What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation

Abstract

Floods can rapidly submerge plants, limiting oxygen to the extent that oxidative phosphorylation no longer generates adequate ATP supplies. Low-oxygen tolerant plants, such as rice, are able to adequately respond to low oxygen by successfully remodelling primary and mitochondrial metabolism to partially counteract the energy crisis that ensues. In this review, we discuss how plants respond to low-oxygen stress at the transcriptomic, proteomic, metabolomic and enzyme activity levels, particularly focusing on mitochondria and interacting pathways. The role of reactive oxygen species and nitrite as an alternative electron acceptor as well as their links to respiratory chain components is discussed. By making intra-kingdom as well as cross-kingdom comparisons, conserved mechanisms of anoxia tolerance are highlighted as well as tolerance mechanisms that are specific to anoxia-tolerant rice during germination and in coleoptiles. We discuss reoxygenation as an often overlooked, yet essential stage of this environmental stress and consider the possibility that changes occurring during low oxygen may also provide benefits upon re-aeration. Finally, we consider what it takes to be low-oxygen tolerant and argue that alternative mechanisms of ATP production, glucose signalling, starch/sucrose signalling as well as reverse metabolism of fermentation end products promote the survival of rice after this debilitating stress.

Plant tolerance of flooding stress – recent advances

“…; Shingaki‐Wells et al . ). These highlight a wealth of insight into the complex ramifications of low O 2 stress at the cell, organ and whole‐plant levels.…”

“…In the second review, Shingaki‐Wells et al . () evaluate more than 125 papers in a discussion of the constraints of O 2 deprivation and reoxygenation on mitochondrial metabolism. The topics addressed range from the reversible change in mitochondrial ultrastructure reported by Vartapetian in the 1970s to the recent description of the O 2 ‐sensing turnover of ethylene responsive transcription factors (ERF‐VIIs) that regulate PDC , ADH and other anaerobic response genes (Gibbs et al .…”

Pathways of nitric oxide metabolism and operation of phytoglobins in legume nodules: Missing links and future directions

“…Under hypoxia, mitochondria undergo various morphological, biochemical, and metabolic changes (Shingaki‐Wells, Millar, Whelan, & Narsai, ). Under these conditions, nitrite can be substituted for O 2 as a terminal electron acceptor of the ETC and consequently contributes to low rates of ATP synthesis by mitochondria.…”

A novel rice protein family of OsHIGDs may be involved in early signalling of hypoxia-promoted stem growth in deepwater rice

“…Plants must inevitably seek alternative energy sources other than oxidative phosphorylation, which drives plants to rely on enhancing fermentation. Numerous studies have thus far noted the importance of the genes regarding fermentation, but only a few have described the potential role of mitochondria in plant hypoxia response (Licausi et al 2011;Shingaki-Wells et al 2014). …”