biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 57:732-738, 2013 | DOI: 10.1007/s10535-013-0338-9

Sex-related differences of two ecologically divergent Salix species in the responses of enzyme activities to atmospheric CO2 enrichment

T. Ruuhola1,*, L. Nybakken1,2, R. Julkunen-Tiitto1
1 Department of Biology, Natural Product Laboratory, University of Eastern Finland, Joensuu, Finland
2 Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway

Sex-related differences in the responses of plants to CO2 enrichment are still rarely studied. In this study, we examined the effects of elevated atmospheric CO2 (720 μmol mol-1) on the activities of polyphenoloxidases (PPOs) and guaiacol peroxidases (PODs) in male and female plants of two ecologically divergent willow species Salix repens and S. phylicifolia. We detected that females invested more in PPO-based defence than did males, whose PPO activity decreased as a result of CO2 enrichment. Moreover, we found that the inherently slow-growing S. repens had markedly higher POD activity than did the more rapid-growing S. phylicifolia. The PODs of these two species also differed in their biochemical properties.

Keywords: peroxidase; polyphenol oxidase; willow
Subjects: sex expression; carbon dioxide elevation; peroxidase; polyphenol oxidase; proteins; water content; ascorbic acid; willow

Received: October 3, 2012; Accepted: March 6, 2013; Published: December 1, 2013  Show citation

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Ruuhola, T., Nybakken, L., & Julkunen-Tiitto, R. (2013). Sex-related differences of two ecologically divergent Salix species in the responses of enzyme activities to atmospheric CO2 enrichment. Biologia plantarum, 57(4), 732-738. doi: 10.1007/s10535-013-0338-9
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    References

