Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways

Abstract

The shoot apical meristem (SAM) of angiosperm plants is a small, highly organized structure that gives rise to all above-ground organs. The SAM is divided into three functional domains: the central zone (CZ) at the SAM tip harbors the self-renewing pluripotent stem cells and the organizing center, providing daughter cells that are continuously displaced into the interior rib zone (RZ) or the surrounding peripheral zone (PZ), from which organ primordia are initiated. Despite the constant flow of cells from the CZ into the RZ or PZ, and cell recruitment for primordium formation, a stable balance is maintained between the distinct cell populations in the SAM. Here we combined an in-depth phenotypic analysis with a comparative RNA-Seq approach to characterize meristems from selected combinations of clavata3 (clv3), jabba-1D (jba-1D) and erecta (er) mutants of Arabidopsis thaliana. We demonstrate that CLV3 restricts meristem expansion along the apical-basal axis, whereas class III HD-ZIP and ER pathways restrict meristem expansion laterally, but in distinct and possibly perpendicular orientations. Our k-means analysis reveals that clv3, jba-1D/+ and er lead to meristem enlargement by affecting different aspects of meristem function; for example, clv3 displays an increase in the stem cell population, whereas jba-1D/+ er exhibits an increase in mitotic activity and in the meristematic cell population. Our analyses demonstrate that a combined genetic and mRNA-Seq comparative approach provides a precise and sensitive method to identify cell type-specific transcriptomes in a small structure, such as the SAM.

Dual CLAVATA3 peptides in Arabidopsis shoot stem cell signaling

“…Notably, these results demonstrate that MCLV3p can also reduce meristem size at physiologically low concentration in addition to [Ara 3 ]CLV3p (Shinohara and Matsubayashi, 2013). Consistent with a key role of CLV3p signaling in controlling stem cell numbers in the SAM (Je et al, 2016; Mandel et al, 2016; Somssich et al, 2016; Yamaguchi et al, 2016), CLV3p-mediated reduction of the shoot meristem size was most significantly reflected in the height of the clv3-2 SAM rather than the width (Fig. 2A, B).…”

CLAVATA-WUSCHEL signaling in the shoot meristem

“…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). However, since the connection between the ER family and the CLVs is indirect, it is tempting to speculate that RPK2 could provide a link between the two pathways.…”

Diversity of phyllotaxis in land plants in reference to the shoot apical meristem structure

“…ABPH1 is believed to regulate the cytokinin-induced expansion of the SAM; thus, in the mutant, the ratio between the size of the meristem and the size of the leaf primordium changed, making the formation of alternative phyllotactic patterns possible [100]. The significance of the geometrical proportions at the SAM for pattern formation is further evidenced by studies on the genes (e.g., WUSCHEL, CLVAVATA, ARGOS, ORGAN SIZE RELATED) that regulate SAM and primordia size, as well as meristem structure and activity [101][102][103]. On the other hand, species with similar geometrical proportions at the SAM can differ in the degree of phyllotaxis diversity and/or stability; for instance, in inflorescences of some Asteraceae species, the primordia packing usually reflects the main Fibonacci series [7,71,104].…”