A meta-analysis of plant tissue O2 dynamics

Abstract

Adequate tissue O2 supply is crucial for plant function. We aimed to identify the environmental conditions and plant characteristics that affect plant tissue O2 status. We extracted data and performed meta-analysis on >1500 published tissue O2 measurements from 112 species. Tissue O2 status ranged from anoxic conditions in roots to >53 kPa in submerged, photosynthesising shoots. Using information-theoretic model selection, we identified ‘submergence’, ‘light’, ‘tissue type’ as well as ‘light × submergence’ interaction as significant drivers of tissue O2 status. Median O2 status were especially low (<50% of atmospheric equilibrium) in belowground rhizomes, potato (Solanum tuberosum) tubers and root nodules. Mean shoot and root O2 were ~25% higher in light than in dark when shoots had atmospheric contact. However, light showed a significant interaction with submergence on plant O2, with a submergence-induced 44% increase in light, compared with a 42% decline in dark, relative to plants with atmospheric contact. During submergence, ambient water column O2 and shoot tissue O2 correlated stronger in darkness than in light conditions. Although use of miniaturised Clark-type O2 electrodes has enhanced understanding of plant O2 dynamics, application of non-invasive methods in plants is still lacking behind its widespread use in mammalian tissues.

Recent progress in understanding the cellular and genetic basis of plant responses to low oxygen holds promise for developing flood-resilient crops

“…Due to the gas exchange constraints imposed by flooding, many studies have examined tissue O 2 status in partially or completely submerged plant tissues. A recent meta-analysis of >500 studies and encompassing 112 species showed that O 2 status ranged from effectively 0 kPa in roots to >50 kPa in submerged, photosynthesizing shoots ( Herzog et al , 2023 ). When flooded, tissue O 2 status was particularly low in rhizomes, potato tubers, and root nodules.…”

“…Surprisingly, root O 2 status is not influenced by light or darkness as long as the shoot is exposed to air due to the effective O 2 exchange between the shoots and the atmosphere ( Herzog et al , 2023 ). However, measurements using miniaturized Clark-type O 2 sensors ( Revsbech, 1989 ) show that the stele operates at a significantly lower O 2 tension than the cortex, even in roots acclimated to soil flooding ( Herzog et al , 2023 ).…”

“…Surprisingly, root O 2 status is not influenced by light or darkness as long as the shoot is exposed to air due to the effective O 2 exchange between the shoots and the atmosphere ( Herzog et al , 2023 ). However, measurements using miniaturized Clark-type O 2 sensors ( Revsbech, 1989 ) show that the stele operates at a significantly lower O 2 tension than the cortex, even in roots acclimated to soil flooding ( Herzog et al , 2023 ). The difference in tissue O 2 status is due to (i) the higher O 2 consumption per tissue mass of the stele ( Aguilar et al , 2003 ), and (ii) the lower diffusivity of the stelar tissues ( Armstrong, 1979 ), both resulting in a lower O 2 status of the stele.…”

Response of underwater photosynthesis to light, CO2, temperature, and submergence time of Taxodium distichum, a flood-tolerant tree

“…Similarly, the availability of molecular O 2 can restrict underwater respiration of submerged terrestrial plants, and an O 2 pressure of almost twice that of atmospheric equilibrium is needed to saturate respiration ( Colmer and Pedersen, 2008 ). A recent meta-analysis encompassing 112 species of both aquatic and terrestrial plants have clearly demonstrated that partial or complete submergence lead to significant declines in tissue O 2 status particularly during darkness when the only source of O 2 for underwater respiration is O 2 dissolved in the floodwater ( Herzog et al., 2023 ). However, some species of wetland plants form numerous adventitious roots emerging from the stem and hanging into the floodwater as response to partial or complete submergence ( Rich et al., 2013 ; Zhang et al., 2017 ; Lin et al., 2023 ).…”

Spatial O2 Profile in Coix lacryma-jobi and Sorghum bicolor along the Gas Diffusion Pathway under Waterlogging Conditions

“…The efficient supply of oxygen to the roots involves considering the characteristics of the above-ground parts as an oxygen supply source and the roots as a sink [ 8 , 13 ]. A meta-analysis integrating 129 studies on tissue oxygen concentrations in plants demonstrated longitudinal oxygen diffusion from the leaves to the roots [ 14 ]. Additionally, evidence from noninvasive methods using N-isotopes showed leaf-to-root gas diffusion in partially submerged rice plants [ 15 ].…”