The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity

Abstract

In plants, the shoot apical meristem (SAM) serves as a reservoir of pluripotent stem cells from which all above ground organs originate. To sustain proper growth, the SAM must maintain homeostasis between the self-renewal of pluripotent stem cells and cell recruitment for lateral organ formation. At the core of the network that regulates this homeostasis in Arabidopsis are the WUSCHEL (WUS) transcription factor specifying stem cell fate and the CLAVATA (CLV) ligand-receptor system limiting WUS expression. In this study, we identified the ERECTA (ER) pathway as a second receptor kinase signaling pathway that regulates WUS expression, and therefore shoot apical and floral meristem size, independently of the CLV pathway. We demonstrate that reduction in class III HD-ZIP and ER function together leads to a significant increase in WUS expression, resulting in extremely enlarged shoot meristems and a switch from spiral to whorled vegetative phyllotaxy. We further show that strong upregulation of WUS in the inflorescence meristem leads to ectopic expression of the AGAMOUS homeotic gene to a level that switches cell fate from floral meristem founder cell to carpel founder cell, suggesting an indirect role for ER in regulating floral meristem identity. This work illustrates the delicate balance between stem cell specification and differentiation in the meristem and shows that a shift in this balance leads to abnormal phyllotaxy and to altered reproductive cell fate.

FASCIATED EAR4Encodes a bZIP Transcription Factor That Regulates Shoot Meristem Size in Maize

“…Additional genes identified as being oppositely modulated by FEA4 and KN1 included the ETTIN/ARF3 putative ortholog (GRMZM5G874163), GENERAL REGULATORY FACTOR1, which encodes a 14-3-3 protein, an LRR kinase (GRMZM2G166413) similar to RECEPTOR LIKE PROTEIN29 from Arabidopsis, and an HD-ZIP TF (GRMZM2G003509) with sequence similarity to PHAVOLUTA/PHABULOSA. In addition, FEA4 and KN1 bound and positively modulated a CUC-like NAC TF (GRMZM2G430522), consistent with positive regulation of CUC genes by SHOOT MERISTEMLESS in Arabidopsis (Spinelli et al, 2011), an LRR kinase (GRMZM5G809695) with sequence similarity to ERECTA and implicated in specification of organs originating at the SAM (Torii et al, 1996;Mandel et al, 2014), and a NPH3 domain protein (GRMZM2G067053) similar to ENHANCER OF PINOID. The latter two have been implicated in regulation of auxin transport (Treml et al, 2005;Chen et al, 2013).…”

CLAVATA-WUSCHEL signaling in the shoot meristem

“…ER is expressed in the SAM, and although er mutants do not exhibit any obvious meristem phenotype, mutants of ER and its family members ERECTA-LIKE1 and ERECTA-LIKE2 enhance clv meristem phenotypes (Durbak and Tax, 2011;Torii et al, 1996;Yokoyama et al, 1998). These effects of mutations in ER family genes on meristem size are the result of enhanced WUS expression, possibly via an HD-ZIPIIIdependent but CLV-independent signaling pathway (Chen et al, 2013;Mandel et al, 2014). In a more recent study, using mutant combination analysis with 2D sectioning of meristems, it was hypothesized that CLV3 controls meristem expansion along the apical-basal axis, while the ER family members control lateral expansion in a perpendicular orientation (Mandel et al, 2016).…”

Demethylation of ERECTA receptor genes by IBM1 histone demethylase affects stomatal development

“…DNA methylation and histone modifications), compared with genetic disruptions, are more flexible and plastic in regulating gene expression. Besides elevated stomatal lineage numbers, the er mutants also display prominent defects at the whole-plant level, including enlarged shoot apical meristem size (Mandel et al, 2014), short plant stature and compact inflorescence (Shpak, 2013;Torii et al, 1996). These phenotypes were not evident in ibm1 and edm2 mutants (Saze et al, 2008).…”