While traditionally considered important mainly in hypoxic roots during flooding, upregulation of fermentation pathways in plants is highlighted to be an evolutionarily conserved strategy under aerobic conditions.
Upregulation of fermentation in plants has mainly been considered important in hypoxic roots during flooding. However, plant fermentation rates remain poorly characterized across diverse plant functional types in managed and natural ecosystems globally. Here, new studies are summarized that demonstrate the upregulation of fermentation pathways in plants during 1) Growth and development, 2) Root hypoxia associated with flooding, and 3) Defense processes during abiotic stress. While maintenance and growth respiration are often modeled separately in terrestrial models, here we propose the concept of “Defense Respiration” fueled by acetate fermentation where upregulation of acetate fermentation contributes acetate substrate for alternative energy production via aerobic respiration, biosynthesis of primary and secondary metabolites, and the acetylation of proteins involved in defense gene regulation.
Fermentation processes, are now recognized to be tightly integrated into plant growth and development as well as responses to abiotic stress. While traditionally considered important mainly in roots during flooding, fermentation in roots, stems, and leaves is now recognized as a critical drought survival strategy. Acetate produced by fermentation may be used as an energy source through “Defense Respiration” and as a stress signaling molecule critical to drought survival. We highlight new frontiers in leaf-atmosphere emission measurements as a potential way to study plant fermentation responses of individual leaves, branches, ecosystems and regions. We conclude that new field studies are urgently needed to resolve the physiological and ecological roles of plant fermentation metabolism under a changing climate.
Plant fermentation is an ancient metabolic pathway that may be critical in surviving hypoxic conditions experienced by roots during flooding. However, emerging evidence suggests that rather than a strict dependence on oxygen availability in tissues, fermentation can also be active under aerobic conditions linked to a drop in cellular energy status. Key adaptations to root hypoxia in flood tolerant species, including enhanced uptake of atmospheric oxygen in aerial tissues and delivery to roots, is lacking in flood intolerant species. This likely explains why much higher foliar emissions of ethanol and acetaldehyde have been observed from some flood intolerant species during flooding compared with flood tolerant species, in contrast to early predictions. Moreover, high tissue concentrations and atmospheric emissions of fermentation volatiles have been observed under aerobic conditions in well drained soils associated with temperature-linked growth processes as well as drought stress. Further, genomic and transcriptomic studies have revealed that a metabolic shift towards acetate fermentation occurs in roots and leaves which coordinates drought tolerance in plants via protein acetylation and the activation of the jasmonate signaling pathway. Additional studies revealed that acetate fermentation under aerobic conditions improves plant growth and that co-occurrence of acetate fermentation, aerobic respiration, and the utilization of acetate in biosynthetic pathways helps plants meet the high energetic and carbon demands of fast growth rates. This recent research appears to resolve the paradox from earlier work of why fermentation enzymes are so abundant in leaves when they are the least likely tissue to experience hypoxia. While destructive methods are mainly used to study fermentation patterns in plants, the emerging frontier of quantifying biosphere-atmosphere fluxes of fermentation volatiles and atmospheric vertical concentration gradients may provide a means to study dynamic fermentation responses in plants during growth and environmental stress from leaves, branches, ecosystems, landscapes and whole regions. This may enable studies aimed at improving the quantitative understanding of the plant physiological and ecological roles of fermentation under hypoxic and aerobic conditions. This includes potential critical roles in supporting productivity during favorable conditions for net carbon assimilation and growth, as well as defense processes linked to survival during abiotic stress in a changing climate.
Although field observations to quantify plant fermentative metabolism patterns across diverse plant functional types are in general lacking, ecosystems regularly exposed to root flooding like mangroves and low-lying tropical forests may be considered to have high rates of fermentative metabolism. For example, in Amazonian floodplain forests, more than 1000 tree species are exposed to extended annual submergence lasting up to 9 months each year, with full submergence of young trees. Despite hypoxia, restricted photosynthesis rates, and extremely low light levels during the submergence, leafed seedlings survival rates are high. Aerobic fermentation metabolism coupled to respiration in fast growing tropical pioneer tree species like Vismia guianensis, may also be important in the re-growth of tropical forests following a disturbance. In addition, high temperature and drought stress characteristic of desert ecosystems may also stimulate high rates of fermentative metabolism as a key survival trait. For example, creosotebush (Larrea tridentata), which grows in well drained sandy soils, is vastly distributed in North American deserts, and was reported to have large temperature-stimulated leaf emissions of the fermentation volatiles acetaldehyde, acetic acid, acetone, ethanol, and methyl acetate during the summer monsoon in the Sonoran desert. Thus, plant fermentation studies across diverse plant functional traits like photosynthetic types (C3, C4, and crassulacean acid metabolism), growth rates, wood density, specific leaf area, etc. may lead to improvements in our predictive understanding of the roles of plant fermentative metabolism in the establishment and resilience of ecosystem structure and function.
Figure. Graphical representation of acetate fermentation metabolism in plant cells and whole trees during root flooding and drought. Also shown are emerging methods of biosphere-atmosphere studies of fermentation volatile emissions from leaf to global scales, and an ecosystem pizza showing globally important ecosystems and the main processes anticipated to dominate fermentation processes in plants. Image credit: Kolby Jardine.
Contact: Kolby Jardine, Research Scientist (LBNL: Earth and Environmental Sciences Area, Ecology Department), email@example.com
This material is based upon work supported by the US Department of Energy (DOE), Office of Science, Office of Biological and Environmental Research (BER), Biological System Science Division (BSSD), Early Career Research Program under Award no. FP00007421 to KJJ and at the Lawrence Berkeley National Laboratory (LBNL). Additional DOE support was provided by the Coastal Observations, Mechanisms, and Predictions Across Scales (COMPASS) project and the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) through contract no. DE-AC02-05CH11231 as part of DOE’s Terrestrial Ecosystem Science Program.
Jardine K and McDowell N. (2023) Fermentation-mediated Growth, Signaling, and Defense in Plants. New Phytologist, Tansley Review. https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.19015.