Spatiotemporal Formation of Glands in Plants is Modulated by MYB-like Transcription Factors

Overview

Journal Nat Commun

Specialty Biology

Date 2024 Mar 16

PMID 38491132

Authors

Jiang Chang

Shurong Wu

Ting You

Jianfeng Wang

Bingjing Sun

Bojun Xu

Xiaochun Xu

Yaping Zhang

Shuang Wu

Affiliations

Soon will be listed here.

Abstract

About one third of vascular plants develop glandular trichomes, which produce defensive compounds that repel herbivores and act as a natural biofactory for important pharmaceuticals such as artemisinin and cannabinoids. However, only a few regulators of glandular structures have been characterized so far. Here we have identified two closely-related MYB-like genes that redundantly inhibit the formation of glandular cells in tomatoes, and they are named as GLAND CELL REPRESSOR (GCR) 1 and 2. The GCR genes highly express in the apical cells of tomato trichomes, with expression gradually diminishing as the cells transition into glands. The spatiotemporal expression of GCR genes is coordinated by a two-step inhibition process mediated by SlTOE1B and GCRs. Furthermore, we demonstrate that the GCR genes act by suppressing Leafless (LFS), a gene that promotes gland formation. Intriguingly, homologous GCR genes from tobacco and petunia also inhibit gland formation, suggesting that the GCR-mediated repression mechanism likely represents a conserved regulatory pathway for glands across different plant species.

Citing Articles

Plant growth Enhancement in Colchicine-Treated Tomato Seeds without Polyploidy Induction.

Obando-Gonzalez R, Martinez-Hernandez L, Nunez-Munoz L, Calderon-Perez B, Ruiz-Medrano R, Ramirez-Pool J Plant Mol Biol. 2024; 115(1):3.

PMID: 39668327 PMC: 11638462. DOI: 10.1007/s11103-024-01521-1.

References

Yuan Y, Xu X, Luo Y, Gong Z, Hu X, Wu M . R2R3 MYB-dependent auxin signalling regulates trichome formation, and increased trichome density confers spider mite tolerance on tomato. Plant Biotechnol J. 2020; 19(1):138-152. PMC: 7769234. DOI: 10.1111/pbi.13448. View

Rowley M, Bohmdorfer G, Wierzbicki A . Analysis of long non-coding RNAs produced by a specialized RNA polymerase in Arabidopsis thaliana. Methods. 2013; 63(2):160-9. PMC: 5107611. DOI: 10.1016/j.ymeth.2013.05.006. View

Yan T, Li L, Xie L, Chen M, Shen Q, Pan Q . A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua. New Phytol. 2018; 218(2):567-578. DOI: 10.1111/nph.15005. View

Churchman M, Brown M, Kato N, Kirik V, Hulskamp M, Inze D . SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell. 2006; 18(11):3145-57. PMC: 1693949. DOI: 10.1105/tpc.106.044834. View

Tu Y . The discovery of artemisinin (qinghaosu) and gifts from Chinese medicine. Nat Med. 2011; 17(10):1217-20. DOI: 10.1038/nm.2471. View

Schilmiller A, Charbonneau A, Last R . Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes. Proc Natl Acad Sci U S A. 2012; 109(40):16377-82. PMC: 3479610. DOI: 10.1073/pnas.1207906109. View

Chun J, Kim S, Kim H, Cho J, Kwon H, Kim J . SlHair2 Regulates the Initiation and Elongation of Type I Trichomes on Tomato Leaves and Stems. Plant Cell Physiol. 2021; 62(9):1446-1459. DOI: 10.1093/pcp/pcab090. View

Krogan N, Hogan K, Long J . APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development. 2012; 139(22):4180-90. PMC: 3478687. DOI: 10.1242/dev.085407. View

Chang J, Yu T, Yang Q, Li C, Xiong C, Gao S . Hair, encoding a single C2H2 zinc-finger protein, regulates multicellular trichome formation in tomato. Plant J. 2018; 96(1):90-102. DOI: 10.1111/tpj.14018. View

10.

Grebe M . The patterning of epidermal hairs in Arabidopsis--updated. Curr Opin Plant Biol. 2011; 15(1):31-7. DOI: 10.1016/j.pbi.2011.10.010. View

11.

Yang C, Gao Y, Gao S, Yu G, Xiong C, Chang J . Transcriptome profile analysis of cell proliferation molecular processes during multicellular trichome formation induced by tomato Wov gene in tobacco. BMC Genomics. 2015; 16:868. PMC: 4623907. DOI: 10.1186/s12864-015-2099-7. View

12.

Varkonyi-Gasic E, Wu R, Wood M, Walton E, Hellens R . Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods. 2007; 3:12. PMC: 2225395. DOI: 10.1186/1746-4811-3-12. View

13.

Balcke G, Bennewitz S, Bergau N, Athmer B, Henning A, Majovsky P . Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites. Plant Cell. 2017; 29(5):960-983. PMC: 5466034. DOI: 10.1105/tpc.17.00060. View

14.

Jones B, Frasse P, Olmos E, Zegzouti H, Li Z, Latche A . Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant J. 2002; 32(4):603-13. DOI: 10.1046/j.1365-313x.2002.01450.x. View

15.

Tissier A, Morgan J, Dudareva N . Plant Volatiles: Going 'In' but not 'Out' of Trichome Cavities. Trends Plant Sci. 2017; 22(11):930-938. DOI: 10.1016/j.tplants.2017.09.001. View

16.

Ghosh B, Westbrook T, Jones A . Comparative structural profiling of trichome specialized metabolites in tomato () and : acylsugar profiles revealed by UHPLC/MS and NMR. Metabolomics. 2014; 10(3):496-507. PMC: 3984663. DOI: 10.1007/s11306-013-0585-y. View

17.

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

18.

Yang C, Ye Z . Trichomes as models for studying plant cell differentiation. Cell Mol Life Sci. 2012; 70(11):1937-48. PMC: 11113616. DOI: 10.1007/s00018-012-1147-6. View

19.

Leong B, Lybrand D, Lou Y, Fan P, Schilmiller A, Last R . Evolution of metabolic novelty: A trichome-expressed invertase creates specialized metabolic diversity in wild tomato. Sci Adv. 2019; 5(4):eaaw3754. PMC: 6482016. DOI: 10.1126/sciadv.aaw3754. View

20.

Kumar N, Harashima H, Kalve S, Bramsiepe J, Wang K, Sizani B . Functional Conservation in the SIAMESE-RELATED Family of Cyclin-Dependent Kinase Inhibitors in Land Plants. Plant Cell. 2015; 27(11):3065-80. PMC: 4682297. DOI: 10.1105/tpc.15.00489. View