WOX Going On: CLE Peptides in Plant Development

Overview

Journal Curr Opin Plant Biol

Specialty Biology

Date 2021 Jun 2

PMID 34077886

Citations 25

Authors

Andrew C Willoughby

Zachary L Nimchuk

Affiliations

Soon will be listed here.

Abstract

The development of plant tissues requires cell-cell communication facilitated by chemical and peptide hormones, including small signaling peptides in the CLAVATA3/EMBRYO-SURROUNDING REGION (CLE) family. The paradigmatic CLE signaling peptide CLAVATA3 regulates the size of the shoot apical meristem and the expression of the stem cell-promoting WUSCHEL transcription factor through an unknown mechanism. This review discusses recent advances in CLE signaling, showing that CLE pathways are conserved in bryophytes, that CLE peptides in Arabidopsis thaliana regulate stem cell identity and cell division in root tissues, and connections to auxin biosynthesis in regulating flower and leaf development. These advances shed light on potential WUSCHEL family-independent aspects of CLE signaling and the overlap between CLE and auxin signaling.

Citing Articles

Ethylene-independent modulation of root development by ACC via downregulation of WOX5 and group I CLE peptide expression.

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A major role of class III HD-ZIPs in promoting sugar beet cyst nematode parasitism in Arabidopsis.

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Antagonistic CLE peptide pathways shape root meristem tissue patterning.

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Reference genome sequence and population genomic analysis of peas provide insights into the genetic basis of Mendelian and other agronomic traits.

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References

Gujas B, Kastanaki E, Sturchler A, Cruz T, Aguila Ruiz-Sola M, Dreos R . A Reservoir of Pluripotent Phloem Cells Safeguards the Linear Developmental Trajectory of Protophloem Sieve Elements. Curr Biol. 2020; 30(5):755-766.e4. DOI: 10.1016/j.cub.2019.12.043. View

Sakakibara K, Reisewitz P, Aoyama T, Friedrich T, Ando S, Sato Y . WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. Development. 2014; 141(8):1660-70. DOI: 10.1242/dev.097444. View

Brand U, Fletcher J, Hobe M, Meyerowitz E, Simon R . Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science. 2000; 289(5479):617-9. DOI: 10.1126/science.289.5479.617. View

Tian H, Lv B, Ding T, Bai M, Ding Z . Auxin-BR Interaction Regulates Plant Growth and Development. Front Plant Sci. 2018; 8:2256. PMC: 5778104. DOI: 10.3389/fpls.2017.02256. View

Qian P, Song W, Yokoo T, Minobe A, Wang G, Ishida T . The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors. Nat Plants. 2018; 4(12):1071-1081. DOI: 10.1038/s41477-018-0317-4. View

Marhava P, Bassukas A, Zourelidou M, Kolb M, Moret B, Fastner A . A molecular rheostat adjusts auxin flux to promote root protophloem differentiation. Nature. 2018; 558(7709):297-300. DOI: 10.1038/s41586-018-0186-z. View

Perales M, Rodriguez K, Snipes S, Yadav R, Diaz-Mendoza M, Reddy G . Threshold-dependent transcriptional discrimination underlies stem cell homeostasis. Proc Natl Acad Sci U S A. 2016; 113(41):E6298-E6306. PMC: 5068294. DOI: 10.1073/pnas.1607669113. View

Kong D, Hao Y, Cui H . The WUSCHEL Related Homeobox Protein WOX7 Regulates the Sugar Response of Lateral Root Development in Arabidopsis thaliana. Mol Plant. 2015; 9(2):261-270. DOI: 10.1016/j.molp.2015.11.006. View

DiGennaro P, Grienenberger E, Dao T, Jun J, Fletcher J . Peptide signaling molecules CLE5 and CLE6 affect Arabidopsis leaf shape downstream of leaf patterning transcription factors and auxin. Plant Direct. 2019; 2(12):e00103. PMC: 6508849. DOI: 10.1002/pld3.103. View

10.

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

11.

Fujinami R, Yamada T, Imaichi R . Root apical meristem diversity and the origin of roots: insights from extant lycophytes. J Plant Res. 2020; 133(3):291-296. DOI: 10.1007/s10265-020-01167-2. View

12.

Biedron M, Banasiak A . Auxin-mediated regulation of vascular patterning in Arabidopsis thaliana leaves. Plant Cell Rep. 2018; 37(9):1215-1229. PMC: 6096608. DOI: 10.1007/s00299-018-2319-0. View

13.

Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke C . Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc Natl Acad Sci U S A. 2013; 110(17):7074-9. PMC: 3637694. DOI: 10.1073/pnas.1222314110. View

14.

Hobe M, Muller R, Grunewald M, Brand U, Simon R . Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol. 2003; 213(8):371-81. DOI: 10.1007/s00427-003-0329-5. View

15.

Cammarata J, Roeder A, Scanlon M . Cytokinin and CLE signaling are highly intertwined developmental regulators across tissues and species. Curr Opin Plant Biol. 2019; 51:96-104. DOI: 10.1016/j.pbi.2019.05.006. View

16.

Han S, Cho H, Noh J, Qi J, Jung H, Nam H . BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth. Nat Plants. 2018; 4(8):605-614. DOI: 10.1038/s41477-018-0180-3. View

17.

Ma Y, Miotk A, Sutikovic Z, Ermakova O, Wenzl C, Medzihradszky A . WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis. Nat Commun. 2019; 10(1):5093. PMC: 6841675. DOI: 10.1038/s41467-019-13074-9. View

18.

Gordon S, Chickarmane V, Ohno C, Meyerowitz E . Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci U S A. 2009; 106(38):16529-34. PMC: 2752578. DOI: 10.1073/pnas.0908122106. View

19.

Lee C, Clark S . A WUSCHEL-Independent Stem Cell Specification Pathway Is Repressed by PHB, PHV and CNA in Arabidopsis. PLoS One. 2015; 10(5):e0126006. PMC: 4444308. DOI: 10.1371/journal.pone.0126006. View

20.

Crook A, Willoughby A, Hazak O, Okuda S, VanDerMolen K, Soyars C . BAM1/2 receptor kinase signaling drives CLE peptide-mediated formative cell divisions in roots. Proc Natl Acad Sci U S A. 2020; 117(51):32750-32756. PMC: 7768756. DOI: 10.1073/pnas.2018565117. View