A Review on How Plant Hormones and Environment Factors Are Involved in Rice Root Hair Development

doi:10.16819/j.1001-7216.2020.9138

Abstract

Abstract:

Plant root hairs are important structures on the root surface for absorption of water, inorganic and organic nutrients. The root hairs which are regulated by both genetic and environmental factors, also play important roles when plants are dealing with environmental stress conditions. In this review, we analyzed how stress such as P deficiency, genetic factors and the core regulatory network composed of ABA,ETH, ABA work together during the regulation of rice root hair development. At last, we come up with issues which remains unclear but are critical and could be potential research focus.

Key words: phytohormone, environmental stress, rice root hair, transgenic factor

摘要：

根毛作为根系吸收水分和养分的重要结构,其生长发育同时受到外界环境与遗传因子的调控,也在植物应对逆境胁迫时发挥着重要的作用。本文对元素缺乏等环境胁迫、遗传因子及脱落酸、乙烯和生长素为核心的激素调控网络在水稻根毛发育中的作用及相互关系进行了总结,并就目前该研究领域内尚未解决的问题及相关研究提出了展望。

关键词: 植物激素, 环境胁迫, 水稻根毛, 遗传因子

CLC Number:

Q418
S511

Bin LI, Jin HUANG, Li WANG, Jin LI, Yueyang LIANG, Ji CHEN. A Review on How Plant Hormones and Environment Factors Are Involved in Rice Root Hair Development[J]. Chinese Journal OF Rice Science, 2020, 34(4): 287-299.

李斌, 黄进, 王丽, 李瑾, 梁越洋, 陈稷. 环境胁迫及相关植物激素在水稻根毛发育过程中的作用[J]. 中国水稻科学, 2020, 34(4): 287-299.

