生长素调控水稻生长发育的研究进展

doi:10.3969/j.issn.1006-8082.2024.01.001

摘要/Abstract

摘要：

生长素（auxin，IAA）是一种重要的植物生长激素，普遍存在于各种植物和藻类中，其参与组织分化、器官发生、形态建成、向性反应和顶端优势等生理过程以及对复杂环境适应过程。目前双子叶植物拟南芥中生长素调控生长发育的机制已经基本清楚，但是生长素怎样在单子叶植物水稻中行使功能，仍有很多未解之谜。本文综述了近20年国内外关于生长素调控单子叶植物水稻根、茎、叶、花和籽粒生长发育的细胞学和生理机制，重点归纳整理了生长素相关基因对水稻生长发育的分子调控机制，展望了未来水稻中依靠生长素途径精准合成运输生长素的调控，以及利用生长素突变体表型变异的开发前景。

关键词: 生长素, 水稻, 器官, 突变体表型, 精准调控

Abstract:

Auxin (IAA) is an important plant growth hormone that is ubiquitous in a variety of plants and algae. Auxin is involved in physiological processes such as tissue differentiation, organogenesis, morphological construction, tropism, and apical dominance. At present, the mechanism of auxin regulating growth and development in Arabidopsis thaliana dicotyledons is basically clear, but there are still many unsolved mysteries about how auxin functions in rice. In this paper, a series of biological events and physiological mechanisms of auxin regulating the growth and development of rice organs of monocots in the past two decades at home and abroad are reviewed, and the regulatory mechanism of auxin-related genes on rice organs is summarized, the precise synthesis of auxin in rice, relying on auxin pathway, and the use of auxin mutant phenotypic variation to develop plants in the future are prospected.

Key words: auxin, rice, organs, mutant phenotype, precise adjustment

中图分类号:

S511

喻梓轩, 刘新勇, 张健, 梁大成. 生长素调控水稻生长发育的研究进展[J]. 中国稻米, 2024, 30(1): 1-9.

YU Zixuan, LIU Xinyong, ZHANG Jian, LIANG Dacheng. Research Progress of Auxin Regulation on Growth and Development of Rice[J]. China Rice, 2024, 30(1): 1-9.

