Abstract
To predict the performance of coppice forests with Japanese oak (Quercus mongolica var. crispula) in future changing environment, we studied the growth, photosynthesis, and powdery mildew (Erysiphe alphitoides) infection of sprouts of Japanese oak under free-air CO2 enrichment. Elevated CO2 reduced powdery mildew infection in both leaves of the shoot emerged in spring (1st flush) and the lammas and proleptic shoots (2nd flush) of sprouts. We observed significant increase in the net photosynthetic rate at growth CO2 concentration (i.e., 370 and 500 μmol mol−1 for ambient and elevated CO2 treatments, respectively) in both 1st and 2nd flush leaves of sprouts grown under elevated CO2. On the other hand, no significant increase in net photosynthetic rate under elevated CO2 was found before cutting. The photosynthetic activity of 2nd flush leaves in the sprouts under ambient condition was greatly reduced by severe infection to powdery mildew. Growth of sprouts was enhanced in the elevated CO2 condition. We conclude the growth enhancement in Japanese oak sprouts under elevated CO2 in the present study was achieved not only by physiological response (i.e., photosynthetic stimulation) but also by disease interaction.
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Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell Environ 30:258–270
Aust H-J, Hoyningen-Huene JV (1986) Microclimate in relation to epidemics of powdery mildew. Annu Rev Phytopathol 24:491–510
Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell Environ 24:253–259
Bernacchi CJ, Calfapietra C, Davey PA, Wittig VE, Scarascia-Mugnozza GE, Raines CA, Long SP (2003) Photosynthesis and stomatal conductance responses of poplars to free-air CO2 enrichment (PopFACE) during the first growing cycle and immediately following coppice. New Phytol 159:609–621
Bobbink R, Ashmore M, Braun S, Flückiger W, Van den Wyngaert IJJ (2003) Empirical nitrogen critical loads for natural and semi-natural ecosystems: 2002 update. In: Achermann B, Bobbink R (eds) Empirical critical loads for nitrogen, Environmental Documentation No. 164, Swiss Agency for the Environment, Forests and Landscape, Berne, pp 43–170
Braun U (1987) A monograph of the Erysiphales (powdery mildews). Beihefte zur Nova Hedwigia 89:1–700
Calfapietra C, Gielen B, Sabatti M, De Angelis P, Miglietta F, Scarascia-Mugnozza G, Ceulemans R (2003) Do above-ground growth dynamics of poplar change with time under CO2 enrichment? New Phytol 160:305–318
Darbah JNT, Jones WS, Burton AJ, Nagy J, Kubiske ME (2011) Acute O3 damage on first year coppice sprouts of aspen and maple spouts in an open-air experiment. J Environ Monit 13:2436–2442
Eastburn DM, McElrone AJ, Bilgin DD (2011) Influence of atmospheric and climatic change on plant–pathogen interactions. Plant Pathol 60:54–69
Edwards MC, Ayres PG (1982) Seasonal changes in resistance of Quercus petraea (sessile oak) leaves to Microsphaera alphitoides. Trans Br Mycol Soc 78:569–571
Eguchi N, Karatsu K, Ueda T, Funada R, Takagi K, Hiura T, Sasa K, Koike T (2008) Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan. Trees 22:437–447
Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Glob Change Biol 10:2121–2138
Ellsworth DS, Thomas R, Crous KY, Palmroth S, Ward E, Maier C, DeLucia E, Oren R (2012) Elevated CO2 affects photosynthetic responses in canopy pine and subcanopy deciduous trees over 10 years: a synthesis from Duke FACE. Glob Chang Biol 18:223–242
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335
Herold A (1980) Regulation of photosynthesis by sink activity: the missing link. New Phytol 86:131–144
Hokkaido Forest Tree Breeding Association (2008) Forest tree breeding and forest genetic resources in Hokkaido. Ebetsu, Hokkaido Forest Tree Breeding Association (in Japanese)