Figures/Tables 3

References 110

[1]	吕亚慈. 水稻激活标签系T-DNA侧翼序列分析[D]. 保定: 河北农业大学, 2007.
	Lu Y C.Analysis of flanking sequences of T-DNA activation-tagging population in rice (Oryza sativa L.) [D]. Baoding: Hebei Agricultural University, 2007. (in Chinese with English abstract)
[2]	王旭明, 赵夏夏, 陈景阳, 李震, 陈佳媚, 许江环, 周鸿凯. 低盐胁迫对5个海水稻种质若干生理生化指标的影响[J]. 热带农业科学, 2018, 38(8): 27-32.
	Wang X M, Zhao X X, Chen J Y, Li Z, Chen M J, Xu J H, Zhou H K.Effect of low salt stress on several physiological and biochemical indicators of five accessions of sea rice[J]. Chinese Journal of Tropical Agriculture, 2018, 38(8): 27-32. (in Chinese with English abstract)
[3]	Upadhyaya H, Panda S K.Chapter 9: Drought stress responses and its management in rice//Hasanuzzaman M, Fujita M, Nahar K, Biswas J K. Advances in Rice Research for Abiotic Stress Tolerance[M]. Chennai, India: Woodhead Publishing, 2019: 177-200.
[4]	Zhang H W, Zhang J F, Quan R D, Pan X W, Wan L Y, Huang R F.EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance[J]. Planta, 2013, 237(6): 1443-1451.
[5]	Cohen S P, Leach J E.Abiotic and biotic stresses induce a core transcriptome response in rice[J]. Scientific Reports, 2019, 9(1): 6273.
[6]	Ni L, Fu X, Zhang H, Li X, Cai X, Zhang P, Liu L, Wang Q, Sun M, Wang QW, Zhang A, Zhang Z, Jiang M.Abscisic acid inhibits rice protein phosphatase PP45 via H2O2 and relieves repression of the Ca2+/CaM-dependent protein kinase DMI3[J]. the Plant Cell, 2019, 31(1): 128-152.
[7]	Yamauchi T, Tanaka A, Inahashi H, Nishizawa N K, Tsutsumi N, Inukai Y, Nakazono M.Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signaling[J]. Proceedings of the National Academy of Sciences, 2019, 116(41): 20770-20775.
[8]	Huang H F, Ullah F, Zhou D X, Yi M, Zhao Y.Mechanisms of ROS regulation of plant development and stress responses[J]. Frontiers in Plant Science, 2019, 10: 1-10.
[9]	Huang J, Kim C M, Xuan Y H, Liu J, Kim T H, Kim B K, Han C D.Formin homology 1 (OsFH1) regulates root-hair elongation in rice (Oryza sativa)[J]. Planta, 2013, 237(5): 1227-1239.
[10]	Richardson A E, Barea J M, Mcneill A, Prigent-Combaret C.Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microor ganisms[J]. Plant and Soil, 2009, 321(1): 305-339.
[11]	Meng F, Xiang D, Zhu J, Li Y, Mao C.Molecular mechanisms of root development in rice[J]. Rice, 2019, 12(1): 1.
[12]	Salazar-Henao J E, Velez-Bermudez I C, Schmidt W. The regulation and plasticity of root hair patterning and morphogenesis[J]. Development, 2016, 143(11): 1848-1858.
[13]	Giehl R F H, Gruber B D, von Wirén N. It’s time to make changes: Modulation of root system architecture by nutrient signals[J]. Journal of Experimental Botany, 2013, 65(3): 769-778.
[14]	Pemberton L M S, Tsai S-L, Lovell P H, Harris P J. Epidermal patterning in seedling roots of eudicoty ledons[J]. Annals of Botany, 2001, 87(5): 649-654.
[15]	Zuchi S, Cesco S, Gottardi S, Pinton R, RöMheld V, Astolfi S. The root-hairless barley mutant brb used as model for assessment of role of root hairs in iron accumulation[J]. Plant Physiology and Biochemistry, 2011, 49(5): 506-512.
[16]	Ding W N, Yu Z M, Tong Y N, Huang W, Chen H M, Wu P.A transcription factor with a bHLH domain regulates root hair development in rice[J]. Cell Rearch, 2009, 19(11): 1309-1311.
[17]	Vissenberg K, Claeijs N, Balcerowicz D, Schoenaers S.Hormonal regulation of root hair growth and responses to the environment in Arabidopsis[J]. Journal of Experi- mental Botany, 2020, 71(8): 2412-2427.
[18]	Meisner C A, Karnok K J.Root hair occurrence and variation with environment[J]. Agronomy Journal, 83(5): 814-818.
[19]	Kwasniewski M, Daszkowska-Golec A, Janiak A, Chwialkowska K, Nowakowska U, Sablok G, Szarejko I.Transcriptome analysis reveals the role of the root hairs as environmental sensors to maintain plant functions under water-deficiency conditions[J]. Journal of Experimental Botany, 67(4): 1079-1094.
[20]	Potters G, Pasternak T P, Guisez Y, Jansen M A K. Different stresses, similar morphogenic responses: Integrating a plethora of pathways[J]. Plant, Cell & Environment, 2009, 32(2): 158-169.
[21]	Cho M, Lee S H, Cho H T.P-Glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells[J]. The Plant Cell, 2007, 19(12): 3930-3943.
[22]	Cui S, Suzaki T, Tominaga-Wada R, Yoshida S.Regulation and functional diversification of root hairs[J]. Seminars in Cell & Developmental Biology, 2018, 83: 115-122.
[23]	Liu B H, Wu J Y, Yang S Q, Schiefelbein J, Gan Y B.Nitrate regulation of lateral root and root hair develop ment in plants[J]. Journal of Experimental Botany, 2019.
[24]	Kohanová J, Martinka M, Vaculík M, White P J, Hauser M-T, Lux A.Root hair abundance impacts cadmium accumulation in Arabidopsis thaliana shoots[J]. Annals of Botany, 2018, 122(5): 903-914.
[25]	Föhse D, Claassen N, Jungk A.Phosphorus efficiency of plants[J]. Plant and Soil, 1991, 110(1): 101-109.
[26]	Bhosale R, Giri J, Pandey B K, Giehl R F H, Hartmann A, Traini R, Truskina J,Leftley N, Hanlon M, Swarup K, Rashed A, Voss U, Alonso J, Stepanova A, Yun J, Ljung K, Brown K M, Lynch J P, Dolan L, Vernoux T, Bishopp A, Wells D, Wirén N V, Bennett M J, Swarup R. A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate[J]. Nature Communications, 2018, 9(1): 1409.
[27]	Giri J, Bhosale R, Huang G Q, Pandey B K, Parker H, Zappala S, Yang J, Dievart A, Bureau C, Ljung K, Price A, Rose T, Larrieu A, Mairhofer S, Sturrock C J, White P, Dupuy L, Hawkesford M, Perin C, Liang W Q, Peret B, Hodgman C T, Lynch J, Wissuwa M, Zhang D B, Pridmore T, Mooney S J, Guiderdoni E, Swarup R, Bennett M J.Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate[J]. Nature Communications, 2018, 9(1): 1408.
[28]	Zhao Y.Auxin biosynthesis and its role in plant development[J]. Annual Review of Plant Biology, 2010, 61(1): 49-64.
[29]	Einav M G, Carolien D C, Sofie G, Tom B, Marnik V, Philip B P, Christine A B, Uri Y, Yulia K, Yael E, Smadar W, Natalie R, Maja C, Yoram K, Hinanit K.Strigolact ones are involved in root response to low phosphate conditions in Arabidopsis[J]. Plant Physiology, 2012, 160(3): 1329-1341.
[30]	Shen C J, Wang S K, Zhang S, Xu Y X, Qian Q, Qi Y H, Jiang D A.OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.)[J]. Plant Cell & Environment, 2013, 36(3): 607-620.
[31]	Yang G, Yu Z, Gao L, Zheng C C.SnRK2s at the crossroads of growth and stress responses[J]. Trends in Plant Science, 2019, 24(8): 672-676.
[32]	Abidur R, Satoko H, Yutaka O, Amakawa T, Goto N, Tsurumi S.Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators[J]. Plant Physiology, 2002, 130(4): 1908-1917.
[33]	Stepanova A N, Hoyt J M, Hamilton A A, Alonso J M.A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis[J]. the Plant Cell, 2005, 17(8): 2230-2242.
[34]	Yi T, Ferrer J-L, Ljung K, Pojer F, Fong F X, Long J A, Li L, Moreno J E, Bowman M E, Lvans L J, Cheng Y F, Lim J, Zhao Y D, Ballaré, Sandberg G, Noel J P, Chory J. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants[J]. Cell, 2008,133(1): 164-176.
[35]	Strader L C, Chen G L, Bartel B.Ethylene directs auxin to control root cell expansion[J]. Plant Journal, 2010, 64(5): 874-884.
[36]	Burg S P, Burg E A.Auxin-induced ethylene formation: its relation to flowering in the pineapple[J]. Science, 1966, 152(3726): 1269-1269.
[37]	Nishimura T, Hayashi K, Suzuki H, Gyohda A, Takaoka C, Sakaguchi Y, Matsumoto S, Kasahara H, Sakai T, Kato J, Kamiya Y, Koshiba T.Yucasin is a potent inhibitor of YUCCA, a key enzyme in auxin biosynthesis[J]. Plant Journal, 2014, 77(3): 352-366.
