Isolation-Inflicted Injury to Mitochondria from Fresh Pollen Gradually Overcome by an Active Strengthening during Germination

Hoekstra, Folkert A.; Roekel, T. van

doi:10.1104/pp.73.4.995

Cited by 18 publications

(12 citation statements)

References 24 publications

(26 reference statements)

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“…1 and 2). Furthermore, our results confirm earlier suggestions that in dry pollen and seeds mitochondria are intact and the electron-transport chain is functional (Wilson and Bonner, 1971;Hoekstra and Van Roekel, 1983;Leopold and Vertucci, 1989;Attuci et al, 1991).…”

Section: Desiccation Induces the Reduction Of Mitochondrial Cyts In Asupporting

confidence: 81%

“…Extraction of mitochondria from dry tissues often leads to loss of structural and functional integrity (Hoekstra and van Roekel, 1983) or, at best, gives a low yield of intact material (Attucci et al, 1991). Moreover, the necessary use of aqueous solvents during isolation from drying tissues implies that the changes in redox states of the Cyts observed in vitro may not reflect the actual in vivo redox state before the extraction.…”

Section: Desiccation Induces the Reduction Of Mitochondrial Cyts In Amentioning

confidence: 99%

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

Leprince

Hoekstra

1998

Plant Physiology

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To characterize the depression of metabolism in anhydrobiotes, the redox state of cytochromes and energy metabolism were studied during dehydration of soaked cowpea (Vigna unguiculata) cotyledons and pollens of Typha latifolia and Impatiens glandulifera. Between water contents (WC) of 1.0 and 0.6 g H 2 O/g dry weight (g/g), viscosity as measured by electron spin resonance spectroscopy increased from 0.15 to 0.27 poise. This initial water loss was accompanied by a 50% decrease in respiration rates, whereas the adenylate energy charge remained constant at 0.8, and cytochrome c oxidase (COX) remained fully oxidized. From WC of 0.6 to 0.2 g/g, viscosity increased exponentially. The adenylate energy charge declined to 0.4 in seeds and 0.2 in pollen, whereas COX became progressively reduced. At WC of less than 0.2 g/g, COX remained fully reduced, whereas respiration ceased. When dried under N 2 , COX remained 63% reduced in cotyledons until WC was 0.7 g/g and was fully reduced at 0.2 g/g. During drying under pure O 2 , the pattern of COX reduction was similar to that of air-dried tissues, although the maximum reduction was 70% in dried tissues. Thus, at WC of less than 0.6 g/g, the reduction of COX probably originates from a decreased O 2 availability as a result of the increased viscosity and impeded diffusion. We suggest that viscosity is a valuable parameter to characterize the relation between desiccation and decrease in metabolism. The implications for desiccation tolerance are discussed.

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Section: Desiccation Induces the Reduction Of Mitochondrial Cyts In Asupporting

confidence: 81%

Section: Desiccation Induces the Reduction Of Mitochondrial Cyts In Amentioning

confidence: 99%

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

Leprince

Hoekstra

1998

Plant Physiology

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“…On the other hand, Hájek et al (2004) and Romagnoli et al (2007) using a novel method for mitochondria isolation from pollen tubes for proteomic analyses, did not evaluate the intactness and the oxidative capacity of these mitochondria. Therefore, to date the use of intact pollen grains has generally been preferred for the study of pollen respiration (Hoekstra and Bruinsma 1980;Hoekstra and van Roekel 1983), as in the present study. In addition, the use of whole pollen grains is facilitated by their permeability to certain respiratory substrates (Hoekstra and van Roekel 1983), respiratory inhibitors and uncouplers of oxidative phosphorylation (Dickinson 1965(Dickinson , 1966(Dickinson , 1967Hoekstra and Bruinsma 1980;Hoekstra and van Roekel 1983;Tadege and Kuhlemeier 1997).…”

Section: Discussionmentioning

confidence: 96%

“…The % change indicates the difference in respiration rate before and after the addition of various substances as a percentage of the initial rate of respiration, minus the respective difference of the control initial and final rate of respiration The % change indicates the difference in respiration rate before and after the addition of various substances as a percentage of the initial rate of respiration, minus the respective difference of the control initial and final rate of respiration Sex Plant Reprod (2009) 22:133-140 137 Although in earlier (Hoekstra 1979) as well as in more recent (Hájek et al 2004;Romagnoli et al 2007) studies, mitochondria were isolated from pollen tubes of several plant species, Hoekstra and van Roekel (1983) report that isolated mitochondria from pollen especially during the initial stages of germination exhibit poor performance, as a result of mechanical damage of the membranes during the isolation procedure. On the other hand, Hájek et al (2004) and Romagnoli et al (2007) using a novel method for mitochondria isolation from pollen tubes for proteomic analyses, did not evaluate the intactness and the oxidative capacity of these mitochondria.…”

