Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (12): 3589-3599    DOI: 10.1016/j.jia.2022.08.032
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Identifying candidate genes involved in trichome formation on carrot stems by transcriptome profiling and resequencing 
WU Zhe1*, YANG Xuan1*, ZHAO Yu-xuan1, JIA Li2
1 College of Horticulture, Shanxi Agricultural University, Taigu 030801, P.R.China
2 Key Laboratory of Genetic Improvement and Ecophysiology of Horticultural Crop of Anhui Province, Institute of Horticulture, Anhui Academy of Agricultural Sciences, Hefei 230001, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      

表皮毛是由表皮细胞发育而来的特殊结构,可以保护植物免受生物和非生物胁迫。胡萝卜在生殖阶段被表皮毛覆盖,但胡萝卜表皮毛的形态和控制表皮毛形成的候选基因仍未知。研究结果表明,胡萝卜表皮毛是非腺毛且不分枝,分布在胡萝卜的茎、叶、叶柄、花梗和种子上。本研究对1个胡萝卜花茎上分布稀而短的表皮突变体(sst)和1个花茎上分布长而密的表皮毛野生型(wt)进行了重测序分析,在sst上共检测到15, 396个非同义突变,包含42个与表皮毛相关的基因。对wtsst长度为10cm的一级侧枝进行了转录组分析,获得了6, 576个差异表达基因(DEG),包括24个表皮毛相关的基因。qRT-PCR验证的这些差异表达基因中,有3个显著上调,20个显著下调,1个没有差异。综合重测序和转录组测序分析发现,12个表皮毛相关的基因含有非同义突变且在sst中显著下调表达,可归类为5个转录因子家族。因此,这些基因是可能的候选基因,他们的非同义突变和下调表达可能是导致sst中胡萝卜花茎的表皮毛短且稀少的突变。


Trichomes are specialized structures developed from epidermal cells and can protect plants against biotic and abiotic stresses.  Trichomes cover carrots during the generative phase.  However, the morphology of the carrot trichomes and candidate genes controlling the formation of trichomes are still unclear.  This study found that carrot trichomes were non-glandular and unbranched hairs distributed on the stem, leaf, petiole, pedicel, and seed of carrot.  Resequencing analysis of a trichome mutant with sparse and short trichomes (sst) and a wild type (wt) with long and dense trichomes on carrot stems was conducted.  A total of 15 396 genes containing nonsynonymous mutations in sst were obtained, including 42 trichome-related genes.  We also analyzed the transcriptome of the trichomes on secondary branches when these secondary branches were 10 cm long between wt and sst and obtained 6 576 differentially expressed genes (DEGs), including 24 trichome-related genes.  qRT-PCR validation exhibited three significantly up-regulated DEGs, 20 significantly down-regulated, and one with no difference.  We considered both the resequencing and transcriptome sequencing analyses and found that 12 trichome-related genes that were grouped into five transcription factor families containing nonsynonymous mutations and significantly down-regulated in sst.  Therefore, these genes are potentially promising candidate genes whose nonsynonymous mutations and down-regulation may result in scarce and short trichomes mutation on carrot stems in sst.

Keywords:  carrot       trichome        resequencing        transcriptome        candidate genes  
Received: 10 March 2022   Accepted: 25 May 2022
Fund: This study was sponsored by the Research Project Supported by Shanxi Scholarship Council of China (2021–066), the National Natural Science Foundation of China (31601751), the Key Research and Development Plan of Shanxi Province, China (201903D221063), the Fundamental Research Program of Shanxi Province, China (20210302123412), and the Science and Technology Innovation Project of Shanxi Agricultural University, China (2016ZZ02).
About author:  Correspondence WU Zhe, E-mail:; JIA Li, Tel: +86-551-65160817, E-mail: * These authors contributed equally to this study.

Cite this article: 

WU Zhe, YANG Xuan, ZHAO Yu-xuan, JIA Li. 2022. Identifying candidate genes involved in trichome formation on carrot stems by transcriptome profiling and resequencing . Journal of Integrative Agriculture, 21(12): 3589-3599.