[38]	Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero P J, Bennett M, Sandberg G.AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling[J]. The Plant Cell, 2002, 14(3): 589-597.
[39]	Cohen J D, Slovin J P, Hendrickson A M.Two genetically discrete pathways convert tryptophan to auxin: More redundancy in auxin biosynthesis[J]. Trends in Plant Science, 2003, 8(5): 197-199.
[40]	Soeno K, Goda H, Ishii T, Ogura T, Tachikawa T, Sasaki E, Yoshida S, Fujioka S, Asami T, Shimada Y.Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis[J]. Plant & Cell Physiology, 2010, 51(4): 524-536.
[41]	Zhao Y D, Christensen S K, Fankhauser C, Cashman J R, Cohen J D, Weigel D, Chory J.A role for flavin monooxygenase-like enzymes in auxin biosynthesis[J]. Science, 2001, 291(5502): 306-309.
[42]	俞晨良. OsAUX/LAX家族表达模式及OsAUX1在水稻根系发育中的功能研究[D]. 杭州: 浙江大学, 2015.
	Yu C L, Studies on expression patterns of OsAUX/LAX family and function of OsAUX1 in rice root development[D]. Hangzhou: Zhejiang University, 2015. (in Chinese with English abstract)
[43]	Yu C, Sun C, Shen C, Wang S, Liu F, Liu Y, Chen Y, Li C, Qian Q, Aryal B, Geisler M, Jiang D A, Qi Y.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.
[44]	Wu D, Shen H, Yokawa K, Baluška F.Alleviation of aluminium-induced cell rigidity by overexpression of OsPIN2 in rice roots[J]. Journal of Experimental Botany, 2014, 65(18): 5305-5315.
[45]	Křeček P, SkůPa P, Libus J Í, Naramoto S, Tejos R, Friml J, Zazímalová E. The PIN-FORMED (PIN) protein family of auxin transporters[J]. Genome Biology, 10(12): 249.
[46]	莫亿伟, 李夏杰, 王海, 陈泽恺, 杨国, 王尉. IAA对水稻根毛形成与水通道蛋白基因表达关系的研究[J]. 中国农业科学, 2015, 48(21): 4227-4239.
	Mo Y W, Li X J, Wang H, Chen Z K, Yang G, Wang W.Effect of auxin treatment on root hair formation and aquaporins genes expression in root hair of rice[J]. Scientia Agricultura Sinica, 2015, 48(21): 4227-4239. (in Chinese with English abstract)
[47]	Ambudkar S V, Kimchi-Sarfaty C, Sauna Z E, Gottesman M M.P-glycoprotein: From genomics to mechanism[J]. Oncogene, 2003, 22(47): 7468-7485.
[48]	Ye L, Liu L, Xing A, Kang D.Characterization of a dwarf mutant allele of Arabidopsis MDR-like ABC transporter AtPGP1 gene[J]. Biochemical and Biophysical Research Communications, 2013, 441(4): 782-786.
[49]	Kubeš M, Yang H, Richter G L, Cheng Y, Młodzińska E, Wang X, Blakeslee J J, Carraro N, Petrášek J, Zažímalová E, Hoyerová K, Peer W A, Murphy A S.The Arabidopsis concentration-dependent influx/ efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis[J]. Plant Journal, 2012, 69: 640-654.
[50]	Xu Y, Zhang S, Guo H, Wang S, Xu L, Li C, Qian Q, Chen F, Geisler M, Qi Y, Jiang D A.OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa L.)[J]. Plant Journal, 2014, 79(1): 106-117.
[51]	Yoo S C, Cho S H, Paek N C.Rice WUSCHEL-related homeobox 3A (OsWOX3A) modulates auxin-transport gene expression in lateral root and root hair development[J/OL]. Plant Signaling & Behavior, 2013, 8(10): e25929.
[52]	Wang S, Zhang S, Sun C, Xu Y, Chen Y, Yu C, Qian Q, Jiang D A, Qi Y.Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa)[J]. New Phytologist, 2014, 201: 91-103.
[53]	Shen C, Yue R, Yang Y, Zhang L, Sun T, Tie S, Wang H.OsARF16 is involved in cytokinin-mediated inhibition of phosphate transport and phosphate signaling in rice (Oryza sativa L.)[J]. PLoS ONE, 2014, 9: e112906.
[54]	Chen C W, Yang Y W, Lur H S, Tsai Y G, Chang M C.A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development[J]. Plant and Cell Physiology, 2006, 47(1): 1-13.
[55]	Gupta K, Gupta B, Ghosh B,Sengupta D N.Spermidine and abscisic acid-mediated phosphorylation of a cytoplasmic protein from rice root in response to salinity stress[J]. Acta Physiologiae Plantarum, 2012, 34: 29-40.
[56]	Wang T, Li C, Wu Z, Jia Y, Wang H, Sun S, Mao C, Wang X.Abscisic acid regulates auxin homeostasis in rice root tips to promote root hair elongation[J]. Frontiers in Plant Science, 2017, 8: 1121.
[57]	Li C, Shen H, Wang T, Wang X.ABA Regulates subcellular redistribution of OsABI-LIKE2, a negative regulator in ABA signaling, to control root architecture and drought resistance in Oryza sativa[J]. Plant & Cell Physiology, 2015, 56(12): 2396-2408.
[58]	Xiao Y, Offringa R. PDK1 has a pleiotropic PINOID- independent role in Arabidopsis development [J/OL]. BioRxiv, 2019, .
[59]	Li Y, Wang Y, Tan S, Li Z, Yuan Z, Glanc M, Domjan D, Wang K, Xuan W, Guo Y, Gong Z, Friml J, Zhang J.Root growth adaptation is mediated by PYLs ABA receptor-PP2A protein phosphatase complex[J/OL].Advanced Science, 2020, 7(3): 1901455.
[60]	Yang S F, Hoffman N E.Ethylene biosynthesis and its regulation in higher plants[J]. Annual Review of Plant Biology, 1984, 35(1): 155-189.
[61]	Muday G K, Rahman A, Binder B M.Auxin and ethylene: Collaborators or competitors?[J]. Trends in Plant Science, 2012, 17(4): 181-195.
[62]	Masucci J D, Schiefelbein J.Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root[J]. the Plant Cell, 1996, 8(9): 1505-1517.
[63]	Pitts R A, Estelle M.Auxin and ethylene promote root hair elongation in Arabidopsis[J]. Plant Journal, 2010, 16(5): 553-560.
[64]	Ju C, Yoon G M, Shemansky J M, Lin D Y, Ying Z I, Chang J, Garrett W M, Kessenbrock M, Groth G, Tucker M L, Cooper B, Kieber J J, Chang C.CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(47): 19486-19491.
[65]	Chuanli J, Caren C.Mechanistic insights in ethylene perception and signal transduction[J]. Plant Physiology, 2015, 169(1): 85-95.
[66]	Song L, Yu H, Dong J, Che X, Jiao Y, Liu D.The molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation[J/OL].PLOS Genetics, 2016, 12(7): e1006194.
[67]	Feng Y, Xu P, Li B S, Li P P, Wen X, An F Y, Gong Y, Xin Y, Zhu Z Q, Wang Y C, Guo H W.Ethylene promotes root hair growth through coordinated EIN3/EIL1 and RHD6/RSL1 activity in Arabidopsis[J]. Proceedings of the National Academy of Sciences, 2017, 114(52): 13834.
[68]	Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H.Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis[J]. Journal of Experimental Botany, 2011, 62(8): 2915-2924.
[69]	Martínrejano E M.Auxin and ethylene are involved in the responses of root system architecture to low boron supply in Arabidopsis[J]. Physiologia Plantarum, 2011, 142(2): 170-178.
[70]	Bahmani R, Kim D G, Kim J A, Hwang S.The density and length of root hairs are enhanced in response to cadmium and arsenic by modulating gene expressions involved in fate determination and morphogenesis of root hairs in Arabidopsis[J/OL]. Frontiers in Plant Science, 2016, 7: 1763.
[71]	Zhang S, Huang L, Yan A, Liu Y, Liu B, Yu C, Zhang A, Schiefelbein J, Gan Y.Multiple phytohormones promote root hair elongation by regulating a similar set of genes in the root epidermis in Arabidopsis[J]. Journal of Experimental Botany, 2016, 67(22): 6363-6372.
[72]	Hu Y, You J, Li C, Williamson V M, Wang C.Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines[J/OL]. Scientific Reports, 2017, 7(1): 41282.
[73]	Birte S, Petra B.FIT, a regulatory hub for iron deficiency and stress signaling in roots, and FIT-dependent and -independent gene signatures[J]. Journal of Experimental Botany, 2020, 71(5): 1694-1705.
[74]	Masucci J D, Schiefelbein J.The rhd6 Mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process[J]. Plant Physiology, 1994, 106(4): 1335-1346.
