Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems

Physiol Plant. 2010 Apr;138(4):447-62. doi: 10.1111/j.1399-3054.2009.01340.x. Epub 2009 Dec 9.

Abstract

Plant mitochondria differ from their mammalian counterparts in many respects, which are due to the unique and variable surroundings of plant mitochondria. In green leaves, plant mitochondria are surrounded by ample respiratory substrates and abundant molecular oxygen, both resulting from active photosynthesis, while in roots and bulky rhizomes and fruit carbohydrates may be plenty, whereas oxygen levels are falling. Several enzymatic complexes in mitochondrial electron transport chain (ETC) are capable of reactive oxygen species (ROS) formation under physiological and pathological conditions. Inherently connected parameters such as the redox state of electron carriers in the ETC, ATP synthase activity and inner mitochondrial membrane potential, when affected by external stimuli, can give rise to ROS formation via complexes I and III, and by reverse electron transport (RET) from complex II. Superoxide radicals produced are quickly scavenged by superoxide dismutase (MnSOD), and the resulting H(2)O(2) is detoxified by peroxiredoxin-thioredoxin system or by the enzymes of ascorbate-glutathione cycle, found in the mitochondrial matrix. Arginine-dependent nitric oxide (NO)-releasing activity of enzymatic origin has been detected in plant mitochondria. The molecular identity of the enzyme is not clear but the involvement of mitochondria-localized enzymes responsible for arginine catabolism, arginase and ornithine aminotransferase has been shown in the regulation of NO efflux. Besides direct control by antioxidants, mitochondrial ROS production is tightly controlled by multiple redundant systems affecting inner membrane potential: NAD(P)H-dependent dehydrogenases, alternative oxidase (AOX), uncoupling proteins, ATP-sensitive K(+) channel and a number of matrix and intermembrane enzymes capable of direct electron donation to ETC. NO removal, on the other hand, takes place either by reactions with molecular oxygen or superoxide resulting in peroxynitrite, nitrite or nitrate ions or through interaction with non-symbiotic hemoglobins or glutathione. Mitochondrial ROS and NO production is tightly controlled by multiple redundant systems providing the regulatory mechanism for redox homeostasis and specific ROS/NO signaling.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Electron Transport Complex I / metabolism
  • Electron Transport Complex II / metabolism
  • Electron Transport Complex III / metabolism
  • Homeostasis
  • Mitochondria / metabolism*
  • Models, Biological
  • Nitric Oxide / metabolism*
  • Oxidation-Reduction
  • Plants / metabolism*
  • Reactive Oxygen Species / metabolism*

Substances

  • Reactive Oxygen Species
  • Nitric Oxide
  • Electron Transport Complex II
  • Electron Transport Complex I
  • Electron Transport Complex III