图/表 1

参考文献 87

[1]	MASUDA Y, KAMISAKA S. Discovery of auxin[M]// UNG S D, YANG S F. Discoveries In Plant Biology: Volume III. Singapore: World Scientific Publishing Co Pte Ltd, 2000: 43-57.
[2]	BENNETT K D. The power of movement in plants[J]. Trends in Ecology & Evolution, 1998, 13(9): 339-340.
[3]	BOYSEN JENSEN P. Uber die Leitung des phototropischen Reizes in Avenakeimpflanzen[J]. Berichte Der Deutschen Botanischen Gesellschaft, 1910, 28: 118-120.
[4]	PAAL A. Uber phototropische Reizleitungen[J]. Berichte Der Deutschen Botanischen Gesellschaft, 1914, 32: 499-502.
[5]	WENT F W. On growth-accelerating substances in the coleoptile of Avena sativa[C]. Proc Kon Akad Wetensch Amsterdam, 1926: 10-19.
[6]	KOGL F, HAAGEN-SMIT A. The Chemistry of the Growth Substance[J]. Proceedings Academy Science Amsterdam, 1931: 1 411-1 416.
[7]	KOGL F, HAAGEN-SMIT A, ERXLEBEN H. Uber ein neues Auxin (Hetero-auxin) aus Harn. 11[J]. Mitteilung Uber Pflanzliche Wachstumsstoffe, 1934: 90-103.
[8]	KOGL F, ERXEBEN H. Uber die Konstitution der Auxine a und b. 10[J]. Mitteilung Uber Pflanzliche Wachstumsstoffe, 1934: 51-73.
[9]	HAAGEN-SMIT A, LEECH W, BERGREN W. The estimation, isolation, and identification of auxins in plant materials[J]. American Journal of Botany, 1942: 500-506.
[10]	HAAGEN-SMIT A, DANDLIKER W, WITTWER S, et al. Isolation of 3-indoleacetic acid from immature corn kernels[J]. American Journal of Botany, 1946: 118-120.
[11]	KEY J L. Hormones and nucleic acid metabolism[J]. Annual Review of Plant Physiology, 1969, 20(1): 449-474.
[12]	RAYLE D L, CLELAND R E. The Acid Growth Theory of auxin-induced cell elongation is alive and well[J]. Plant Physiology, 1992, 99(4): 1 271-1 274.
[13]	HAGER A, MENZEL H, KRAUSS A. [Experiments and hypothesis concerning the primary action of auxin in elongation growth][J]. Planta, 1971, 100(1): 47-75.
[14]	VANDERHOEF L N, STAHL C A. Separation of two responses to auxin by means of cytokinin inhibition[J]. Proceedings of the National Academy of Sciences, 1975, 72(5): 1 822-1 825.
[15]	VANDERHOEF L N, STAHL C A, WILLIAMS C A, et al. Additional evidence for separable responses to auxin in soybean hypocotyl[J]. Plant Physiology, 1976, 57(5): 817-819.
[16]	LIN W, ZHOU X, TANG W, et al. TMK-based cell-surface auxin signalling activates cell-wall acidification[J]. Nature, 2021, 599(7884): 278-282.
[17]	LI L, VERSTRAETEN I, ROOSJEN M, et al. Cell surface and intracellular auxin signalling for H⁺ fluxes in root growth[J]. Nature, 2021, 599(7884): 273-277.
[18]	WANG Y, ZHANG T, WANG R, et al. Recent advances in auxin research in rice and their implications for crop improvement[J]. Journal of Experiment Botany, 2018, 69(2): 255-263.
[19]	ZHAO H, MA T, WANG X, et al. OsAUX 1 controls lateral root initiation in rice (Oryza sativa L.)[J]. Plant, Cell & Environment, 2015, 38(11): 2 208-2 222.
[20]	YU C, SUN C, SHEN C, et al. The auxin transporter, OsAUX1, is involved in primary root and root hair elongation and in Cd stress responses in rice (Oryza sativa L.)[J]. The Plant Journal, 2015, 83(5): 818-830.
[21]	GIRI J, BHOSALE R, HUANG G, et al. Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate[J]. Nature Communications, 2018, 9(1): 1-7.
[22]	WANG M, QIAO J, YU C, et al. The auxin influx carrier, OsAUX3, regulates rice root development and responses to aluminium stress[J]. Plant, Cell & Environment, 2019, 42(4): 1 125-1 138.
[23]	YE R, WU Y, GAO Z, et al. Primary root and root hair development regulation by OsAUX4 and its participation in the phosphate starvation response[J]. Journal of Integrative Plant Biology, 2021, 63(8): 1 555-1 567.
