Needle age and season influence photosynthetic temperature response and total annual carbon uptake in mature Picea mariana trees

Jensen, Anna M.; Warren, Jeffrey; Hanson, Paul J.; Childs, Joanne; Wullschleger, Stan D.

doi:10.1093/aob/mcv115

Title: Needle age and season influence photosynthetic temperature response and total annual carbon uptake in mature Picea mariana trees

Journal Article · Wed Dec 31 23:00:00 EST 2014 · Annals of Botany

DOI: https://doi.org/10.1093/aob/mcv115 · OSTI ID:1223065

Jensen, Anna M. ^[1]; Warren, Jeffrey ^[1]; Hanson, Paul J. ^[1]; Childs, Joanne ^[1]; Wullschleger, Stan D. ^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Using seasonal- and cohort-specific photosynthetic temperature response functions, we quantified the physiological significance of maintaining multiple foliar cohorts in mature (~40-45 year old) Picea mariana trees in an ombrotrophic Sphagnum-bog, northern Minnesota, USA. We measured photosynthetic capacity, foliar respiration (Rd), biochemistry and morphology to estimate annual carbon (C) uptake by cohort, season and canopy position. Temperature response of key photosynthetic parameters at 25 C (i.e., light-saturated rate of CO₂ assimilation (Asat), light-saturated rate of Rubisco carboxylation (Vcmax), light-saturated electron transport rate (Jmax)) were clearly dependent on season and were generally less responsive in younger needles. Temperature optimums range between 18.7-23.7, 31.3-38.3 and 28.7-36.7 C for Asat, Vcmax and Jmax respectively. Current-year (Y0) foliage had lower photosynthetic capacities compared to one-year-old (Y1) and two-year-old (Y2) foliage. As Y0 needles matured, values of Asat, Vcmax, Jmax, foliar LMA and nitrogen increased. Values of Vcmax, Jmax and Rd were related to foliar nitrogen but only in the youngest (Y0) cohort. Foliar ontogeny affected photosynthetic capacity more than growth temperature. Morphological and physiological cohort differences were reflected by their annual contribution to modeled C uptake, with a ~36% lower estimated annual C uptake by Y0 needles (LAI 0.52 m²m^-2) compared to Y1&2 cohorts (LAI 0.67 m²m^-2). Collectively, these results illustrate the physiological and ecological significance of characterizing multiple foliar cohorts during bud break and throughout the growth season, and for cumulative C uptake model estimates.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1223065

Journal Information:: Annals of Botany, Journal Name: Annals of Botany Journal Issue: 5 Vol. 116; ISSN 0305-7364

Country of Publication:: United States

Language:: English

References (52)

