The <scp>CLAVATA</scp> signaling pathway mediating stem cell fate in shoot meristems requires Ca<sup>2+</sup> as a secondary cytosolic messenger

Chou, Hsuan; Zhu, Yingfang; Ma, Yi; Berkowitz, Gerald A.

doi:10.1111/tpj.13123

Cited by 30 publications

(27 citation statements)

References 61 publications

(116 reference statements)

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“…Because the isolated, enriched shoot apex tissues were used in this study but not whole seedlings, the use of different tissues may lead to the different results in the clv1 mutant. In addition, CLV1 has been reported to be expressed outside the SAM (Chou et al 2016). Based on our observation of MAPK activation, these results showed that CLV3p-mediated phosphorylation of MPK3 and MPK6 is positively regulated by both CLV1 and BAM1 receptors.…”

Section: Discussionsupporting

confidence: 58%

Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem

et al. 2018

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The CLAVATA peptide-receptor (CLV3p-CLV1) pathway modulates a homeodomain master regulator WUSCHEL (WUS) transcription factor in the shoot apical meristem (SAM) with poorly defined signaling mechanisms. Here, we report that mitogen-activated protein kinases (MAPKs, also known as MPKs in plants) act in an intracellular signaling cascade to play an important role in the maintenance of SAM development. Interestingly, the application of exogenous CLV3p triggers rapid signaling in the SAM via dynamic activation of MPK3 and MPK6, which are positively regulated by both CLV1 and BARELY ANY MERISTEM 1 (BAM1) receptors. Surprisingly, the timing of MAPK activation is tightly correlated with the transcriptional repression of WUS expression in the SAM, indicating a fast CLV3p-CLV1/BAM1 signaling event. Furthermore, conditional mpk3,6 double mutants exhibited CLV3p insensitivity in stem cell maintenance manifested by the persistent SAM growth in the presence of exogenous CLV3p signals, as well as elevated WUS expression and repressed WUS-specific target genes. Taken together, these results suggest that MPK3 and MPK6 activated by CLV3p signals through mainly CLV1 and BAM1 receptors are key regulators controlling stem cell homeostasis in the SAM.

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Section: Discussionsupporting

confidence: 58%

Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem

et al. 2018

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“…WUS and FAF2 expression is inhibited by the CLV3 peptide in wild-type plants and impaired with Ca 2+ channel blockers and GC inhibitors. This inhibition was also observed in the DEFENSE NO DEATH 1 ( dnd1 ) and 2 ( dnd2 ) mutants that lack the CNGC 2 and 4, respectively ( Chou et al, 2016 ). This may suggest that when CLV3 binds to the CLV1 receptor in the meristem, an increase in cGMP results and that may in turn activate CNGC2 channels and consequently increase cytoplasmic Ca 2+ .…”

Section: Expanding the Search And Discovery Of Novel Cyclase In Highementioning

confidence: 70%

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

Gehring

Turek

2017

Front. Plant Sci.

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The cyclic nucleotide monophosphates (cNMPs), and notably 3′,5′-cyclic guanosine monophosphate (cGMP) and 3′,5′-cyclic adenosine monophosphate (cAMP) are now accepted as key signaling molecules in many processes in plants including growth and differentiation, photosynthesis, and biotic and abiotic defense. At the single molecule level, we are now beginning to understand how cNMPs modify specific target molecules such as cyclic nucleotide-gated channels, while at the systems level, a recent study of the Arabidopsis cNMP interactome has identified novel target molecules with specific cNMP-binding domains. A major advance came with the discovery and characterization of a steadily increasing number of guanylate cyclases (GCs) and adenylate cyclases (ACs). Several of the GCs are receptor kinases and include the brassinosteroid receptor, the phytosulfokine receptor, the Pep receptor, the plant natriuretic peptide receptor as well as a nitric oxide sensor. We foresee that in the near future many more molecular mechanisms and biological roles of GCs and ACs and their catalytic products will be discovered and further establish cNMPs as a key component of plant responses to the environment.

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“…Peptides are typically released as pro-peptides into the apoplast and, once cleaved, bind to LRR kinases. Interestingly, 3 pathways that are initiated by peptides (CLAVATA3 (CLV3), phytosulfokine (PSK) and peptide PEP3) use cGMP as a secondary messenger to link with downstream signals (Qi et al 2010;Kwezi et al 2011;Chou et al 2016). Several of these receptors contain a GC domain within their kinase domain (i.e PEPR1, CLV1).…”

Section: The Role Of Cgmp In Basic Plant Functionsmentioning

confidence: 99%

cGMP signalling in plants: from enigma to main stream

Isner

Maathuis

2018

Functional Plant Biol.

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All living organisms communicate with their environment, and part of this dialogue is mediated by secondary messengers such as cyclic guanosine mono phosphate (cGMP). In plants, most of the specific components that allow production and breakdown of cGMP have now been identified apart from cGMP dependent phosphodiesterases, enzymes responsible for cGMP catabolism. Irrespectively, the role of cGMP in plant signal transductions is now firmly established with involvement of this nucleotide in development, stress response, ion homeostasis and hormone function. Within these areas, several consistent themes where cGMP may be particularly relevant are slowly emerging: these include regulation of cation fluxes, for example via cyclic nucleotide gated channels and in stomatal functioning. Many details of signalling pathways that incorporate cGMP remain to be unveiled. These include downstream targets other than a small number of ion channels, in particular cGMP dependent kinases. Improved genomics tools may help in this respect, especially since many proteins involved in cGMP signalling appear to have multiple and often overlapping functional domains which hampers identification on the basis of simple homology searches. Another open question regards the topographical distribution of cGMP signals are they cell limited? Does long distance cGMP signalling occur and if so, by what mechanisms? The advent of non-disruptive fluorescent reporters with high spatial and temporal resolution will provide a tool to accelerate progress in all these areas. Automation can facilitate large scale screens of mutants or the action of effectors that impact on cGMP signalling.

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The CLAVATA signaling pathway mediating stem cell fate in shoot meristems requires Ca²⁺ as a secondary cytosolic messenger

Abstract: , and that this cytosolic secondary messenger is involved in the signal transduction cascade linking CLV3/CLV1 to control of gene expression and stem cell fate in the SAM.

Cited by 30 publications

References 61 publications

Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem

Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

cGMP signalling in plants: from enigma to main stream

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The CLAVATA signaling pathway mediating stem cell fate in shoot meristems requires Ca2+ as a secondary cytosolic messenger

Abstract: , and that this cytosolic secondary messenger is involved in the signal transduction cascade linking CLV3/CLV1 to control of gene expression and stem cell fate in the SAM.

Cited by 30 publications

References 61 publications

Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem

Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

cGMP signalling in plants: from enigma to main stream

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The CLAVATA signaling pathway mediating stem cell fate in shoot meristems requires Ca²⁺ as a secondary cytosolic messenger