Abstract
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After 3 years of CO 2 treatments, A stimulation from ambient to elevated CO 2 was strongly related to the total dry mass change (%), supporting the sink demand A hypothesis.
Abstract
Adaptations related to gas exchange are important fitness traits in plants and have significant growth and ecological implications. Assimilation (A) and assimilation to internal CO2 (AC i ) response curve parameters were quantified from a red spruce (RS) (Picea rubens Sarg.)—black spruce (BS) [P. mariana (Mill.) B.S.P.] controlled-cross hybrid complex grown under ambient and elevated CO2 conditions. Under ambient conditions, maximum A (A max), maximum rate of carboxylation by rubisco (V cmax), maximum rate of electron transport (J max), and carboxylation efficiency (CE) generally increased with increasing BS content; however, under elevated CO2 conditions, hybrid index 50 (hybrid index number is the percentage of RS, balance BS) often had greater values than the other indices. There were significant hybrid index, CO2, and hybrid index × CO2 effects for A growth at 360 ppm (A 360) and 720 ppm (A 720). The net A stimulation (A stim), from ambient to elevated CO2 treatment after 3 years was 10.8, 57.8, 74.1, 69.8, and 58.7 %, for hybrid indices 0 (BS), 25, 50, 75, and 100 (RS), respectively. Why does BS have the least A stim, hybrid index 50 the most, and RS a moderate level? There was a significant relationship between A 360 and ambient total biomass among indices (P = 0.096), but none was found between A 720 and elevated total biomass. However, A stim (%) was strongly related to the change in total dry mass (%) in response to elevated CO2 (R 2 = 0.931, P = 0.008), supporting the hypothesis that sink demand drives A. Traits A max, V cmax and J max were correlated to total chlorophyll concentration. Moreover, A max V cmax and J max also showed a significant underlying male effect, particularly under ambient conditions consistent with the paternal inheritance of the chloroplast genome.






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Atkin OK, Schortemeyer M, McFarlane N, Evans JR (1999) The response of fast- and slow-growing Acacia species to elevated atmospheric CO2: an analysis of the underlying components of relative growth rate. Oecologia 120:544–554
Barsi DC, Major JE, Mosseler A, Campbell M (2009) Genetic variation and control of chloroplast pigment concentrations and related needle-level traits in Picea rubens, Picea mariana, and their hybrids: moisture and light environmental effects. Trees 23:555–571
Bauer GA, Berntson GM, Bazzaz FA (2001) Regenerating temperate forests under elevated CO2 and nitrogen deposition: comparing biochemical and stomatal limitations of photosynthesis. New Phytol 152:249–266
Beylor J (1999) Management of tolerant softwoods: a provincial perspective from Nova Scotia. In: Harrison G, Whitney R, Swift DE (eds) Proceedings of the Tolerant Softwood Workshop. Maritime Forest Ranger School, Fredericton, pp 1–21
Bobola MS, Eckert RT, Klein AS, Stapelfeldt L, Smith DE, Guenette D (1996) Using nuclear and organelle DNA markers to discriminate among Picea rubens, Picea mariana, and their hybrids. Can J For Res 26:433–443
Centritto M, Jarvis PG (1999) Long-term effects of elevated carbon dioxide concentration and provenance on four clones of Sitka spruce (Picea sitchensis). II. Photosynthetic capacity and nitrogen use efficiency. Tree Physiol 19:807–814
Crous KY, Ellsworth DS (2004) Canopy position affects photosynthetic adjustments to long-term elevated CO2 concentration (FACE) in aging needles in a mature Pinus taeda forest. Tree Physiol 24:961–970
Crous KY, Walters MB, Ellsworth DS (2008) Elevated CO2 concentration affects leaf photosynthesis—nitrogen relationships in Pinus teada over nine years in FACE. Tree Physiol 28:607–614
DeHayes DH, Waite CE, Ingle MA, Williams MW (1990) Winter injury susceptibility and cold tolerance of current and year-old needles of red spruce trees from several provenances. For Sci 36:982–994
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Ghannoum O, Phillips NG, Conroy JP, Smith RA, Attard RD, Woodfield R, Logan BA, Lewis JD, Tissue DT (2010) Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Glob Chg Biol 16:303–319
Gordon AG (1976) The taxonomy and genetics of Picea rubens and its relationship to Picea mariana. Can J Bot 54:781–813