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, 52.
Balkunde R, Pesch M, Hülskamp M. 2010. Trichome patterning in Arabidopsis thaliana: From geneic to molecular models. Current Topics in Developmental Biology, 91, 299–321.
Bloomer R H, Juenger T E, Symonds V V. 2012. Natural variation in GL1 and its effects on trichome density in Arabidopsis thaliana. Molecular Ecology, 21, 3501–3515.
Bouyer D, Geier F, Kragler F, Schnittger A, Pesch M, Wester K, Balkunde R, Timmer J, Fleck C, Hülskamp M. 2008. Two-dimensional patterning by a trapping/depletion mechanism: The role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biology, 6, e141. 
Chalvin C, Drevensek S, Dron M, Bendahmane A, Boualem A. 2020. Genetic control of glandular trichome development. Trends in Plant Science, 25, 477–487.
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 a single C2H2 zinc-finger protein, regulates multicellular trichome formation in tomato. The Plant Journal, 96, 90–102.
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 SlbHLH95, a basic helix-loop-helix transcription factor family member, impacts trichome formation via regulating gibberellin biosynthesis in tomato. Journal of Experimental Botany, 71, 3450–3462.
Chun J I, Kim S M, Kim H J, Cho J Y, Kwon H W, Kim J I, Seo J K, Jung C K, Kang J H. 2021. SlHair2 regulates the initiation and elongation of type I trichomes on tomato leaves and stems. Plant and Cell Physiology, 62, 1446–1459.
Eulgem T, Rushton P J, Robatzek S, Somssich I E. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science, 5, 1360–1385.
Ewas M, Gao Y Q, Wang S C, Liu X Q, Zhang H Y, 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, 1413–1418.
Glas J J, Schimmel B C, Schimmel B C J, Alba J M, Escobar-Bravo R, Schuurink R C, Kant M R. 2012. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. International Journal of Molecular Sciences, 13, 17077–17103.
Huang C Z, Jiao X M, Yang L, Zhang M M, Dai M M, Wang L, Wang K, Bai L, Song C P. 2018. ROP-GEF signal transduction is involved in AtCAP1-regulated root hair growth. Plant Growth Regulation, 87, 1–8.
Hülskamp M, Schnittger A, Folkers U. 1998. Pattern formation and cell differentiation, trichomes in Arabidopsis as a genetic model system. International Review of Cytology, 186, 147–178.
Johnson C S, Kolevski B, Smyth D R. 2002. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of grabidopsis, encodes a WRKY transcription factor. The Plant Cell, 14, 1359–1375.
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, 1053–1064.
Kim S Y, Hyoung S J, So W M, Shin J S. 2018. The novel transcription factor TRP interacts with ZFP5, a trichome initiation-related transcription factor, and negatively regulates trichome initiation through gibberellic acid signaling. Plant Molecular Biology, 96, 315–326.
Kirik V, Lee M M, Wester K, Herrmann U, Zheng Z G, Oppenheimer D, Schiefelbein J, Hulskamp M. 2005. Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development, 132, 1477–1485.
Koornneef M, Dellaert L W, Van der Veen J H. 1982. EMS- and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutation Research, 93, 109–120.
Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25, 1754–1760.
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, 945–960.
Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I. 2003. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science, 300, 1427–1430.
Pattanaik S, Patra B, Singh S K, Yuan L. 2014. An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Frontiers in Plant Science, 5, 259.
Peiffer M, Tooker J F, Luthe D S, Felton G W. 2009. Plants on early alert, glandular trichomes as sensors for insect herbivores. New Phytologist, 184, 644–656.
Rerie W G, Feldmann K A, Marks M D. 1994. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes & Development, 8, 1388–1399.
Schellmann S, Hülskamp M. 2005. Epidermal differentiation, trichomes in Arabidopsis as a model system. International Journal of Developmental Biology, 49, 579–584.
Sun L L, Zhang A D, Zhou Z J, Zhao Y Q, Yan A, Bao S J, Yu H, Gan Y B. 2015. GLABROUS INFLORESCENCE STEMS3 (GIS3) regulates trichome initiation and development in Arabidopsis. New Phytologist, 206, 220–230.
Sun L L, Zhou Z J, An L J, An Y, Zhao Y Q, Meng X F, Steele-King C, Gan Y B. 2013. GLABROUS INFLORESCENCE STEMS regulates trichome branching by genetically interacting with SIM in Arabidopsis. Journal of Zhejiang University (Science B), 14, 563–569.
Tian D G, Tooker J, Peiffer M, Chung S H, Felton G W. 2012. Role of trichomes in defense against herbivores, comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta, 236, 1053–1066.
Traw M B, Bergelson J. 2003. Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology, 133, 1367–1375.
Werker E. 2000. Trichome diversity and development. Advances in Botanical Research, 31, 1–35.
Xu J S, van Herwijnen Z O, Drager 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. The Plant Cell, 30, 2988–3005.
Yan A, Pan J B, An L Z, Gan Y B, Feng H Y. 2012. The responses of trichome mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana. Journal of Photochemistry and Photobiology (B: Biology), 113, 29–35.
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, 11836–11841.
Ying S Y, Su M, Wu Y, Zhou L, Fu R, Li Y, Guo H, Luo J, Wang S C, Zhang Y. 2020. Trichome regulator SlMX1TA-like directly manipulates primary metabolism in tomato fruit. Plant Biotechnology Journal, 18, 354–363.
Zhang N, Yang L, Luo S, Wang X T, Wang W, Cheng Y X, Tian H N, Zheng K J, Cai L, Wang S C. 2018. Genetic evidence suggests that GIS functions downstream of TCL1 to regulate trichome formation in Arabidopsis. BMC Plant Biology, 18, 63.
Zhou Z J, An L J, Sun L L, Zhu S J, Xi W Y, Broun P, Yu H, Gan Y B. 2011. Zinc Finger Protein5 is required for the control of trichome initiation by acting upstream of zinc finger protein 8 in Arabidopsis. Plant Physiology, 157, 673–682.
Zhou Z J, Sun L L, Zhao Y Q, An L J, Yan A, Meng X F, Gan Y B. 2013. Zinc Finger Protein 6 (ZFP6) regulates trichome initiation by integrating gibberellin and cytokinin signaling in Arabidopsis thaliana. New Phytologist, 198, 699–708.
Zhu P Y, He L Y, Li Y Q, Huang W P, Xi F, Lin L, Zhi Q H, Zhang W W, Tang Y T, Geng C Y, Lu Z Y, Xu X. 2014. OTG-snpcaller, an optimized pipeline based on TMAP and GATK for SNP calling from ion torrent data. PLoS ONE, 9, e97507.
[1] FAN Xiao-xue, BIAN Zhong-hua, SONG Bo, XU Hai. Transcriptome analysis reveals the differential regulatory effects of red and blue light on nitrate metabolism in pakchoi (Brassica campestris L.)[J]. >Journal of Integrative Agriculture, 2022, 21(4): 1015-1027.
[2] WANG Qing, ZUO Jin-hua, WANG Qian, NA Yang, GAO Li-pu. Inhibitory effect of chitosan on growth of the fungal phytopathogen, Sclerotinia sclerotiorum, and sclerotinia rot of carrot[J]. >Journal of Integrative Agriculture, 2015, 14(4): 691-697.
No Suggested Reading articles found!