In high-mountains, cold spells can occur at any time during the growing season and plants may be covered with snow for several days. This raises the question to what extent sexual processes are impaired by low temperatures. We tested pollen performance and fertilization capacity of high-mountain species with different elevational distribution in the European Alps ( Cerastium uniflorum, Gentianella germanica, Ranunculus glacialis, R. alpestris, Saxifraga bryoides, S. caesia, S. moschata) during simulated cold snaps in the laboratory. Plants were exposed to 0 °C (the temperature below the snow) for 12, 36, 60 and 84 h. In S. caesia, the experiment was verified in situ during a cold snap. Sexual processes coped well with large temperature differences and remained functional at near-freezing temperatures for a few days. During the cooling-down phase a high percentage (67–97%) of pollen grains germinated and grew tubes into the style. At zero degrees, tube growth continued slowly both in the laboratory and in situ below the snow. Fertilization occurred in up to 100% of flowers in the nival species and in G. germanica, but was strongly delayed or absent in the alpine species. During rewarming, fertilization continued. Overall, progamic processes in high-mountain plants appear fairly robust toward weather extremes increasing the probability of successful reproduction.
References
[1]
Stephenson, A.G.; Lau, T.-C.; Quesada, M.; Winsor, J.A. Factors that Affect Pollen Performance. In Ecology and Evolution of Plant Reproduction; Wyatt, R., Ed.; Chapman and Hall: New York, NY, USA, 1992. Chapter 3; p. 119.
[2]
De Graaf, B.H.J.; Derksen, J.W.M.; Mariani, C. Pollen and pistil in the progamic phase. Sex. Plant Reprod. 2001, 14, 41–55, doi:10.1007/s004970100091.
[3]
Hedhly, A.; Hormaza, J.I.; Herrero, M. Global warming and sexual plant reproduction. Trends Plant Sci. 2008, 14, 30–36, doi:10.1016/j.tplants.2008.11.001.
[4]
Zinn, K.E.; Tunc-Ozdemir, M.; Harper, J.F. Temperature stress and plant sexual reproduction: Uncovering the weakest links. J. Exp. Bot. 2010, 61, 1959–1968, doi:10.1093/jxb/erq053.
[5]
Hedhly, A. Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ. Exp. Bot. 2011, 74, 9–16, doi:10.1016/j.envexpbot.2011.03.016.
[6]
Luza, J.G.; Polito, V.S.; Weinbaum, S.A. Staminate bloom date and temperature responses of pollen germination and tube growth in 2 walnut (Juglans) species. Am. J. Bot. 1987, 74, 1898–1903, doi:10.2307/2443973.
[7]
McKee, J.; Richards, A.J. The effect of temperature on reproduction of five Primula species. Ann. Bot. 1998, 82, 359–374, doi:10.1006/anbo.1998.0697.
[8]
Pirlak, L. The effect of temperature on pollen germination and pollen tube growth of apricot and sweet cherry. Europ. J. Hort. Sci. 2002, 67, 61–64.
[9]
Hedhly, A.; Hormaza, J.I.; Herrero, M. The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium L.). Plant Cell Environ. 2003, 26, 1673–1680, doi:10.1046/j.1365-3040.2003.01085.x.
[10]
Hedhly, A.; Hormaza, J.I.; Herrero, M. Effect of temperature on pollen tube kinetics and dynamics in sweet cherry, Prunus avium (Rosaceae). Am. J. Bot. 2004, 91, 558–564, doi:10.3732/ajb.91.4.558.
[11]
Hedhly, A.; Hormaza, J.I.; Herrero, M. The effect of temperature on pollen germination, pollen tube growth, and stigmatic receptivity in peach. Plant Biol. 2005, 7, 476–483, doi:10.1055/s-2005-865850.
[12]
Lewis, D. The physiology of incompatibility in plants I. The effect of temperature. Proc. R. Soc. Lond. B Biol. Sci. 1942, 131, 13–26, doi:10.1098/rspb.1942.0015.
