Progress in Plant Trichome Development Research

doi:10.16420/j.issn.0513-353x.2020-0407

Acta Horticulturae Sinica ›› 2021, Vol. 48 ›› Issue (4): 705-718.doi: 10.16420/j.issn.0513-353x.2020-0407

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Progress in Plant Trichome Development Research

LIU Xiaomeng¹, TANG Ning², CHEN Zexiong², LUO Chengrong³, ZHANG Weiwei¹, XU Feng¹^,^*()

¹College of Horticulture and Gardening,Yangtze University,Jingzhou,Hubei 434025,China
²College of Landscape Architecture and Life Science,Chongqing University of Arts and Sciences,Chongqing Key Laboratory of Economic Plant Biotechnology,Chongqing 402160,China
³Sichuan Academy of Forestry Sciences,Chengdu 610081,China

Received:2020-07-27 Online:2021-04-25 Published:2021-04-29
Contact: XU Feng E-mail:xufeng@yangtzeu.edu.cn

Abstract

Abstract:

Trichome is a specialized structure appendage developed from plant epidermal cells,and is widely present in plants in different forms. It plays an important role in plant defense against biotic and abiotic stress. In the meantime,its secretions,containing various secondary metabolites,have been exerting a considerable socio economic impact. The genes regulating the development of trichome have been cloned and functionally verified in various plants. Particular in Arabidopsis thaliana,regulatory genes which code mostly transcription factors related to development of trichome have been extensively studied. In the present paper,we attempt to intergrate the recent progress in the studies on developmental characteristics and biological function of trichome in various plants,and reviewed the factors and regulatory genes related to trichome development.

Key words: plant, trichome, development, hormone, biological functions, transcription factors

CLC Number:

LIU Xiaomeng, TANG Ning, CHEN Zexiong, LUO Chengrong, ZHANG Weiwei, XU Feng. Progress in Plant Trichome Development Research[J]. Acta Horticulturae Sinica, 2021, 48(4): 705-718.

Figures/Tables 1

Fig. 1 Regulation model of trichome development in Arabidopsis Positive regulation:(1) JA can regulate GL1 in TTG1-GL1- GL3/EGL3 complex through JAZ protein,and mediate the growth and development of trichome;GIS,GIS2 and ZFP8can integrate GA and CK signal transduction pathways,in which GIS and ZFP8 cooperatively control the transcription ofGL1 in TTG1-GL1- GL3/EGL3 complex,and GIS2further regulates the expression of GL2,which ultimately promotes the development of trichomes. Negative regulation:(1) CPC,TRY,ETC1,ETC2,ETC3 and TCL1 can compete for bHLH-WD40 to combine into R3 MYB-bHLH-WD40 transcription complex,which negatively regulates the formation of trichome in adjacent epidermal cells;The miRNA156 targets SPL9 gene,activates TRY and TCL1 genes,and then negatively regulates the development of trichome. (2) SA showed negative correlation regulation on the occurrence of trichomes.