[24]	MIYASHITA Y, TAKASUGI T, ITO Y. Identification and expression analysis of PIN genes in rice[J]. Plant Science, 2010, 178(5): 424-428.
[25]	XU M, ZHU L, SHOU H X, et al. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice[J]. Plant and Cell Physiology, 2005, 46(10): 1 674-1 681.
[26]	LI P J, WANG Y H, QIAN Q, et al. LAZY1 controls rice shoot gravitropism through regulating polar auxin transport[J]. Cell Research, 2007, 17(5): 402-410.
[27]	SUN H W, TAO J Y, BI Y, et al. OsPIN1b is involved in rice seminal root elongation by regulating root apical meristem activity in response to low nitrogen and phosphate[J]. Scientific Reports, 2018, 8(1): 1-11.
[28]	QI Y H, WANG S K, SHEN C J, et al. OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa)[J]. New Phytologist, 2012, 193(1): 109-120.
[29]	INUKAI Y, SAKAMOTO T, UEGUCHI-TANAKA M, et al. Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling[J]. The Plant Cell, 2005, 17(5): 1 387-1 396.
[30]	KITOMI Y, OGAWA A, KITANO H, et al. CRL4 regulates crown root formation through auxin transport in rice[J]. Plant Root, 2008, 2: 19-28.
[31]	ZHANG G, XU N, CHEN H, et al. OsMADS25 regulates root system development via auxin signalling in rice[J]. The Plant Journal, 2018, 95(6): 1 004-1 022.
[32]	XU N, CHU Y, CHEN H, et al. Rice transcription factor OsMADS25 modulates root growth and confers salinity tolerance via the ABA-mediated regulatory pathway and ROS scavenging[J]. PLoS Genetics, 2018, 14(10): e1007662.
[33]	LI H, SUN H Y, JIANG J H, et al. TAC4 controls tiller angle by regulating the endogenous auxin content and distribution in rice[J]. Plant Biotechnology Journal, 2021, 19(1): 64-73.
[34]	JEONG D-H, PARK S, ZHAI J, et al. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage[J]. The Plant Cell, 2011, 23(12): 4 185-4 207.
[35]	YUE E, LI C, LI Y, et al. MiR529a modulates panicle architecture through regulating SQUAMOSA PROMOTER BINDING-LIKE genes in rice (Oryza sativa)[J]. Plant Molecular Biology, 2017, 94(4): 469-480.
[36]	LI Y, HE Y, LIU Z, et al. OsSPL14 acts upstream of OsPIN1b and PILS6b to modulate axillary bud outgrowth by fine‐tuning auxin transport in rice[J]. The Plant Journal, 2022, 111(4): 1 167-1 182.
[37]	ZHAO S Q, XIANG J J, XUE H W. Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control[J]. Molecular Plant, 2013, 6(1): 174-187.
[38]	ZHANG S N, WANG S K, XU Y X, et al. The auxin response factor, OsARF 19, controls rice leaf angles through positively regulating OsGH 3-5 and OsBRI 1[J]. Plant, Cell & Environment, 2015, 38(4): 638-654.
[39]	HUANG G Q, HU H, VAN DE MEENE A, et al. AUXIN RESPONSE FACTORS 6 and 17 control the flag leaf angle in rice by regulating secondary cell wall biosynthesis of lamina joints[J]. The Plant Cell, 2021, 33(9): 3 120-3 133.
[40]	QIAO J, ZHANG Y, HAN S, et al. OsARF4 regulates leaf inclination via auxin and brassinosteroid pathways in rice[J]. Frontiers in Plant Science, 2022, 13: 979 033.
[41]	HU Z, LU S J, WANG M J, et al. A novel QTL qTGW3 encodes the GSK3/SHAGGY-like kinase OsGSK5/OsSK41 that interacts with OsARF4 to negatively regulate grain size and weight in rice[J]. Molecular Plant, 2018, 11(5): 736-749.
[42]	LIN L, ZHAO Y, LIU F, et al. Narrow leaf1 (NAL1) regulates leaf shape by affecting cell expansion in rice (Oryza sativa L.)[J]. Biochemical and Biophysical Research Communications, 2019, 516(3): 957-962.
[43]	CHEN M, LUO J, SHAO G, et al. Fine mapping of a major QTL for flag leaf width in rice, qFLW4, which might be caused by alternative splicing of NAL1[J]. Plant Cell Reports, 2012, 31(5): 863-872.
