ATP Production by Respiration and Fermentation, and Energy Charge during Aerobiosis and Anaerobiosis in Twelve Fatty and Starchy Germinating Seeds

Abstract

The respiration and fermentation rates were compared in germinating seeds of 12 different cultivated species from five families. In air, fermentation contributes significantly to the energy metabolism only in some species (pea, maize), but is generally negligible when compared to respiration. The fermentation rate under anoxia was related either to the metabolic activity under air or to the adenine nucleotide content of the seeds: it was generally higher in seeds which contain starchy reserves (rice, maize, sorghum, pea), than in seeds which do not contain starch (lettuce, sunflower, radish, turnip, cabbage, flax); however, it was similar in wheat, sorghum (starchy seeds), and soya (nonstarchy seeds). The value of the energy charge of all the seeds was lower under anoxia than in air: after 24 hours under anoxia, it was higher than 0.5 in the starchy seeds and in soya and it was around 0.25 in the other fatty seeds.anaerobiosis in seed germination.The present work is part of a study in which we used a comparative, physiological approach with seeds of 12 different species belonging to five families. When studying the effect of the P02 on the rate of germination (2), we found that the seeds could be classed in two groups: group I included fatty seeds; in these seeds, radicle emergence did not occur below I kPa 02. Group II included starchy species, which were able to germinate at 02 partial pressures below 0.1 kPa. In the present work, the rate of 02 uptake, the rate of ethanol and lactate synthesis, and the value of AdN ratios (ATP/ADP or AEC), were used as indicators of ATP regeneration.We found that, in aerated conditions, respiration was the dominating ATP-regenerating pathway in all seeds, whereas fermentation contributed significantly only in some species. Starchy seeds appeared to maintain a higher energy metabolism under anoxia than the fatty seeds, although the two groups overlap to some extent.When dry seeds are imbibed, the respiratory activity, characterized by 02 uptake and CO2 evolution, starts extremely rapidly (5). For a long time, it was thought that this oxidative process was not coupled to ATP production and some original mechanisms were recently proposed (17) to explain the origin of the ATP needed for the biosynthetic work done during germination. Even under well-aerated conditions, ethanol and lactate accumulation may occur. It is generally considered that, during the first hours of imbibition, seeds are under 'natural anaerobiosis' (15). However, oxidative phosphorylation was demonstrated in mitochondria of the freshly imbibed Arachis hypogea axis (28), and, using an in vivo method, in lettuce seeds after 15 min of imbibition (12). Hence, the respiration of seeds is probably an important source ofATP during the initial phases ofgermination (19).In a recent study, we found that the fermentative pathways contributed very little to ATP regeneration in germinating lettuce seeds (21). Moreover, their respiratory activity is saturated by PO2' below that of air (2,22). Such characteristics a...

The Responses of Cytochrome Redox State and Energy Metabolism to Dehydration Support a Role for Cytoplasmic Viscosity in Desiccation Tolerance

“…At WC of less than 0.5 g/g, the AEC decreased to 0.4. Similar observations have been made for other plant systems in which the energy metabolism was limited by a total or partial deprivation of O 2 (Pradet and Raymond, 1983;Raymond et al, 1985). In both dry seeds and pollen before imbibition, AEC was approximately 0.2 (Fig.…”

“…First, the decrease in diffusion rates during drying of our material could be so large that increasing the O 2 gradient from outside to inside of the tissues will not significantly increase the O 2 flux to the mitochondria and O 2 availability to the COX. Second, previous studies Raymond et al, 1985) have shown that the respiratory metabolism in hydrated seeds is sustained at O 2 partial pressures as low as 0.2 kPa. Furthermore, at 21 kPa, COX is saturated with substrates, judging from the low K m for O 2 (Kariman et al, 1983;Leštan et al, 1993).…”

Ecophysiology and respiratory metabolism during the germination of Inga sessilis (Vell.) Mart. (Mimosaceae) seeds subjected to hypoxia and anoxia

“…The studies carried out during the last 25 years have consensually revealed that plants and their seeds, as most of other organisms under low oxygen tension conditions as those found in flooded or completely waterlogged soils, substitute the fermentative metabolism for the aerobic respiration (Mc Mannon & Crawford 1971, Davies 1980Mocquot et al 1981, Joly & Crawford 1982, 1983, Raymond et al 1985, Joly, 1991, 1994, Crawford 1992, Joly & Brändle 1995, Crawford & Brändle 1996, as observed in the seeds of Inga sessilis.…”

Oxidative Phosphorylation by Mitochondria Extracted from Dry Sunflower Seeds

“…It was believed, in particular, that mitochondria were damaged and had to be repaired during the germination period to become functional at the time of radicle emergence (13). Because fermentation has a low activity in most germinating seeds under aerated conditions (20), new pathways for ATP synthesis have been sought ( 17).…”