Japan Meteorological Agency (2012) Statistical information of meteorology. Available via DIALOG. http://www.jma.go.jp/jma/menu/report.html. Accessed 3 Dec 2012 (in Japanese)
Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14C-labeled hardwood forest. New Phytol 172:523–535
Karnosky DF, Pregitzer KS, Zak DR, Kubiske ME, Hendrey GR, Weinstein D, Nosal M, Percy KE (2005) Scaling ozone responses of forest trees to the ecosystem level in a changing climate. Plant, Cell Environ 28:965–981
Kitamura S, Murata G (1979) Colored illustrations of woody plants of Japan, vol II. Hoikusha Publishing Co. Ltd, Osaka
Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York, p 604
Liberloo M, Gielen B, Calfapietra C, Veys C, Pigliacelli R, Scarascia-Mugnozza G, Ceulemans R (2004) Growth of a poplar short rotation coppice under elevated atmospheric CO2 concentrations (EUROFACE) depends on fertilization and species. Ann For Sci 61:299–307
Liberloo M, Lukac M, Calfapietra C, Hoosbeek MR, Gielen B, Miglietta F, Scarascia-Mugnozza GE, Ceulemans R (2009) Coppicing shifts CO2 stimulation of poplar productivity to above-ground pools: a synthesis of leaf to stand level results from the POP/EUROFACE experiment. New Phytol 182:331–346
Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401
Loomis WE (1953) Growth and differentiation—and introduction and summary. In: Loomis WE (ed) Growth and differentiation in plants. Iowa State College Press, Ames, pp 1–17
Luedemann G, Matyssek R, Winkler JB, Grams TEE (2009) Contrasting ozone × pathogen interaction as mediated through competition between juvenile European beech (Fagus sylvatica) and Norway spruce (Picea abies). Plant Soil 323:47–60
Maruyama T, Miyaura T (2007) Recommendation of SATOYAMA study. Showado, Kyoto, p 379 (in Japanese)
Matsuda K, Shibuya M, Koike T (2002) Maintenance and rehabilitation of the mixed conifer-broadleaf forests in Hokkaido, northern Japan. Eurasian J For Res 5:119–130
Mattson WJ, Julkunen-Tiitto R, Herms DA (2005) CO2 enrichment and carbon partitioning to phenolics: do plant responses accord better with the protein competition or the growth-differentiation balance models? Oikos 111:337–347
Matyssek R, Schnyder H, Elstner EF, Munch JC, Pretzsch H, Sandermann H (2002) Growth and parasite defence in plants; the balance between resource sequestration and retention: in lieu of a guest editorial. Plant Biol 4:133–136
Matyssek R, Agerer R, Ernst D, Munch J-C, Oßwald W, Pretzsch H, Priesack E, Schnyder H, Treutter D (2005) The plant’s capacity in regulating resource demand. Plant Biol 7:560–580
Matyssek R, Koricheva J, Schnyder H, Ernst D, Munch JC, Oßwald W, Pretzsch H (2012) The balance between resource sequestration and retention: a challenge in plant science. In: Matyssek R, Schnyder H, Oßwald W, Ernst D, Munch JC, Pretzsch H (eds) Growth and defence in plants: resource allocation at multiple scales, ecological studies 220. Springer, Berlin, pp 3–24
Mcelrone AJ, Reid CD, Hoye KA, Hart E, Jackson RB (2005) Elevated CO2 reduces disease incidence and severity of a red maple fungal pathogen via changes in host physiology and leaf chemistry. Glob Change Biol 11:1828–1836
Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao Z-C (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, NY, pp 747–846
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107:19368–19373
Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280
Oßwald W, Fleischmann F, Treutter D (2012) Host–parasite interactions and trade-offs between growth- and defence-related metabolism under changing environments. In: Matyssek R, Schnyder H, Oßwald W, Ernst D, Munch JC, Pretzsch H (eds) Growth and defence in plants: resource allocation at multiple scales, ecological studies 220. Springer, Berlin, pp 53–83
Pallardy SG (2008) Physiology of woody plants, 3rd edn. Academic Press, New York, p 464
Peltonen PA, Vapaavuori E, Julkunen-Tiitto R (2005) Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Glob Change Biol 11:1305–1324
Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol 18:665–670
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, Available via DIALOG. http://www.r-project.org/index.html. Accessed 3 Dec 2012
Sato T (1989) Growths and distribution characteristics of roots of some trees in Hokkaido. Koushunai Kihoh 74:8–12 (in Japanese)
Sato T (1999) Management of forest with broad-leaved trees by using regeneration of sprouting. Koushunai Kihoh 116:14–17 (in Japanese)
Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant, Cell Environ 22:583–621
Takagi K, Eguchi N, Ueda T, Sasa K, Koike T (2004) CO2 control in a FACE system for tree saplings. J Agr Meteorol 56:9–16 (In Japanese)
Takamatsu S, Braun U, Limkaisang S, Kom-un S, Sato T, Cunnington JH (2007) Phylogeny and taxonomy of the oak powdery mildew Erysiphe alphitoides sensu lato. Mycol Res 111:809–826
Thomas RB, Strain BR (1991) Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiol 96:627–634
Tissue DT, Lewis JD (2010) Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO2] vary with phosphorus supply. Tree Physiol 30:1361–1372
Tissue DT, Oechel WC (1987) Response of Eriophorum vaginatum to elevated CO2 and temperature in the Alaskan tussock tundra. Ecology 68:401–410
Tissue DT, Thomas RB, Strain BR (1993) Long-term effects of elevated CO2 and nutrients on photosynthesis and rubisco in loblolly pine seedlings. Plant, Cell Environ 16:859–865
Underwood AJ (1981) Techniques of analysis of variance in experimental marine biology and ecology. Oceanogr Mar Biol Annu Rev 19:513–605
Wang X, Curtis P (2002) A meta-analytical test of elevated CO2 effects on plant respiration. Plant Ecol 161:251–261
Watanabe Y, Satomura T, Sasa K, Funada R, Koike T (2010) Differential anatomical responses to elevated CO2 in saplings of four hardwood species. Plant, Cell Environ 33:1101–1111
Watanabe M, Watanabe Y, Kitaoka S, Utsugi H, Kita K, Koike T (2011) Growth and photosynthetic traits of hybrid larch F1 under elevated CO2 concentration with low nutrient availability. Tree Physiol 31:965–975
Yarwood CE (1957) Powdery mildews. Bot Rev 23:235–301
Acknowledgments
We greatly indebted to Prof. Dr. Rainer Matyseek for his encouragement to our FACE experiment with special attention to biotic stresses. We are grateful to Prof. Dr. Algirdas Augustaitis for his special encouragement to our research. We thank Mr. T. Ueda (DALTON corporation) and Mr. K. Ichikawa (Field Science Center for Northern Biosphere, Hokkaido University) for their maintenance of the FACE system and experimental field. Thanks are also due to the member of laboratory for Silviculture and Forest Ecological Studies, Hokkaido University. This study was supported partly by Grant-in-Aid from the Japan Society for the Promotion of Science through the programs of a Grant-in-Aid for Young Scientists (B) (24710027, to M. Watanabe) and a Grant-in-Aid for Scientific Research on Innovative Areas (21114008, to T. Koike).
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Communicated by R. Matyssek.
This article originates from the IUFRO Conference “Biological Reactions of Forests to Climate Change and Air Pollution,” held in Kaunas/Lithuania during May 18–27, 2012, as organized by IUFRO Research Group 7.01.00 in cooperation with COST Action FP 0903 “MAFor,” North American Air Pollution workshop ENVeurope and ICP monitoring task force (local organizer: Algirdas Augustaitis).
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Watanabe, M., Kitaoka, S., Eguchi, N. et al. Photosynthetic traits and growth of Quercus mongolica var. crispula sprouts attacked by powdery mildew under free-air CO2 enrichment. Eur J Forest Res 133, 725–733 (2014). https://doi.org/10.1007/s10342-013-0744-8
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DOI: https://doi.org/10.1007/s10342-013-0744-8