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

Abstract

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.

Receptor-Like Protein Kinases Function Upstream of MAPKs in Regulating Plant Development

“…It was reported that the CLV3 signaling can activate MPK6 to maintain SAM homeostasis [ 187 ]. A recent study showed that exogenous CLV3 can activate MPK3/6, and the mpk3/6 double mutant is insensitive to CLV3 treatment [ 10 ]. The transcription levels of WUS-target genes, such as ARABIDOPSIS RESPONSE REGULATOR 7/15 ( ARR7/15 ), GROWTH-REGULATING FACTOR 6 ( GRF6 ) and YABBY 3 ( YAB3 ), are decreased in mpk3/6 .…”

“…However, the SAM is still normal in most mpk3/6 mutants treated with exogenous CLV3. Moreover, the size of the SAM in mpk3/6 is larger than the wild type [ 10 ]. All these findings suggest that the CLV3-CLV1 signaling pathway regulates stem cell homeostasis in the SAM possibly via activating a MAPK cascade including MPK3/6.…”

“…Consistent with their extensive functions, expression pattern analyses revealed that MAPKs are widely expressed in many plant tissues and organs, such as inflorescences, anthers, embryos, shoot and root apical meristems, root hairs and stomata [ 10 , 19 , 31 , 57 , 58 ]. Although most of them are ubiquitously expressed, some MAPKs are tissue- or organ-specific.…”

“…The MPKs with a TEY motif form three groups (A–C), and the TDY subtype is classified as a distinct group D [ 7 ]. Group A MPKs have been widely studied and found to be involved in environmental stresses, hormonal responses, and development in plants [ 8 , 9 , 10 , 11 , 12 ]. Group B MPKs are involved in microtubule organization, cytokinesis, and stress responses [ 13 , 14 , 15 ].…”

The receptor-like cytoplasmic kinase MAZZA and CLAVATA-family receptors interactin vivo, together mediating developmental processes inArabidopsis thaliana

“…Mitogen-activated protein kinase (MAPK) cascades, which display a classical mode of intracellular signal transduction in RLK pathways (reviewed in (He et al, 2018)), have been proposed to mediate downstream CLE signaling (Betsuyaku et al, 2011;Lee et al, 2019).…”