CLAVATA Signaling Ensures Reproductive Development in Plants across Thermal Environments

Daniel S Jones,Amala John,Kylie R Vandermolen,Zachary L Nimchuk

doi:10.1016/j.cub.2020.10.008

Daniel S Jones, Amala John + Show 2 more

Open Access

https://doi.org/10.1016/j.cub.2020.10.008

Copy DOI

Abstract

The ability to thrive in diverse environments requires that species maintain development and reproduction despite dynamic conditions. Many developmental processes are stabilized through robust signaling pathways that cooperatively ensure proper development.1 During reproduction, plants like Arabidopsis thaliana continuously generate flowers on growing indeterminate inflorescences.2 Flower primordia initiation and outgrowth depends on the hormone auxin and is robust across diverse environments.3-6 Here, we show that reproductive development under different thermal conditions requires the integration of multiple pathways regulating auxin-dependent flower production. In colder/ambient temperatures, the receptor complex CLAVATA2/CORYNE (CLV2/CRN) is necessary for continuous flower outgrowth during inflorescence development. CLV2/CRN signaling is independent of CLAVATA1 (CLV1)-related receptor signaling but involves the CLAVATA3 INSENSITIVE RECEPTOR KINASE (CIK) family co-receptors, with higher order cik mutant combinations phenocopying clv2/crn flower outgrowth defects. Developing crn inflorescences display reduced auxin signaling, and restoration of auxin biosynthesis is sufficient to restore flower outgrowth in colder and ambient temperatures. In contrast, at higher temperatures, both clv2/crn signaling and heat-induced auxin biosynthesis via YUCCA family genes are synergistically required to maintain flower development. Our work reveals a novel mechanism integrating peptide hormone and auxin signaling in the regulation of flower development across diverse thermal environments.

Highlights

The CLV2/CRN Receptor Complex Promotes Flower Primordia Outgrowth and Development After the production of 1–5 normal flowers in crn-null mutants, we noticed a novel phenotype in which flower primordia initiate but fail to develop further and inflorescence internode elongation stalls (Figures 1A and 1B; the termination phase)
Using standardized flower primordia staging, we found that crn primordia outgrowth deviated from WT at flower primordia stage three (FP3), with little proliferation occurring afterward (Figures 1F and 1G; staging as in Reddy et al.[23] or stage 2 using Smyth et al.[22] stages)
We found no flower primordia outgrowth defects in null clv[] mutants in Ler, explaining why this phenotype has not been described in this ecotype (Figures S1D, S1E, S1I, and S1J)

Summary

Introduction

The CLV2/CRN Receptor Complex Promotes Flower Primordia Outgrowth and Development After the production of 1–5 normal flowers in crn-null mutants (crn-10; in the Col-0 ecotype), we noticed a novel phenotype in which flower primordia initiate but fail to develop further and inflorescence internode elongation stalls (Figures 1A and 1B; the termination phase). Clv2-null mutants (rlp[]; in Col-0) displayed a similar phenotype to crn (Figure 1C), which was previously observed in clv[2] in a survey of mutants in receptor-like protein genes, but not characterized.[21] To quantify primordia termination, we classified the first 30 attempts to make flowers along the primary inflorescence as normal (complete flowers; formation of all four flower organs),[22] terminated flower primordia (no flower organs develop), or terminated flowers (some flower organs develop, but no gynoecium). We classified the first 30 attempts to make flowers along the primary inflorescence as normal (complete flowers; formation of all four flower organs),[22] terminated flower primordia (no flower organs develop), or terminated flowers (some flower organs develop, but no gynoecium). crn and clv[2] single mutants displayed equivalent defects in flower production (Figure 1E), observed in clv[2] crn double mutants, consistent with the documented co-function of CLV2/CRN (Figures 1B–1E). clv2/crn flower outgrow

Methods

Results

Conclusion