Gratani L, Ghia E (2002) Changes in morphological and physiological traits during leaf expansion of Arbutus unedo. Environ Exp Bot 48:51–60
Greenep H, Turnbull MH, Whitehead D (2003) Response of photosynthesis in second-generation Pinus radiata trees to long-term exposure to elevated carbon dioxide partial pressure. Tree Physiol 23:569–576
Greenwood MS, Volkaert HA (1992) Morphophysiological traits as markers for the early selection of conifer genetic families. Can J For Res 22:1001–1008
Griffin KL, Tissue DT, Turnbull MH, Whitehead D (2000) The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D. Don. after 4 years. Plant Cell Environ 23:1089–1098
Guo D-P, Guo Y-P, Zhao J-P, Liu H, Peng Y, Wang Q-M, Chen J-S, Rao GZ (2005) Photosynthetic rate and chlorophyll fluorescence in leaves of stem mustard (Brassica juncea var. tsatsai) after turnip mosaic virus infection. Plant Sci 168:57–63
Hamburg SP, Cogbill CV (1988) Historical decline of red spruce populations and climate warming. Nature 331:428–431
Harley PC, Sharkey TD (1991) An improved model of C3 photosynthesis at high CO2. Reversed O2 sensitivity explained by lack of glycerate re-entry into the chloroplast. Photosynth Res 27:168–178
Harley PC, Thomas RB, Reynolds JF, Strain BR (1992) Modelling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ 15:271–282
Hattenschwiller S, Korner C (1996) System-level adjustments to elevated CO2 in model spruce ecosystems. Glob Change Biol 2:377–387
Hoddinott J, Scott R (1996) The influence of light quality and carbon dioxide enrichment on the growth and physiology of seedlings of three conifer species. II. Physiological responses. Can J Bot 74:391–402
Jach ME, Ceulemans R (2000) Effects of season, needle age and elevated atmospheric CO2 on photosynthesis in Scots pine (Pinus sylvestris). Tree Physiol 20:145–157
Johnsen KH (1993) Growth and ecophysiological responses of black spruce seedlings to elevated CO2 under varied water and nutrient additions. Can J For Res 23:1033–1042
Johnsen KH, Major JE, Loo J, McPhee D (1998) Negative heterosis not apparent in 22-year-old hybrids of Picea mariana and Picea rubens. Can J Bot 76:434–439
Johnsen KH, Flanagan LB, Huber DA, Major JE (1999) Genetic variation in growth and carbon isotope discrimination in Picea mariana: analyses from a half-diallel mating design using field grown trees. Can J For Res 29:1727–1735
Kalina J, Èajánek M, Špunda V, Marek MV (1997) Changes of the primary photosynthetic reactions of Norway spruce under elevated CO2. In: Mohren GMJ, Kramer K, Sabaté S (eds) Impacts of global change on tree physiology and forest ecosystems. Kluwer Academic Publishers, Dordrecht, pp 59–66
Korstian CF (1937) Perpetuation of spruce on cut-over and burned lands in the higher southern Appalachian Mountains. Ecol Monogr 7:126–167
Le Thiec D, Dixon M (1996) Acclimation of photosynthesis in Norway spruce and red oak grown in open-top chambers and subjected to natural drought and elevated CO2. Can J For Res 26:87–94
Leak WB, Smith ML (1996) Sixty years of management and natural disturbance in a New England forested landscape. For Ecol Manag 81:63–73
Lichtenthaler HK, Rinderle U (1988) The role of chlorophyll fluorescence in the detection of stress conditions in plants. CRC Crit Rev Anal Chem 19:529–585
Lindbladh M, Jacobson GL Jr, Schauffler M (2003) The postglacial history of three Picea species in New England, USA. Quat Res 59:61–69
Liu J, Zhou G, Xu Z, Duan H, Li Y, Zhang D (2011) Photosynthesis acclimation, leaf nitrogen concentration, and growth of four tree species over 3 years in response to elevated carbon dioxide and nitrogen treatment, in subtropical China. J Soil Sedim 11:1155–1164
Logan BA, Combs A, Myers K, Kent R, Stanley L, Tissue DT (2009) Seasonal response of photosynthetic electron transport and energy dissipation in the eighth year of exposure to elevated atmospheric CO2 (FACE) in Pinus taeda (loblolly pine). Tree Physiol 29:789–797
Luomala E-M, Laitinen K, Kellomaki S, Vapaavuori E (2003) Variable photosynthetic acclimation in consecutive cohorts of Scots pine needles during 3 years of growth at elevated CO2 and elevated temperature. Plant Cell Environ 26:645–660
Major JE, Johnsen KH (1996) Family variation in photosynthesis of 22-year-old black spruce: a test of two models of physiological response to water stress. Can J For Res 26:1922–1933