[44]	SAZUKA T, KAMIYA N, NISHIMURA T, et al. A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos[J]. The Plant Journal, 2009, 60(2): 227-241.
[45]	SONG S, CHEN Y, LIU L, et al. OsFTIP7 determines auxin-mediated anther dehiscence in rice[J]. Nature Plants, 2018, 4(7): 495-504.
[46]	OHMORI S, KIMIZU M, SUGITA M, et al. MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice[J]. The Plant Cell, 2009, 21(10): 3 008-3 025.
[47]	AGRAWAL G K, ABE K, YAMAZAKI M, et al. Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene[J]. Plant Molecular Biology, 2005, 59(1): 125-135.
[48]	PRASAD K, PARAMESWARAN S, VIJAYRAGHAVAN U. OsMADS1, a rice MADS‐box factor, controls differentiation of specific cell types in the lemma and palea and is an early‐acting regulator of inner floral organs[J]. The Plant Journal, 2005, 43(6): 915-928.
[49]	KHANDAY I, YADAV S R, VIJAYRAGHAVAN U. Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways[J]. Plant Physiology, 2013, 161(4): 1 970-1 983.
[50]	PRASAD K, SRIRAM P, KUMAR S C, et al. Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals[J]. Development Genes and Evolution, 2001, 211(6): 281-290.
[51]	ATTIA K A, ABDELKHALIK A F, AMMAR M H, et al. Antisense phenotypes reveal a functional expression of OsARF1, an auxin response factor, in transgenic rice[J]. Current Issues in Molecular Biology, 2009, 11(S1): 29-34.
[52]	HUANG J, LI Z, ZHAO D. Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice[J]. Scientific Reports, 2016, 6(1): 1-14.
[53]	MORITA Y, KYOZUKA J. Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport[J]. Plant and Cell Physiology, 2007, 48(3): 540-549.
[54]	HE Y, YAN L, GE C, et al. PINOID is required for formation of the stigma and style in rice[J]. Plant Physiology, 2019, 180(2): 926-936.
[55]	XU M, TANG D, CHENG X, et al. OsPINOID regulates stigma and ovule initiation through maintenance of the floral meristem by auxin signaling[J]. Plant Physiology, 2019, 180(2): 952-965.
[56]	WU H M, XIE D J, TANG Z S, et al. PINOID regulates floral organ development by modulating auxin transport and interacts with MADS16 in rice[J]. Plant Biotechnology Journal, 2020, 18(8): 1 778-1 795.
[57]	ZHAO Z, WANG C, YU X, et al. Auxin regulates source-sink carbohydrate partitioning and reproductive organ development in rice[J]. Proceeding of National Academy of Science of the United States of America, 2022, 119(36): e2121671119.
[58]	YAMAMOTO Y, KAMIYA N, MORINAKA Y, et al. Auxin biosynthesis by the YUCCA genes in rice[J]. Plant Physiology, 2007, 143(3): 1 362-1 371.
[59]	XU Y X, XIAO M Z, LIU Y, et al. The small auxin-up RNA OsSAUR45 affects auxin synthesis and transport in rice[J]. Plant Molecular Biology, 2017, 94(1): 97-107.
[60]	ZHAO J, LI W, SUN S, et al. The rice small auxin-up RNA gene OsSAUR33 regulates seed vigor via sugar pathway during early seed germination[J]. International Journal of Molecular Sciences, 2021, 22(4): 1 562.
[61]	OVERVOORDE P, FUKAKI H, BEECKMAN T. Auxin control of root development[J]. Cold Spring Harbor Perspectives in Biology, 2010, 2(6): a001537.
[62]	SIEBERER T, LEYSER O. Auxin transport, but in which direction?[J]. Science, 2006, 312(5775): 858-860.
[63]	ROSS J J, O'NEILL D P, WOLBANG C M, et al. Auxin-gibberellin interactions and their role in plant growth[J]. Journal of Plant Growth Regulation, 2001, 20(4): 336-353.
