In the heat of the night – alternative pathway respiration drives thermogenesis in Philodendron bipinnatifidum

Abstract

Summary• Philodendron bipinnatifidum inflorescences heat up to 42°C and thermoregulate. We investigated whether they generate heat via the cytochrome oxidase pathway uncoupled by uncoupling proteins (pUCPs), or the alternative oxidase (AOX).• Contribution of AOX and pUCPs to heating in fertile (FM) and sterile (SM) male florets was determined using a combination of oxygen isotope discrimination, protein and substrate analyses.• Both FM and SM florets thermoregulated independently for up to 30 h ex planta. In both floret types, AOX contributed > 90% of respiratory flux during peak heating. The AOX protein increased fivefold with the onset of thermogenesis in both floret types, whereas pUCP remained low throughout development. These data indicate that AOX is primarily responsible for heating, despite FM and SM florets potentially using different substrates, carbohydrates or lipids, respectively. Measurements of discrimination between O 2 isotopes in strongly respiring SM florets were affected by diffusion; however, this diffusional limitation was largely overcome using elevated O 2 .• The first in vivo respiratory flux measurements in an arum show AOX contributes the bulk of heating in P. bipinnatifidum. Fine-scale regulation of AOX activity is post-translational. We also demonstrate that elevated O 2 can aid measurement of respiratory pathway fluxes in dense tissues.

Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants

“…A small group of “thermogenic” plants are able to heat their reproductive tissues to temperatures well above ambient by maintaining a very high rate of uncoupled and hence heat-releasing AOX respiration [40–42]. This can function to attract pollinators or provide optimal temperatures for floral development.…”

Alternative oxidase inhibitors: Mitochondrion‐targeting as a strategy for new drugs against pathogenic parasites and fungi

“…Genes encoding AOX are ubiquitous in the Kingdom Plantae, where the enzyme plays a crucial role in thermogenesis, cellular metabolism, and energy homeostasis; it is also generally believed to be a major stress‐induced protein . For instance, a small group of “thermogenic” plants were able to maintain a very high rate of uncoupled, and hence heat‐releasing AOX respiration, thereby heat‐up their reproductive tissues to temperatures that are well above ambient . This provides the needed optimal temperatures for floral development or serves to attract pollinators.…”

Role of the mitochondrial alternative oxidase pathway in hydrogen photoproduction in Chlorella protothecoides

“…The respiratory electron transport in mitochondria of plants uses two different pathways, the cytochrome oxidase (COX) pathway and the alternative oxidase (AOX) pathway (Raghavendra and Padmasree 2003;Searle et al 2011). The COX pathway produces most of the ATP in mitochondria, whereas proton translocation and ATP synthesis are uncoupled in the AOX pathway (Siedow and Umbach 2000;Millenaar and Lambers 2003;Miller et al 2011). Therefore, the AOX pathway can efficiently oxidize reducing equivalents, NAD(P)H, in cells without being restricted by the proton gradient across the mitochondrial inner membrane or cellular ATP/ADP ratio (Fig.…”