The Effect of Temperature on Pollen Germination, Pollen Tube Growth, and Stigmatic Receptivity in Peach

Abstract

Temperature is a major climatic factor that limits geographical distribution of plant species, and the reproductive phase has proven to be one of the most temperature-vulnerable stages. Here, we have used peach to evaluate the effect of temperature on some processes of the progamic phase, from pollination to the arrival of pollen tubes in the ovary. Within the range of temperatures studied, 20 °C in the laboratory and, on average, 5.7 °C in the field, the results show an accelerating effect of increasing temperature on pollen germination and pollen tube growth kinetics, as well as an increase in the number of pollen tubes that reach the style base. For the last two parameters, although the range of temperature registered in the field was much lower, the results obtained in the laboratory paralleled those obtained in the field. Increasing temperatures drastically reduced stigmatic receptivity. Reduction was sequential, with stigmas first losing the capacity to sustain pollen tube penetration to the transmitting tissue, then their capacity to offer support for pollen germination and, finally, their capacity to support pollen grain adhesion. Within a species-specific range of temperature, this apparent opposite effect of temperature on the male and female side could provide plants with the plasticity to withstand changing environmental effects, ensuring a good level of fertilization.

Pollen germination - pollen tube growth - Prunus persica - stigmatic receptivity - temperature stress.

