Abstract
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 CO2 production during 8 h incubation in vitro at 30°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°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 β-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°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°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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References
Affourtit C, Krab K, Moore AL (2001) Control of plant mitochondrial respiration. BBA 1504:58–69
Binder WD, Ballantyne DJ (1975) The respiration and fertility of Pseudotsuga menziesii (Douglas fir) pollen. Can J Bot 53:819–823
Dane F, Hunter AG, Chambliss OL (1991) Fruit set, pollen fertility and combining ability of selected tomato genotypes under high-temperature field conditions. J Am Soc Hortic Sci 116:906–910
Dempsey WH (1970) Effects of temperature on pollen germination and tube growth. Tomato Genet Coop Rep 20:15–16
Dickinson DB (1965) Germination of lily pollen: respiration and tube growth. Science 150:1818–1819
Dickinson DB (1966) Inhibition of pollen respiration by oligomycin. Nature 210:1362–1363
Dickinson DB (1967) Permeability and respiratory properties of germinating pollen. Physiol Plant 20:118–127
Dickinson DB (1968) Rapid starch synthesis associated with increased respiration in germinating lily pollen. Plant Physiol 43:1–8
Downs CA, Heckathorn SA (1998) The mitochondrial small heat-shock protein protects NADH:ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. FEBS Lett 430:246–250
Frankis RC, Grayson GK (1990) Heat-shock response in germinating pine pollen. Sex Plant Reprod 3:195–199
Gass N, Glagotskaia T, Mellema S, Stuurman J, Barone M, Mandel T, Roessner-Tunali U, Kuhlemeier C (2005) Pyruvate decarboxylase provides growing pollen tubes with a competitive advantage in Petunia. Plant Cell 17:2355–2368
Hájek T, Honys D, Čapková V (2004) New method of plant mitochondria isolation and sub-fractionation for proteomic analyses. Plant Sci 167:389–395
Hellmers H, Machlis L (1956) Exogenous substrate utilization and fermentation by the pollen of Pinus ponderosa. Plant Physiol 31:284–289
Hoekstra FA (1979) Mitochondrial development and activity of binucleate and trinucleate pollen during germination in vitro. Planta 145:25–36
Hoekstra FA, Bruinsma J (1975) Respiration and vitality of binucleate and trinucleate pollen. Physiol Plant 34:221–225
Hoekstra FA, Bruinsma J (1980) Control of respiration of binucleate and trinucleate pollen under humid conditions. Physiol Plant 48:71–77
Hoekstra FA, van Roekel T (1983) Isolation-inflicted injury to mitochondria from fresh pollen gradually overcome by an active strengthening during germination. Plant Physiol 73:995–1001
Kandasamy MK, Kristen U (1989) Ultrastructural responses of tobacco pollen tubes to heat shock. Protoplasma 153:104–110
Karapanos IC (2007) Study on factors that influence microsporogenesis of greenhouse tomato (Lycopersicon esculentum Mill). Ph D Thesis, Agricultural University of Athens, p 221
Karapanos IC, Fasseas K, Olympios C, Passam HC (2006) Factors affecting the efficacy of agar-based substrates for the study of tomato pollen germination. J Hortic Sci Biotech 81:631–638
Levy A, Rabinowitch HD, Kedar N (1978) Morphological and physiological characters affecting flower drop and fruit set of tomatoes at high temperatures. Euphytica 27:211–218
Mascarenhas JP, Crone DE (1996) Pollen and the heat shock response. Sex Plant Reprod 9:370–374
Mearns LO, Easterling W, Hays C, Marx D (2001) Comparison of agricultural impacts of climate change calculated from high and low resolution climate change scenarios. Part I. The uncertainty due to spatial scale. Clim Change 51:131–172
Meehl TGA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997
Mellema S, Eichenberger W, Rawyler A, Suter M, Tadege M, Kuhlemeier C (2002) The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J 30:329–336
Møller IM, Lin W (1986) Membrane bound NAD(P)H dehydrogenases in higher plant cells. Annu Rev Plant Physiol 37:309–334
Nakamura N, Sado M, Arai Y (1980) Sucrose metabolism during the growth of Camelia japonica pollen. Phytochemistry 19:205–209
Nygaard P (1969) Studies on the germination of pine pollen (Pinus mugo) in vitro. I. Growth conditions and effects of pH and temperature on germination. Physiol Plant 22:338–346
O’Kelley JC (1955) External carbohydrates in growth and respiration of pollen tubes in vitro. Am J Bot 42:322–327
Palmer JM (1976) The organization and regulation of electron transport in plant mitochondria. Annu Rev Plant Physiol 27:133–157
Peet MM, Willits DH, Gardner R (1997) Response of ovule development and post-pollen production processes in male-sterile tomatoes to chronic, sub-acute high temperature stress. J Exp Bot 48:101–112
Peet MM, Sato S, Gardner RG (1998) Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant Cell Environ 21:225–231
Raja-Reddy K, Kakani VG (2007) Screening Capsicum species of different origins for high temperature tolerance by in vitro pollen germination and pollen tube length. Sci Hortic 112:130–135
Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M (2007) Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol 48:345–361
Sato S, Peet MM (2005) Effects of moderately elevated temperature stress on the timing of pollen release and its germination in tomato (Lycopersicon esculentum Mill.). J Hortic Sci Biotech 80:23–28
Sato S, Peet MM, Thomas JF (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant Cell Environ 23:719–726
Sato S, Peet MM, Thomas JF (2002) Determining critical pre- and post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures. J Exp Bot 53:1187–1195
Sato S, Kamiyama M, Iwata T, Makita N, Furukawa H, Ikeda H (2006) Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann Bot 97:731–738
Song J, Nada K, Tachibana S (1999) Ameliorative effect of polyamines on the high temperature inhibition of in vitro pollen germination in tomato (Lycopersicon esculentum Mill). Sci Hortic 80:203–212
Stainforth D, Aina T, Christensen C, Collins M, Faull N, Frame D, Kettleborough J, Knight S, Martin A, Murphy JM, Piani C, Sexton D, Smith LA, Spicer S, Thorpe A, Allen M (2005) Uncertainty in predictions of the climate response to rising levels of greenhouse gases. Nature 433:403–406
Tadege M, Kuhlemeier C (1997) Aerobic fermentation during tobacco pollen development. Plant Mol Biol 35:343–354
Taylor LP, Hepler PK (1997) Pollen germination and tube growth. Ann Rev Plant Physiol 48:461–491
Tukeeva MI, Matveeva NP, Degasyuk AN, Ermakov IP (1998) Changes in respiratory pathways during tobacco pollen grain development. Russ J Plant Physiol 45:34–38
Vasil IK (1987) Physiology and culture of pollen. Int Rev Cytol 107:127–174
Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol 42:579–620
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Communicated by Mauro Cresti.
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Karapanos, I.C., Akoumianakis, K.A., Olympios, C.M. et al. The effect of substrate, ADP and uncoupler on the respiration of tomato pollen during incubation in vitro at moderately high temperature. Sex Plant Reprod 22, 133–140 (2009). https://doi.org/10.1007/s00497-009-0098-z
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DOI: https://doi.org/10.1007/s00497-009-0098-z