References 109

[1]	Akhtar M Q, Qamar N, Yadav P, Kulkarni P, Kumar A, Shasany A K. 2017. Comparative glandular trichome transcriptome-based gene characterization reveals reasons for differential (-)-menthol biosynthesis in Mentha species. Physiologia Plantarum, 160 (2):128-141. doi: 10.1111/ppl.2017.160.issue-2 URL
[2]	Andrade M C, Da Silva A A, Neiva I P, Oliveira I R C, De Castro E M, Francis D M, Maluf W R. 2017. Inheritance of type IV glandular trichome density and its association with whitefly resistance from Solanum galapagense accession LA1401. Euphytica, 213 (2):52. doi: 10.1007/s10681-016-1792-1 URL
[3]	Balkunde R, Pesch M, Hulskamp M. 2010. Trichome patterning in Arabidopsis thaliana:from genetic to molecular models. Plant Development, 91:299-321.
[4]	Bedon F, Ziolkowski L, Walford S A, Dennis E S, Llewellyn D J. 2014. Members of the MYBMIXTA-like transcription factors may orchestrate the initiation of fibre development in cotton seeds. Frontiers Plant Science, 5:e179.
[5]	Biswas K K, Foster A J, Aung T, Mahmoud S S. 2008. Essential oil production:relationship with abundance of glandular trichomes in aerial surface of plants. Acta Physiologiae Plantarum, 31 (1):13-19. doi: 10.1007/s11738-008-0214-y URL
[6]	Bryant L, Patole C, Cramer R. 2016. Proteomic analysis of the medicinal plant Artemisia annua:data from leaf and trichome extracts. Data in Brief, 7:325-331. doi: 10.1016/j.dib.2016.02.038 pmid: 26977431
[7]	Caissard J C, Olivier T, Delbecque C, Palle S, Garry P P, Audran A, Valot N, Moja S, Nicole F, Magnard J L, Legrand S, Baudino S, Jullien F. 2012. Extracellular localization of the diterpene sclareol in clary sage(Salvia sclarea L.,Lamiaceae). PLoS ONE, 7 (10):e48253. doi: 10.1371/journal.pone.0048253 URL
[8]	Chang J, Yu T, Yang Q H, Li C X, Xiong C, Gao S H, Xie Q M, Zheng F Y, Li H X, Tian Z D, Yang C X, Ye Z B. 2018. Hair,encoding asingle C2H2 zinc-finger protein,regulates multicellular trichome formation in tomato. Plant Journal, 96 (1):90-102. doi: 10.1111/tpj.14018 URL
[9]	Chen G, Klinkhamer P G L, Escobar-Bravo R, Leiss K A. 2018. Type VI glandular trichome density and their derived volatiles are differently induced by jasmonicacid in developing and fully developed tomato leaves:implications for thrips resistance. Plant Science, 276:87-98. doi: 10.1016/j.plantsci.2018.08.007 URL
[10]	Chen Y, Su D, Li J, Ying S Y, Deng H, He X Q, Zhu Y Q, Li Y, Chen Y, Pirrello J, Bouzayen M, Liu Y S, Liu M C. 2020. Overexpression of bHLH95,a basic helix-loop-helix transcription factor family member,impacts trichome formation via regulating gibberellin biosynthesis in tomato. Journal of Experimental Botany,eraa 114.
[11]	Chini A, Fonseca S, Fernandez G, Adie B, Chico J M, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano F M, Ponce M R, Micol J L, Solano R. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448:666-671. pmid: 17637675
[12]	Chini A, Gimenez-Ibanez S, Goossens A, Solano R. 2016. Redundancy and specificity in jasmonate signaling. Current Opinion in Plant Biology, 33:147-156. doi: 10.1016/j.pbi.2016.07.005 URL
[13]	Cui J Y, Miao H, Ding L H, Wehner T C, Liu P N, Wang Y, Zhang S P, Gu X F. 2016. A new glabrous gene( csgl3)identified in trichome development in cucumber (Cucumis sativus L.). PLoS ONE, 11:e0148422. doi: 10.1371/journal.pone.0148422 URL
[14]	Chalvin C, Drevensek S, Dron M, Bendahmane A, Boualem A. 2020. Genetic control of glandular trichome development. Trends in Plant Science, 25 (5):477-487. doi: 10.1016/j.tplants.2019.12.025 URL
[15]	Champagne A, Boutry M. 2017. A comprehensive proteome map of glandular trichomes of hop( Humulus lupulus L.)female cones:identification of biosynthetic pathways of the major terpenoid-related compounds and possible transport proteins. Proteomics, 17 (8):1600411. doi: 10.1002/pmic.v17.8 URL
