsis and rice[J]. Gene, 2008, 407(1-2): 1-11.
[11]	Tang M, Zhou C, Meng L, Mao D, Peng C, Zhu Y, Huang D, Tan Z, Chen C, Liu C, Zhang D. Overexpression of OsSPL9 enhances accumulation of Cu in rice grain and improves its digestibility and metabolism[J]. Journal of Genetics and Genomics, 2016, 43(11): 673-676.
[12]	Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q, Zhang G, Fu X. Control of grain size, shape and quality by OsSPL16 in rice[J]. Nature Genetics, 2012, 44(8): 950-954.
[13]	Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q, Fu X, Wang Y, Li J. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture[J]. Plant Cell, 2013, 25(10): 3743-3759.
[14]	Yuan H, Qin P, Hu L, Zhan S, Wang S, Gao P, Li J, Jin M, Xu Z, Gao Q, Du A, Tu B, Chen W, Ma B, Wang Y, Li S. OsSPL18 controls grain weight and grain number in rice[J]. Journal of Genetics and Genomics, 2019, 46(1): 41-51.
[15]	Zhang X F, Yang C Y, Lin H X, Wang J W, Xue H W. Rice SPL12 coevolved with GW5 to determine grain shape[J]. Science Bulletin, 2021, 66(23): 2353-2357.
[16]	Yue E, Li C, Li Y, Liu Z, Xu J H. MiR529a modulates panicle architecture through regulating SQUAMOSA PROMOTER BINDING-LIKE genes in rice (Oryza sativa)[J]. Plant Molecular Biology, 2017, 94(4-5): 469-480.
[17]	Zhang L L, Huang Y Y, Zheng Y P, Liu X X, Zhou S X, Yang X M, Liu S L, Li Y, Li J L, Zhao S L, Wang H, Ji Y P, Zhang J W, Pu M, Zhao Z X, Fan J, Wang W M. Osa-miR535 targets SQUAMOSA promoter binding protein-like 4 to regulate blast disease resistance in rice[J]. Plant Journal, 2022, 110(1): 166-178.
[18]	Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C, Wang F, Huang H, Fu X. The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality[J]. Nature Genetics, 2015, 47(8): 949-954.
[19]	Wang H, Li Y, Chern M, Zhu Y, Zhang L L, Lu J H, Li X P, Dang W Q, Ma X C, Yang Z R, Yao S Z, Zhao Z X, Fan J, Huang Y Y, Zhang J W, Pu M, Wang J, He M, Li W T, Chen X W, Wu X J, Li S G, Li P, Li Y, Ronald P C, Wang W M. Suppression of rice miR168 improves yield, flowering time and immunity[J]. Nature Plants, 2021, 7(2): 129-136.
[20]	Yan Y, Wei M, Li Y, Tao H, Wu H, Chen Z, Li C, Xu J H. MiR529a controls plant height, tiller number, panicle architecture and grain size by regulating SPL target genes in rice (Oryza sativa L.)[J]. Plant Science, 2021, 302(110728.
[21]	Sun M, Shen Y, Li H, Yang J, Cai X, Zheng G, Zhu Y, Jia B, Sun X. The multiple roles of OsmiR535 in modulating plant height, panicle branching and grain shape[J]. Plant Science, 2019, 283(60-69.
[22]	Duan E, Wang Y, Li X, Lin Q, Zhang T, Wang Y, Zhou C, Zhang H, Jiang L, Wang J, Lei C, Zhang X, Guo X, Wang H, Wan J. OsSHI1 regulates plant architecture through modulating the transcriptional activity of IPA1 in rice[J]. Plant Cell, 2019, 31(5): 1026-1042.
[23]	Song X, Lu Z, Yu H, Shao G, Xiong J, Meng X, Jing Y, Liu G, Xiong G, Duan J, Yao X F, Liu C M, Li H, Wang Y, Li J. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice[J]. Cell Research, 2017, 27(9): 1128-1141.
[24]	Zhang L, Yu H, Ma B, Liu G, Wang J, Wang J, Gao R, Li J, Liu J, Xu J, Zhang Y, Li Q, Huang X, Xu J, Li J, Qian Q, Han B, He Z, Li J. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice[J]. Nature Communications, 2017, 8: 14789.
[25]	Wang J, Yu H, Xiong G, Lu Z, Jiao Y, Meng X, Liu G, Chen X, Wang Y, Li J. Tissue-specific ubiquitination by IPA1 INTERACTING PROTEIN1 modulates IPA1 protein levels to regulate plant architecture in rice[J]. Plant Cell, 2017, 29(4): 697-707.
