Reversible Inhibition of the Pollen Germination and the Stigma Penetration in Crocus vernus ssp. vernus (Iridaceae) Following Fumigations with NO₂, CO, and O₃ Gases

Abstract

We assessed the pollen hydration, the pollen germination, and the stigma papilla penetration of Crocus vernus subsp. vernus (Iridaceae) after 2 h fumigations with O₃, NO₂, and CO gases within humidified (90 - 100 % RH) box experiments. When the pollen and the pistil were separately fumigated, the pollen retained the capacity to emit a tube which penetrated papilla, and the stigma papillae retained the receptivity; when the pistils were first pollinated and then fumigated, the capacity of pollen to hydrate was not affected, but the germination was significantly reduced. The vulnerability to gases became evident at 0.3 ppm O₃, 0.2 ppm NO₂, and 0.5 ppm CO. The inhibition curves as a function of the gas concentrations were of an exponential type, and they saturated at 2 ppm NO₂, 25 ppm CO, and 0.5 ppm O₃, with germination percentages of 17 %, 27 %, and 60 %, respectively. Both the pollen germination and the papilla penetration were fully restored by prolonging for 60 - 90 min the incubation at 90 - 100 % RH, after the cessation of fumigations. The vulnerability of the pollen-papilla system is discussed.

Key words

Crocus vernus ssp. vernus - nitrogen dioxide - carbon monoxide - ozone - pollen hydration and germination.