[13]
Jefferies, C.J.; Brain, P.; Stott, K.G.; Belcher, A.R. Experimental systems and a mathematical model for studying temperature effects on pollen-tube growth and fertilization in plum. Plant Cell Environ. 1982, 5, 231–236.
Pasonen, H.L.; Kapyla, M.; Pulkkinen, P. Effects of temperature and pollination site on pollen performance in Betula pendula Roth—Evidence for genotype-environment interactions. Theor. Appl. Genet. 2000, 100, 1108–1112, doi:10.1007/s001220051393.
[16]
Kremer, D.; Jemric, T. Pollen germination and pollen tube growth in Fraxinus pennsylvanica. Biologia 2006, 61, 79–83, doi:10.2478/s11756-006-0011-2.
[17]
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.). Sex. Plant Reprod. 1989, 2, 225–230.
[18]
Jakobsen, H.B.; Martens, H. Influence of temperature and ageing of ovules and pollen on reproductive success in Trifolium repens L. Ann. Bot. 1994, 74, 493–501, doi:10.1006/anbo.1994.1146.
[19]
Luzar, N.; Gottsberger, G. Flower heliotropism and floral heating of five alpine plant species and the effect on flower visiting in Ranunculus montanus in the Austrian Alps. Arct. Antarct. Alp. Res. 2001, 33, 93–99, doi:10.2307/1552282.
[20]
Philipp, M.; B？cher, J.; Mattsson, O.; Woodell, S.R.J. A quantitative approach to the sexual reproductive biology and population structure in some arctic flowering plants: Dryas integrifolia, Silene acaulis and Ranunculus nivalis. Medd. Gr？nl. Biosci. 1990, 34, 3–60.
[21]
Kevan, P.G. Sun-tracking solar furnaces in high arctic flowers: Significance for pollination and insects. Science 1975, 189, 723–726.
[22]
Totland, ？. Flower heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): Effect on flower temperature, insect visitation, and seed production. Am. J. Bot. 1996, 83, 452–458, doi:10.2307/2446214.
[23]
Galen, C.; Stanton, M.L. Sunny-side up: Flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus (Ranunculaceae). Am. J. Bot. 2003, 90, 724–729, doi:10.3732/ajb.90.5.724.
[24]
Galen, C. Solar furnaces or swamp coolers: Costs and benefits of water use by solar-tracking flowers of the alpine snow buttercup, Ranunculus adoneus. Oecologia 2006, 148, 195–201, doi:10.1007/s00442-006-0362-y.
[25]
Larcher, W.; Wagner, J. High mountain bioclimate: Temperatures near the ground recorded from the timberline to the nival zone in the Central Alps. Contrib. Nat. Hist. Berne 2009, 12, 857–874.
[26]
K？rner, C. Coldest place on earth with angiosperm plant life. Alp. Bot. 2011, 121, 11–22, doi:10.1007/s00035-011-0089-1.
[27]
Ladinig, U.; Hacker, J.; Neuner, G.; Wagner, J. How endangered is sexual reproduction of high-mountain plants by summer frosts?—Frost resistance, frequency of frost events and risk assessment. Oecologia 2013, 171, 743–760, doi:10.1007/s00442-012-2581-8.
[28]
K？rner, C. Alpine Plant Life, 2nd ed. ed.; Springer: Berlin, Germany, 2003; p. 33.
[29]
Ladinig, U.; Wagner, J. Dynamics of flower development and vegetative shoot growth in the high mountain plant Saxifraga bryoides L. Flora 2009, 204, 63–73, doi:10.1016/j.flora.2008.01.007.
[30]
Steinacher, G.; Wagner, J. Effect of temperature on the progamic phase in high-mountain plants. Plant Biol. 2012, 14, 295–305, doi:10.1111/j.1438-8677.2011.00498.x.
[31]
Pauli, H.; Gottfried, M.; Grabherr, G. Vascular plant distribution patterns at the low temperature limits of plant life—The alpine-nival ecotone of Mount Schrankogel (Tyrol, Austria). Phytocoenologia 1999, 29, 297–325.