[26]	Wang S, Wu K, Qian Q, Liu Q, Li Q, Pan Y, Ye Y, Liu X, Wang J, Zhang J, Li S, Wu Y, Fu X. Non-canonical regulation of SPL transcription factors by a human OTUB1-like deubiquitinase defines a new plant type rice associated with higher grain yield[J]. Cell Research, 2017, 27(9): 1142-1156.
[27]	Jia M, Luo N, Meng X, Song X, Jing Y, Kou L, Liu G, Huang X, Wang Y, Li J, Wang B, Yu H. OsMPK4 promotes phosphorylation and degradation of IPA1 in response to salt stress to confer salt tolerance in rice[J]. Journal of Genetics and Genomics, 2022, 49(8): 766-775.
[28]	Jia M, Meng X, Song X, Zhang D, Kou L, Zhang J, Jing Y, Liu G, Liu H, Huang X, Wang Y, Yu H, Li J. Chilling-induced phosphorylation of IPA1 by OsSAPK6 activates chilling tolerance responses in rice[J]. Cell Discovery, 2022, 8(1): 71.
[29]	Yue E, Liu Z, Li C, Li Y, Liu Q, Xu J H. Overexpression of miR529a confers enhanced resistance to oxidative stress in rice (Oryza sativa L.)[J]. Plant Cell Reports, 2017, 36(7): 1171-1182.
[30]	Shao Y, Zhou H Z, Wu Y, Zhang H, Lin J, Jiang X, He Q, Zhu J, Li Y, Yu H, Mao C. OsSPL3, an SBP-domain protein, regulates crown root development in rice[J]. Plant Cell, 2019, 31(6): 1257-1275.
[31]	Zhou M, Tang W. MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells[J]. Molecular Genetics and Genomics, 2019, 294(2): 379-393.
[32]	Hu J, Zeng T, Xia Q, Huang L, Zhang Y, Zhang C, Zeng Y, Liu H, Zhang S, Huang G, Wan W, Ding Y, Hu F, Yang C, Chen L, Wang W. Identification of key genes for the ultrahigh yield of rice using dynamic cross-tissue network analysis[J]. Genomics Proteomics Bioinformatics, 2020, 18(3): 256-270.
[33]	Hu J, Huang L, Chen G, Liu H, Zhang Y, Zhang R, Zhang S, Liu J, Hu Q, Hu F, Wang W, Ding Y. The elite alleles of OsSPL4 regulate grain size and increase grain yield in rice[J]. Rice, 2021, 14(1): 90.
[34]	Wang Q L, Sun A Z, Chen S T, Chen L S, Guo F Q. SPL6 represses signalling outputs of ER stress in control of panicle cell death in rice[J]. Nature Plants, 2018, 4(5): 280-288.
[35]	Dai Z, Wang J, Yang X, Lu H, Miao X, Shi Z. Modulation of plant architecture by the miR156f- OsSPL7-OsGH3.8 pathway in rice[J]. Journal of Experimental Botany, 2018, 69(21): 5117-5130.
[36]	Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, Xu C, Li X, Xiao J, Zhang Q. Coordinated regulation of vegetative and reproductive branching in rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(50): 15504-15509.
[37]	Wang L, Ming L, Liao K, Xia C, Sun S, Chang Y, Wang H, Fu D, Xu C, Wang Z, Li X, Xie W, Ouyang Y, Zhang Q, Li X, Zhang Q, Xiao J, Zhang Q. Bract suppression regulated by the miR156/529-SPLs-NL1-PLA1 module is required for the transition from vegetative to reproductive branching in rice[J]. Molecular Plant, 2021, 14(7): 1168-1184.
[38]	Lee J, Park J J, Kim S L, Yim J, An G. Mutations in the rice liguleless gene result in a complete loss of the auricle, ligule, and laminar joint[J]. Plant Molecular Biology, 2007, 65(4): 487-499.
[39]	Ishii T, Numaguchi K, Miura K, Yoshida K, Thanh P T, Htun T M, Yamasaki M, Komeda N, Matsumoto T, Terauchi R, Ishikawa R, Ashikari M. OsLG1 regulates a closed panicle trait in domesticated rice[J]. Nature Genetics, 2013, 45(4): 462-465, 465e461-462.
[40]	Zhu Z, Tan L, Fu Y, Liu F, Cai H, Xie D, Wu F, Wu J, Matsumoto T, Sun C. Genetic control of inflorescence architecture during rice domestication[J]. Nature Communications, 2013, 4(1): 2200.