SPRUCE S1 Bog Pretreatment Photosynthesis and Respiration for Black Spruce: 2010-2013 Jensen, A.; Warren, J.; Hanson, P. ORNLTESSFA (Oak Ridge National Lab's Terrestrial Ecosystem Science Scientific Focus Area (ORNL TES SFA)) https://doi.org/10.3334/cdiac/spruce.007	dataset	January 2015
Is long-lived foliage in Picea mariana an adaptation to nutrient-poor conditions? Greenway, Ken J.; Macdonald, S. Ellen; Lieffers, Victor J. Oecologia, Vol. 91, Issue 2 https://doi.org/10.1007/BF00317782	journal	August 1992
Climatic influences on net ecosystem CO2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest Monson, Russell K.; Sparks, Jed P.; Rosenstiel, Todd N. Oecologia, Vol. 146, Issue 1 https://doi.org/10.1007/s00442-005-0169-2	journal	August 2005
Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration Way, Danielle A.; Yamori, Wataru Photosynthesis Research, Vol. 119, Issue 1-2 https://doi.org/10.1007/s11120-013-9873-7	journal	June 2013
Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation Yamori, Wataru; Hikosaka, Kouki; Way, Danielle A. Photosynthesis Research, Vol. 119, Issue 1-2 https://doi.org/10.1007/s11120-013-9874-6	journal	June 2013
Response of tree growth to a changing climate in boreal central Canada: A comparison of empirical, process-based, and hybrid modelling approaches Girardin, Martin P.; Raulier, Frédéric; Bernier, Pierre Y. Ecological Modelling, Vol. 213, Issue 2 https://doi.org/10.1016/j.ecolmodel.2007.12.010	journal	May 2008
Physiological responses of a black spruce forest to weather Goulden, Michael L.; Daube, Bruce C.; Fan, Song-Miao Journal of Geophysical Research: Atmospheres, Vol. 102, Issue D24 https://doi.org/10.1029/97JD01111	journal	December 1997
Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate Reich, P. B.; Walters, M. B.; Tjoelker, M. G. Functional Ecology, Vol. 12, Issue 3 https://doi.org/10.1046/j.1365-2435.1998.00209.x	journal	June 1998
Effects of soil warming during spring on photosynthetic recovery in boreal Norway spruce stands Bergh, Johan; Linder, SunE. Global Change Biology, Vol. 5, Issue 3 https://doi.org/10.1046/j.1365-2486.1999.00205.x	journal	March 1999
Air temperature triggers the recovery of evergreen boreal forest photosynthesis in spring Tanja, Suni; Berninger, Frank; Vesala, Timo Global Change Biology, Vol. 9, Issue 10 https://doi.org/10.1046/j.1365-2486.2003.00597.x	journal	October 2003
Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.) Medlyn, B. E.; Loustau, D.; Delzon, S. Plant, Cell and Environment, Vol. 25, Issue 9 https://doi.org/10.1046/j.1365-3040.2002.00890.x	journal	September 2002
Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data Medlyn, B. E.; Dreyer, E.; Ellsworth, D. Plant, Cell and Environment, Vol. 25, Issue 9 https://doi.org/10.1046/j.1365-3040.2002.00891.x	journal	September 2002
Temperature dependence of two parameters in a photosynthesis model Leuning, R. Plant, Cell and Environment, Vol. 25, Issue 9 https://doi.org/10.1046/j.1365-3040.2002.00898.x	journal	September 2002
Temperature and ontogeny mediate growth response to elevated CO2 in seedlings of five boreal tree species Tjoelker, M. G.; Oleksyn, J.; Reich, P. B. New Phytologist, Vol. 140, Issue 2 https://doi.org/10.1046/j.1469-8137.1998.00272.x	journal	October 1998
The hot and the cold: unravelling the variable response of plant respiration to temperature Atkin, Owen K.; Bruhn, Dan; Hurry, Vaughan M. Functional Plant Biology, Vol. 32, Issue 2 https://doi.org/10.1071/FP03176	journal	January 2005
Field Photosynthesis Measurements on Black Spruce ( Picea mariana ): Does Needle Age Matter? Hébert, François; Thiffault, Nelson; Munson, Alison D. Communications in Soil Science and Plant Analysis, Vol. 42, Issue 22 https://doi.org/10.1080/00103624.2011.622821	journal	December 2011