Major JE, Barsi DC, Mosseler A, Campbell M, Rajora OP (2003a) Light-energy processing and freezing-tolerance traits in red spruce and black spruce: species and seed-source variation. Tree Physiol 23:685–694
Major JE, Mosseler A, Barsi DC, Campbell M, Rajora OP (2003b) Morphometric allometric, and developmentally adaptive traits in red spruce and black spruce. I. Species and seed source variation. Can J For Res 33:885–896
Major JE, Mosseler A, Barsi DC, Campbell M, Rajora OP (2003c) Morphometric, allometric, and developmentally adaptive traits in red spruce and black spruce. II. Seedling and mature tree assessment of controlled intra- and inter-specific hybrids. Can J For Res 33:897–909
Major JE, Mosseler A, Johnsen KH, Rajora OP, Barsi DC, Kim K-H, Park J-M, Campbell M (2005) Reproductive barriers and hybridity in two spruces, Picea rubens and Picea mariana, sympatric in eastern North America. Can J Bot 83:163–175
Major JE, Barsi DC, Mosseler A, Campbell M (2007a) Genetic variation and control of chloroplast pigment content in Picea rubens, Picea mariana, and their hybrids. I. Under ambient and elevated CO2 environments. Tree Physiol 27:353–364
Major JE, Barsi DC, Mosseler A, Rajora OP, Campbell M (2007b) Predominant paternal inheritance pattern of light-energy processing adaptive traits in red and black spruce hybrids. Can J For Res 37:293–305
Major JE, Mosseler A, Malcolm J, Barsi DC, Campbell M (2014) Biomass and allocation response of Picea rubens, Picea mariana, and their hybrids under CO2 treatments (in preparation)
Manley SAM (1971) Identification of red, black, and hybrid spruces. NRCan, Cdn For Serv Publ. No. 1301, Ottawa
Manley SAM (1972) The occurrence of hybrid swarms of red and black spruces in central New Brunswick. Can J For Res 2:381–391
Manley SAM (1975) Genecology of hybridization in red spruce (Picea rubens Sarg.) and black spruce [Picea mariana (Mill.) BSP.]. Dissertation, Yale University, New Haven
Manley SAM, Ledig FT (1979) Photosynthesis in black and red spruce and their hybrid derivatives: ecological isolation and hybrid adaptive inferiority. Can J Bot 57:305–314
Marek MV, Šprtov M, Kalina K (1997) The photosynthetic irradiance response of Norway spruce exposed to a long-term elevation of CO2 concentration. Photosynthetica 33:259–268
McLaughlin SB, Downing DJ, Blasing TJ, Cook ER, Adams HS (1987) An analysis of climate and competition as contributors to the decline of red spruce in high elevation Appalachian forests of the eastern United States. Oecologia 72:487–501
Morgenstern EK, Farrar JL (1964) Introgressive hybridization in red and black spruce. Univsity of Toronto, Fac For Tech Rep 4
Mosseler A, Major JE, Simpson JD, Daigle B, Lange K, Park Y-S, Johnsen KH, Rajora OP (2000) Indicators of population viability in red spruce, Picea rubens: I. Reproductive traits and fecundity. Can J Bot 78:928–940
Oren R, Ellsworth DS, Johnsen KH et al (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472
Ormrod DP, Lesser VM, Olszyk DM, Tingey DT (1999) Elevated temperature and carbon dioxide affect chlorophylls and carotenoids in Douglas-fir seedlings. Int J Plant Sci 160:529–534
Palmer JD (1985) Comparative organization of chloroplast genomes. Ann Rev Genet 19:325–354
Parent S, Messier C (1996) A simple and efficient method to estimate microsite light availability under a forest canopy. Can J For Res 26:151–154
Parker WC, Colombo SJ, Cherry ML, Flannigan MD, Greifenhagen S, McAlpine RS, Papadopol C, Scarr T (2000) Third millennium forestry: what climate change might mean to forests and forest management in Ontario. For Chron 76:445–461
Pereira JS (1994) Gas exchange and growth. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer-Verlag, Berlin, pp 147–181
Peters RL (1990) Effects of global warming on forests. For Ecol Manag 35:13–33
Petit RJ, Pineau E, Demesure B, Bacilier R, Ducousso A, Dremer A (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci USA 94:9996–10001
Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198
Proietti P (2003) Changes in photosynthesis and fruit characteristics in olive in response to assimilate availability. Photosynthetica 41:559–564
Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Buschena C (1998) Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Funct Ecol 12:327–338
Roberntz P, Stockfors J (1998) Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance and needle respiration of field-grown Norway spruce trees. Tree Physiol 18:233–241
