A signal cascade originated from epidermis defines apical-basal patterning of Arabidopsis shoot apical meristems

Abstract

In multicellular organisms, a long-standing question is how spatial patterns of distinct cell types are initiated and maintained during continuous cell division and proliferation. Along the vertical axis of plant shoot apical meristems (SAMs), stem cells are located at the top while cells specifying the stem cells are located more basally, forming a robust apical-basal pattern. We previously found that in Arabidopsis SAMs, the HAIRY MERISTEM (HAM) family transcription factors form a concentration gradient from the epidermis to the interior cell layers, and this gradient is essential for the stem cell specification and the apical-basal patterning of the SAMs. Here, we uncover that epidermis specific transcription factors, ARABIDOPSIS THALIANA MERISTEM LAYER 1 (ATML1) and its close homolog, define the concentration gradient of HAM in the SAM through activating a group of microRNAs. This study provides a molecular framework linking the epidermis-derived signal to the stem cell homeostasis in plants.

The Overlapping and Distinct Roles of HAM Family Genes in Arabidopsis Shoot Meristems

“…Under the control of the endogenous HAM1 promoter and 3' terminator, the YPET-HAM1 protein is not expressed in the epidermal L1 layer, barely expressed in the L2 layer, and highly expressed in the rib meristem and peripheral zone of the corpus ( Figures 1A-F). In parallel, we imaged the pHAM2::YPET-HAM2 translational reporter (Zhou et al, 2015;Zhou et al, 2018;Han et al, 2020b) in the ham123 SAM (Figures 2A-C). pHAM2:: YPET-HAM2 is highly expressed in the rib meristem and peripheral zone of the corpus, but it is repressed or completely off in the L1 and L2 layers (Figures 2A-F), a pattern comparable to that of pHAM1::YPET-HAM1 ( Figures 1A-F).…”

“…Vegetative shoots were fixed with 4% paraformaldehyde overnight at 4°C. Tissues were embedded, sectioned, hybridized and washed as described previously ( Krizek, 1999 ; Han et al, 2020b ). The CLV3 probe was described previously ( Zhou et al, 2018 ).…”

Epidermal restriction confers robustness to organ shapes

“…The epidermis not only provides mechanical restriction to inner tissues, but also serves as a source of biochemical signals that directs development (Chickarmane et al 2012;Knauer et al 2013;Gruel et al 2016;Han et al 2020). ATML1 and PDF2 are key regulators of epidermal cell differentiation, and the atml1 pdf2 mutants are expected to lose, at least partially, both mechanical restriction and epidermisderived biochemical signals (Abe et al 2001).…”

A Quarter Century History of ATML1 Gene Research

“…The epidermis also influences pattern formation in the shoot apical meristem (SAM), as several reports have suggested that certain microRNAs (miRNAs), generated in the outermost cell layer of the SAM, form an inhibitory gradient that contributes to the positioning of the stem cell niche at away from the epidermis [7,8]. Consistently, epidermal deficient mutants often show ectopic SAM activity in the leaves [9].…”