ZLL/AGO10 maintains shoot meristem stem cells during Arabidopsis embryogenesis by down-regulating ARF2-mediated auxin response

Plant meristems carry pools of continuously active stem cells, whose activity is controlled by developmental and environmental signals. After stem cell division, daughter cells that exit the stem cell domain acquire transit amplifying cell identity before they are incorporated into organs and differentiate. In this study, we used an integrated approach to elucidate the role of HECATE (HEC) genes in regulating developmental trajectories of shoot stem cells in Arabidopsis thaliana. Our work reveals that HEC function stabilizes cell fate in distinct zones of the shoot meristem thereby controlling the spatio-temporal dynamics of stem cell differentiation. Importantly, this activity is concomitant with the local modulation of cellular responses to cytokinin and auxin, two key phytohormones regulating cell behaviour. Mechanistically, we show that HEC factors transcriptionally control and physically interact with MONOPTEROS (MP), a key regulator of auxin signalling, and modulate the autocatalytic stabilization of auxin signalling output.

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Integration of pluripotency pathways regulates stem cell maintenance in theArabidopsisshoot meristem

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2015248117 ◽

2020 ◽

Vol 117 (36) ◽

pp. 22561-22571 ◽

Cited By ~ 1

Author(s):

Ying Hua Su ◽

Chao Zhou ◽

Ying Ju Li ◽

Yang Yu ◽

Li Ping Tang ◽

...

Keyword(s):

Stem Cells ◽

Stem Cell ◽

Expression Patterns ◽

Cell Activity ◽

Direct Interaction ◽

Shoot Meristem ◽

Stem Cell Maintenance ◽

Spatiotemporal Expression ◽

Undifferentiated State ◽

Stem Cell Activity

In the shoot meristem, both WUSCHEL (WUS) and SHOOT MERISTEMLESS (STM), two transcription factors with overlapping spatiotemporal expression patterns, are essential for maintaining stem cells in an undifferentiated state. Despite their importance, it remains unclear how these two pathways are integrated to coordinate stem cell development. Here, we show that the WUS and STM pathways inArabidopsis thalianaconverge through direct interaction between the WUS and STM proteins. STM binds to the promoter ofCLAVATA3(CLV3) and enhances the binding of WUS to the same promoter through the WUS–STM interaction. Both the heterodimerization and simultaneous binding of WUS and STM at two sites on theCLV3promoter are required to regulateCLV3expression, which in turn maintains a constant number of stem cells. Furthermore, the expression ofSTMdepends on WUS, and this WUS-activatedSTMexpression enhances the WUS-mediated stem cell activity. Our data provide a framework for understanding how spatial expression patterns within the shoot meristem are translated into regulatory units of stem cell homeostasis.

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Pattern of Auxin and Cytokinin Responses for Shoot Meristem Induction Results from the Regulation of Cytokinin Biosynthesis by AUXIN RESPONSE FACTOR3

PLANT PHYSIOLOGY ◽

10.1104/pp.112.203166 ◽

2012 ◽

Vol 161 (1) ◽

pp. 240-251 ◽

Cited By ~ 119

Author(s):

Zhi Juan Cheng ◽

Liang Wang ◽

Wei Sun ◽

Yan Zhang ◽

Chao Zhou ◽

...

Keyword(s):

Shoot Meristem ◽

Auxin Response ◽

Cytokinin Biosynthesis

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Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

10.1101/2021.08.03.454935 ◽

2021 ◽

Author(s):

Adrienne HK Roeder ◽

Michael J Scanlon ◽

Joseph Cammarata ◽

Christopher Morales Farfan

Keyword(s):

Stem Cells ◽

Stem Cell ◽

Flowering Plant ◽

Shoot Meristem ◽

Cytokinin Signaling ◽

Cytokinin Receptor ◽

Stem Cell Maintenance ◽

Stem Cell Regulation ◽

Evolutionarily Conserved ◽

Cell Organization

Plant shoots grow from stem cells within Shoot Apical Meristems (SAMs), which produce lateral organs while maintaining the stem cell pool. In the model flowering plant Arabidopsis, the CLAVATA (CLV) pathway functions antagonistically with cytokinin signaling to control the size of the multicellular SAM via negative regulation of the stem cell organizer WUSCHEL (WUS). Although comprising just a single cell, the SAM of the model moss Physcomitrium patens (formerly Physcomitrella) performs equivalent functions during stem cell maintenance and organogenesis, despite the absence of WUS-mediated stem cell organization. Our previous work showed that the stem cell-delimiting function of the CLV pathway receptors CLAVATA1 (CLV1) and RECEPTOR-LIKE PROTEIN KINASE2 (RPK2) is conserved in the moss P. patens. Here, we use P. patens to assess whether CLV-cytokinin crosstalk is also an evolutionarily conserved feature of stem cell regulation. Genetic analyses reveal that CLV1 and RPK2 regulate SAM proliferation via separate pathways in moss. Surprisingly, cytokinin receptor mutants also form ectopic stem cells in the absence of cytokinin signaling. Through modeling, we identified regulatory network archtectures that recapitulated the stem cell phenotypes of clv1 and rpk2 mutants, cytokinin application, cytokinin receptor mutations, and higher-order combinations of these perturbations. These models predict that CLV1 and RPK2 act through separate pathways wherein CLV1 represses cytokinin-mediated stem cell initiation and RPK2 inhibits this process via a separate, cytokinin-independent pathway. Our analysis suggests that crosstalk between CLV1 and cytokinin signaling is an evolutionarily conserved feature of SAM homeostasis that preceded the role of WUS in stem cell organization.

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