[16]	Dai X, Zhou L, Zhang W, Cai L, Guo H, Tian H, Schiefelbein J, Wang C. 2016. A single amino acid substitution in the R3 domain of GLABRA1 leads to inhibition of trichome formation in Arabidopsis without affecting its interaction with GLABRA3. Plant Cell and Environment, 39 (4):897-907. doi: 10.1111/pce.12695 URL
[17]	Deng W, Yang Y, Ren Z, Audran-Delalande C, Mila I, Wang X, Song H L, Hu Y H, Bouzayen M, Li Z G. 2012. The tomato SLIAA15 is involved in trichome formation and axillary shoot development. New Phytologist, 194 (2):379-390. doi: 10.1111/nph.2012.194.issue-2 URL
[18]	Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trend in Science, 15 (10):573-581.
[19]	Duke S O, Paul R N. 1993. Development and fine structure of the glandular trichomes of Artemisia annua L. Trends in Plant Science, 154 (10):107-118.
[20]	Ewas M, Gao Y Q, Ali F, Nishawy E M, Shahzad R, Subthain H, Amar M, Martin C, Luo J. 2017. RNA-seq reveals mechanisms of SlMXI for enhanced carotenoids and terpenoids accumulation along with stress resistance in tomato. Science Bulletin, 62 (7):476-485. doi: 10.1016/j.scib.2017.03.018 URL
[21]	Ewas M, Gao Y, Wang S, Liu X, Zhang H, Nishawy E M E, Ali F, Shahzad R, Ziaf K, Subthain H, Martin C, Luo J. 2016. Manipulation of SlMX1 for enhanced carotenoids accumulation and drought resistance in tomato. Science Bulletin, 61 (18):1413-1418. doi: 10.1007/s11434-016-1108-9 URL
[22]	Feng L G, Luan X F, Wang J, Xia W, Wang M, Sheng L X. 2015. Cloning and expression analysis of transcription factor RRTTG1 related to prickle development in rose (Rosa rugosa). Archives of Biological Sciences, 67 (4):1219-1225. doi: 10.2298/ABS150310098F URL
[23]	Gan L, Xia K, Chen J G, Wang S. 2011. Functional characterization of TRICHOMELESS2,a new single-repeat R3 MYB transcription factor in the regulation of trichome patterning in Arabidopsis. BMC Plant Biology, 11 (1):176. doi: 10.1186/1471-2229-11-176 URL
[24]	Gan Y B, Liu C, Yu H, Broun P. 2007. Integration of cyto kinin and gibberellin signaling by Arabidopsis transcription factors GIS, ZFP8and GIS2 in the regulation of epidermal cell fate. Development, 134:2073-2081. doi: 10.1242/dev.005017 URL
[25]	Gan Y, Kumimoto R, Chang L, Ratcliffe O, Hao Y, Broun P. 2006. GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell, 18 (6):1383-1395. doi: 10.1105/tpc.106.041533 URL
[26]	Gao S H, Gao Y N, Xiong C, Yu G, Chang J, Yang Q H, Yang C X, Ye Z B. 2017. The tomato B-type cyclin gene, SlCycB21,plays key roles in reproductive organ development,trichome initiation,terpenoids biosynthesis and Prodenia litura defense. Plant Science, 262:103-114. doi: 10.1016/j.plantsci.2017.05.006 URL
[27]	Glover B J, Bunnewell S, Martin C. 2004. Convergent evolution within the genus Solanum:the specialised anther cone develops through alternative pathways. Gene, 331:1-7. doi: 10.1016/j.gene.2004.01.027 URL
[28]	Grebe M. 2012. The patterning of epidermal hairs in Arabidopsis-updated. Current Opinion in Plant Biology, 15 (1):31-37. doi: 10.1016/j.pbi.2011.10.010 URL
[29]	Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J, Olszewski N, Ori N, Eshed Y, Weiss D. 2005. Cross talk between gibberellin and cytokinin:the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell, 17 (1):92-102. pmid: 15608330
[30]	Guan X, Lee J J, Pang M, Shi X, Stelly D M, Chen Z J. 2011. Activation of Arabidopsis seed hair development by cotton fiber-related genes. PLoS ONE, 6 (7):e21301. doi: 10.1371/journal.pone.0021301 URL
[31]	Guan X, Pang M, Nah G, Shi X, Ye W, Stelly D M, Chen Z J. 2014. miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nature Communications, 5:3050. doi: 10.1038/ncomms4050 URL