    1. Åhman, I.: Growth, herbivory and disease in relation to gender in Salix viminalis L. - Oecologia 111: 61-68, 1997. Go to original source...
    2. Barbehenn, R., Dukatz, C., Holt, C., Reese, A., Martiskainen, O., Salminen, J.-P., Yip, L., Tran, L., Constabel, C.P.: Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. - Oecologia 164: 993-1004, 2010. Go to original source...
    3. Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    4. Bi, J.L., Felton, G.W: Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. - J. chem. Ecol. 21: 1511-1530, 1995. Go to original source...
    5. Coley, P.D., Bryant, J.P., Chapin, F.S. III: Resource availability and plant antiherbivore defense. - Science 230: 895-899, 1985. Go to original source...
    6. Cornelissen, T., Stiling, P.: Sex-biased herbivory: a metaanalysis of the effects of gender on plant-herbivore interactions. - Oikos 111: 488-500, 2005. Go to original source...
    7. Danell, K., Elmqvist, T., Ericson L., Salomonsson, A.: Sexuality in willows and preference by bark-eating voles: defence or not? - Oikos 44: 82-90, 1985. Go to original source...
    8. Endara, M.-J., Coley, P.D.: The resource availability hypothesis revisited: a meta-analysis. - Funct. Ecol. 25: 389-398, 2011. Go to original source...
    9. Gillespie, K.M., Rogers, A., Ainsworth, E.A.: Growth at elevated ozone or elevated carbon dioxide concentration alters antioxidant capacity and response to acute oxidative stress in soybean (Glycine max). - J. exp. Bot. 62: 2667-2678, 2011. Go to original source...
    10. Häikiö, E., Makkonen, M., Julkunen-Tiitto, R., Sitte, J., Freiwald, V., Silfer, T., Panday, V., Beuker, E., Holopainen, T., Oksanen, E.: Performance and secondary chemistry of two hybrid aspen (Populus tremula L. × P. tremuloides Michx.) clones in long-term elevated ozone exposure. - J. chem. Ecol. 35: 664-678, 2009. Go to original source...
    11. Hämet-Ahti, L., Suominen, J., Ulvinen, T., Uotila, P. (ed.): Retkeilykasvio [Field Flora of Finland]. - Finnish Museum of Natural History and Botanical Museum, Helsinki 1998.
    12. Hiraga, S., Sasaki, K., Ito, H., Ohashi, Y., Matsui, H.: A large family of class III plant peroxidases. - Plant Cell Physiol. 42: 462-468, 2001. Go to original source...
    13. Hjältén, J.: Plant sex and hare feeding preferences. - Oecologia 89: 253-256, 1992. Go to original source...
    14. Ibrahim, M.H., Jaafar, H.Z.E.: Impact of elevated carbon dioxide on primary, secondary metabolites and antioxidant responses of Eleais guineensis Jacq. (oil palm) seedlings. - Molecules 17: 5195-5211, 2012. Go to original source...
    15. Kellomäki, S., Wang, K.-Y.: Growth and resource use of birch seedlings under elevated carbon dioxide and temperature. - Ann. Bot. 87: 669-682, 2007. Go to original source...
    16. Lavola, A., Julkunen-Tiitto, R., Lehto, T., Aphalo, P.J.: Allocation of carbon to growth and secondary metabolites in birch seedlings under UV-B radiation and CO2 exposure. - Physiol. Plant. 109: 260-267, 2000. Go to original source...
    17. Li, J.-H., Dijkstra, P., Hinkle, C.R., Wheeler, R.M., Drake, B.G.: Photosynthetic acclimation to elevated atmospheric CO2 concentration in the Florida scrub-oak species Quercus geminata and Quercus myrtifolia growing in their native environment. - Tree Physiol. 19: 229-234, 1999. Go to original source...
    18. Li, X.-M., He, X.-Y., Zhang, L.-H., Chen, W., Chen, Q.: Influence of elevated CO2 and O3 on IAA, IAA oxidase and peroxidases in the leaves of ginkgo trees. - Biol. Plant. 53: 339-342, 2009. Go to original source...
    19. Lindroth, R.L., Arteel, G.E., Kinney, K.K.: Responses of three saturniid species to paper birch grown under enriched CO2 atmospheres. - Funct. Ecol. 9: 306-311, 1995. Go to original source...
    20. Marabottini, R., Schraml, C., Paolacci, R.C., Sorgona, A., Raschi, A., Rennenberg H., Badiani M.: Foliar antioxidant status of adult Mediterranean oak species (Quercus ilex L. and Q. pubescens Willd.) exposed to permanent CO2- enrichment and to seasonal water stress. - Environ. Pollut. 113: 413-423, 2001. Go to original source...
    21. Niinemets, U.: Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. - Forest Ecol. Manage. 260: 1623-1639, 2010. Go to original source...
    22. Noctor, G., Foyer. C.H.: Ascorbate and glutathione: keeping active oxygen under control.- Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 249-279, 1998. Go to original source...
    23. Nybakken, L., Hörkkä, R., Julkunen-Tiitto, R.: Combined enhancements of temperature and UV-B influence growth and phenolics in clones of the sexually dimorphic Salix myrsinifolia. - Physiol. Plant. 145: 551-564, 2012. Go to original source...
    24. Peltonen, P., Julkunen-Tiitto, R., Vapaavuori, E., Heinonen, J., Holopainen, J.: Do elevated atmospheric CO2 and O3 affect food quality and performance of folivorous insects on silver birch? - Global Change Biol. 16: 918-935, 2010. Go to original source...
