Precise Transcriptional Control of Cellular Quiescence by BRAVO/WOX5 Complex in Arabidopsis Roots

Overview

Journal Mol Syst Biol

Specialty Molecular Biology

Date 2021 Jun 16

PMID 34132490

Citations 12

Authors

Isabel Betegon-Putze

Josep Mercadal

Nadja Bosch

Ainoa Planas-Riverola

Mar Marques-Bueno

Josep Vilarrasa-Blasi

David Frigola

Rebecca C Burkart

Cristina Martinez

Ana Conesa

Rosangela Sozzani

Yvonne Stahl

Salome Prat

Marta Ibanes

Ana I Cano-Delgado

Affiliations

Soon will be listed here.

Abstract

Understanding stem cell regulatory circuits is the next challenge in plant biology, as these cells are essential for tissue growth and organ regeneration in response to stress. In the Arabidopsis primary root apex, stem cell-specific transcription factors BRAVO and WOX5 co-localize in the quiescent centre (QC) cells, where they commonly repress cell division so that these cells can act as a reservoir to replenish surrounding stem cells, yet their molecular connection remains unknown. Genetic and biochemical analysis indicates that BRAVO and WOX5 form a transcription factor complex that modulates gene expression in the QC cells to preserve overall root growth and architecture. Furthermore, by using mathematical modelling we establish that BRAVO uses the WOX5/BRAVO complex to promote WOX5 activity in the stem cells. Our results unveil the importance of transcriptional regulatory circuits in plant stem cell development.

Citing Articles

Modeling Arabidopsis root growth and development.

Ibanes M Plant Physiol. 2025; 197(2).

PMID: 40036788 PMC: 11878784. DOI: 10.1093/plphys/kiaf045.

Deciphering the molecular logic of WOX5 function in the root stem cell organizer.

Zhang N, Bitterli P, Oluoch P, Hermann M, Aichinger E, Groot E EMBO J. 2024; 44(1):281-303.

PMID: 39558109 PMC: 11696986. DOI: 10.1038/s44318-024-00302-2.

A coherent feed-forward loop in the Arabidopsis root stem cell organizer regulates auxin biosynthesis and columella stem cell maintenance.

Sharma M, Friedrich T, Oluoch P, Zhang N, Peruzzo F, Jha V Nat Plants. 2024; 10(11):1737-1748.

PMID: 39394505 DOI: 10.1038/s41477-024-01810-z.

Single-cell network analysis reveals gene expression programs for Arabidopsis root development and metabolism.

Han E, Geng Z, Qin Y, Wang Y, Ma S Plant Commun. 2024; 5(8):100978.

PMID: 38783601 PMC: 11369779. DOI: 10.1016/j.xplc.2024.100978.

Stem cell quiescence and dormancy in plant meristems.

Eljebbawi A, Dolata A, Strotmann V, Stahl Y J Exp Bot. 2024; 75(19):6022-6036.

PMID: 38721716 PMC: 11480668. DOI: 10.1093/jxb/erae201.

References

Yin Y, Wang Z, Mora-Garcia S, Li J, Yoshida S, Asami T . BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell. 2002; 109(2):181-91. DOI: 10.1016/s0092-8674(02)00721-3. View

Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp-Peters S, Pinto K . Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol. 2013; 23(5):362-71. DOI: 10.1016/j.cub.2013.01.045. View

Kodaira K, Qin F, Tran L, Maruyama K, Kidokoro S, Fujita Y . Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol. 2011; 157(2):742-56. PMC: 3192566. DOI: 10.1104/pp.111.182683. View

Clark N, Fisher A, Berckmans B, Van den Broeck L, Nelson E, Nguyen T . Protein complex stoichiometry and expression dynamics of transcription factors modulate stem cell division. Proc Natl Acad Sci U S A. 2020; 117(26):15332-15342. PMC: 7334585. DOI: 10.1073/pnas.2002166117. View

Kim K, Lai Z, Fan B, Chen Z . Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell. 2008; 20(9):2357-71. PMC: 2570728. DOI: 10.1105/tpc.107.055566. View

van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B . Short-range control of cell differentiation in the Arabidopsis root meristem. Nature. 1997; 390(6657):287-9. DOI: 10.1038/36856. View

Weidtkamp-Peters S, Stahl Y . The Use of FRET/FLIM to Study Proteins Interacting with Plant Receptor Kinases. Methods Mol Biol. 2017; 1621:163-175. DOI: 10.1007/978-1-4939-7063-6_16. View

Occhialini A, Gouzerh G, Di Sansebastiano G, Neuhaus J . Dimerization of the Vacuolar Receptors AtRMR1 and -2 from Arabidopsis thaliana Contributes to Their Localization in the trans-Golgi Network. Int J Mol Sci. 2016; 17(10). PMC: 5085694. DOI: 10.3390/ijms17101661. View

Gietz R, Woods R . Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 2002; 350:87-96. DOI: 10.1016/s0076-6879(02)50957-5. View

10.

Gonzalez-Garcia M, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E . Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development. 2011; 138(5):849-59. DOI: 10.1242/dev.057331. View

11.

Fulcher N, Sablowski R . Hypersensitivity to DNA damage in plant stem cell niches. Proc Natl Acad Sci U S A. 2009; 106(49):20984-8. PMC: 2791609. DOI: 10.1073/pnas.0909218106. View

12.

Burkart R, Strotmann V, Kirschner G, Akinci A, Czempik L, Dolata A . PLETHORA-WOX5 interaction and subnuclear localization control Arabidopsis root stem cell maintenance. EMBO Rep. 2022; 23(6):e54105. PMC: 9171415. DOI: 10.15252/embr.202154105. View

13.

Cheung T, Rando T . Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol. 2013; 14(6):329-40. PMC: 3808888. DOI: 10.1038/nrm3591. View

14.

Tian H, Jia Y, Niu T, Yu Q, Ding Z . The key players of the primary root growth and development also function in lateral roots in Arabidopsis. Plant Cell Rep. 2014; 33(5):745-53. DOI: 10.1007/s00299-014-1575-x. View

15.

Wang K, Zhang T, Dong Q, Nice E, Huang C, Wei Y . Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis. 2013; 4:e537. PMC: 3613828. DOI: 10.1038/cddis.2013.50. View

16.

Lozano-Elena F, Planas-Riverola A, Vilarrasa-Blasi J, Schwab R, Cano-Delgado A . Paracrine brassinosteroid signaling at the stem cell niche controls cellular regeneration. J Cell Sci. 2017; 131(2). PMC: 5818034. DOI: 10.1242/jcs.204065. View

17.

Shimotohno A, Heidstra R, Blilou I, Scheres B . Root stem cell niche organizer specification by molecular convergence of PLETHORA and SCARECROW transcription factor modules. Genes Dev. 2018; 32(15-16):1085-1100. PMC: 6075145. DOI: 10.1101/gad.314096.118. View

18.

Fuentes S, Pires N, Ostergaard L . A clade in the QUASIMODO2 family evolved with vascular plants and supports a role for cell wall composition in adaptation to environmental changes. Plant Mol Biol. 2010; 73(6):605-15. DOI: 10.1007/s11103-010-9640-5. View

19.

Mendoza L, Alvarez-Buylla E . Genetic regulation of root hair development in Arabidopsis thaliana: a network model. J Theor Biol. 2000; 204(3):311-26. DOI: 10.1006/jtbi.2000.2014. View

20.

Clark N, Buckner E, Fisher A, Nelson E, Nguyen T, Simmons A . Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks. Nat Commun. 2019; 10(1):5574. PMC: 6897965. DOI: 10.1038/s41467-019-13132-2. View