[75]	Dolan L.The role of ethylene in root hair growth in Arabidopsis[J]. Journal of Plant Nutrition and Soil Science, 2001, 164(2): 141-145.
[76]	Jung J Y, Shin R, Schachtman D P.Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis[J]. the Plant Cell, 2009, 21(2): 607-621.
[77]	Gernier H D, Pessemier J D, Xu J J, Cristescu S M, Straeten D V D, Verbruggen N, Hermans C. A comparative study of ethylene emanation upon nitrogen deficiency in natural accessions of Arabidopsis thaliana[J]. Frontiers in Plant Science, 2016, 7: 70.
[78]	Moon S, Cho L H, Kim Y J, Gho Y S, Jeong H Y, Hong W J, Lee C, Park H, Jwa N S, Dangol S, Chen Y, Park H, Cho H S, An G, Jung K H.RSL class II transcription factors guide the nuclear localization of RHL1 to regulate root hair development[J]. Plant Physiology, 2019, 179(2): 558-568.
[79]	Doron S I, Dudy B Z.ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis[J]. the Plant Cell, 2011, 22(5): 3560-3573.
[80]	Lee S H, Cho H T.PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells[J]. The Plant Cell, 2006, 18(7): 1604.
[81]	Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R.The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport[J]. Development, 2001, 128(20): 4057-4067.
[82]	黄家庆. OsRopGEF7在水稻发育中的功能研究[D]. 广州:华南农业大学.
	Huang J Q.Function analyaisi of OsRopGEF7 in rice development[D]. Guangzhou: South China Agricultural University, 2016. (in Chinese with English abstract)
[83]	Hu Y, Vandenbussche F, Der Straeten D V. Regulation of seedling growth by ethylene and the ethylene-auxin crosstalk[J]. Planta, 2017, 245(3): 467-489.
[84]	Han X, Zhang M, Yang M, Hu Y. Arabidopsis JAZ proteins interact with and suppress RHD6 transcription factor to regulate jasmonate-stimulated root hair development[J]. The Plant Cell, 2020: tpc.00617.2019.
[85]	Tsuchisaka A, Theologis A.Unique and overlapping expression patterns among the Arabidopsis 1-Amino- Cyclopropane-1-Carboxylate synthase gene family members[J]. Plant Physiology, 2004, 136(2): 2982-3000.
[86]	Petricka J J, Winter C M, Benfey P N.Control of Arabidopsis root development[J]. Annual Review of Plant Biology, 2012, 63(1): 563-590.
[87]	Cho H-T, Cosgrove, D J.Regulation of root hair initiation and expansion gene expression in Arabidopsis[J]. the Plant Cell, 2002, 14(12): 3237-3253.
[88]	Nakamura A, Nakajima N, Goda H, Shimada Y, Hayashi K, Nozaki H, Asami T, Yoshida S, Fujioka S.Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type[J]. the Plant Journal, 2006, 45(2):193-205.
[89]	Ludwików A, Cieśla A, Kasprowicz-Maluśki A, Mituła F, Tajdel M, Gałgański Ł, Ziółkowski P A, Kubiak P, Małecka A, Piechalak A, Szabat M, Górska A, Dąbrowski M, Ibragimow I, Sadowski J.Arabidopsis protein phosphatase 2C ABI1 interacts with type I ACC synthases and is involved in the regulation of ozone -induced ethylene biosynthesis[J]. Molecular Plant, 2014, 7(6): 960-976.
[90]	郭栋梁, 李玲. ABA对植物侧根发生的调节(综述)[J]. 亚热带植物科学, 2008(1): 69-71, 77.
	Dong D L, Li L.ABA regulation of lateral root development in plant[J]. Subtropical Plant Science, 2008(1): 69-71, 77. (in Chinese with English abstract)
[91]	王凤茹, 时翠平, 董金皋. 油菜素内酯对拟南芥和水稻根毛发育的影响[J]. 河南农业大学学报, 2010, 33(6): 105-109.
	Wang F R, Shi C P, Dong J G.The response of root hair on brassinosteroids in Arabidopsis and rice[J]. Journal of Agricultural University of Hebei, 2010, 33(6): 105-109. (in Chinese with English abstract)
[92]	赵雪松, 王倩, 闫青地, 赵亚林, 王凤茹, 董金皋. 油菜素内酯对水稻根系发育的调控作用[J]. 中国细胞生物学学报, 2016, 38(10): 1191-1198.
	Zhao X S, Wang Q, Yan Q D, Zhao Y L, Wang F R, Dong J G.Function of brassinolide in the regulation of root development in rice[J]. Chinese Journal of Cell Biology, 2016, 38(10): 1191-1198. (in Chinese with English abstract)
[93]	Zhu C, Gan L, Shen Z, Xia K.Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis[J]. Journal of Experimental Botany, 2006, 57(6): 1299-1308.
[94]	Chen C-L, Cui Y, Cui M, Zhou W J, Wu H L, Ling H Q.A FIT-binding protein is involved in modulating iron and zinc homeostasis in Arabidopsis[J]. Plant, Cell & Environment, 2018, 41(7): 1698-1714.
[95]	Jones B, Gunnerås S A, Petersson S V, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K.Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction[J]. the Plant Cell, 2010, 22(9): 2956-2969.
[96]	刘昉. 细胞分裂素对OsAUX1调控水稻根系发育的影响[D]. 杭州: 浙江大学, 2016.
	Liu F.Effects of cytokinin on the OsAUX1 regulating root development of rice[D]. Hangzhou: Zhejiang University, 2016. (in Chinese with English abstract)
[97]	Elshowk S, Ruonala R, Helariutta Y.Crossing paths: cytokinin signalling and crosstalk[J]. Development, 2013, 140(7): 1373-1383.
[98]	Šimášková M, O'Brien J A, Khan M, van Noorden G, Ötvös K, Vieten A, de Clercq I, van Haperen J M A, Cuesta C, Hoyerová K, Vanneste S, Marhavý P, Wabnik K, Van Breusegem F, Nowack M, Murphy A, Friml J, Weijers D, Beeckman T, Benková E. Cytokinin response factors regulate PIN-FORMED auxin transporters[J]. Nature Communications, 2015, 6(1): 8717-8717.
[99]	Cheng S, Zhou D X, Zhao Y.WUSCHEL-related homeobox gene WOX11 increases rice drought resistance by controlling root hair formation and root system development[J]. Plant Signaling & Behavior, 2016, 11: e1130198.
[100]	Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O. MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule[J]. Current Biology, 2004, 14(14): 1232-1238.
[101]	Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H, Belausov E, Wininger S, Abu-Abied M, Kapulnik Y, Koltai H.Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture[J]. New Phytologist, 2014, 202(4): 1184-1196.
[102]	王秀梅, 梁越洋, 李玲. OsMAX1a和OsMAX1e通过参与独角金内酯的合成调控水稻分蘖[J]. 中国水稻科学, 2015, 29(3): 223-231.
	Wang X M. Liang Y Y, Li L.OsMAX1a and OsMAX1e, involved in the biosynthesis of strigolactones, regulate rice tillering[J]. Chinese Journal of Rice Science, 2015, 29(3): 223-231. (in Chinese with English abstract)
[103]	Kapulnik Y, Delaux P M, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier J P, Bécard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H.Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis[J]. Planta, 2011, 233(1): 209-216.
[104]	Koltai H.Strigolactones are regulators of root development[J]. New Phytologist, 2011, 190(3): 545-549.
[105]	Sun H, Xu F, Guo X, Wu D, Zhang X, Lou M, Luo F, Zhao Q, Xu G, Zhang Y.A strigolactone signal inhibits secondary Lateral root development in rice[J]. Frontiers in Plant Science, 2019, 10: 1527.
[106]	Sun H, Tao J, Liu S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G.Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice[J]. Journal of Experimental Botany, 2014, 65(22): 6735-6746.
[107]	Woo Y M, Park H J, Su'udi M, Yang J I, Park J J, Back K, Park Y M, An G. Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio[J]. Plant Molecular Biology, 2007, 65(2): 125-136.
[108]	吕江峰. 水稻短根毛突变体krhs2的筛选及其基因克隆[D]. 杭州: 浙江大学, 2008.
	Lu J F.Isolation and gene cloning of rice root hair short mutant, krhs2[D]. Hangzhou: Zhejiang University, 2008. (in Chinese with English abstract)
[109]	Huang J, Kim C M, Xuan Y H, Park S J, Piao H L, Je B I, Liu J, Kim T H, Kim B K, Han C D.OsSNDP1, a Sec14-nodulin domain-containing protein, plays a critical role in root hair elongation in rice[J]. Plant Molecular Biology, 2013, 82(1): 39-50.
[110]	Moon S, Chandran A K N, An G, Lee C, Jung K H. Genome-wide analysis of root hair-preferential genes in rice[J]. Rice, 2018, 11(1): 48.