[32]	Guan Yuan. 2008. Mapping and cloning of related gene for fruit spines formation in cucumber[Ph. D. Dissertation]. Shanghai:Shanghai Jiao Tong University. (in Chinese)
	关媛. 2008. 黄瓜果刺形成相关基因的定位与克隆[博士论文]. 上海:上海交通大学.
[33]	Guo Guangjun, Sun Shuai, Wang Xiaoxuan, Guo Yanmei, John CS, Wang Shubin, Du Yongchen, Gao Jianchang. 2016. Analysis of characteristics of leaf trichome and secondary metabolites related to resistance to type B Bemisia tabaci of tomato. Acta Horticulturae Sinica, 43 (8):1493-1503. (in Chinese)
	郭广君, 孙帅, 王孝宣, 国艳梅, John C. Snyder, 王述彬, 杜永臣, 高建昌. 2016. 番茄抗B型烟粉虱相关叶表腺毛性状及其次生代谢物质分析. 园艺学报, 43 (8):1493-1503.
[34]	Heil M. 2010. Indirect defence via tritrophic interactions. New Phytologist, 178 (1):41-61. doi: 10.1111/nph.2008.178.issue-1 URL
[35]	Hu B, Wan Y, Li X, Zhang F, Yan W, Xie J. 2013. Phenotypic characterization and genetic analysis of rice with pubescent leaves and glabrous hulls. Crop Science, 53 (5):1878-1886. doi: 10.2135/cropsci2012.09.0522 URL
[36]	Huang C Z, Jiao X M, Yang L, Zhang M M, Dai M M, Wang L, Wang K, Bai L, Song C P. 2019a. ROP-GEF signal transduction is involved in AtCAP1-regulated root hair growth. Plant Growth Regulation, 87 (1):1-8. doi: 10.1007/s10725-018-0448-7 URL
[37]	Huang X, Yan H, Zhai L, Yi Y. 2019b. GLABROUS1 from Rosa roxburghii Tratt regulates trichome formation by interacting with the GL3/EGL3 protein. Gene, 692:60-67. doi: 10.1016/j.gene.2018.12.071 URL
[38]	Huang Xiao-long, Chen Ting-ting, Zhang Qin-qin, Mo Jia-jia, Gong Pan-qin, Yan Hiu-qing. 2020. Cloning,phylogenic and expression analysis of GL2 homology gene in Rosa roxburghii. Guihaia, 40 (1):119-127. (in Chinese)
	黄小龙, 陈婷婷, 张琴琴, 莫佳佳, 龚盼琴, 闫慧清. 2020. 刺梨GL2同源基因的克隆、系谱树和表达分析. 广西植物, 40 (1):119-127.
[39]	Huang Yun-ji, Deng Ren-yu, Gao Fei, Luo Xiao-peng, Wu Qi. 2015. Cloning and expression analysis of transcription factor gene FtMYB21 from tartary buckwheat under abiotic stress. Genomics and Applied Biology, 34 (9):1939-1945. (in Chinese)
	黄云吉, 邓仁榆, 高飞, 雒晓鹏, 吴琦. 2015. 苦荞转录因子基因 FtMYB21的克隆及其非生物胁迫下的表达分析. 基因组学与应用生物学, 34 (9):1939-1945.
[40]	Ilgenfritz H, Bouyer D, Schnittger A, Mathur J, Kirik V, Schwab B, Chua N H, Jurgens G, Hulskamp M. 2003. The Arabidopsis STICHEL gene is a regulator of trichome branch number and encodes a novel protein. Plant Physiology, 131 (2):643-655. doi: 10.1104/pp.014209 URL
[41]	Kang J H, Campos M L, Zemelis-Durfee S, Al-Haddad J M, Jones A D, Telewski F W, Brandizzi F, Howe G A. 2016. Molecular cloning of the tomato hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue. Journal of Experimental Botany, 67 (18):5313-5324. doi: 10.1093/jxb/erw292 URL
[42]	Kang J H, McRoberts J, Shi F, Moreno J E, Jones A D, Howe G A. 2014. The flavonoid biosynthetic enzyme chalcone isomerase modulates terpenoid production in glandular trichomes of tomato. Plant Physiology, 164 (3):1161-1174. doi: 10.1104/pp.113.233395 URL
[43]	Kang J H, Shi F, Jones A D, Marks M D, Howe G A. 2010. Distortion of trichome morphology by the hairless mutation of tomato affects leaf surface chemistry. Journal of Experimental Botany, 61 (4):1053-1064. doi: 10.1093/jxb/erp370 URL
[44]	Kasili R, Huang C C, Walker J D, Simmons L A, Zhou J, Faulk C, Hulskamp M, Larkin J C. 2011. BRANCHLESS TRICHOMES links cell shape and cell cycle control in Arabidopsis trichomes. Development, 138:2379-2388. doi: 10.1242/dev.058982 URL pmid: 21558384
[45]	Katiyar A, Smita S, Lenka S K, Rajwanshi R, Chinnusamy V, Bansal K C. 2012. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics, 13 (1):544. doi: 10.1186/1471-2164-13-544 URL
[46]	Larkin J C, Oppenheimer D G, Pollock S, Marks M D. 1993. Arabidopsis GLABROUSI gene requires downstream sequences for function. Plant Cell, 5:1739-1748. doi: 10.2307/3869690 URL
