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Journal of Integrative Agriculture  2022, Vol. 21 Issue (10): 2926-2942    DOI: 10.1016/j.jia.2022.07.050
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
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Comparative transcriptomic analysis of Rosa sterilis inflorescence branches with different trichome types reveals an R3-MYB transcription factor that negatively regulates trichome formation

MA Wen-tao1, 2, LU Min1, AN Hua-ming1, 2, YI Yin3

1 Guizhou Engineering Research Center for Fruit Crops, Agricultural College, Guizhou University, Guiyang 550025, P.R.China
2 Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), Institute of Agro-bioengineering, College of Life Science, Guizhou University, Guiyang 550025, P.R.China
3 Key Laboratory of Plant Physiology and Development Regulation, Guizhou Normal University, Guiyang 550025, P.R.China
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摘要  无籽刺梨(Rosa sterilis S. D. Shi)果实富含营养及保健成分,是原产我国的特有经济树种,因其地上部分遍布不同类型的表皮毛或刺直接影响了果实外观品质及生产管理。该研究利用RNA-Seq技术比较分析了的发育早期花序轴(仅具鞭状毛)和果柄(具鞭状毛和长柄头状腺毛)中表皮毛形成相关基因的表达差异,其中R3-MYB类转录因子RsETC1在花序轴中的转录水平显著高于果柄。进一步qRT-PCR分析表明,在花芽萌发后初期的前三阶段,RsETC1在花序轴中的表达均显著高于果柄;而且其在无毛或去毛组织中的转录水平也明显高于有毛组织,表明该基因对表皮毛尤其是腺状表皮毛的起始形成具有负调控作用。在拟南芥中异源过量表达RsETC1会显著抑制除AtTTG1外的内源表皮毛起始基因的表达,从而导致转基因植株光滑无毛的表型。此外,果柄中JA、GA3和CKs等内源激素的含量显著高于花序轴,并且与内源激素生物合成和信号转导相关的基因表达模式也表现出一致的趋势,表明该几类激素可能对无籽刺梨表皮毛的形成和发育起着重要作用。本研究为揭示和完善蔷薇科植物表皮毛形成的分子机制提供了新的视角。


Rosa sterilis S. D. Shi is an important economic tree in China that produces fruits with high nutritional and medicinal value.  Many of Rsterilis’ organs are covered with different types of trichomes or prickles that directly affect fruit appearance and plant management.  This study used RNA sequencing technology to analyze the transcriptomes of two parts of the inflorescence branch, namely inflorescence stems with flagellated trichomes and pedicels with both flagellated and glandular trichomes.  Comparative transcriptomic analysis showed that many transcription factors (TFs) are potentially involved in the formation and development of trichomes.  The accumulation of RsETC1, a TF of the R3-MYB family, was significantly higher in inflorescence stems than in pedicels; quantitative reverse transcription PCR (qRT-PCR) verified that its expression was significantly higher in inflorescence stems than in pedicels during the first three development stages, indicating its inhibitory action on the initiation of glandular trichomes in Rsterilis.  The mRNA level of RsETC1 accumulated to significantly higher levels in trichomeless tissues than in tissues with trichromes, suggesting that this gene may inhibit the formation of trichomes in Rsterilis.  Over-expression of RsETC1 in Arabidopsis resulted in glabrous phenotypes, and the expression of trichome-related endogenous genes, except for TTG1, was markedly reduced.  In addition, the contents of the phytohormones jasmonic acid (JA), gibberellin A3 (GA3), and cytokinins (CKs) in pedicels were significantly higher than those in inflorescence stems, and the expression patterns of the genes related to hormone biosynthesis and signal transduction presented consistent responses, suggesting that the transduction of these hormones might be crucial for trichome initiation and development.  These data provide a new perspective for revealing the molecular mechanism of trichome formation in Rsterilis.