基因 Gene	功能 Function	突变体根毛表型 Root hair phenotype of mutant	环境因素 Environmental factor	激素 Phytohormone	基因ID Locus No.	参考文献 Reference
AUX1	参与IAA运输和生长素信号传导,响应重金属镉胁迫,调控根毛伸长生长	短根毛Short root hair	镉、磷胁迫Cd, P stress	CTK/IAA	Os01g0856500	[27, 43]
PIN1	参与IAA运输和信号传导,参与根、芽和花序发育,调控根毛伸长	长根毛Long root hair	未知Unknown	IAA	Os06g0232300	[46]
ARF12	IAA受体	未知Unknown	磷、铁胁迫P, Fe stress	IAA	Os04g0671900	[52]
ARF16	IAA受体	未知Unknown	磷、铁胁迫P, Fe stress	CTK/IAA	Os01g0236300	[53]
TIR1	F-Box IAA受体蛋白,调控初生根生长、根毛伸长	短根毛Short root hair	磷胁迫P stress	IAA	Os05g0150500	[22]
ABIL2	ABA信号传导元件,调控根系发育,响应抗旱胁迫	长根毛Long root hair	干旱胁迫Drought stress	ABA	Os05g0592800	[56]
SAPK10	参与高渗应激反应,ABA信号转导	短根毛Short root hair	干旱胁迫Drought stress	ABA	Os03g0610900	[57]
WOX11	WUSCHEL相关同源异型框基因,细胞分裂素信号传导因子	短根毛Short root hair	干旱胁迫Drought stress	CTK	Os07g0684900	[98]

