Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis

PLoS Genet. 2018 Jan 11;14(1):e1007144. doi: 10.1371/journal.pgen.1007144. eCollection 2018 Jan.

Abstract

The brassinosteroids (BRs) represent a class of phytohormones, which regulate numerous aspects of growth and development. Here, a det2-9 mutant defective in BR synthesis was identified from an EMS mutant screening for defects in root length, and was used to investigate the role of BR in root development in Arabidopsis. The det2-9 mutant displays a short-root phenotype, which is result from the reduced cell number in root meristem and decreased cell size in root maturation zone. Ethylene synthesis is highly increased in the det2-9 mutant compared with the wild type, resulting in the hyper-accumulation of ethylene and the consequent inhibition of root growth. The short-root phenotype of det2-9 was partially recovered in the det2-9/acs9 double mutant and det2-9/ein3/eil1-1 triple mutant which have defects either in ethylene synthesis or ethylene signaling, respectively. Exogenous application of BR showed that BRs either positively or negatively regulate ethylene biosynthesis in a concentration-dependent manner. Different from the BR induced ethylene biosynthesis through stabilizing ACSs stability, we found that the BR signaling transcription factors BES1 and BZR1 directly interacted with the promoters of ACS7, ACS9 and ACS11 to repress their expression, indicating a native regulation mechanism under physiological levels of BR. In addition, the det2-9 mutant displayed over accumulated superoxide anions (O2-) compared with the wild-type control, and the increased O2- level was shown to contribute to the inhibition of root growth. The BR-modulated control over the accumulation of O2- acted via the peroxidase pathway rather than via the NADPH oxidase pathway. This study reveals an important mechanism by which the hormone cross-regulation between BRs and ethylene or/and ROS is involved in controlling root growth and development in Arabidopsis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Arabidopsis* / drug effects
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • Brassinosteroids / metabolism
  • Brassinosteroids / pharmacology*
  • Ethylenes / biosynthesis*
  • Gene Expression Regulation, Plant / drug effects
  • Homeostasis / drug effects
  • Homeostasis / genetics
  • Metabolic Networks and Pathways / drug effects
  • Metabolic Networks and Pathways / genetics
  • Plant Growth Regulators / metabolism
  • Plant Growth Regulators / pharmacology
  • Plant Roots / drug effects*
  • Plant Roots / growth & development*
  • Plant Roots / metabolism
  • Plants, Genetically Modified
  • Reactive Oxygen Species / metabolism*

Substances

  • Arabidopsis Proteins
  • Brassinosteroids
  • DET2 protein, Arabidopsis
  • Ethylenes
  • Plant Growth Regulators
  • Reactive Oxygen Species

Grants and funding

This study is funded by grants from the Shandong Provincial Funds for Distinguished Young Scholars (2014JQ201408 to ZD), the National Natural Science Foundation of China (Projects 31470371 and 31670275 to ZD), Ministry of Science and Technology of China (2015CB942901 to ZD), and the Special Support for Post-doc Creative Funding in Shangdong Province (201701007 to BL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.