Surviving floods: leaf gas films improve O₂ and CO₂ exchange, root aeration, and growth of completely submerged rice

Abstract

SummaryWhen completely submerged, the leaves of some species retain a surface gas film. Leaf gas films on submerged plants have recently been termed 'plant plastrons', analogous with the plastrons of aquatic insects. In aquatic insects, surface gas layers (i.e. plastrons) enlarge the gas-water interface to promote O 2 uptake when under water; however, the function of leaf gas films has rarely been considered. The present study demonstrates that gas films on leaves of completely submerged rice facilitate entry of O 2 from floodwaters when in darkness and CO 2 entry when in light. O 2 microprofiles showed that the improved gas exchange was not caused by differences in diffusive boundary layers adjacent to submerged leaves with or without gas films; instead, reduced resistance to gas exchange was probably due to the enlarged water-gas interface (cf. aquatic insects). When gas films were removed artificially, underwater net photosynthesis declined to only 20% of the rate with gas films present, such that, after 7 days of complete submergence, tissue sugar levels declined, and both shoot and root growth were reduced. Internal aeration of roots in anoxic medium, when shoots were in aerobic floodwater in darkness or when in light, was improved considerably when leaf gas films were present. Thus, leaf gas films contribute to the submergence tolerance of rice, in addition to those traits already recognized, such as the shoot-elongation response, aerenchyma and metabolic adjustments to O 2 deficiency and oxidative stress.

Waterproofing Crops: Effective Flooding Survival Strategies

“…Plants that inhabit wetlands may also display adaptive features that facilitate the exchange of gases between aerial and flooded organs, including the ethylene-driven formation of constitutive or induced aerenchyma and adventitious roots as well as thinning of the leaf cuticle and reorientation of chloroplasts to optimize gas exchange. Additionally, leaves may have a sufficiently hydrophobic cuticle to maintain a surface layer of gas that sustains the rapid diffusion of oxygen and carbon dioxide to allow continued stomatal activity, benefiting underwater photosynthesis and respiration (Pedersen et al, 2009;Colmer et al, 2011;Winkel et al, 2011).…”

The study of plant adaptation to oxygen deficiency in Saint Petersburg University

“…Apart from aerenchyma, the formation of aerial films on non-wettable leaf/stem surface also facilitates gas flow between the air and the flooded part of the plant (Pedersen, Rich, and Colmer, 2009;Voesenek and Bailey-Serres, 2015). In wetland monocots hydrophobic wax cuticle on the leaf surface enlarges the gas-water interface and allows fast O 2 and CO 2 diffusion, which is important not only for respiration, but also for underwater photosynthesis (Pedersen, Colmer, and Sand-Jensen, 2013).…”

Flooding and low oxygen responses in plants

“…The trait confers flood tolerance because these films enhance gas exchange with the floodwater and thus stimulate O 2 uptake in the darkness and CO 2 uptake -and thus carbohydrate and O 2 production -in the light (Colmer and Pedersen 2008;Pedersen et al 2009). Also the dryland crop, wheat, possesses superhydrophobic leaf cuticles (Raskin and Kende 1983) and initially a gas film is retained when submerged, but the superhydrophobic properties are lost in time and the gas film subsequently vanishes (Winkel et al 2014(Winkel et al , 2016.…”