Biochemical Limitations to Carbon Assimilation in C ₃ Plants—A Retrospective Analysis of the A/C _i Curves from 109 Species Wullschleger, Stan D. Journal of Experimental Botany, Vol. 44, Issue 5 https://doi.org/10.1093/jxb/44.5.907	journal	January 1993
Acclimation of photosynthesis to low temperature in Spinacia oleracea L. II. Effects of nitrogen supply Martindale, Wayne; Leegood, Richard C. Journal of Experimental Botany, Vol. 48, Issue 10 https://doi.org/10.1093/jxb/48.10.1873	journal	January 1997
Leaf Rubisco turnover in a perennial ryegrass (Lolium perenne L.) mapping population: genetic variation, identification of associated QTL, and correlation with plant morphology and yield Khaembah, Edith N.; Irving, Louis J.; Thom, Errol R. Journal of Experimental Botany, Vol. 64, Issue 5 https://doi.org/10.1093/jxb/ers384	journal	March 2013
Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species Dreyer, E.; Le Roux, X.; Montpied, P. Tree Physiology, Vol. 21, Issue 4 https://doi.org/10.1093/treephys/21.4.223	journal	March 2001
Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris Niinemets, U. Tree Physiology, Vol. 22, Issue 8 https://doi.org/10.1093/treephys/22.8.515	journal	June 2002
Acclimation of photosynthetic capacity in Scots pine to the annual cycle of temperature Makela, A.; Hari, P.; Berninger, F. Tree Physiology, Vol. 24, Issue 4 https://doi.org/10.1093/treephys/24.4.369	journal	April 2004
Seasonal and interannual variability of photosynthetic capacity in relation to leaf nitrogen in a deciduous forest plantation in northern Italy Grassi, G.; Vicinelli, E.; Ponti, F. Tree Physiology, Vol. 25, Issue 3 https://doi.org/10.1093/treephys/25.3.349	journal	March 2005
Wintertime photosynthesis and water uptake in a boreal forest Sevanto, S.; Suni, T.; Pumpanen, J. Tree Physiology, Vol. 26, Issue 6 https://doi.org/10.1093/treephys/26.6.749	journal	June 2006
Dark respiration rate increases with plant size in saplings of three temperate tree species despite decreasing tissue nitrogen and nonstructural carbohydrates Machado, J. -L.; Reich, P. B. Tree Physiology, Vol. 26, Issue 7 https://doi.org/10.1093/treephys/26.7.915	journal	July 2006
Seasonal changes in the temperature response of photosynthesis in canopy leaves of Quercus crispula in a cool-temperate forest Hikosaka, K.; Nabeshima, E.; Hiura, T. Tree Physiology, Vol. 27, Issue 7 https://doi.org/10.1093/treephys/27.7.1035	journal	July 2007
Springtime resumption of photosynthesis in balsam fir (Abies balsamea) Goodine, G. K.; Lavigne, M. B.; Krasowski, M. J. Tree Physiology, Vol. 28, Issue 7 https://doi.org/10.1093/treephys/28.7.1069	journal	July 2008
Carbon dioxide exchange of buds and developing shoots of boreal Norway spruce exposed to elevated or ambient CO2 concentration and temperature in whole-tree chambers Hall, M.; Rantfors, M.; Slaney, M. Tree Physiology, Vol. 29, Issue 4 https://doi.org/10.1093/treephys/tpn047	journal	February 2009
Ecosystem warming does not affect photosynthesis or aboveground autotrophic respiration for boreal black spruce Bronson, D. R.; Gower, S. T. Tree Physiology, Vol. 30, Issue 4 https://doi.org/10.1093/treephys/tpq001	journal	February 2010
Why does leaf nitrogen decline within tree canopies less rapidly than light? An explanation from optimization subject to a lower bound on leaf mass per area Dewar, R. C.; Tarvainen, L.; Parker, K. Tree Physiology, Vol. 32, Issue 5 https://doi.org/10.1093/treephys/tps044	journal	May 2012
Development and growth of primordial shoots in Norway spruce buds before visible bud burst in relation to time and temperature in the field Sutinen, S.; Partanen, J.; Vihera-Aarnio, A. Tree Physiology, Vol. 32, Issue 8 https://doi.org/10.1093/treephys/tps063	journal	August 2012
Biochemical photosynthetic responses to temperature: how do interspecific differences compare with seasonal shifts? Lin, Y. -S.; Medlyn, B. E.; De Kauwe, M. G. Tree Physiology, Vol. 33, Issue 8 https://doi.org/10.1093/treephys/tpt047	journal	July 2013