Keywords:  comparative transcriptome       inflorescence stem        pedicels        R3-MYB transcription factor        trichome  
Received: 11 January 2022   Accepted: 11 May 2022
Fund: This work was supported by grants from the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province, China (U1812401), and the Talent Project of Guizhou Province, China (20164016).
About author:  Correspondence AN Hua-ming, Tel/Fax: +86-851-88305271, E-mail:; YI Yin, E-mail:

Cite this article: 

MA Wen-tao, LU Min, AN Hua-ming, YI Yin. 2022. Comparative transcriptomic analysis of Rosa sterilis inflorescence branches with different trichome types reveals an R3-MYB transcription factor that negatively regulates trichome formation. Journal of Integrative Agriculture, 21(10): 2926-2942.

Andrade M C, Silva A A D, Neiva I P, Oliveira I R C, Castro E, 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, doi: 10.1007/s10681-016-1792-1.
Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J, Davis A, Dolinski K, Dwight S, Eppig J, Harris M, Issel-Tarver L, Kasarskis A, Lewis S, Matese J, Richardson J, Ringwald M, Rubin G, Sherlock G. 2000. Gene ontology: Tool for the unifification of biology. Nature Genetics, 25, 25–29.
Burns K. 2014. Are there general patterns in plant defence against megaherbivores? Biological Journal of the Linnean Society, 111, 38–48. 
Chen C H, Liu M L, Jiang L, Liu X F, Zhao J Y, Yan S S, Yang S, Ren H Z, Liu R Y, Zhang X L. 2014. Transcriptome profiling reveals roles of meristem regulators and polarity genes during fruit trichome development in cucumber (Cucumis sativus L.). Journal of Experimental Botany, 65, 4943–4958.
Chen M H, Yan T X, Shen Q, Lu X, Pan Q F, Huang Y R, Tang Y L, Fu X Q, Liu M, Jiang W M, Lv Z Y, Shi P, Ma Y N, Hao X L, Zhang L D, Li L, Tang K X. 2017. GLANDULAR TRICHOME-SPECIFIC WRKY 1 promotes artemisinin biosynthesis in Artemisia annua. New Phytologist, 214, 304–316.
Chopra D, Mapar M C, Stephan L. 2019. Genetic and molecular analysis of trichome development in Arabisalpina. Proceedings of the National Academy of Sciences of the United States of America, 116, 12078–12083.
Clough S, Bent A. 1998. Floral dip: A simplifed method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743.
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends in Plant Science, 15, 573–581.
Feng Z X, Bartholomew S, Liu Z Y, Cui Y Y, Dong Y M, Li S, Wu H Y, Ren H Z, Liu X W. 2021. Glandular trichomes: New focus on horticultural crops. Horticulture Research, 8, 158.
He J Y, Zhang Y H, Ma N, Zhang X L, Liu M H, Fu W M. 2016. Comparative analysis of multiple ingredients in Rosa roxburghii and R. sterilis fruits and their antioxidant activities. Journal of Functional Foods, 27, 29–41.
Hua B, Chang J, Han X Q, Xu Z J, Hu S R, Li S, Wang R Y, Yang L L, Yang M N, Wu S S, Shen J Y, Yu X M, Wu S. 2022. H and HL synergistically regulate jasmonate-triggered trichome formation in tomato. Horticulture Research, 9, doi: 10.1093/hortre/uhab080.
Hua B, Chang J, Xu Z J, Han X Q, Xu M Y, Yang M N, Yang C X, Ye Z B, Wu S. 2021. HOMEODOMAIN PROTEIN8 mediates jasmonate-triggered trichome elongation in tomato. New Phytologist, 230, 1063–1077.
Hülskamp M. 2004. Plant trichomes: A model for cell differentiation. Nature Reviews Molecular Cell Biology, 5, 471–480.
Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Research, 32, 277–280.
Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P. 2020. Protective and defensive roles of non‑glandular trichomes against multiple stresses: Structure–function coordination. Journal for Research, 31, 1–12.
Kellogg A, Branaman T, Jones N, Little Z, Swanson J. 2011. Morphological studies of developing Rubus prickles suggest that they are modified glandular trichomes. Botany, 89, 217–226. 