基因 Gene	功能 Function	突变体根毛表型 Root hair phenotype of mutant	环境因素 Environmental factor	激素 Phytohormone	基因ID Locus No.	参考文献 Reference
AUX1	参与IAA运输和生长素信号传导,响应重金属镉胁迫,调控根毛伸长生长	短根毛Short root hair	镉、磷胁迫Cd, P stress	CTK/IAA	Os01g0856500	[27, 43]
PIN1	参与IAA运输和信号传导,参与根、芽和花序发育,调控根毛伸长	长根毛Long root hair	未知Unknown	IAA	Os06g0232300	[46]
ARF12	IAA受体	未知Unknown	磷、铁胁迫P, Fe stress	IAA	Os04g0671900	[52]
ARF16	IAA受体	未知Unknown	磷、铁胁迫P, Fe stress	CTK/IAA	Os01g0236300	[53]
TIR1	F-Box IAA受体蛋白,调控初生根生长、根毛伸长	短根毛Short root hair	磷胁迫P stress	IAA	Os05g0150500	[22]
ABIL2	ABA信号传导元件,调控根系发育,响应抗旱胁迫	长根毛Long root hair	干旱胁迫Drought stress	ABA	Os05g0592800	[56]
SAPK10	参与高渗应激反应,ABA信号转导	短根毛Short root hair	干旱胁迫Drought stress	ABA	Os03g0610900	[57]
WOX11	WUSCHEL相关同源异型框基因,细胞分裂素信号传导因子	短根毛Short root hair	干旱胁迫Drought stress	CTK	Os07g0684900	[98]