[32]
Hegi, G. lustrierte Flora von Mitteleuropa; Paul Parey: Berlin, Germany, 1975; Volume V/3, pp. 2036–2040.
[33]
Kaplan, K. Saxifragaceae. In Gustav Hegi—Illustrierte Flora von Mitteleuropa; Weber, H.E., Ed.; Blackwell: Berlin, Germany, 1995; Volume 4/2A, pp. 130–229.
[34]
Landolt, E. Unsere Alpenflora; Fischer: Stuttgart, Germany, 1992; pp. 166–225.
[35]
Zimmermann, W. Ranunculaceae. In Gustav Hegi—Illustrierte Flora von Mitteleuropa; Rechinger, K.H., Damboldt, J., Eds.; Paul Parey: Berlin, Germany, 1975; Volume 3/3, pp. 295–300.
[36]
Arroyo, M.T.K.; Armesto, J.; Primack, R. Community studies in pollination ecology in the high temperate Andes of Central Chile. II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst. Evol. 1985, 149, 187–203, doi:10.1007/BF00983305.
[37]
Inouye, D.W.; Pyke, G.H. Pollination biology in the Snowy Mountains of Australia: Comparisons with montane Colorado, USA. Aust. J. Ecol. 1988, 13, 191–210, doi:10.1111/j.1442-9993.1988.tb00968.x.
[38]
McCall, C.; Primack, R.B. Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am. J. Bot. 1992, 79, 434–442, doi:10.2307/2445156.
[39]
Totland, ？. Influence of climate, time of day and season, and flower density on insect flower visitation in alpine Norway. Arct. Alp. Res. 1994, 26, 66–71, doi:10.2307/1551879.
[40]
Pacini, E. Pollination. In Encyclopedia of Ecology; Jorgensen, S.E., Fath, B., Eds.; Elsevier: Oxford, UK, 2008; pp. 2857–2861.
[41]
Ishiguro, S.; Kawai-Oda, A.; Ueda, J.; Nishida, I.; Okada, K. The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidops. Plant Cell 2001, 13, 2191–2209.
[42]
Linskens, H.F.; Cresti, M. The effect of temperature, humidity, and light on the dehiscence of tobacco anthers. Proc. K. Ned. Akad. Wet. C 1988, 91, 369–375.
[43]
Lisci, M.; Tanda, C.; Pacini, E. Pollination ecophysiology of Mercurialis annua L. (Euphorbiaceae), an anemophilous species flowering all year round. Ann. Bot. 1994, 74, 125–135, doi:10.1006/anbo.1994.1102.
[44]
Keijzer, C.J.; Lefering-Ten Klooster, H.B.; Reinders, M.C. The mechanics of the grass flower: Anther dehiscence and pollen shedding in maize. Ann. Bot. 1996, 78, 15–21, doi:10.1006/anbo.1996.0089.
[45]
Pacini, E. From anther and pollen ripening to pollen presentation. Plant Syst. Evol. 2000, 222, 19–43, doi:10.1007/BF00984094.
[46]
García, C.; Nepi, M.; Pacini, E. Structural aspects and ecophysiology of anther opening in Allium triquetrum. Ann. Bot. 2006, 97, 521–527, doi:10.1093/aob/mcl015.
[47]
Hiscock, S.J.; Allen, A.M. Diverse cell signalling pathways regulate pollen-stigma interactions: The search for consensus. New Phytol. 2008, 179, 286–317, doi:10.1111/j.1469-8137.2008.02457.x.
[48]
Wu, J.-Y.; Jin, C.; Qu, H.-J.; Tao, S.-T.; Xu, G.-H.; Wu, J.; Wu, H.-Q.; Zhang, S.-L. Low temperature inhibits pollen viability by alteration of actin cytoskeleton and regulation of pollen plasma membrane ion channels in Pyrus pyrifolia. Environ. Exp. Bot. 2012, 78, 70–75, doi:10.1016/j.envexpbot.2011.12.021.
[49]
Herrero, M. Changes in the ovary related to pollen tube guidance. Ann. Bot. 2000, 85, 79–85, doi:10.1006/anbo.1999.1014.