    25. Peltonen, P., Julkunen-Tiitto, R., Vapaavuori, E., Holopainen, J.: Effects of elevated carbon dioxide and ozone on aphid oviposition preference and birch bud exudate phenolics. - Global Change Biol. 12: 1670-1679, 2006. Go to original source...
    26. Poorter, H., Van Berkel, Y., Baxter, R., DenHertog, J., Dijkstra, P., Gifford, R.M., Griffin, K.L., Roumet, C., Roy, J., Wong, S.C.: The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. - Plant Cell Environ. 20: 472-482, 1997. Go to original source...
    27. Ranocha, P., Chabannes, M., Chamayou, S., Danoun, S., Jauneau, A., Boudet, A.M., Goffner, D.: Laccase downregulation causes alterations in phenolic metabolism and cell wall structure in poplar. - Plant Physiol. 129: 145-155, 2002. Go to original source...
    28. Ruuhola, T., Julkunen-Tiitto, R., Vainiotalo, P.: In vitro degradation of willow salicylates. - J. chem. Ecol. 29: 1083-1097, 2003. Go to original source...
    29. Ruuhola, T., Leppänen, T., Julkunen-Tiitto, R., Rantala, M.J., Lehto, T.: Boron fertilization enhances the induced defense of silver birch. - J. chem. Ecol. 37: 460-471, 2011. Go to original source...
    30. Ruuhola, T., Rantala, L., Neuvonen, S., Yang, S., Rantala M.J.: Effects of long-term simulated acid rain on a plantherbivore interaction. - Basic appl. Ecol. 10: 589-596, 2009. Go to original source...
    31. Ruuhola, T., Tikkanen, O.-P., Tahvanainen, J.: Differences in host use efficiency of larvae of a generalist moth Operophtera brumata (Lepidoptera: Geometridae) on three chemically divergent Salix species. - J. chem. Ecol. 27: 1-21, 2001. Go to original source...
    32. Ruuhola, T., Yang, S., Ossipov, V., Haukioja, E.: Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Epirrita autumnata. - Oecologia 154: 725-730, 2008. Go to original source...
    33. Schwanz, P., Polle, A.: Antioxidative systems, pigment and protein contents in leaves of adult Mediterranean oak species (Quercus pubescens and Q. ilex) with lifetime exposure to elevated CO2. - New Phytol. 140: 411-423, 1998. Go to original source...
    34. Stiling, P., Cornelissen, T.: How does elevated carbon dioxide (CO2) affect plant-herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. - Global Change Biol. 13: 1823-1842, 2007.
    35. Tegelberg, R., Julkunen-Tiitto, R., Vartiainen, M., Paunonen, R., Rousi M., Kellomäki. S.: Exposures to elevated CO2, elevated temperature and enhanced UV-B radiation modify activities of polyphenol oxidase and guaiacol peroxidases and concentrations of chlorophylls, polyamines and soluble proteins in the leaves of Betula pendula seedlings. - Environ. exp. Bot. 62: 308-315, 2008. Go to original source...
    36. Takahama, U., Oniki, T.: A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. - Physiol. Plant. 101: 845-852, 1997. Go to original source...
    37. Talukdar, D.: Ascorbate deficient semi-dwarf asfL1 mutant of Lathyrus sativus exhibits alterations in antioxidant defense. - Biol. Plant. 56: 675-682, 2012. Go to original source...
    38. Trebst, A., Depka, B.: Polyphenol oxidase and photosynthesis research. - Photosynth. Res. 46: 41-44, 1995. Go to original source...
    39. Vaughn, K.C., Duke, S.O.: Function of polyphenol oxidase in higher plants. - Physiol. Plant. 60: 106-112, 1984. Go to original source...
    40. Veteli, T.O., Kuokkanen, K., Julkunen-Tiitto, R., Roininen, H., Tahvanainen, J.: Effects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry. - Global Change Biol. 8: 1240-1252, 2002. Go to original source...
    41. Xu, X., Peng, G., Wu, C., Korpelainen, H., Li, C.: Drought inhibits photosynthetic capacity more in females than in males of Populus cathayana. - Tree Physiol. 28: 1751-1759, 2008. Go to original source...
    42. Yang, S., Haviola, S., Ruuhola, T.: Temporal and spatial variation in mountain birch foliar enzyme activities during the larval period of Epirrita autumnata. - Chemoecology 17: 71-80, 2007. Go to original source...
    43. Ye, L., Fu X., Ge, F.: Elevated CO2 alleviates damage from Potato virus Y infection in tobacco plants. - Plant Sci. 179: 219-224, 2010. Go to original source...
    44. Zhang, S., Lu, S., Xu, X., Korpelainen, H., Li, C.: Changes in antioxidant enzyme activities and isozyme profiles in leaves of male and female Populus cathayana infected with Melampsora larici-populina. - Tree Physiol. 30: 116-128, 2010. Go to original source...
    45. Zhang, S., Chen, L., Duan, B., Korpelainen, H., Li, C.: Populus cathayana males exhibit more efficient protective mechanisms than females under drought stress. - Molecules 275: 68-78, 2012. Go to original source...
    46. Zhou, X., Ge, Z.M., Kellomäki, S., Wang, K.Y., Peltola, H., Martikainen, P.J., Lemettinen, M., Hassinen A., Ikonen, R.: Multi-objective environment chamber system for studying plant responses to climate change. - Photosynthetica 50: 24-34, 2012. Go to original source...

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