References

• 1 Abdulbaki A. A., Stommel J. R.. Pollen viability and fruit set of tomato genotype under optimum- and high-temperature regimes.  HortScience. (1995);  30 115-117
• 2 Austin P. T., Hewett E. W., Noiton D., Plummer J. A.. Self incompatibility and temperature affect pollen tube growth in “Sundrop” apricot (Prunus armeniaca L.).  Journal of Horticultural Science and Biotechnology. (1998);  73 375-386
• 3 Buitink J., Leprince O., Hemminga M. A., Hoekstra F. A.. Effect of moisture and temperature on the ageing kinetics of pollen: interpretation based on cytoplasmic mobility.  Plant, Cell and Environment. (2000);  23 967-974
• 4 Cerovic R., Ruzic D.. Pollen tube growth in sour cherry (Prunus cerasus) at different temperatures.  Journal of Horticultural Science. (1992);  67 333-340
• 5 Cerovic R., Ruzic D., Micic N.. Viability of plum ovules at different temperatures.  Annals of Applied Biology. (2000);  137 53-59
• 6 Cross R. H., Mckay S. A. B., McHughen A. G., Bonham-Smith P. C.. Heat-stress effects on reproduction and seed set in Linum usitatissimum L. (flax).  Plant, Cell and Environment. (2003);  26 1013-1020
• 7 Cuevas J., Rallo L., Rapaport H. F.. Initial fruit set at high temperature in olive, Olea europaea L.  Journal of Horticultural Science. (1994);  69 665-672
• 8 Dafni A., Firmage D.. Pollen viability and longevity: practical, ecological and evolutionary implications.  Plant Systematics and Evolution. (2000);  222 113-132
• 9 Elgersma A., Stephenson A. G., Den Nijs A. P. M.. Effects of genotype and temperature on pollen tube growth in perennial ryegrass (Lolium perenne L.).  Sexual Plant Reproduction. (1989);  2 225-230
• 10 Hall A. E.. Breeding for heat tolerance.  Plant Breeding Reviews. (1992);  10 129-168
• 11 Hedhly A., Hormaza J. I., Herrero M.. The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium L.).  Plant, Cell and Environment. (2003);  26 1673-1680
• 12 Hedhly A., Hormaza J. I., Herrero M.. Effect of temperature on pollen tube kinetics and dynamics in sweet cherry, Prunus avium (Rosaceae).  American Journal of Botany. (2004);  91 558-564
• 13 Hedhly A., Hormaza J. I., Herrero M.. Influence of genotype-temperature interaction on pollen performance.  Journal of Evolutionary Biology. (2005);  DOI: 10.1111/j.1420.9101.2005.00939.x
• 14 Herrero M.. Male female synchrony and the regulation of mating in flowering plants.  Philosophical Transaction of the Royal Society, London, B. (2003);  358 1019-1024
• 15 Herrero M., Arbeloa A.. Influence of the pistil on pollen tube kinetics in peach (Prunus persica). .  American Journal of Botany. (1989);  76 1441-1447
• 16 Hormaza J. I., Herrero M.. Pollen performance as affected by the pistilar genotype in sweet cherry (Prunus avium L.).  Protoplasma. (1999);  208 129-135
• 17 Hormaza J. I., Pinney K., Polito V. S.. Correlation in the tolerance to ozone between sporophytes and male gametophytes of several fruit and nut tree species (Rosaceae).  Sexual Plant Reproduction. (1996);  9 44-48
• 18 IPCC . Intergovernmental Panel on Climate Change. Impacts, Adaptation and Vulnerability. McCarthy, J. J., Canziani, O. F., Leary, N. A., Dokken, D. J., and White, K. S., eds. Contribution of Working Group II to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, UK (2001): 1000
• 19 Jefferies C. J., Belcher A. R.. A fluorescent brightener used for pollen tube identification in vivo.  Stain Technology. (1974);  49 199-202
• 20 Jefferies C. J., Brain P., Stott K. G., Belcher A. R.. Experimental systems and mathematical models for studying temperature effects on pollen-tube growth and fertilization in plum.  Plant, Cell and Environment. (1982);  5 231-236
• 21 Johansen D. A.. Plant Microtechniques. New York; McGraw-Hill (1940)
• 22 Kakani V. G., Prasad P. V. V., Craufurd P. Q., Wheeler T. R.. Response of in vitro pollen germination and pollen tube growth of groundnut (Arachis hypogaea L.) genotypes to temperature.  Plant, Cell and Environment. (2002);  25 1651-1661
• 23 Katepa-Mupondwa F. M., Barnes D. K., Smith. S. R.. Influence of parent and temperature during pollination on alfalfa seed weight and number of seeds per pod.  Canadian Journal of Plant Science. (1996);  76 259-262
• 24 Keulemans J., Van Laer H.. Effective pollination period of plums: the influence of temperature on pollen germination and pollen tube growth. Wright, C. J., ed. Manipulation of Fruiting. London, UK; Butterworths (1989): 159-171
• 25 Kozai N., Beppu K., Mochioka R., Boonprakob U., Subhadrabandhu S., Kataoka I.. Adverse effects of high temperature on the development of reproductive organs in “Hakuho” peach trees.  Journal of Horticultural Science and Biotechnology. (2004);  79 533-537
• 26 Kuo C. G., Peng J. S., Tsay J. S.. Effect of high temperature on pollen grain germination, pollen tube growth, and seed yield of chinese cabbage.  HortScience. (1981);  16 67-68
• 27 Lewis D.. The physiology of incompatibility in plants. I. Effect of temperature.  Proceedings of the Royal Society London, Series B, Biological Science. (1942);  131 13-26