[47]	Li L, Zhao Y, McCaig B C, Wingerd B A, Wang J H, Whalon M E, Pichersky E, Howe G A. 2004. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation,jasmonate-signaled defense responses,and glandular trichome development. Plant Cell, 16:126-143. doi: 10.1105/tpc.017954 URL
[48]	Li Q, Cao C, Cunjia Zhang, Zheng S, Wang Z, Wang L, Ren Z. 2015. The identification of Cucumis sativus Glabrous 1( CsGLl)required for the formation of trichomes uncovers a novel function for the homeodomain-leucine zipper I gene. Jourmal of Experimental Botany, 66:2515-2526.
[49]	Lin Q, Ohashi Y, Kato M, Tsuge T, Gu H Y, Qu L J, Aoyama T. 2015. GLABRA2 directly suppresses basic Helix-Loop-Helix transcription factor genes with diverse functions in root hair development. Plant Cell, 27 (10):2894-2906.
[50]	Liu Jin-qiu. 2017. The role of SlHZ45 gene in the development of trichome in tomato [M. D. Dissertation]. Harbin:Northeast Agricultural University. (in Chinese)
	刘金秋. 2017. 番茄 SlHZ45基因在表皮毛发育中的角色[硕士论文]. 哈尔滨:东北农业大学.
[51]	Ma D, Hu Y, Yang C Q, Liu B L, Fang L, Wan Q, Liang W H, Mei G F, Wang L J, Wang H P, Ding L Y, Dong C G, Pan M Q, Chen J D, Wang S, Chen S Q, Cai C P, Zhu X F, Guan X Y, Zhou B L, Zhu S J, Wang J W, Guo W Z, Chen X Y, Zhang T Z. 2016. Genetic basis for glandular trichome formation in cotton. Nature Communications, 7:10456. doi: 10.1038/ncomms10456 URL
[52]	Maes L, Van Nieuwerburgh F C W, Zhang Y S, Reed D W, Pollier J, Casteele S, Inze D, Covello P S, Deforce D L D, Goossens A. 2011. Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytologist, 189 (1):176-189. doi: 10.1111/nph.2010.189.issue-1 URL
[53]	Makkar H P S, Siddhuraju P, Becker K. 2007. Plant secondary metabolites. Methods in Molecular Biology, 393:1-122.
[54]	Martin C, Bhatt K, Baumann K, Jin H, Zachgo S, Roberts K, Schwarz-Sommer Z, Glover B, Perez-Rodrigues M. 2002. The mechanics of cell fate determination in petals. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 357 (1422):809-813.
[55]	Matias-Hernandez L, Jiang W M, Yang K, Tang K X, Brodelius P E, Pelaz S. 2017. Aa MYB1,and its orthologue At MYB61,affect terpene metabolism and trichome development in Artemisia annua and Arabidopsis thaliana. Plant Journal, 90 (3):520-534. doi: 10.1111/tpj.13509 URL
[56]	Nadakuduti S S, Pollard M, Kosma D K, Allen C, Ohlrogge J B, Barry C S. 2012. Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato. Plant Physiology, 159 (3):945-960. doi: 10.1104/pp.112.198374 URL pmid: 22623518
[57]	Nagata T, Todoriki S, Hayashi T, Shibata Y, Mori M, Kanegae H, Kikuchi S. 1999. Gamma-radiation induces leaf trichome formation in Arabidopsis. Plant Physiology, 120 (1):113-120. doi: 10.1104/pp.120.1.113 URL
[58]	Pan Y P, Bo K L, Cheng Z H, Weng Y Q. 2015. The loss-of-function GLABROUS 3 mutation in cucumber is due to LTR-retrotransposon insertion in a class IV HD-ZIP transcription factor gene CsGL3 that is epistatic over CsGLl. BMC Plant Biology, 15:302. doi: 10.1186/s12870-015-0693-0 URL
[59]	Paterson A H, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker K C, Shu S, Udall J, Yoo M, Byers R, Chen W, Doron-Faigenboim A, Duke M V, Gong L, Grimwood J, Grover C, Grupp K, Hu G, Lee T, Li J, Lin L, Liu T, Marler B S, Page J T, Roberts A W, Romanel E, Sanders W S, Szadkowski E, Tan X, Tang H, Xu C, Wang J, Wang Z, Zhang D, Zhang L, Ashrafi H, Bedon F, Bowers J E, Brubaker C L, Chee P W, Das S, Gingle A R, Haigler C H, Harker D, Hoffmann L V, Hovav R, Jones D C, Lemke C, Mansoor S, Rahman M, Rainville L N, Rambani A, Reddy U K, Rong J, Saranga Y, Scheffler B E, Scheffler J A, Stelly D M, Triplett BA, van Deynze A, Vaslin M F S, Waghmare V N, Walford S A, Wright R J, Zaki E A, Zhang T, Dennis E S, Mayer K F X, Peterson D G, Rokhsar D S, Wang X, Schmutz J. 2012. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature, 492:423-427. doi: 10.1038/nature11798 URL pmid: 23257886