Li Q, Nan Y, Qin J, Yang Y, Hao X, Yang X. 2016. Chemical constituents from medical and edible plants of Rosa roxburghii. China Journal of Chinese Materia Medica, 41, 451–455. (in Chinese)
Liu S, Chen W, Qu L, Gai Y, Jiang X. 2013. Simultaneous determination of 24 or more acidic and alkaline phytohormones in femtomole quantities of plant tissues by high-performance liquid chromatography-electrospray ionization-ion trap mass spectrometry. Analytical and Bioanalytical Chemistry, 405, 1257–1266.
Liu X, Bartholomew E, Cai Y, Ren H. 2016. Trichome-related mutants provide a new perspective on multicellular trichome initiation and development in cucumber (Cucumis sativus L). Frontiers in Plant Science, 7, 1187.
Livak K, Schmittgen T. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.
Ma W T, Lu M, Ludlow R, Wang D J, Zeng J W, An H M. 2021. Contrastive analysis of trichome distribution, morphology, structure, and associated gene expression reveals the formation factors of different trichome types in two commercial Rosa species. Scientia Horticulturae, 285, 110131.
Ma Z, Wen J, Stefanie M, Chen L, Liu X. 2016. Morphology, structure, and ontogeny of trichomes of the grape genus (Vitis, Vitaceae). Frontiers in Plant Science, doi: 10.3389/fpls.2016.00704.
Machado A, Wu Y, Yang Y, Llewellyn D, Dennis E. 2009. The MYB transcription factor GhMYB25 regulates early fibre and trichome development. The Plant Journal, 59, 52–62.
Maes L, Goossens A. 2010. Hormone-mediated promotion of trichome initiation in plants is conserved but utilizes species and trichome-specific regulatory mechanisms. Plant Signaling & Behavior, 5, 205–207.
Pan J, Zhang L, Chen G, Wen H, Chen Y, Du H, Zhao J L, He H L, Lian H L, Chen H M, Shi J X, Cai R, Wang G, Pan J. 2021. Study of micro-trichome (mict) reveals novel connections between transcriptional regulation of multicellular trichome development and specific metabolism in cucumber. Horticulture Research, 8, 21.
Pattanaik S, Patra B, Singh S, Yuan L. 2014. An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Frontiers in Plant Science, doi: 10.3389/fpls.2014.00259.
Schellmann S, Hülskamp M. 2005. Epidermal differentiation: Trichomes in Arabidopsis as a model system. International Journal of Developmental Biology, 49, 579–584.
Tan Z, Guo F, Yang F, Liu L, Zhang X, Ren H Z. 2012. Overexpression of cucumber CsTRY greatly represses trichome formation in Arabidopsis. Acta Horticulturae Sinica, 39, 91–100. (in Chinese)
Tominaga-Wada 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, e54019.
Tominaga-Wada R, Wada T. 2017. Extended C termini of CPC-LIKE MYB proteins confer functional diversity in Arabidopsis epidermal cell differentiation. Development, 144, 2375–2380.
Wang S, Chen J. 2014. Regulation of cell fate determination by single-repeat R3MYB transcription factors in Arabidopsis. Frontiers in Plant Science, 5, 133.
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, 191–198.
Yuan R, Cao Y F, Li T Y, Yang F, Yu L, Qin Y, Du X M, Liu F, Ding M Q, Jiang Y R, Zhang H, Paterson A H, Rong J K. 2021. Differentiation in the genetic basis of stem trichome development between cultivated tetraploid cotton species. BMC Plant Biology, 21, 115.
Zhang Y, Zhang J, Shao C, Bao Z, Liu G, Bao M. 2019. Single‑repeat R3 MYB transcription factors from Platanus acerifolia negatively regulate trichome formation in Arabidopsis. Planta, 249, 861–877.
Zhong M C, Jiang X D, Yang G Q, Cui W H, Suo Z Q, Wang W J, Sun Y B, Wang D, Cheng X C, Li X M, Dong X, Tang K X, Li D Z, Hu J Y. 2021. A genomic link in China roses: and they all lived prickly but water deficient ever after? National Science Review, 8, 154–170.

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