[50]
Herrero, M. Ovary signals for directional pollen tube growth. Sex. Plant Reprod. 2001, 14, 3–7, doi:10.1007/s004970100082.
[51]
Arroyo, M.T.K.; Armesto, J.J.; Villagran, C. Plant phenological patterns in the High Andean Cordillera of Central Chile. J. Ecol. 1981, 69, 205–223, doi:10.2307/2259826.
Blionis, G.J.; Vokou, D. Structural and functional divergence of Campanula spatula subspecies on Mt Olympos (Greece). Plant Syst. Evol. 2002, 232, 89–105, doi:10.1007/s006060200029.
[55]
Fabbro, T.; K？rner, C. Altitudinal differences in flower traits and reproductive allocation. Flora 2004, 199, 70–81, doi:10.1078/0367-2530-00128.
[56]
Steinacher, G.; Wagner, J. Flower longevity and duration of pistil receptivity in high mountain plants. Flora 2010, 205, 376–387, doi:10.1016/j.flora.2009.12.012.
[57]
Arathi, H.S.; Rasch, A.; Cox, C.; Kelly, J.K. Autogamy and floral longevity in Mimulus guttatus. Int. J. Plant Sci. 2002, 163, 567–573, doi:10.1086/340444.
[58]
Clark, M.J.; Husband, B.C. Plasticity and timing of flower closure in response to pollination in Chamerion angustifolium (Onagraceae). Int. J. Plant Sci. 2007, 168, 619–625, doi:10.1086/513486.
[59]
Lundemo, S.; Totland, ？. Within-population spatial variation in pollinator visitation rates, pollen limitation on seed set, and flower longevity in alpine species. Acta Oecol. 2007, 32, 262–268, doi:10.1016/j.actao.2007.05.007.
[60]
Wagner, J.; Ladinig, U.; Steinacher, G.; Larl, I. From the flower bud to the mature seed: Timing and dynamics of flower and seed development in high-mountain plants. In Plants in Alpine Regions: Cell Physiology of Adaptation and Survival Strategies; Lütz, C., Ed.; Springer: Vienna, Austria, 2012. Chapter 10; pp. 135–152.
[61]
Wagner, J.; Mitterhofer, E. Phenology, seed development, and reproductive success of an alpine population of Gentianella germanica in climatically varying years. Bot. Acta 1998, 111, 159–166.
[62]
Neuner, G.; Erler, A.; Ladinig, U.; Hacker, J.; Wagner, J. Frost resistance of reproductive tissues during various stages of development in high mountain plants. Physiol. Plant. 2013, 147, 88–100, doi:10.1111/j.1399-3054.2012.01616.x.
[63]
Hacker, J.; Ladinig, U.; Wagner, J.; Neuner, G. Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling. Plant Sci. 2011, 180, 149–156, doi:10.1016/j.plantsci.2010.07.013.
[64]
Ozenda, P. Die Vegetation der Alpen im europ？ischen Gebirgsraum; Gustav Fischer: Stuttgart, Germany, 1988; pp. 230–232.
[65]
Wagner, J.; Steinacher, G.; Ladinig, U. Ranunculus glacialis L.: Successful reproduction at the altitudinal limits of higher plant life. Protoplasma 2010, 243, 117–128, doi:10.1007/s00709-009-0104-1.
[66]
Ladinig, U.; Wagner, J. Sexual reproduction of the high mountain plant Saxifraga moschata Wulfen at varying lengths of the growing season. Flora 2005, 200, 502–515, doi:10.1016/j.flora.2005.06.002.
[67]
Ladinig, U.; Wagner, J. Timing of sexual reproduction and reproductive success in the high mountain plant Saxifraga bryoides L. Plant Biol. 2007, 9, 683–693, doi:10.1055/s-2007-965081.
[68]
Linskens, H.F.; Esser, K.L. über eine spezifische Anf？rbung der Pollenschl？uche im Griffel und die Zahl Kallosepfropfen nach Selbstung und Fremdung. Naturwissenschaften 1957, 44, 16, doi:10.1007/BF00629340.
