Brassinosteroid-mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

Plant J. 2020 Jun;102(5):931-947. doi: 10.1111/tpj.14672. Epub 2020 Feb 26.

Abstract

Phytohormone brassinosteroids (BRs) are essential for plant growth and development, but the mechanisms of BR-mediated pollen development remain largely unknown. In this study, we show that pollen viability, pollen germination and seed number decreased in the BR-deficient mutant d^im , which has a lesion in the BR biosynthetic gene DWARF (DWF), and in the bzr1 mutant, which is deficient in BR signaling regulator BRASSINAZOLE RESISTANT 1 (BZR1), compared with those in wild-type plants, whereas plants overexpressing DWF or BZR1 exhibited the opposite effects. Loss or gain of function in the DWF or BZR1 genes altered the timing of reactive oxygen species (ROS) production and programmed cell death (PCD) in tapetal cells, resulting in delayed or premature tapetal degeneration, respectively. Further analysis revealed that BZR1 could directly bind to the promoter of RESPIRATORY BURST OXIDASE HOMOLOG 1 (RBOH1), and that RBOH1-mediated ROS promote pollen and seed development by triggering PCD and tapetal cell degradation. In contrast, the suppression of RBOH1 compromised BR signaling-mediated ROS production and pollen development. These findings provide strong evidence that BZR1-dependent ROS production plays a critical role in the BR-mediated regulation of tapetal cell degeneration and pollen development in Solanum lycopersicum (tomato) plants.

Keywords: Solanum lycopersicum; BRASSINAZOLE RESISTANT 1 (BZR1); RESPIRATORY BURST OXIDASE HOMOLOG 1 (RBOH1); anther; brassinosteroids (BRs); pollen development; programmed cell death (PCD); reactive oxygen species (ROS).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / genetics
  • Apoptosis / physiology
  • Brassinosteroids / metabolism
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Pollen / metabolism*
  • Pollen / physiology
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Solanum lycopersicum / metabolism*
  • Solanum lycopersicum / physiology

Substances

  • Brassinosteroids
  • Plant Proteins
  • Reactive Oxygen Species