Nitric oxide is essential for the development of aerenchyma in wheat roots under hypoxic stress

Plant Cell Environ. 2017 Dec;40(12):3002-3017. doi: 10.1111/pce.13061. Epub 2017 Oct 13.

Abstract

In response to flooding/waterlogging, plants develop various anatomical changes including the formation of lysigenous aerenchyma for the delivery of oxygen to roots. Under hypoxia, plants produce high levels of nitric oxide (NO) but the role of this molecule in plant-adaptive response to hypoxia is not known. Here, we investigated whether ethylene-induced aerenchyma requires hypoxia-induced NO. Under hypoxic conditions, wheat roots produced NO apparently via nitrate reductase and scavenging of NO led to a marked reduction in aerenchyma formation. Interestingly, we found that hypoxically induced NO is important for induction of the ethylene biosynthetic genes encoding ACC synthase and ACC oxidase. Hypoxia-induced NO accelerated production of reactive oxygen species, lipid peroxidation, and protein tyrosine nitration. Other events related to cell death such as increased conductivity, increased cellulase activity, DNA fragmentation, and cytoplasmic streaming occurred under hypoxia, and opposing effects were observed by scavenging NO. The NO scavenger cPTIO (2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt) and ethylene biosynthetic inhibitor CoCl2 both led to reduced induction of genes involved in signal transduction such as phospholipase C, G protein alpha subunit, calcium-dependent protein kinase family genes CDPK, CDPK2, CDPK 4, Ca-CAMK, inositol 1,4,5-trisphosphate 5-phosphatase 1, and protein kinase suggesting that hypoxically induced NO is essential for the development of aerenchyma.

Keywords: aerenchyma; ethylene; nitrate reductase; nitric oxide; nitrite; reactive oxygen species.

MeSH terms

  • Benzoates / pharmacology
  • Cobalt / pharmacology
  • Ethylenes / antagonists & inhibitors*
  • Imidazoles / pharmacology
  • Nitrate Reductase / genetics
  • Nitrate Reductase / metabolism*
  • Nitric Oxide / metabolism*
  • Nitrites / metabolism
  • Oxygen / metabolism
  • Plant Growth Regulators / antagonists & inhibitors*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Roots / enzymology
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / physiology
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / drug effects*
  • Stress, Physiological
  • Triticum / drug effects
  • Triticum / genetics
  • Triticum / growth & development
  • Triticum / physiology*

Substances

  • Benzoates
  • Ethylenes
  • Imidazoles
  • Nitrites
  • Plant Growth Regulators
  • Plant Proteins
  • Reactive Oxygen Species
  • 1,3-dihydroxy-4,4,5,5-tetramethyl-2-(4-carboxyphenyl)tetrahydroimidazole
  • Nitric Oxide
  • Cobalt
  • ethylene
  • Nitrate Reductase
  • cobaltous chloride
  • Oxygen