基因 Gene	功能 Function	突变体根毛表型 Root hair phenotype of mutant	环境因素 Environmental factor	激素 Phytohormone	基因ID Locus No.	参考文献 Reference
CTR1	ETH信号转导途径中负调节剂,与ETH受体ETR1和ERS相互作用	根毛数量变多 Increased root hair quantity	盐胁迫Salt stress	ETH	At5g03730	[62, 66]
EIL1	ETH信号通路转录因子EIL1,响应ETH	短根毛Short root hair	铁胁迫Fe stress	ETH	At2g27050	[67]
EIN2	ETH信号通路转录因子EIL2,在ETH中起正向调控作用	短根毛Short root hair	镉,砷胁迫Cd, As stress	ETH	At5g03280	[70]
EIN3	启动ETH应答的下游转录级联反应的核转录因子	短根毛Short root hair	磷胁迫P stress	ETH	At3g20770	[66, 67]
RSL1	编码涉及种子寿命RING型锌指泛素连接酶,参与根毛生长调控	短根毛Short root hair	未知Unknown	ETH/JA	At2g26130	[67]
RSL2	RSL2与RSL4同时表达,受RHD6和RSL1控制,参与根毛伸长	短根毛Short root hair	未知Unknown	ETH	At4g33880	[67]
RSL4	类似bHLH结合结构域的蛋白质,响应IAA,RSL4与RHD6共同调控根毛发育	短根毛,数量变少 Short root hair, decreased root hair quantity	磷胁迫P stress	ETH/IAA	At1g27740	[17]
RHD6	DNA结合转录激活剂活性,转录因子活性,调控根毛发育	短根毛Short root hair	镉,砷胁迫Cd, As stress	IAA/ ETH/JA	At1g66470	[67, 70]
ETO1	ETH生物合成中限速步骤,ETO1降解ACSS酶,提高ETH的生物合成	长根毛,数量变多 Long root hair, increased root hair quantity	未知Unknown	ETH	At3g51770	[70]
ETR1	ETH信号传导途径成员,调控幼苗发育、气孔运动、响应ABA	短根毛Short root hair	镉,砷胁迫Cd, As stress	ETH/ABA	At1g66340	[70]
PGP4	IAA流入运输蛋白,介导根中IAA的转运	长根毛Long root hair	未知Unknown	IAA	At2g47000	[49]

