Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways

Stem cell homeostasis in plant shoot meristems requires tight coordination between stem cell proliferation and cell differentiation. In Arabidopsis, stem cells express the secreted dodecapeptide CLAVATA3 (CLV3), which signals through the leucine-rich repeat (LRR)-receptor kinase CLAVATA1 (CLV1) and...

Full description

Bibliographic Details
Main Authors: Jenia Schlegel, Gregoire Denay, Rene Wink, Karine Gustavo Pinto, Yvonne Stahl, Julia Schmid, Patrick Blümke, Rüdiger GW Simon
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/70934
_version_ 1811227693105020928
author Jenia Schlegel
Gregoire Denay
Rene Wink
Karine Gustavo Pinto
Yvonne Stahl
Julia Schmid
Patrick Blümke
Rüdiger GW Simon
author_facet Jenia Schlegel
Gregoire Denay
Rene Wink
Karine Gustavo Pinto
Yvonne Stahl
Julia Schmid
Patrick Blümke
Rüdiger GW Simon
author_sort Jenia Schlegel
collection DOAJ
description Stem cell homeostasis in plant shoot meristems requires tight coordination between stem cell proliferation and cell differentiation. In Arabidopsis, stem cells express the secreted dodecapeptide CLAVATA3 (CLV3), which signals through the leucine-rich repeat (LRR)-receptor kinase CLAVATA1 (CLV1) and related CLV1-family members to downregulate expression of the homeodomain transcription factor WUSCHEL (WUS). WUS protein moves from cells below the stem cell domain to the meristem tip and promotes stem cell identity, together with CLV3 expression, generating a negative feedback loop. How stem cell activity in the meristem centre is coordinated with organ initiation and cell differentiation at the periphery is unknown. We show here that the CLE40 gene, encoding a secreted peptide closely related to CLV3, is expressed in the SAM in differentiating cells in a pattern complementary to that of CLV3. CLE40 promotes WUS expression via BAM1, a CLV1-family receptor, and CLE40 expression is in turn repressed in a WUS-dependent manner. Together, CLE40-BAM1-WUS establish a second negative feedback loop. We propose that stem cell homeostasis is achieved through two intertwined pathways that adjust WUS activity and incorporate information on the size of the stem cell domain, via CLV3-CLV1, and on cell differentiation via CLE40-BAM1.
first_indexed 2024-04-12T09:46:11Z
format Article
id doaj.art-10f0ee34285e4c0b881ce5e44e015330
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T09:46:11Z
publishDate 2021-10-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-10f0ee34285e4c0b881ce5e44e0153302022-12-22T03:37:56ZengeLife Sciences Publications LtdeLife2050-084X2021-10-011010.7554/eLife.70934Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathwaysJenia Schlegel0https://orcid.org/0000-0003-0434-4479Gregoire Denay1https://orcid.org/0000-0002-8850-3029Rene Wink2Karine Gustavo Pinto3Yvonne Stahl4Julia Schmid5Patrick Blümke6https://orcid.org/0000-0001-7315-6792Rüdiger GW Simon7https://orcid.org/0000-0002-1317-7716Institute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyInstitute for Developmental Genetics and Cluster of Excellence on Plant Sciences, Heinrich Heine University, Düsseldorf, GermanyStem cell homeostasis in plant shoot meristems requires tight coordination between stem cell proliferation and cell differentiation. In Arabidopsis, stem cells express the secreted dodecapeptide CLAVATA3 (CLV3), which signals through the leucine-rich repeat (LRR)-receptor kinase CLAVATA1 (CLV1) and related CLV1-family members to downregulate expression of the homeodomain transcription factor WUSCHEL (WUS). WUS protein moves from cells below the stem cell domain to the meristem tip and promotes stem cell identity, together with CLV3 expression, generating a negative feedback loop. How stem cell activity in the meristem centre is coordinated with organ initiation and cell differentiation at the periphery is unknown. We show here that the CLE40 gene, encoding a secreted peptide closely related to CLV3, is expressed in the SAM in differentiating cells in a pattern complementary to that of CLV3. CLE40 promotes WUS expression via BAM1, a CLV1-family receptor, and CLE40 expression is in turn repressed in a WUS-dependent manner. Together, CLE40-BAM1-WUS establish a second negative feedback loop. We propose that stem cell homeostasis is achieved through two intertwined pathways that adjust WUS activity and incorporate information on the size of the stem cell domain, via CLV3-CLV1, and on cell differentiation via CLE40-BAM1.https://elifesciences.org/articles/70934shoot meristemstem cellsCLE40CLAVATAsignallingWUS
spellingShingle Jenia Schlegel
Gregoire Denay
Rene Wink
Karine Gustavo Pinto
Yvonne Stahl
Julia Schmid
Patrick Blümke
Rüdiger GW Simon
Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways
eLife
shoot meristem
stem cells
CLE40
CLAVATA
signalling
WUS
title Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways
title_full Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways
title_fullStr Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways
title_full_unstemmed Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways
title_short Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways
title_sort control of arabidopsis shoot stem cell homeostasis by two antagonistic cle peptide signalling pathways
topic shoot meristem
stem cells
CLE40
CLAVATA
signalling
WUS
url https://elifesciences.org/articles/70934
work_keys_str_mv AT jeniaschlegel controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT gregoiredenay controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT renewink controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT karinegustavopinto controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT yvonnestahl controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT juliaschmid controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT patrickblumke controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways
AT rudigergwsimon controlofarabidopsisshootstemcellhomeostasisbytwoantagonisticclepeptidesignallingpathways