The oxygen supply to thermogenic flowers

Abstract

Thermogenic flowers produce heat by intense respiration, and the rates of O2 consumption (Ṁo2) in some species can exceed those of all other tissues of plants and most animals. By exposing intact flowers to a range of O2 pressures (Po2) and measuring Ṁo2, we demonstrate that the highest respiration rates exceed the capacity of the O2 diffusive pathway and become diffusion limited in atmospheric air. The male florets on the inflorescence of Arum concinnatum have the highest known mass-specific Ṁo2 and can be severely diffusion limited. Intact spadices of Japanese skunk cabbage Symplocarpus renifolius are diffusion limited in air only when Ṁo2 is maximal, but not at lower levels. True flowers of the sacred lotus Nelumbo nucifera and the appendix of Arum concinnatum are never diffusion limited in air. Ṁo2 - Po2 curves are evaluated quantitatively with the 'Regulation Index', a new tool to measure dependence of Ṁo2 on ambient Po2 , as well as the conventional 'Critical Po2 '. The study also includes measurements of Po2 within thermogenic tissues with O2-sensitive fibre optics, and reveals that the diffusion pathway is complicated and that O2 can be provided not only from the surface of the tissues but also from the pith of the flower's peduncle.

Respiration of thermogenic inflorescences of skunk cabbage Symplocarpus renifolius in heliox

“…However, if Ṁ o 2 depends on Po 2 near 21 kPa, then the system is diffusion‐limited, and some mitochondria are normally not O 2 saturated. Our experiments have indicated that some moderately thermogenic species are not diffusion‐limited, but the most thermogenic species are (Seymour, Ito, Umekawa, Matthews, & Pirintsos, ). In particular, Ṁ o 2 of inflorescences of the Japanese skunk cabbage Symplocarpus renifolius declines at all Po 2 levels below 21 kPa in the most thermogenic individuals (i.e.…”

“…If the respiratory quotient (Ṁ co 2 /Ṁ o 2 ) in S. renifolius is approximately 1.0, as it is in S. foetidus (Seymour & Blaylock, ), the previous Ṁ CO 2 data correspond well with the present data. In further experiments on S. renifolius designed to test for diffusion limitation by varying ambient Po 2 , Ṁ o 2 varied between 117 and 356 nmol O 2 s −1 g −1 when T s was 15 °C and Po 2 was 20.9 kPa (Seymour et al, ). Two inflorescences with the lowest Ṁ o 2 (117 and 148 nmol O 2 s −1 g −1 ) did not appear to be diffusion‐limited, because the regression of Ṁ o 2 on Po 2 nearly plateaued (98% asymptotic) at 20.9 kPa.…”

“…Nothing is known about the structure of these spaces that would allow morphometric analysis of the diffusion pathway. However, Po 2 transects of the thermogenic spadix of S. renifolius made with O 2 ‐sensing, fibre‐optic probes reveal a complex architecture (Seymour et al, ). Po 2 does not decrease uniformly with depth, but varies widely, probably as the probe tip encounters either the gas network or the cytoplasm of parenchymal cells.…”

“…Excurrent oxygen fraction ( Feo 2 ) was measured 3 min later when its value was stable. The rate of oxygen consumed by the plant was calculated simply as Ṁ o 2 = Ṁ i ( Fio 2 – Feo 2 ) × 1.022, where 1.022 corrects for CO 2 production rate as measured in a previous study (Seymour et al, ). The data were standardized on a mass‐specific basis in which mass is the fresh weight of the entire spadix, including pith.…”

Parts-Prospecting for a High-Efficiency Thiamin Thiazole Biosynthesis Pathway

“…Assuming that Ala adequately mimics dehydro-Ala in the THI4 active site, these results indicate that C. bicolor THI4 could function catalytically in male flower tissue after an initial suicide reaction, provided that the oxygen level is low and the sulfide level is relatively high. Aroid spadices are known to become internally hypoxic at the flowering (thermogenic) stage (Seymour et al, 2015), and classical data on oxygen consumption rates indicate that they also may be hypoxic at earlier stages when tightly wrapped in the spathe (James and Beevers, 1950;Seymour et al, 1984). As noted above, sulfide levels in plant tissues may exceed those in E. coli.…”