[60]	Patzold H, Garms S, Battam S, Wiecorek J, Urs-Creia E M, Manuel RodrÍguez-ConcepciÓn, Boland W, Strack D, Hause B, Walter M H. 2010. The isogene 1-dexy-xyulose S-phosphate sythase 2 controls isoprenoid profiles precursor pathway location,and density of tomato tichomes. Molecular Plan, 3:904-916.
[61]	Payne C T, Zhang F, Lloyd A M. 2000. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics, 156 (3):1349-1362. pmid: 11063707
[62]	Pesch M, Hülskamp M. 2009. One,two,three… models for trichome patterning in Arabidopsis? Current Opinion in Plant Biology, 12 (5):587-592. doi: 10.1016/j.pbi.2009.07.015 URL
[63]	Pu Li, Suo Jin-feng, Xue Yong-biao. 2003. Molecular control of plant trichome development. Acta Genetica Sinica, 30 (11):1078-1084. (in Chinese)
	普莉, 索金凤, 薛勇彪. 2003. 植物表皮毛发育的分子遗传控制. 遗传学报, 30 (11):1078-1084.
[64]	Qi T C, Song S S, Ren Q C, Wu D W, Huang H, Chen Y, Fan M, Peng W, Ren C M, Xie D X. 2011. The jasmonate-ZIM-Domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell, 23 (5):1795-1814. doi: 10.1105/tpc.111.083261 URL
[65]	Rowe H C, Ro D K, Rieseberg L H. 2012. Response of sunflower( Helianthus annuus L.)leaf surface defenses to exogenous methyl jasmonate. PLoS ONE, 7:e37191. doi: 10.1371/journal.pone.0037191 URL
[66]	Schellmann S, Hulskamp M. 2005. Epidermal differentiation:trichomes in Arabidopsis as a model system. International Journal of Developmental Biology, 49 (5-6):579-584.
[67]	Shi P, Fu X, Shen Q, Liu M, Tang K. 2018. The roles of AaMIXTA1 in regulating the initiation of glandular trichomes and cuticle biosynthesis in Artemisia annua. New Phytologist, 217 (1):261-276. doi: 10.1111/nph.2018.217.issue-1 URL
[68]	Simmons A T, Gurr G M. 2005. Trichomes of Lycopersicon species and their hybrids:effects on pests and natural enemies. Agricultural and Forest Entomology, 7 (4):265-276. doi: 10.1111/afe.2005.7.issue-4 URL
[69]	Suo J, Liang X, Pu L, Zhang Y, Xue Y. 2003. Identification of GhMYB109 encoding a R2R3 MYB transcription factor that expressed specifically in fiber initials and elongating fibers of cotton(Gossypium hirsutum L.) Biochimica et Biophysica Acta, 1630 (1):25-34.
[70]	Szymanski D B, Lloyd A M, Marks M D. 2000. Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends in Plant Science, 5 (5):214-219. doi: 10.1016/S1360-1385(00)01597-1 URL
[71]	Tattini M, Gravano E, Pinelli P, Mulinacci N, Romani A. 2000. Flavonoids accumulate in leaves and glandular trichomes of Phillyrea latifolia exposed to excess solar radiation. New Phytologist, 148 (1):69-77. doi: 10.1046/j.1469-8137.2000.00743.x URL
[72]	Thines B, Katsir L, Melotto M, Niu Y J, Mandaokar A, Liu G H, Nomura K, He S Y, Howe G A, Browse J. 2007. JAZ repressor proteins are targets of the SCF(COI1)complex during jasmonate signalling. Nature, 448:661-665. pmid: 17637677
[73]	Tiwari P. 2016. Recent advances and challenges in trichome research and essential oil biosynthesis in Mentha arvensis L. Industrial Crops and Products, 82:141-148. doi: 10.1016/j.indcrop.2015.11.069 URL
[74]	Tominaga W R, Nukumizu Y, Sato S, Wada T. 2013. Control of plant trichome and root-hair development by a tomato( Solanum lycopersicum)R3 MYB transcription factor. PLoS ONE, 8 (1):54019.
[75]	Tominaga W R, Nukumizu Y. 2012. Expression analysis of an R3-Type MYB transcription factor CPC-LIKE MYB4( TRICHOMELESS2)and CPL4-related transcripts in Arabidopsis. International Journal of Molecular Sciences, 13 (3):3478-3491. doi: 10.3390/ijms13033478 URL
[76]	Traw M B, Bergelson J. 2003. Interactive effects of jasmonic acid,salicylic acid and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology, 133 (3):1367-1375. doi: 10.1104/pp.103.027086 URL
[77]	Vernoud V, Laigle G, Rozier F, Meeley R B, Perez P, Rogowsky P M. 2009. The HD-ZIP IV transcription factor OCL4is necessary for trichome patterning and anther development in maize. Plant Journal, 59 (6):883-894. doi: 10.1111/tpj.2009.59.issue-6 URL