Rogers A, Ellsworth DS (2002) Photosynthetic acclimation of Pinus taeda (loblolly pine) to long-term growth in elevated pCO2 (FACE). Plant Cell Environ 25:851–858
Samuelson LJ, Seiler JR (1994) Red spruce seedling gas exchange in response to elevated CO2, water stress and soil fertility treatments. Can J For Res 24:954–959
Schauffler M, Jacobson GL Jr (2002) Persistence of coastal spruce refugia during the Holocene in northern New England, USA, detected by stand-scale pollen stratigraphies. J Ecol 90:235–250
Springer CJ, Thomas RB (2007) Photosynthetic responses of forest understory tree species to long-term exposure to elevated carbon dioxide concentration at the Duke FACE experiment. Tree Physiol 27:25–32
Springer CJ, DeLucia EH, Thomas RB (2005) Relationships between net photosynthesis and foliar nitrogen concentrations in a loblolly pine forest ecosystem grown in elevated atmospheric carbon dioxide. Tree Physiol 25:385–394
Sutton BCS, Flanagan DJ, Gawley JR, Newton CH, Lester DT, El-Kassaby YA (1991) Inheritance of chloroplast and mitochondrial DNA in Picea and composition of hybrids from introgression zones. Theor Appl Genet 82:242–248
Teskey RO (1997) Combined effects of elevated CO2 and air temperature on carbon assimilation of Pinus taeda trees. Plant Cell Environ 20:373–380
Tissue DT, Griffin KL, Ball T (1999) Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevated CO2. Tree Physiol 19:221–228
Tissue DT, Griffin KL, Turnbull MH, Whitehead D (2001) Canopy position and needle age affect photosynthetic response in field grown Pinus radiata after five years exposure to elevated carbon dioxide partial pressure. Tree Physiol 21:915–923
Tjoelker MG, Oleksyn J, Reich PB (1998a) Temperature and ontogeny mediate growth response to elevated CO2 in seedlings of five boreal tree species. New Phytol 140:197–210
Tjoelker MG, Oleksyn J, Reich PB (1998b) Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature. Tree Physiol 18:715–726
Urban O, Marek MV (1999) Seasonal changes of selected parameters of CO2 fixation biochemistry of Norway spruce under the long-term impact of elevated CO2. Photosynthetica 36:533–545
Viereck LA, Johnston WF (1990) Picea mariana (Mill.) BSP—black spruce. In: Burns RM, Honkala, BH (tech coords) Vol. 1 Conifers. Silvics of North America. USDA, For Serv, Agriculture Handbook 654, Washington, DC, pp 227–237
von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and gas exchange of leaves. Planta 153:376–387
Wagner DB, Furnier GR, Saghai-Maroof MA, Williams SM, Dancik BP, Allard RW (1987) Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc Natl Acad Sci USA 84:2097–2100
Wang K-Y, Kellomaki S, Laitinen K (1996) Acclimation of photosynthetic parameters in Scots pine after three years exposure to elevated temperature and CO2. Agric For Meteor 82:195–217
Wertin TM, McGuire MA, Teskey RO (2010) The influence of elevated temperature, elevated atmospheric CO2 concentration and water stress on net photosynthesis of loblolly pine (Pinus taeda L.) at northern, central and southern sites in its native range. Glob Change Biol 16:2089–2103
Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of A/C i curves from 109 species. J Exp Bot 44:907–920
Yoo SD, Greer DH, Laing WA, MacManus MT (2003) Changes in photosynthetic efficiency and carotenoid composition in leaves of white clover at different developmental stages. Plant Physiol Biochem 41:887–893
Zhou Y-M, Han S-J (2005) Photosynthetic response and stomatal behaviour of Pinus koraiensis during the fourth year of exposure to elevated CO2 concentration. Photosynthetica 43(3):445–449
Zhou Y-M, Wang C-G, Han S-J, Cheng X-B, Li M-H, Fan A-N, Wang X–X (2011) Species-specific and needle age-related responses of photosynthesis in two Pinus species to long-term exposure to elevated CO2 concentration. Trees 25:163–173
Acknowledgments
We gratefully acknowledge useful comments received from Drs. Kurt Johnsen, Guy Larocque, and Yuhui Weng. In addition, the greenhouse and growth-chamber growing skills of Laurie Yeates and Terry Hay and the technical skills of Stephanie West are thankfully acknowledged.
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Major, J.E., Mossler, A., Barsi, D.C. et al. Carbon assimilation variation and control in Picea rubens, Picea mariana, and their hybrids under ambient and elevated CO2 . Trees 28, 329–344 (2014). https://doi.org/10.1007/s00468-013-0952-3
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DOI: https://doi.org/10.1007/s00468-013-0952-3