Section: Discussionmentioning

confidence: 99%

The effect of substrate, ADP and uncoupler on the respiration of tomato pollen during incubation in vitro at moderately high temperature

et al. 2009

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Pollen of tomato cv. Supermarmande was collected from greenhouse-grown plants at various intervals throughout the year and arbitrarily classified as of high, medium or low respiratory activity on the basis of CO(2) production during 8 h incubation in vitro at 30 degrees C, a temperature that is considered to be moderately high for tomato fruit set. After an initial burst of respiration during the first stage of hydration at 30 degrees C (>1 h), the respiration rate of pollen of all three categories declined, the decrease being greater in the lots with a low or medium respiratory activity than in the high category. During hydration (10 min after the start of incubation), the addition of succinate or reduced beta-nicotinamide adenine dinucleotide (NADH) to the substrate increased the respiratory rate of slowly-respiring pollen more than that of fast-respiring pollen, but carbonyl cyanide 3-chlorophenylhydrazone (CCCP) and adenosine 5'-diphosphate (ADP) had less effect. After 1-4 h incubation, the respiration rate of the slow- or medium-respiring pollen lots had decreased, but was stimulated by succinate or NADH, and to a lesser degree by ADP. By 7 h, the respiration rate of all pollen lots had declined and was stimulated less by substrate, ADP or CCCP. The oxidation of NADH by tomato pollen contrasts with the failure of other pollen species to utilize this substrate; moreover, a synergistic effect of NADH and succinate was consistently observed. We conclude that the decline in respiration during incubation for up to 4 h at 30 degrees C may reflect a lack of respiratory substrate. After 7 h, however, the decreased response to substrate indicates a loss of mitochondrial integrity or an accumulation of metabolic inhibitors. It is concluded that at 30 degrees C (a moderately high temperature for tomato pollen), the initially high rate of respiration leads to exhaustion of the endogenous respiratory substrates (particularly in pollen with low to medium respiratory activity), but subsequently to ageing and a loss of mitochondrial activity.

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“…These procedures were carried out to prevent imbibitional damage (21) and to increase the yield of membranes (22), respectively. After sieving, pollen was mixed with 40 mL of a 10 mm ice cold Tes buffer, pH 7.0, containing 5 mM Na-EDTA, and the suspension was passed through a precooled French pressure cell at 15,000 p.s.i.…”

Section: Microsomal Membrane Isolationmentioning

confidence: 99%

Effect of Sucrose on Phase Behavior of Membranes in Intact Pollen of Typha latifolia L., as Measured with Fourier Transform Infrared Spectroscopy

Hoekstra

Crowe²,

Crowe³

1991

Plant Physiol.

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In previous studies, we have shown that the temperature dependent vibrational frequency of the CH2 stretch in hydrocarbons in intact pollen grains can be recorded with Fourier transform infrared spectroscopy and used to measure phase transition temperatures (Tm) in these hydrocarbons. Circumstantial evidence was provided that the major contribution to the signal seen in these samples was from membrane phospholipids, and that sucrose in the dry pollen grains reduced Tm of those phospholipids. In the current study, we clarify why a major constituent of the pollen grains, neutral lipids contained in discrete lipid droplets, does not contribute significantly to the signal. Further, we have isolated membranes from the pollen and show that Tm in the isolated membranes rises from -60C in the hydrated membranes to 580C when the membranes are dried without the addition of sucrose. However, when the isolated membranes are dried in the presence of increasing amounts of sucrose, Tm fell steadily, reaching a minimal value of 310C, a figure in good agreement with that seen in the intact pollen grains. The amount of sucrose required to depress Tm maximally in these membranes is also apparently in agreement with that found in the intact pollen, suggesting that sucrose depresses Tm in the pollen.Certain disaccharides, such as trehalose and sucrose, apparently play a role in the acquisition of desiccation tolerance in living organisms. This suggestion was based on the occurrence of high levels of disaccharides in desiccation-tolerant organisms (1,8,24,25,28) and on studies in vitro of their protective effect on isolated membranes (7), liposomal membranes (15, 31), and proteins (4, 5) during drying and rehydration. Trehalose is the predominant disaccharide in organisms such as yeasts, fungi, the desert resurrection plant Selaginella (19), and microscopic animals (8), whereas anhydrobiotic organs of higher plants accumulate mainly sucrose (1,24,25)

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Isolation-Inflicted Injury to Mitochondria from Fresh Pollen Gradually Overcome by an Active Strengthening during Germination

Cited by 18 publications

References 24 publications

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

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

The effect of substrate, ADP and uncoupler on the respiration of tomato pollen during incubation in vitro at moderately high temperature

Effect of Sucrose on Phase Behavior of Membranes in Intact Pollen of Typha latifolia L., as Measured with Fourier Transform Infrared Spectroscopy

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