• 28 Linskens H. F.. Recognition during the progamic phase. Cresti, M. and Dallai, R., eds. Biology of Reproduction and Cell Motility in Plants and Animals. Siena, Italy; University of Siena (1986): 21-31
• 29 Linskens H. F., Esser K.. Über eine spezifische Anfärbung der Pollenschläuche im Griffel und die Zahl der Kallosepfropfen nach Selbstdung und Fremddung.  Naturwissenschaften. (1957);  44 1-2
• 30 Lombard P. B., Williams R. R., Scott K. G., Jeffries C. J.. Temperature effects on pollen tube growth in styles of “Williams” pear with a note on pollination deficiencies of “Comice” pear. Compte rendue du symposium “Culture du Poirier”. (1972): 265-279
• 31 McKee J., Richards A. J.. The effect of temperature on reproduction of five Primula species.  Annals of Botany. (1998);  82 359-374
• 32 McCormick S.. Control of male gametophyte development.  Plant Cell. (2004);  16 S142-S153
• 33 Mellenthin W. M., Wang C. Y., Wang S. Y.. Influence of temperature on pollen tube growth and initial fruit development in “d'Anjou” pear.  HortScience. (1972);  7 557-559
• 34 Mulcahy D. L.. The rise of angiosperms: a gynecological factor.  Science. (1979);  206 20-23
• 35 Ottaviano E., Mulcahy D. L.. Genetics of angiosperm pollen.  Advances in Genetics. (1989);  26 1-64
• 36 Parmeson C., Yohe G.. A globally coherent fingerprint of climate change impacts across natural systems.  Nature. (2003);  421 37-42
• 37 Pasonen H. -L., Käpylä M., Pulkkinen P.. Effect of temperature and pollination site on pollen performance in Betula pendula Roth - evidence for genotype-environment interactions.  Theoretical and Applied Genetics. (2000);  100 1108-1112
• 38 Peet M. M., Sato S., Gardner R. G.. Comparing heat stress effects on male-fertile and male-sterile tomatoes.  Plant, Cell and Environment. (1998);  21 225-231
• 39 Peet M. M., Willits D. H., Gardener R.. Response of ovule development and post-pollen production processes in male-sterile tomatoes to chronic, sub-acute high temperature stress.  Journal of Experimental Botany. (1997);  48 101-111
• 40 Petropoulou S. P., Alston F. H.. Selecting for improved pollination at low temperature in apple.  Journal of Horticultural Science and Biotechnology. (1998);  73 507-512
• 41 Postweiler K., Stösser R., Anvari S. F.. The effect of different temperatures on the viability of ovules in cherries.  Scientia Horticulturae. (1985);  25 235-239
• 42 Prasad P. V. V., Boote K. J., Allen L. H., Thomas J. M. G.. Super-optimal temperatures are detrimental to peanut (Arachis hypogaea L.) reproductive processes and yield at both ambient and elevated carbon dioxide.  Global Change Biology. (2003);  9 1775-1787
• 43 Rodrigo J., Hormaza J. I., Herrero M.. Ovary starch reserves and flower development in apricot (Prunus armeniaca). .  Physiologia Plantarum. (2000);  108 35-41
• 56 Rodrigo J., Herrero M.. Effects of pre-blossom temperatures on flower development and fruit set in apricot.  Scientia Horticulturae. (2001);  1680 1-11
• 44 Root T. L., Price J. T., Hall K. R., Schneider S. H., Rosenzweig C., Pounds J. A.. Fingerprints of global warming on wild animals and plants.  Nature. (2003);  421 57-60
• 45 Sanzol J., Herrero M.. The “effective pollination period” in fruit trees.  Scientia Horticulturae. (2001);  90 1-17
• 46 Sanzol J., Rallo P., Herrero M.. Asynchronous development of stigmatic receptivity in the pear (Pyrus communis L. Rosaceae) flower.  American Journal of Botany. (2003);  90 78-84
• 47 Saxe H., Cannel M. G. R., Johnsen O., Ryan M. G., Vourlitis G.. Tree and forest functioning in response to global warming.  New Phytologist. (2001);  149 369-400
• 48 Shivanna K. R., Linskens H. F., Cresti M.. Pollen viability and pollen vigor.  Theoretical and Applied Genetics. (1991 a);  81 38-42
• 49 Shivanna K. R., Linskens H. F., Cresti M.. Response of tobacco pollen to high humidity and heat stress: viability and germinability in vitro and in vivo. .  Sexual Plant Reproduction. (1991 b);  4 104-109
• 50 Socías i Company R., Kester D. E., Bradley M. V.. Effects of temperature and genotype on pollen tube growth in some self-incompatible and self-compatible almond cultivars.  Journal of the American Society for Horticultural Science. (1976);  101 490-493
• 51 Taylor L. P., Hepler P. K.. Pollen germination and tube growth.  Annual Reviews in Plant Physiology and Plant Molecular Biology. (1997);  48 461-491
• 52 Thompson M. M., Liu L. J.. Temperature, fruit set, and embryo sac development in “Italian” prune.  Journal of the American Society for Horticultural Science. (1973);  98 193-197
• 53 Vasilakakis M., Porlingis I. C.. Effect of temperature on pollen germination, pollen tube growth, effective pollination period, and fruit set of pear.  HortScience. (1985);  20 733-735
• 54 Williams T. A., Abberton M. T.. Earlier flowering between 1962 and 2003 in agricultural varieties of white clover.  Oecologia. (2004);  138 122-126
• 55 Young L. W., Wilen R. W., Bonham-Smith P. C.. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production.  Journal of Experimental Botany. (2004);  55 485-495

Editor: S. S. Renner