Energy charge and emergence of the coleoptile and radicle at varying oxygen levels in Echinochloa crus‐galli

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112

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...

Section: Discussionmentioning

confidence: 51%

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

Raymond¹,

Alani²,

Pradet³

1985

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112

“…The germination of some of the seeds (classed in group I) was stopped below 3 to 1 kPa O2, whereas the germination of others (group II) still occurred at 0.1 kPa. The seeds of Echinochloa are similar to those of group 11 (26). We found no species exhibiting an intermediate behavior, but it may be expected that such seeds exist among other cultivated, or wild species.…”

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confidence: 59%

“…The 4 monocots studied here belong to the graminae and their germination occurs at very low P02. The seeds of E. crus galli, which is also a graminae, exhibit similar properties (26).…”

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confidence: 90%

“…These differences in the germination rates and adenylate energy charge values could not be explained by differences in the sensitivity of respiration to 02-The effect of P02' on seed germination has been studied by only a few authors (9,15,17,28). In two graminae, rice and Echinochloa crus galli, the coleoptile is able to grow under anaerobiosis (10,26,30) and the coleorhiza of Echinochloa is able to emerge (29). Apart from these two exceptions, seed germination, as well as other growth processes in higher plants, requires 02-The respiration of seeds increases dramatically during the first hours of imbibition, which corresponds to germination phase I ( 11); afterwards, it stabilizes, or increases more slowly (germination phase II), until rootlet protrusion which completes the germination process (5).…”

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confidence: 99%

See 1 more Smart Citation

Germination, Respiration, and Adenylate Energy Charge of Seeds at Various Oxygen Partial Pressures

Alani¹,

Bruzau²,

Raymond³

et al. 1985

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131

The effect of 02 partial pressure on the germination and the respiration of 12 cultivated species was studied. The reciprocal of the time necessary to observe rootlet emergence in 50% of the seeds was used to approach the germination rate. The maximum germination and respiration rates were reached in most seeds at 02 pressures close to that ofair. Decreasing the 02 pressure produced a gradual decrease of the germination rate. The seeds could be classed in two groups according to their response to IOW 02 pressures. Group I includes lettuce, sunflower, radish, turnip, cabbage, flax, and soybean: at 02 pressures close to 2 kilopascals, the germination in this group was stopped and the adenylate energy charge was lower than 0.6. Group II includes rice, wheat, maize, sorghum, and pea. The germination rate of these seeds was also gradually decreased by lowering the 02 partial pressure but germination still occured, very slowly, at 0.1 kilopascal; the adenylate energy charge remained higher than 0.6. These differences in the germination rates and adenylate energy charge values could not be explained by differences in the sensitivity of respiration to 02-The effect of P02' on seed germination has been studied by only a few authors (9,15,17,28). In two graminae, rice and Echinochloa crus galli, the coleoptile is able to grow under anaerobiosis (10,26,30) and the coleorhiza of Echinochloa is able to emerge (29). Apart from these two exceptions, seed germination, as well as other growth processes in higher plants, requires 02-The respiration of seeds increases dramatically during the first hours of imbibition, which corresponds to germination phase I ( 11); afterwards, it stabilizes, or increases more slowly (germination phase II), until rootlet protrusion which completes the germination process (5). Heichel and Day (9) observed that the germination of monocots occurs at P02 as low as 2 kPa, whereas the germination of most dicots required higher P02. They concluded that oxidation systems involved in germination require 02 levels greater than 2 kPa and that these systems differ in monocots and dicots. The Cyt oxidase is the site of most respiratory oxidations (12,19 about 15 kPa (18). This has been explained by the presence of barriers to the diffusion of 02 from the surface of the seed envelopes, to the internal membrane ofthe mitochondria (7,20). Thus, it could be hypothesized that those seeds which are unable to grow below 2 kPa O2 require higher P02 for respiration than the other seeds.Oxidative phosphorylation is not the only mechanism that produces ATP in seeds. It has been shown that fermentation is very active during the initial phases ofgermination ofsome seeds (14). Nevertheless, it was shown recently that fermentation contributes very little to ATP regeneration in lettuce seeds (24). This observation led to a second hypothesis (1): the seeds which are unable to germinate at P02 lower than 2 kPa regenerate less ATP by fermentation than the others.It has been established that the value of the ATP/ADP ratio,...