[41]	Yao S, Yang Z, Yang R, Huang Y, Guo G, Kong X, Lan Y, Zhou T, Wang H, Wang W, Cao X, Wu J, Li Y. Transcriptional regulation of miR528 by OsSPL9 orchestrates antiviral response in rice[J]. Molecular Plant, 2019, 12(8): 1114-1122.
[42]	Yao S, Kang J, Guo G, Yang Z, Huang Y, Lan Y, Zhou T, Wang L, Wei C, Xu Z, Li Y. The key micronutrient copper orchestrates broad-spectrum virus resistance in rice[J]. Science Advances, 2022, 8(26): eabm0660.
[43]	Hu L, Chen W, Yang W, Li X, Zhang C, Zhang X, Zheng L, Zhu X, Yin J, Qin P, Wang Y, Ma B, Li S, Yuan H, Tu B. OsSPL9 regulates grain number and grain yield in rice[J]. Frontiers in Plant Science, 2021, 12: 682018.
[44]	Lan T, Zheng Y, Su Z, Yu S, Song H, Zheng X, Lin G, Wu W. OsSPL10, a SBP-box gene, plays a dual role in salt tolerance and trichome formation in rice (Oryza sativa L.)[J]. G3 (Bethesda), 2019, 9(12): 4107-4114.
[45]	Li J, Tang B, Li Y, Li C, Guo M, Chen H, Han S, Li J, Lou Q, Sun W, Wang P, Guo H, Ye W, Zhang Z, Zhang H, Yu S, Zhang L, Li Z. Rice SPL10 positively regulates trichome development through expression of HL6 and auxin-related genes[J]. Journal of Integrative Plant Biology, 2021, 63(8): 1521-1537.
[46]	Li Y, Han S, Sun X, Khan N U, Zhong Q, Zhang Z, Zhang H, Ming F, Li Z, Li J. Variations in OsSPL10 confer drought tolerance by directly regulating OsNAC2 expression and ROS production in rice[J]. Journal of Integrative Plant Biology, 2022, 65(4): 918-933.
[47]	Qin M, Zhang Y, Yang Y, Miao C, Liu S. Seed-specific overexpression of SPL12 and IPA1 improves seed dormancy and grain size in rice[J]. Frontiers in Plant Science, 2020, 11: 532771.
[48]	Si L, Chen J, Huang X, Gong H, Luo J, Hou Q, Zhou T, Lu T, Zhu J, Shangguan Y, Chen E, Gong C, Zhao Q, Jing Y, Zhao Y, Li Y, Cui L, Fan D, Lu Y, Weng Q, Wang Y, Zhan Q, Liu K, Wei X, An K, An G, Han B. OsSPL13 controls grain size in cultivated rice[J]. Nature Genetics, 2016, 48(4): 447-456.
[49]	Sun H, Guo X, Qi X, Feng F, Xie X, Zhang Y, Zhao Q. SPL14/17 act downstream of strigolactone signalling to modulate rice root elongation in response to nitrate supply[J]. Plant Journal, 2021, 106(3): 649-660.
[50]	Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice[J]. Nature Genetics, 2010, 42(6): 541-544.
[51]	Miura K, Ikeda M, Matsubara A, Song X J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M. OsSPL14 promotes panicle branching and higher grain productivity in rice[J]. Nature Genetics, 2010, 42(6): 545-549.
[52]	Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J, Zhu X, Li Y, Li W, Liu J, Wang J, Chen X, Qing H, Wang Y, Liu G, Wang W, Li P, Wu X, Zhu L, Zhou J M, Ronald P C, Li S, Li J, Chen X. A single transcription factor promotes both yield and immunity in rice[J]. Science, 2018, 361(6406): 1026-1028.
[53]	Chen F, Zhang H, Li H, Lian L, Wei Y, Lin Y, Wang L, He W, Cai Q, Xie H, Zhang H, Zhang J. IPA1 improves drought tolerance by activating SNAC1 in rice[J]. BMC Plant Biology, 2023, 23(1): 55.
[54]	Sun Y, Fu M, Wang L, Bai Y, Fang X, Wang Q, He Y, Zeng H. OsSPLs regulate male fertility in response to different temperatures by flavonoid biosynthesis and tapetum PCD in PTGMS rice[J]. International Journal of Molecular Sciences, 2022, 23(7): 3744.
