Local and Systemic Effects of Brassinosteroid Perception in Developing Phloem

First author: Moritz Graeff; Affiliations: University of Lausanne (洛桑大学): Lausanne, Switzerland

Corresponding author: Christian S. Hardtke

The plant vasculature is an essential adaptation to terrestrial growth. Its phloem component permits efficient transfer of photosynthates between source and sink organs but also transports signals that systemically coordinate physiology and development. Here, we provide evidence that developing phloem orchestrates cellular behavior of adjacent tissues in the growth apices of plants, the meristems. Arabidopsis thaliana plants that lack the three receptor kinases BRASSINOSTEROID INSENSITIVE 1 (BRI1), BRI1-LIKE 1 (BRL1), and BRL3 (“bri3” mutants) can no longer sense brassinosteroid phytohormones and display severe dwarfism as well as patterning and differentiation defects, including disturbed phloem development. We found that, despite the ubiquitous expression of brassinosteroid receptors in growing plant tissues, exclusive expression of the BRI1 receptor in developing phloem is sufficient to systemically correct cellular growth and patterning defects that underlie the bri3 phenotype. Although this effect is brassinosteroid-dependent, it cannot be reproduced with dominant versions of known downstream effectors of BRI1 signaling and therefore possibly involves a non-canonical signaling output. Interestingly, the rescue of bri3 by phloem-specific BRI1 expression is associated with antagonism toward phloem-specific CLAVATA3/EMBRYO SURROUNDING REGION-RELATED 45 (CLE45) peptide signaling in roots. Hyperactive CLE45 signaling causes phloem sieve element differentiation defects, and consistently, knockout of CLE45 perception in bri3 background restores proper phloem development. However, bri3 dwarfism is retained in such lines. Our results thus reveal local and systemic effects of brassinosteroid perception in the phloem: whereas it locally antagonizes CLE45 signaling to permit phloem differentiation, it systemically instructs plant organ formation via a phloem-derived, non-cell-autonomous signal.

植物的维管组织是其适应陆地生活所必需的。维管组织中的韧皮部可用于光合产物在“源”和“库”器官之间的转移，同样也可用于系统性协调植物生长和发育的信号转导。本文中，作者发现在植物生长点中，发育中的韧皮部会调控邻近组织中的细胞行为。缺少三个受体激酶BRI1、BRL1和BRL3的拟南芥bri3突变体植株不能够再感应植物激素油菜素内酯，并且植株出现严重的矮化，而且在模式建成和分化等方面也存在缺陷，包括韧皮部发育也遭受紊乱。作者发现，虽然油菜素内酯受体在生长中的植物组织中广泛表达，但BRI1受体仅在正在发育中的韧皮部中表达便足以系统性纠正bri3突变体植株中细胞生长和模式建成缺陷。尽管该影响是依赖于油菜素内酯的，但其无法用任何BRI1信号已知的下游因子进行表型复制，说明可能涉及了非经典的BR信号输出。有趣的是，通过BRI1在韧皮部特异性表达来拯救bri3突变体表型与根中韧皮部特异性CLE45多肽信号的拮抗相关。超激活的CLE45信号会导致韧皮部筛分子（sieve element）的分化缺陷，且bri3突变体背景下CLE45感知的敲除能够使得韧皮部恢复到正确的发育。然而，bri3突变体的矮化表型仍然没有恢复。本文的结果揭示了韧皮部中油菜素内酯感知的局部和系统性效应，其在局部上与CLE45信号拮抗以保证韧皮部的分化，而其在系统性上通过一个韧皮部来源的、非细胞自主性信号来指导植物器官的形成。

Highlights

• BR perception in developing phloem rescues the dwarfism of receptor mutants

• 正在发育中韧皮部的BR感知能够恢复BR受体激酶突变体的矮化缺陷

  
  

• BR perception antagonizes CLE45 peptide signaling in the root protophloem

• 根的原生韧皮部中，BR感知拮抗CLE45多肽信号

  
  

• Local and systemic effects of BR perception in the phloem are genetically distinct

• 韧皮部中BR感知到的局部和系统性效应具有遗传上的异质性

  
  

• Developing phloem can orchestrate cellular behavior of adjacent tissues

• 发育中的韧皮部能够调控邻近组织的细胞行为

  
  

通讯：Christian S. Hardtke (https://wp.unil.ch/hardtkelab)

个人简介：1997年，慕尼黑大学，博士；1998年，多伦多大学，博士后；1998-2000年，耶鲁大学，博士后。

研究方向：植物的生长和发育。

doi: https://doi.org/10.1016/j.cub.2020.02.029

Journal: Current Biology

Published date: March 26, 2020