Tolerance of roots to low oxygen: 'Anoxic' cores, the phytoglobin-nitric oxide cycle, and energy or oxygen sensing

William Armstrong; Peter M Beckett; Timothy D Colmer; Timothy L Setter; Hank Greenway

doi:10.1016/j.jplph.2019.04.010

Tolerance of roots to low oxygen: 'Anoxic' cores, the phytoglobin-nitric oxide cycle, and energy or oxygen sensing

J Plant Physiol. 2019 Aug:239:92-108. doi: 10.1016/j.jplph.2019.04.010. Epub 2019 Apr 26.

Authors

William Armstrong¹, Peter M Beckett², Timothy D Colmer³, Timothy L Setter⁴, Hank Greenway⁵

Affiliations

¹ School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, 6009, Perth, WA, Australia; Department of Biological Sciences, The University of Hull, Hull, UK.
² Department of Mathematics, The University of Hull, Hull, UK.
³ School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, 6009, Perth, WA, Australia. Electronic address: timothy.colmer@uwa.edu.au.
⁴ Agricultural and Environmental Consultant, P.O. Box 305, Bull Creek, 6149, WA, Australia.
⁵ School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, 6009, Perth, WA, Australia.

PMID: 31255944
DOI: 10.1016/j.jplph.2019.04.010

Abstract

Acclimation by plants to hypoxia and anoxia is of importance in various ecological systems, and especially for roots in waterlogged soil. We present evidence for acclimation by roots via 'anoxic' cores rather than being triggered by O₂ sensors. The evidence for 'anoxic' cores comes from radial O₂ profiles across maize roots and associated metabolic changes such as increases in the 'anaerobic enzymes' ADH and PDC in the 'anoxic' core, and inhibition of Cl^- transport to the xylem. These cores are predicted to develop within 15-20 min after sudden transfer of a root to hypoxia, so that the cores are 'anoxically-shocked'. We suggest that 'anoxic' cores could emanate a signal(s), such as ACC the precursor of ethylene and/or propagation of a 'Ca²⁺ wave', to other tissue zones. There, the signalling would result in acclimation of the tissues to energy crisis metabolism. An O₂ diffusion model for tissues with an 'anoxic' core, indicates that the phytoglobin-nitric oxide (Pgb-NO) cycle would only be engaged in a thin 'shell' (annulus) of tissue surrounding the 'anoxic' core, and so would only contribute small amounts of ATP on a whole organ basis (e.g. whole roots). A key feature within this annulus of tissue, where O₂ is likely to be limiting, is that the ratio (ATP formed) / (O₂ consumed) is 5-6, both when the NAD(P)H of glycolysis is converted to NAD(P)⁺ by the Pgb-NO cycle or by the TCA cycle linked to the electron transport chain. The main function of the Pgb-NO cycle may be the modulating of NO levels and O₂ scavenging, thus preventing oxidative damage. We speculate that an 'anoxic' core in hypoxic plant organs may have a particularly high tolerance to anoxia because cells might receive a prolonged supply of carbohydrates and/or ATP from the regions still receiving sufficient O₂ for oxidative phosphorylation. Severely hypoxic or 'anoxic' cores are well documented, but much research on responses of roots to hypoxia is still based on bulk tissue analyses. More research is needed on the interaction between 'anoxic' cores and tissues still receiving sufficient O₂ for oxidative phosphorylation, both during a hypoxic exposure and during subsequent anoxia of the tissue/organ as a whole.

Keywords: Anoxic shock; Energy crisis; Ethylene; Modelling; Plant waterlogging tolerance; Root hypoxia.

Publication types

Review

MeSH terms

Acclimatization / physiology*
Anaerobiosis
Energy Metabolism*
Nitric Oxide / metabolism*
Oxygen / metabolism*
Plant Proteins / metabolism*
Plant Roots / metabolism*

Substances

Plant Proteins
Nitric Oxide
Oxygen