[55]	Moreno M A, Harper L C, Krueger R W, Dellaporta S L, Freeling M. Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis[J]. Genes & Development, 1997, 11(5): 616-628.
[56]	Rossini L, Vecchietti A, Nicoloso L, Stein N, Franzago S, Salamini F, Pozzi C. Candidate genes for barley mutants involved in plant architecture: an in silico approach[J]. Theoretical and Applied Genetics, 2006, 112(6): 1073-1085.
[57]	Li Y, He Y, Liu Z, Qin T, Wang L, Chen Z, Zhang B, Zhang H, Li H, Liu L, Zhang J, Yuan W. OsSPL14 acts upstream of OsPIN1b and PILS6b to modulate axillary bud outgrowth by fine-tuning auxin transport in rice[J]. Plant Journal, 2022, 111(4): 1167-1182.
[58]	Duan P, Xu J, Zeng D, Zhang B, Geng M, Zhang G, Huang K, Huang L, Xu R, Ge S, Qian Q, Li Y. Natural Variation in the promoter of GSE5 contributes to grain size diversity in rice[J]. Molecular Plant, 2017, 10(5): 685-694.
[59]	秦苗苗. 水稻SPL家族基因SPL12调控种子休眠及作用机理研究[D]. 杭州: 浙江农林大学, 2020.
	Qin M M. Study on a member SPL12 of SQUAMOSA promoter binding protein-like gene family in regulating seed dormancy in rice[D]. Hangzhou: Zhejiang A&F University, 2020. (in Chinese with English abstract)
[60]	宋海冰. 水稻OsSPL10基因的功能分析[D]. 福州: 福建农林大学, 2017.
	Song H B. Functional analysis of OsSPL10 in rice[D]. Fuzhou: Fujian Agriculture and Forestry University, 2017. (in Chinese with English abstract)
[61]	Yang R, Li P, Mei H, Wang D, Sun J, Yang C, Hao L, Cao S, Chu C, Hu S, Song X, Cao X. Fine-tuning of MiR528 accumulation modulates flowering time in rice[J]. Molecular Plant, 2019, 12(8): 1103-1113.
[62]	Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Lu Y, Weng Q, Han B. Genomic architecture of heterosis for yield traits in rice[J]. Nature, 2016, 537(7622): 629-633.
[63]	Takatsuji H. Regulating tradeoffs to improve rice production[J]. Frontiers in Plant Science, 2017, 8: 171.
[64]	Wang J, Long X, Chern M, Chen X. Understanding the molecular mechanisms of trade-offs between plant growth and immunity[J]. Science China-Life Sciences, 2021, 64(2): 234-241.
[65]	Wang L, Wang D, Yang Z, Jiang S, Qu J, He W, Liu Z, Xing J, Ma Y, Lin Q, Yu F. Roles of FERONIA-like receptor genes in regulating grain size and quality in rice[J]. Science China-Life Sciences, 2021, 64(2): 294-310.
[66]	Wang L, Zhang Q. Boosting rice yield by fine-tuning SPL gene expression[J]. Trends in Plant Science, 2017, 22(8): 643-646.
[67]	Song X, Meng X, Guo H, Cheng Q, Jing Y, Chen M, Liu G, Wang B, Wang Y, Li J, Yu H. Targeting a gene regulatory element enhances rice grain yield by decoupling panicle number and size[J]. Nature Biotechnology, 2022, 40(9): 1403-1411.