[78]	Wan Q, Zhang H, Ye W X, Wu H T, Zhang T Z. 2014. Genome-Wide transcriptome profiling revealed cotton fuzz fiber development having a similar molecular model as Arabidopsis trichome. PLoS ONE, 9:e97313. doi: 10.1371/journal.pone.0097313 URL
[79]	Wang D J, Zeng J W, Ma W T, Lu M, An H M. 2019. Morphological and structural characters of trichomes on various organs of Rosa roxburghii. Hortscience, 54 (1):45-51. doi: 10.21273/HORTSCI13485-18 URL
[80]	Wang G, Zhao G H, Jia Y H, Du X M. 2013. Identification and characterization of cotton genes involved in fuzz-fiber development. Journal of Integrative Plant Biology, 55:619-630. doi: 10.1111/jipb.12072 URL
[81]	Wang S, Hubbard L, Chang Y, Guo J, Schiefelbein J, Chen J G. 2008. Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. BMC Plant Biology, 8:81. doi: 10.1186/1471-2229-8-81 URL
[82]	Wang S, Wang J W, Yu N, Li C H, Luo B, Gou J Y, Wang L J, Chen X Y. 2004. Control of plant trichome development by a cotton fiber MYB gene. Plant Cell, 16 (9):2323-2334. doi: 10.1105/tpc.104.024844 URL
[83]	Wang Y L, Nie J T, Chen H M, Guo C L, Pan J, He H L, Pan J S, Cai R. 2016. Identification and mapping of Tril,a homeodomain-leucine zipper gene involved in multicellular trichome initiation in Cucumis sativus. Theoretical and Applied Genetics, 129 (2):305-316. doi: 10.1007/s00122-015-2628-4 URL
[84]	Wang Y T, Fu X Q, Xie L H, Qin W, Li L, Sun X F, Xing S H, Tang K X. 2019. Stress associated protein 1 regulates the development of glandular trichomes in Artemisia annua. Plant Cell, 139:249-259.
[85]	Wang Yan-ge, Li Zu-liang, Yang Jin-na, Cao Ying. 2019. Progress on R3- MYB transcription factors in plant trichome development. Molecular Plant Breeding, 17 (14):4667-4673. (in Chinese)
	王艳鸽, 李祖亮, 杨金娜, 曹颖. 2019. R3-MYB类转录因子在植物表皮毛发育中的研究进展. 分子植物育种, 17 (14):4667-4673.
[86]	Wang Y J, Zeng J, Xia X L, Xu Y, Sun J, Gu J, Sun H N, Lei H N, Chen F D, Jiang J F, Fang W M, Chen S M. 2020. Comparative analysis of leaf trichomes,epidermal wax and defense enzymes activities in response to Puccinia horiana in Chrysanthemum and Ajania species. Horticultural Plant Journal, 6 (3):191-198. doi: 10.1016/j.hpj.2020.03.006 URL
[87]	Wasternack C, Hause B. 2013. Jasmonates:biosynthesis,perception,signal transduction and action in plant stress response,growth and development. An update to the 2007 review in annals of botany. Annals of Botany, 111 (6):1021-1058. doi: 10.1093/aob/mct067 URL pmid: 23558912
[88]	Weinhold A, Meinwald B J. 2011. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proceedings of the National Academy of Sciences of United States of Ameirica, 108 (19):7855-7859.
[89]	Wendel J F, Cronn R C. 2003. Polyploidy and the evolutionary history of cotton. Advances in Agronomy, 78:139-186.
[90]	Werker E. 2000. Trichome diversity and development. Advances in Botanical Research incorporating Advances in Plant Pathology, 31:1-35.
[91]	Wilkins T A, Rajasekaran K, Anderson D M. 2000. Cotton biotechnology. Critical Reviews in Plant Sciences, 19 (6):511-550. doi: 10.1080/07352680091139286 URL
[92]	Xi A L, Yang X Y, Deng M, Chen Y, Shao J X, Zhao J, An L J. 2018. Isolation and identification of two new alleles of STICHEL in Arabidopsis. Biochemical and Biophysical Research Communications, 499 (3):605-610. doi: 10.1016/j.bbrc.2018.03.197 URL
[93]	Xie Z, Kapteyn J, Gang D R. 2008. A systems biology investigation of the MEP/terpenoid and shikimate/phenylpropanoid pathways points to multiple levels of metabolic control in sweet basil glandular trichomes. Plant Journal, 54 (3):349-361. doi: 10.1111/j.1365-313X.2008.03429.x URL