References

• 1 Bell J. N. B., Treshow M.. Air Pollution and Plant Life. Chichester, UK; J. Wiley and Sons (2002): 1-480
• 2 Black V. J., Black C. R., Roberts J. A., Stewart C. A.. Impact of ozone on the reproductive development of plants.  New Phytologist. (2000);  147 421-447
• 3 Brown G. C., Borutaite V.. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols.  Biochimica et Biophysica Acta. (2004);  1658 44-49
• 4 Castillo R., Fernandèz J., Gòmez-Gòmez L.. Implications of carotenoid biosynthetic genes in apocarotenoid formation during the stigma development of Crocus sativus and its closer relatives.  Plant Physiology. (2005);  139 674-689
• 5 Chichiriccò G.. Developmental stages of the pollen wall and tapetum in some Crocus species.  Grana. (1999);  38 31-41
• 6 Chichiriccò G.. Viability-germinability of Crocus (Iridaceae) pollen in relation to cyto- and ecophysiological factors.  Flora. (2000);  195 193-199
• 7 Chichiriccò G.. In vivo hydration and pollen germination in Crocus vernus ssp. vernus as a function of humidity.  Israel Journal of Plant Sciences. (2004);  52 307-314
• 8 Chichiriccò G.. Post-shedding dehydration and in vivo temporal germination of Crocus pollen.  Grana. (2005);  44 142-147
• 9 Davison A. W., Cape J. N.. Atmospheric nitrogen-issues related to agricultural systems.  Environment International. (2003);  29 181-187
• 10 Elagoz V., Manning W.. Responses of sensitive and tolerant bush beans (Phaseolus vulgaris L.) to ozone in open-top chambers are influenced by phenotypic differences, morphological characteristics, and the chamber environment.  Environment Pollution. (2005);  136 371-383
• 11 Feder W. A.. Reduction in tobacco pollen germination and tube elongation induced by low levels of ozone.  Science. (1968);  160 1122
• 12 Feder W. A., Sullivan F.. Differential susceptibility of pollen grains to ozone injury.  Phytopathology. (1969);  59 399
• 13 Fiscus E. L., Booker F. L., Burkey K. O.. Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning.  Plant, Cell and Environment. (2005);  28 997-1011
• 14 Furness C. A., Rudall P. J.. Inaperturate pollen in monocotyledons.  International Journal of Plant Science. (1999);  160 395-414
• 15 Gimeno B. S., Bermelo V., Sanz J., de la Torre D., Gil J. M.. Assessment of the effects of ozone exposure and plant competition on the reproductive ability of three therophytic clover species from Iberian pastures.  Atmospheric Environment. (2004);  38 2295-2303
• 16 Gottardini E., Cristofolini F., Paletti E., Lazzeri P., Pepponi G.. Pollen viability for air pollution bio-monitoring.  Journal Atmospheric Chemistry. (2004);  49 149-159
• 17 Gravano E., Bussotti F., Strasser R., Schaub M., Novak K., Skelly J., Tani C.. Ozone symptoms in leaves of woody plants in open top chambers: ultrastructural and physiological characteristics.  Physiologia Plantarum. (2004);  121 620-633
• 18 Harrison B. H., Feder W. A.. Ultrastructural changes in pollen exposed to ozone.  Phytopathology. (1974);  64 257-258
• 19 Herman F., Smidt S., Huber S., Englisch M., Knoflacher M.. Evaluation of pollution-related stress factors for forest ecosystems in Central Europe.  Environment Science Pollution Research. (2001);  4 231-242
• 20 Heslop-Harrison J., Heslop-Harrison Y.. Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate.  Stain Technology. (1970);  45 111-120
• 21 Heslop-Harrison Y.. The pollen-stigma interaction: pollen-tube penetration in Crocus.  Annals of Botany. (1977);  41 913-922
• 22 Heslop-Harrison Y., Shivanna S. R.. The receptive surface of the angiosperm stigma.  Annals of Botany. (1977);  41 1233-1258
• 23 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
• 24 Junk J., Helbig A., Krein A.. Screening and scenarios of traffic emission at Trier, Germany.  Environment Science Pollution Research. (2004);  5 297-301
• 25 Kangasjärvi J., Jaspers P., Kollist H.. Signalling and cell death in ozone-exposed plants.  Plant, Cell and Environment. (2005);  28 1021-1036
• 26 Kho Y. O., Baer J.. Observing pollen tubes by means of fluorescence.  Euphytica. (1968);  17 298-303
• 27 Klumpp A., Ansel W., Klumpp G., Belluzzo N., Calatayud V., Chaplin N., Garrec J. P., Gutsche H. J., Hayes M., Hentze H. W., Kambezidis H., Laurent O.. Eurobionet: a pan-european biomonitoring network for urban air Q.  Environmental Science Pollution Research. (2002);  3 199-203
• 28 Koch J. R., Scherzer A. J., Eshita S. M., Davis K. R.. Ozone sensitivity in hybrid poplar is correlated with a lack of defense-gene activation.  Plant Physiology. (1998);  118 1243-1252
• 29 Loibl W., Bolhàr-Nordenkampf H., Herman F., Smidt S.. Modelling critical levels of ozone for the forested area of Austria. Modifications of the AOT 40 concept.  Environmental Science Pollution Research. (2004);  3 171-180
• 30 Lowe G. M., Vlismas K., Young A. J.. Carotenoids as prooxidants?.  Molecular Aspects of Medicine. (2003);  24 363-369
• 31 Manning W. J., Godzik B.. Bioindicator plants for ambient ozone in Central and Eastern Europe.  Environment Pollution. (2004);  130 33-39
• 32 Nali C., Paletti E., Marabottini R., Della Rocca G., Lorenzini G., Paolacci A. R., Ciuffi M., Badiani M.. Ecophysiological and biochemical strategies of response to ozone in Mediterranean evergreen broadleaf species.  Atmospheric Environment. (2004);  38 2247-2257
• 33 Nisoli E., Clementi E., Tonello C., Moncada S., Carruba M. O.. Can endogenous gaseous messengers control mitochondrial biogenesis in mammalian cells?.  Prostaglandin and Other Lipid Mediators. (2004);  73 9-27
• 34 Omasa K., Saji H., Youssefian S., Kondo N.. Air Pollution and Plant Biotechnology. Tokio; Springer-Verlag (2002): 1-480
• 35 Palitzsch K., Göllner S., Lupa K., Matschullat J., Messal C., Pleßow K., Schipek M., Schnabel I., Weller C., Zimmermann F.. Ozone concentrations in forest ecosystems from the viewpoint of atmosphere chemistry and plant physiology - a synopsis.  Environmental Science Pollution Research. (2005);  4 231-241
• 36 Rezanejad F., Majd A., Shariatzadeh S. M. A., Moein M., Aminzadeh M., Mirzaeian M.. Effect of air pollution on soluble proteins, structure and cellular material release in pollen of Lagerstroemia indica L. (Lytraceae).  Acta Biologica Cracoviensia Botanica. (2003);  45 129-132
• 37 Rodriguez-Riano T., Dafni A.. A new procedure to assess pollen viability.  Sexual Plant Reproduction. (2000);  12 241-244
• 38 Roshchina V. V., Mel'nikova E. V.. Pollen chemosensitivity to ozone and peroxides.  Russian Journal of Plant Physiology. (2001);  48 74-83
• 39 Roshchina V. V., Roshchina V. D.. Ozone and Plant Cell. Dordrecht; Kluwer Academic Publishers (2003): 1-240
• 40 Schaub M., Skelly J. M., Zhang J. W., Ferdinand J. A., Savage J. E., Stevenson R. E., Davis D. D., Stainer K. C.. Physiological and foliar symptom response in the crowns of Prunus serotina, Fraxinus americana and Acer rubrum canopy trees to ambient ozone under field conditions.  Environment Pollution. (2005);  133 553-567
• 41 Sikora E. J., Chappelka A. H.. Air pollution damage to plants. Alabama Cooperative Extension System, Auburn and Alabama Universities.  Circular ANR‐913. (1996);  1-5
• 42 Treshow M., Anderson F. K.. Plant Stress from Air Pollution. Chichester; J. Wiley and Sons (1989): 1-283
• 43 Wheeler M. J., Franklin-Tong V. E., Franklin F. C. H.. The molecular and genetic basis of pollen-pistil interactions.  New Phytologist. (2001);  151 565-584
• 44 White A., Handle R. P., Smith E. L.. Principles of Biochemistry. Tokio; Kōgakusha Company (1968): 369-372
• 45 Young A. J., Lowe G. M.. Antioxidants and prooxidant properties of carotenoids.  Archivies Biochemistry Biophysics. (2001);  385 20-27
• 46 Yu T. Y., Chang I. C.. Spatiotemporal features of severe air pollution in northern Taiwan.  Environmental Science Pollution Research. (2006);  4 268-275
• 47 Werner H., Fabian P.. Free-air fumigation on mature trees. A novel system for controlled ozone enrichment in growth-up beech and spruce canopies.  Environmental Science Pollution Research. (2002);  2 117-121

Editor: J. P. Sparks