Study of Micro-trichome (mict) Reveals Novel Connections Between Transcriptional Regulation of Multicellular Trichome Development and Specific Metabolism in Cucumber

Overview

Journal Hortic Res

Publisher Oxford University Press

Date 2021 Feb 1

PMID 33518711

Citations 9

Authors

Jian Pan

Leyu Zhang

Guanqun Chen

HaiFan Wen

Yue Chen

Hui Du

Junlong Zhao

Huanle He

Hongli Lian

Huiming Chen

Jianxin Shi

Run Cai

Gang Wang

Junsong Pan

Affiliations

Soon will be listed here.

Abstract

Trichomes that cover the epidermis of aerial plant organs play multiple roles in plant protection. Compared with a unicellular trichome in model plants, the development mechanism of the multicellular trichome is largely unclear. Notably, variations in trichome development are often accompanied by defects in the biosynthesis of cuticle and secondary metabolites; however, major questions about the interactions between developmental differences in trichomes and defects in metabolic pathways remain unanswered. Here, we characterized the glabrous mutant mict/csgl1/cstbh via combined metabolomic and transcriptomic analyses to extend our limited knowledge regarding multicellular trichome development and metabolism in cucumber. Mict was found to be explicitly expressed within trichome cells. Transcriptomic analysis indicated that genes involved in flavonoid and cuticle metabolism are significantly downregulated in mict mutants. Further metabolomic analysis confirmed that flavonoids, lipids, and cuticle compositions are dramatically altered in mict mutants. Additional studies revealed that Mict regulates flavonoid, lipid, and cuticle biosynthesis by likely directly binding to downstream functional genes, such as CsTT4, CsFLS1, CsCER26, and CsMYB36. These findings suggest that specific metabolic pathways (e.g., flavonoids and cuticle components) are co-regulated by Mict and provide insights into transcriptional regulation mechanisms of multicellular trichome development and its specific metabolism in cucumber.

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References

Takeda S, Iwasaki A, Tatematsu K, Okada K . The Half-Size ABC Transporter FOLDED PETALS 2/ABCG13 Is Involved in Petal Elongation through Narrow Spaces in Arabidopsis thaliana Floral Buds. Plants (Basel). 2016; 3(3):348-58. PMC: 4844351. DOI: 10.3390/plants3030348. View

Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L . The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol. 2007; 145(3):653-67. PMC: 2048791. DOI: 10.1104/pp.107.107300. View

Oshima Y, Mitsuda N . The MIXTA-like transcription factor MYB16 is a major regulator of cuticle formation in vegetative organs. Plant Signal Behav. 2013; 8(11):e26826. PMC: 4091352. DOI: 10.4161/psb.26826. View

Choi Y, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T . Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta. 2001; 213(1):45-50. DOI: 10.1007/s004250000487. View

Li L, Zhao Y, McCaig B, Wingerd B, Wang J, Whalon M . 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. 2003; 16(1):126-43. PMC: 301400. DOI: 10.1105/tpc.017954. View

Wang Y, Nie J, Chen H, Guo C, Pan J, He H . Identification and mapping of Tril, a homeodomain-leucine zipper gene involved in multicellular trichome initiation in Cucumis sativus. Theor Appl Genet. 2015; 129(2):305-16. DOI: 10.1007/s00122-015-2628-4. View

Yeats T, Rose J . The formation and function of plant cuticles. Plant Physiol. 2013; 163(1):5-20. PMC: 3762664. DOI: 10.1104/pp.113.222737. View

Kuhn B, Geisler M, Bigler L, Ringli C . Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol. 2011; 156(2):585-95. PMC: 3177260. DOI: 10.1104/pp.111.175976. View

Chen M, Yan T, Shen Q, Lu X, Pan Q, Huang Y . GLANDULAR TRICHOME-SPECIFIC WRKY 1 promotes artemisinin biosynthesis in Artemisia annua. New Phytol. 2016; 214(1):304-316. DOI: 10.1111/nph.14373. View

10.

Li F, Wu X, Lam P, Bird D, Zheng H, Samuels L . Identification of the wax ester synthase/acyl-coenzyme A: diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol. 2008; 148(1):97-107. PMC: 2528131. DOI: 10.1104/pp.108.123471. View

11.

Borisjuk N, Hrmova M, Lopato S . Transcriptional regulation of cuticle biosynthesis. Biotechnol Adv. 2014; 32(2):526-40. DOI: 10.1016/j.biotechadv.2014.01.005. View

12.

Pascal S, Bernard A, Sorel M, Pervent M, Vile D, Haslam R . The Arabidopsis cer26 mutant, like the cer2 mutant, is specifically affected in the very long chain fatty acid elongation process. Plant J. 2013; 73(5):733-46. DOI: 10.1111/tpj.12060. View

13.

Marks M, Wenger J, Gilding E, Jilk R, Dixon R . Transcriptome analysis of Arabidopsis wild-type and gl3-sst sim trichomes identifies four additional genes required for trichome development. Mol Plant. 2009; 2(4):803-822. PMC: 2713768. DOI: 10.1093/mp/ssp037. View

14.

Kurdyukov S, Faust A, Trenkamp S, Bar S, Franke R, Efremova N . Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain alpha-,omega-dicarboxylic fatty acids and formation of extracellular matrix. Planta. 2006; 224(2):315-29. DOI: 10.1007/s00425-005-0215-7. View

15.

Falcone Ferreyra M, Rius S, Emiliani J, Pourcel L, Feller A, Morohashi K . Cloning and characterization of a UV-B-inducible maize flavonol synthase. Plant J. 2010; 62(1):77-91. DOI: 10.1111/j.1365-313X.2010.04133.x. View

16.

Yang C, Li H, Zhang J, Luo Z, Gong P, Zhang C . A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci U S A. 2011; 108(29):11836-41. PMC: 3141934. DOI: 10.1073/pnas.1100532108. View

17.

Li G, Meng Z, Kong H, Chen Z, Theissen G, Lu A . Characterization of candidate class A, B and E floral homeotic genes from the perianthless basal angiosperm Chloranthus spicatus (Chloranthaceae). Dev Genes Evol. 2005; 215(9):437-49. DOI: 10.1007/s00427-005-0002-2. View

18.

Tian N, Liu F, Wang P, Yan X, Gao H, Zeng X . Overexpression of , a Lipid Transfer Protein of , Results in Increased Trichome Density and Altered Concentration of Secondary Metabolites. Int J Mol Sci. 2018; 19(6). PMC: 6032385. DOI: 10.3390/ijms19061733. View

19.

Kang J, Shi F, Jones A, Marks M, Howe G . Distortion of trichome morphology by the hairless mutation of tomato affects leaf surface chemistry. J Exp Bot. 2009; 61(4):1053-64. PMC: 2826649. DOI: 10.1093/jxb/erp370. View

20.

Hu C, Zhao H, Wang W, Xu M, Shi J, Nie X . Identification of Conserved and Diverse Metabolic Shift of the Stylar, Intermediate and Peduncular Segments of Cucumber Fruit during Development. Int J Mol Sci. 2018; 19(1). PMC: 5796084. DOI: 10.3390/ijms19010135. View