基因 Gene	功能 Function	突变体根毛表型 Root hair phenotype of mutant	环境因素 Environmental factor	激素 Phytohormone	基因ID Locus No.	参考文献 Reference
CTR1	ETH信号转导途径中负调节剂,与ETH受体ETR1和ERS相互作用	根毛数量变多 Increased root hair quantity	盐胁迫Salt stress	ETH	At5g03730	[62, 66]
EIL1	ETH信号通路转录因子EIL1,响应ETH	短根毛Short root hair	铁胁迫Fe stress	ETH	At2g27050	[67]
EIN2	ETH信号通路转录因子EIL2,在ETH中起正向调控作用	短根毛Short root hair	镉,砷胁迫Cd, As stress	ETH	At5g03280	[70]
EIN3	启动ETH应答的下游转录级联反应的核转录因子	短根毛Short root hair	磷胁迫P stress	ETH	At3g20770	[66, 67]
RSL1	编码涉及种子寿命RING型锌指泛素连接酶,参与根毛生长调控	短根毛Short root hair	未知Unknown	ETH/JA	At2g26130	[67]
RSL2	RSL2与RSL4同时表达,受RHD6和RSL1控制,参与根毛伸长	短根毛Short root hair	未知Unknown	ETH	At4g33880	[67]
RSL4	类似bHLH结合结构域的蛋白质,响应IAA,RSL4与RHD6共同调控根毛发育	短根毛,数量变少 Short root hair, decreased root hair quantity	磷胁迫P stress	ETH/IAA	At1g27740	[17]
RHD6	DNA结合转录激活剂活性,转录因子活性,调控根毛发育	短根毛Short root hair	镉,砷胁迫Cd, As stress	IAA/ ETH/JA	At1g66470	[67, 70]
ETO1	ETH生物合成中限速步骤,ETO1降解ACSS酶,提高ETH的生物合成	长根毛,数量变多 Long root hair, increased root hair quantity	未知Unknown	ETH	At3g51770	[70]
ETR1	ETH信号传导途径成员,调控幼苗发育、气孔运动、响应ABA	短根毛Short root hair	镉,砷胁迫Cd, As stress	ETH/ABA	At1g66340	[70]
PGP4	IAA流入运输蛋白,介导根中IAA的转运	长根毛Long root hair	未知Unknown	IAA	At2g47000	[49]