Control of proliferation in the haploid meristem by CLE peptide signaling in Marchantia polymorpha.

Yuki Hirakawa,John L Bowman,Yasuka L Yamaguchi,Shinichiro Sawa,Ryuichi Nishihama,Kimitsune Ishizaki,Ryo Tabata,Takayuki Kohchi,Naoyuki Uchida,Sakiko Ishida

doi:10.1371/journal.pgen.1007997

Abstract

The homeostasis of meristems in flowering plants is maintained by cell-to-cell communication via CLE (CLAVATA3/EMBRYO SURROUNDING REGION-related) peptide hormones. In contrast, cell signals that regulate meristem activity remains elusive in bryophytes that maintain apical meristems in the gametophyte (haploid) body and undergo a gametophyte-dominant life cycle. We here show that MpCLE1 confines the proliferative activity of gametophytic meristem and affects the overall size of gametangiophores (reproductive organs) in Marchantia polymorpha, which is in sharp contrast with the meristem-promoting function of its ortholog TDIF/CLE41/CLE44 in Arabidopsis vascular meristems. Expression analysis suggests that MpCLE1 and its receptor gene MpTDR are expressed in distinct patterns across the apical meristem. These data suggest that local CLE peptide signaling may have had a role in regulating cell proliferation in the shoot meristem in the ancestral land plant and acts in both sporophytic and gametophytic meristems of extant plants.

Highlights

Land plants have evolved unique peptide hormones to control various physiological processes including development and stress responses [1, 2]
To test if MpCLE1 is functionally equivalent to AtCLE41, a TDIF-encoding gene of Arabidopsis, we generated gain-of-function alleles in Arabidopsis
Similar results were obtained in assays with 20 μM peptide (S2 Fig). These data indicate that MpCLE1 cannot functionally replace AtCLE41/TDIF in Arabidopsis

Summary

Introduction

Land plants have evolved unique peptide hormones to control various physiological processes including development and stress responses [1, 2]. A notable example is CLE (CLAVATA3/ EMBRYO SURROUNDING REGION-related) family peptides involved in various developmental contexts in flowering plants, such as stem cell maintenance in meristems, vascular development, seed formation and growth control in response to environmental cues [3, 4]. Mature CLE peptides bind to specific membrane receptors that transmit signals to direct cell behavior, thereby manifesting cell-to-cell communication [9, 10]. A phylogenetically related receptor, TDR/PXY (TDIF RECEPTOR/PHLOEM INTERCALATED WITH XYLEM), mediates TDIF (tracheary element differentiation inhibitory factor) peptide signaling essential for stem cell maintenance in the vasculature [14]. CLV3 and TDIF peptides possess characteristic residues for exclusive interaction with their specific receptors [15] and represent two major subclasses of CLE peptide family

Methods

Results

Conclusion