“…Of the 20 wetland species examined by Barclay and Crawford (1) using an anaerobic workbench to carefully remove all traces of oxygen from the growing environment, 13 survived in the dark for at least 7 d at 22C, as evidenced by an ability to grow when reexposed to air. Such observations, as well as those of limited growth processes in anoxic leaves ofSchoenoplectus lacustris, Scirpus maritimus and Typha latifolia (1), embryos and coleoptiles of rice (2,17) and Echinochloa crus-galli var oryzicola (23,24), suggest In nature, 02 concentrations in the soil water decline over hours or days (5,29), so that cells that gradually become 02 deficient may be able to acclimate. Few if any published studies have examined specifically the metabolic response of roots to a more gradual decrease in ambient 02.…”

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confidence: 99%

Metabolic Acclimation to Anoxia Induced by Low (2-4 kPa Partial Pressure) Oxygen Pretreatment (Hypoxia) in Root Tips of Zea mays

Saglio¹,

Drew²,

Pradet³

1988

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146

104

ABSTRACFYoung intact plants of maize (Zea mays L cv INRA 508) were exposed to 2 to 4 kilopascals partial pressure oxygen (hypoxic pretratment) for 18 hours before excision of the 5 millimeter root apex and treatment with sictly anaerobic conditions (anoxia). Hypoxic accUmation pve rise to lrer amounts of ATP, to larger ATP/ADP and adenylate energy charge ratios, and to higher rates of ethanol production when excised root tips were subsequently made anaerobic, compared with root tips trferred directly from aerobic to anaerobic media. Improved energy metabolism following hypoxic pretreatment was assoted with incsed activity of alcohol dehydrogenase (ADH), and indction of ADH-2 isozymes. Roots of Adbl-mutant plants lacked constitutive ADH and only slowly produced ethanol when made anaerobic. Those that were hypoxically pretreated acclimated to anoxia with induction of ADH2 and a higher energy metabolism, and a rate of ethanol production comparable to that of nonmutants. All these responses were insensitive to the presence or absence of N03-. Additionally, the rate of ethanol production was about 50 times greater than the rate of reduction of NOi-to NO2-. These tips (9-11, 25) is strongly suggestive of such acclimation, but the 02 concentrations to which cells were exposed during published experiments often were not controlled or defined closely, and were rarely, if ever, strictly anaerobic. Anaerobic polypeptides were induced by hypoxia in roots of rice (PO2 < 5 kPa) and wheat (PO2 < 2 kPa) continuously maintained at different constant concentrations of 02 (3, 4). However, the significance of these proteins, which include ADH2 and some of the glycolytic enzymes was not examined and remains unclear.Nitrate ion may play a special role during anoxia, by acting possibly as a terminal electron acceptor in respiration in the absence of molecular 02, with NADH-dependent reduction of nitrate to nitrite via NR in 'nitrate respiration' (7,12,18). It's significance lies in the regeneration of NAD+, essential for the continuation of glycolysis. Additionally, it has been suggested that competition for cytoplasmic pools of NADH between NR and ADH can occur, thereby lowering the rate of ethanol production (7,12 Anaerobic Treatment. Root apices, 5 mm long, were excised and placed in groups of 10 in 10 ml-volume glass vials with rubber puncture caps in 2.0 ml of the solution in which the roots had been pretreated, but supplemented with 100 mm glucose.Hypodermic needles through the rubber caps were used to gas the solution and headspace, one needle bubbling gas into the solution, the other to give gas exit from the vial. Equilibrium between these small volumes and a new gaseous atmosphere was attained in a few minutes. Roots from the fully aerobic and the hypoxic pretreatments were gassed either with 40 to 50% (v/v) 02 in N2, or with O2-free N2 (the anaerobic treatment, N2 = 99.99%). There was 3-fold replication.Extraction and Estimation of Adenine Nucleotides. Solution was forced out from each vial by the gas mixture with...