[64]	YIN C X, GAN L J, DENNY N G, et al. Decreased panicle-derived indole-3-acetic acid reduces gibberellin A1 level in the uppermost internode, causing panicle enclosure in male sterile rice Zhenshan 97A[J]. Journal of Experimental Botany, 2007, 58(10): 2 441-2 449.
[65]	FERARU E, VOSOLSOBE S, FERARU M I, et al. Evolution and structural diversification of PILS putative auxin carriers in plants[J]. Frontiers in Plant Science, 2012, 3: 227.
[66]	BEZIAT C, BARBEZ E, FERARU M I, et al. Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition[J]. Nature Plants, 2021, 3: 17 105.
[67]	BOGAERT K A, BLOMME J, BEECKMAN T, et al. Auxin's origin: do PILS hold the key?[J]. Trends in Plant Science, 2022, 27(3): 227-236.
[68]	ZHOU L J, XIAO L T, XUE H W. Dynamic cytology and transcriptional regulation of rice lamina joint development[J]. Plant Physiology, 2017, 174(3): 1 728-1 746.
[69]	ZHANG S W, LI C H, CAO J, et al. Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation[J]. Plant Physiology, 2009, 151(4): 1 889-1 901.
[70]	DU H, WU N, FU J, et al. A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice[J]. Journal of Experimental Botany, 2012, 63(18): 6 467-6 480.
[71]	YOSHIDA H, NAGATO Y. Flower development in rice[J]. Journal of Experimental Botany, 2011, 62(14): 4 719-4 730.
[72]	BARAZESH S, MCSTEEN P. Hormonal control of grass inflorescence development[J]. Trends in Plant Science, 2008, 13(12): 656-662.
[73]	PAGNUSSAT G C, ALANDETE-SAEZ M, BOWMAN J L, et al. Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte[J]. Science, 2009, 324(5935): 1 684-1 689.
[74]	SUNDBERG E, OSTERGAARD L. Distinct and dynamic auxin activities during reproductive development[J]. Cold Spring Harbor Perspectives in Biology, 2009, 1(6): a001628.
[75]	MCSTEEN P. Auxin and monocot development[J]. Cold Spring Harbor Perspectives in Biology, 2010, 2(3): a001479.
[76]	BLAZQUEZ M A, FERRANDIZ C, MADUENO F, et al. How floral meristems are built[J]. Plant Molecular Biology, 2006, 60(6): 855-870.
[77]	WEIGEL D, ALVAREZ J, SMYTH D R, et al. LEAFY controls floral meristem identity in Arabidopsis[J]. Cell, 1992, 69(5): 843-859.
[78]	张亚萍, 习珺珺, 于丽霞, 等. LEAFY(LFY)基因在花发育网络调控中的研究进展[J]. 现代农业科技, 2012(9): 11-13.
[79]	LI W, ZHOU Y, LIU X, et al. LEAFY controls auxin response pathways in floral primordium formation[J]. Science Signaling, 2013, 6(270): ra23-ra23.
[80]	MOYROUD E, KUSTERS E, MONNIAUX M, et al. LEAFY blossoms[J]. Trends in Plant Science, 2010, 15(6): 346-352.
[81]	LIU X, HUANG J, WANG Y, et al. The role of floral organs in carpels, an Arabidopsis loss‐of‐function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression[J]. The Plant Journal, 2010, 62(3): 416-428.
[82]	WANG J W, WANG L J, MAO Y B, et al. Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis[J]. The Plant Cell, 2005, 17(8): 2 204-2 216.
[83]	MALLORY A C, BARTEL D P, BARTEL B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes[J]. The Plant Cell, 2005, 17(5): 1 360-1 375.
[84]	LIU P P, MONTGOMERY T A, FAHLGREN N, et al. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post‐germination stages[J]. The Plant Journal, 2007, 52(1): 133-146.
[85]	LIU X, ZHANG H, ZHAO Y, et al. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis[J]. Proceedings of the National Academy of Sciences, 2013, 110(38): 15 485-15 490.
[86]	WON C, SHEN X, MASHIGUCHI K, et al. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES of ARABIDOPSIS and YUCCAs in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(45): 18 518-18 523.
[87]	XU X, E Z, ZHANG D, et al. OsYUC11-mediated auxin biosynthesis is essential for endosperm development of rice[J]. Plant Physiology, 2021, 185(3): 934-950.