基因名称 Gene name	基因号 Gene ID	染色体 Chr.	miRNA靶位点 miRNA target	生物学功能 Biological function	参考文献 Reference
OsSPL1	LOC_Os01g18850	1	/	未知
OsSPL2	LOC_Os01g69830	1	miRNA156/529	调控分蘖和穗分枝；负调控水稻氧化胁迫耐性	[16,29]
OsSPL3	LOC_Os02g04680	2	miRNA156	抑制不定根发育；负调控水稻低温耐性	[30,31]
OsSPL4	LOC_Os02g07780	2	miRNA156/535	调控穗粒数和粒型；正调控稻瘟病抗性	[17,32,33]
OsSPL5	LOC_Os02g08070	2	/	未知
OsSPL6	LOC_Os03g61760	3	/	控制穗顶端细胞死亡	[34]
OsSPL7	LOC_Os04g46580	4	miRNA156/529/535	调控株高、分蘖、穗粒数、根系发育；抑制穗部苞片生长	[35⇓-37]
OsSPL8	LOC_Os04g56170	4	/	调控叶舌叶耳发育，正调控穗分枝角度	[38⇓-40]
OsSPL9	LOC_Os05g33810	5	/	正调控穗粒数、铜吸收；负调控水稻条纹病毒抗性；	[11,41⇓ -43]
OsSPL10	LOC_Os06g44860	6	/	负调控水稻耐盐性和耐旱性；正调控毛状体形成	[44⇓-46]
OsSPL11	LOC_Os06g45310	6	miRNA156	未知
OsSPL12	LOC_Os06g49010	6	miRNA156/535	抑制不定根发育，增强种子休眠；负调控粒宽	[15,30,47]
OsSPL13	LOC_Os07g32170	7	miRNA156	正调控穗粒数，粒长和粒厚	[48]
OsSPL14	LOC_Os08g39890	8	miRNA156/529/535	调控分蘖和穗粒数、稻瘟病抗性，响应氮供应、种子休眠；抑制穗部苞片生长；负调控水稻耐盐性，正调控耐冷性和耐旱性	[24,25,27⇓ -29,37,49⇓⇓⇓ -53]
OsSPL15	LOC_Os08g40260	8	/	未知
OsSPL16	LOC_Os08g41940	8	miRNA156/529/535	正调控粒宽和灌浆；负调控穗分枝和稻米外观品质	[12,18]
OsSPL17	LOC_Os09g31438	9	miRNA156/529	调控分蘖和穗粒数；抑制穗部苞片生长；响应氮供应；调控水稻雄性育性	[36,37,54]
OsSPL18	LOC_Os09g32944	9	miRNA156/529	负调控分蘖，正调控穗粒数、粒宽和粒厚	[14]
OsSPL19	LOC_Os11g30370	11	miRNA156	未知

基因名称 Gene name	基因号 Gene ID	染色体 Chr.	miRNA靶位点 miRNA target	生物学功能 Biological function	参考文献 Reference
OsSPL1	LOC_Os01g18850	1	/	未知
OsSPL2	LOC_Os01g69830	1	miRNA156/529	调控分蘖和穗分枝；负调控水稻氧化胁迫耐性	[16,29]
OsSPL3	LOC_Os02g04680	2	miRNA156	抑制不定根发育；负调控水稻低温耐性	[30,31]
OsSPL4	LOC_Os02g07780	2	miRNA156/535	调控穗粒数和粒型；正调控稻瘟病抗性	[17,32,33]
OsSPL5	LOC_Os02g08070	2	/	未知
OsSPL6	LOC_Os03g61760	3	/	控制穗顶端细胞死亡	[34]
OsSPL7	LOC_Os04g46580	4	miRNA156/529/535	调控株高、分蘖、穗粒数、根系发育；抑制穗部苞片生长	[35⇓-37]
OsSPL8	LOC_Os04g56170	4	/	调控叶舌叶耳发育，正调控穗分枝角度	[38⇓-40]
OsSPL9	LOC_Os05g33810	5	/	正调控穗粒数、铜吸收；负调控水稻条纹病毒抗性；	[11,41⇓ -43]
OsSPL10	LOC_Os06g44860	6	/	负调控水稻耐盐性和耐旱性；正调控毛状体形成	[44⇓-46]
OsSPL11	LOC_Os06g45310	6	miRNA156	未知
OsSPL12	LOC_Os06g49010	6	miRNA156/535	抑制不定根发育，增强种子休眠；负调控粒宽	[15,30,47]
OsSPL13	LOC_Os07g32170	7	miRNA156	正调控穗粒数，粒长和粒厚	[48]
OsSPL14	LOC_Os08g39890	8	miRNA156/529/535	调控分蘖和穗粒数、稻瘟病抗性，响应氮供应、种子休眠；抑制穗部苞片生长；负调控水稻耐盐性，正调控耐冷性和耐旱性	[24,25,27⇓ -29,37,49⇓⇓⇓ -53]
OsSPL15	LOC_Os08g40260	8	/	未知
OsSPL16	LOC_Os08g41940	8	miRNA156/529/535	正调控粒宽和灌浆；负调控穗分枝和稻米外观品质	[12,18]
OsSPL17	LOC_Os09g31438	9	miRNA156/529	调控分蘖和穗粒数；抑制穗部苞片生长；响应氮供应；调控水稻雄性育性	[36,37,54]
OsSPL18	LOC_Os09g32944	9	miRNA156/529	负调控分蘖，正调控穗粒数、粒宽和粒厚	[14]
OsSPL19	LOC_Os11g30370	11	miRNA156	未知