[94]	Xu J, van Herwijnen Z O, Dräger D B, Sui C, Haring M A, Schuurink R C. 2018. SlMYC1 regulates type VI glandular trichome formation and terpene biosynthesis in tomato glandular cells. Plant Cell, 30:2988-3005. doi: 10.1105/tpc.18.00571 URL
[95]	Xu Q, He J, Dong J H, Hou X J, Zhang X. 2018. Genomic survey and expression profiling of the MYB gene family in watermelon. Horticultural Plant Journal, 4 (3):1-15. doi: 10.1016/j.hpj.2017.12.001 URL
[96]	Yan T X, Chen M H, Shen Q, Li L, Fu X Q, Pan Q F, Tang Y L, Shi P, Lv Z Y, Jiang W M, Ma Y N, Hao X L, Sun X F, Tang K X. 2017. HOMEODOMAIN PROTEIN 1 is required for jasmonate-mediated glandular trichome initiation in Artemisia annua. New Phytologist, 213 (3):1145-1155. doi: 10.1111/nph.14205 URL
[97]	Yan T X, Li L, Xie L h, Chen M H, Shen Q, Pan Q F, Fu X Q, Shi P, Tang Y L, Huang H Y, Huang Y W, Huang Y R, Tang K X. 2018. A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua. New Phytologist, 218 (2):567-578. doi: 10.1111/nph.15005 URL
[98]	Yang C X, Li H X, Zhang J H, Luo Z D, Gong P J, Zhang C J, Li J H, Wang T T, Zhang Y Y, Lu Y E, Ye Z B. 2011. A regulatory gene induces trichome formation and embryo lethality in tomato. Proceedings of the National Academy of Sciences of the United States of America, 108 (29):11836-11841.
[99]	Yang C X, Ye Z B. 2013. Trichomes as models for studying plant cell differentiation. Cellular and Molecular Life Sciences, 70 (11):1937-1948. doi: 10.1007/s00018-012-1147-6 URL
[100]	Yang S X, Tian H Y, Sun B G, Liu Y G, Hao Y F, Lv Y Y. 2016. One-pot synthesis of (-)-Ambrox. Scientific Reports, 6:32650. doi: 10.1038/srep32650 URL
[101]	Yang Shan-shan, Wang Xin-yu, Zhu Shao-dong, Chen Guan-liang. 2019. Study on the molecular mechanism of plant trichome development. Shanxi Agricultural Economy, 244 (4):137. (in Chinese)
	杨珊珊, 王欣宇, 朱少东, 陈冠良. 2019. 植物表皮毛发育的分子机制研究. 山西农经, 244 (4):137.
[102]	Ying S, Su M, Wu Y, Zhou L, Fu R, Li Y, Gao H, Luo J, Wang S C, Zhang Y. 2020. Trichome regulator SlMIXTA-like directly manipulates primary metabolism in tomato fruit. Plant Biotechnology Journal, 18 (2):3541-363.
[103]	Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K. 2009. Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development, 136 (6):1039-1048. doi: 10.1242/dev.030585 pmid: 19234066
[104]	Yu N, Cai W, Wang S, Shan C, Wang L, Chen X. 2010. Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell, 22 (7):2322-2335. doi: 10.1105/tpc.109.072579 URL
[105]	Yu X, Chen G, Tang B, Zhang J, Zhou S, Hu Z. 2018. The jasmonate ZIM-domain protein gene SlJAZ2 regulates plant morphology and accelerates flower initiation in solanum lycopersicum plants. Plant Science, 267:65-73. doi: 10.1016/j.plantsci.2017.11.008 URL
[106]	Zhang H, Wang L, Zheng S, Liu Z, Wu X, Gao Z, Cao C, Li Q, Ren Z. 2016. A fragment substitution in the promoter of CsHDZIV11/CsGL3 is responsible for fruit spine density in cucumber (Cucumis sativus L.). Theoretical and applied genetics, 129 (7):1289-1301. doi: 10.1007/s00122-016-2703-5 URL
[107]	Zhao J L, Pan J S, Guan Y, Nie J T, Yang J J, Qu M L, He H L, Cai R. 2015a. Transcriptome analysis in Cucumis sativus identifies genes involved in multicellular trichome development. Genomics, 105 (5-6):296-303. doi: 10.1016/j.ygeno.2014.10.013 URL
[108]	Zhao J L, Wang Y L, Yao D Q, Zhu W Y, Chen L, He H L, Pan J S, Cai R. 2015b. Transcriptome profiling of trichome-less reveals genes associated with multicellular trichome development in Cucumis sativus. Molecular Genetics and Genomics, 290 (5):2007-2018. doi: 10.1007/s00438-015-1057-z URL
[109]	Zou J J, Zheng Z Y, Xue S, Li H H, Wang Y R, Le J. 2016. The role of Arabidopsis actin-related protein 3 in amyloplast sedimentation and polar auxin transport in root gravitropism. Journal of Experimental Botany, 67 (18):5325-5337. doi: 10.1093/jxb/erw294 URL

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