Transcript profiles in cortical cells of maize primary root during ethylene-induced lysigenous aerenchyma formation under aerobic conditions

Ann Bot. 2015 May;115(6):879-94. doi: 10.1093/aob/mcv018. Epub 2015 Apr 8.

Abstract

Background and aims: Internal aeration is important for plants to survive during periods of waterlogging, and the ability to form aerenchyma contributes by creating a continuous gas space between the shoots and the roots. Roots of maize (Zea mays) react to prolonged waterlogging by forming aerenchyma in root cortical cells by programmed cell death (PCD) in response to ethylene. The aim of this study was to understand the molecular mechanisms of ethylene-induced aerenchyma formation by identifying genes that are either up- or downregulated by ethylene treatment in maize root cortical cells.

Methods: Three-day-old maize seedlings were treated with ethylene for several hours under aerobic conditions. Cortical cells were isolated from the primary roots using laser microdissection (LM), and transcript profiles with and without ethylene treatment were compared by microarray. In addition, the effect on ethylene-induced aerenchyma formation of diphenyleneiodonium (DPI), an inhibitor of NADPH oxidases, was examined in order to assess the involvement of reactive oxygen species (ROS).

Key results: A total of 223 genes were identified whose transcript levels were significantly increased or decreased by ethylene treatment in root cortical cells under aerobic conditions. Subsequent tissue-specific quantitative reverse-transcription PCR analyses revealed that ethylene increased the transcript levels of genes related to ethylene signalling in all of the root tissues examined (stelar cells, cortical cells and outer cell layers), whereas it increased the transcript levels of genes related to cell wall modification and proteolysis specifically in the cortical cells. DPI treatment inhibited the ethylene-induced aerenchyma formation and suppressed expression of some cell wall modification-related genes.

Conclusions: Several genes related to cell wall modification and proteolysis are specifically up- or downregulated in cortical cells during lysigenous aerenchyma formation under aerobic conditions with ethylene treatment. The results suggest that ethylene is perceived in stelar cells, cortical cells and outer cell layers in the maize primary root, and that the cortical cell-specific PCD is controlled downstream of ethylene perception through subsequent gene expression, which is partly regulated by ROS, in the cortical cells.

Keywords: Lysigenous aerenchyma; PCD; ROS; Zea mays; anaerobic stress; ethylene; laser microdissection; maize; microarray; primary root; programmed cell death; reactive oxygen species; transcript profile; waterlogging.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aerobiosis
  • Cell Separation
  • Cell Wall / metabolism
  • Cluster Analysis
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Ethylenes / pharmacology*
  • Gene Expression Profiling*
  • Gene Expression Regulation, Plant / drug effects*
  • Genes, Plant
  • Lasers
  • Microdissection
  • Oligonucleotide Array Sequence Analysis
  • Onium Compounds / pharmacology
  • Organ Specificity / genetics
  • Plant Roots / cytology*
  • Plant Roots / genetics
  • Proteolysis / drug effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Time Factors
  • Up-Regulation / drug effects
  • Up-Regulation / genetics
  • Zea mays / cytology*
  • Zea mays / drug effects
  • Zea mays / genetics*

Substances

  • Ethylenes
  • Onium Compounds
  • RNA, Messenger
  • diphenyleneiodonium
  • ethylene