Importance of changing CO2, temperature, precipitation, and ozone on carbon and water cycles of an upland-oak forest: incorporating experimental results into model simulations Hanson, Paul J.; Wullschleger, Stan D.; Norby, Richard J. Global Change Biology, Vol. 11, Issue 9 https://doi.org/10.1111/j.1365-2486.2005.00991.x	journal	September 2005
Elevated growth temperatures reduce the carbon gain of black spruce [Picea mariana (Mill.) B.S.P.] Way, Danielle A.; Sage, Rowan F. Global Change Biology, Vol. 14, Issue 3 https://doi.org/10.1111/j.1365-2486.2007.01513.x	journal	March 2008
Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate: PHOTOSYNTHETIC ACCLIMATION TO WARMER CLIMATES Gunderson, Carla A.; O'Hara, Keiran H.; Campion, Christina M. Global Change Biology, Vol. 16, Issue 8 https://doi.org/10.1111/j.1365-2486.2009.02090.x	journal	September 2009
Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO ₂ Smith, Nicholas G.; Dukes, Jeffrey S. Global Change Biology, Vol. 19, Issue 1 https://doi.org/10.1111/j.1365-2486.2012.02797.x	journal	September 2012
Modelling photosynthesis of cotton grown in elevated CO2 Harley, P. C.; Thomas, R. B.; Reynolds, J. F. Plant, Cell and Environment, Vol. 15, Issue 3 https://doi.org/10.1111/j.1365-3040.1992.tb00974.x	journal	April 1992
Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees Niinemets, U.; Kull, O.; Tenhunen, J. D. Plant, Cell and Environment, Vol. 27, Issue 3 https://doi.org/10.1111/j.1365-3040.2003.01143.x	journal	February 2004
Temperature responses are a window to the physiology of dark respiration: differences between CO ₂ release and O ₂ reduction shed light on energy conservation Kruse, JÖRg; Hopmans, Peter; Adams, Mark A. Plant, Cell & Environment, Vol. 31, Issue 7 https://doi.org/10.1111/j.1365-3040.2008.01808.x	journal	July 2008
Thermal acclimation of photosynthesis in black spruce [ Picea mariana (Mill.) B.S.P.] Way, Danielle A.; Sage, Rowan F. Plant, Cell & Environment, Vol. 31, Issue 9 https://doi.org/10.1111/j.1365-3040.2008.01842.x	journal	September 2008
Thermal acclimation of photosynthesis: a comparison of boreal and temperate tree species along a latitudinal transect: Photosynthetic thermal acclimation in boreal and temperate trees Dillaway, Dylan N.; Kruger, Eric L. Plant, Cell & Environment, Vol. 33, Issue 6 https://doi.org/10.1111/j.1365-3040.2010.02114.x	journal	January 2010
Reliable estimation of biochemical parameters from C3 leaf photosynthesis-intercellular carbon dioxide response curves: Estimating FvCB model parameters Gu, Lianhong; Pallardy, Stephen G.; Tu, Kevin Plant, Cell & Environment, Vol. 33, Issue 11 https://doi.org/10.1111/j.1365-3040.2010.02192.x	journal	June 2010
Ontogeny and leaf gas exchange mediate the carbon isotopic signature of herbaceous plants: Ontogeny, carbon isotopes and carbon discrimination Salmon, Yann; Barnard, Romain L.; Buchmann, Nina Plant, Cell & Environment, Vol. 34, Issue 3 https://doi.org/10.1111/j.1365-3040.2010.02256.x	journal	January 2011
C ₃ plants enhance rates of photosynthesis by reassimilating photorespired and respired CO ₂ : Intracellular CO Busch, Florian A.; Sage, Tammy L.; Cousins, Asaph B. Plant, Cell & Environment, Vol. 36, Issue 1 https://doi.org/10.1111/j.1365-3040.2012.02567.x	journal	July 2012
Gas exchange in a 20-year-old stand of Scots pine. I. Net photosynthesis of current and one-year-old shoots within and between seasons Troeng, E.; Linder, S. Physiologia Plantarum, Vol. 54, Issue 1 https://doi.org/10.1111/j.1399-3054.1982.tb00569.x	journal	January 1982
Bud break and spring frost hardiness in Picea abies seedlings in response to photoperiod and temperature treatments Fløistad, Inger Sundheim; Granhus, Aksel Canadian Journal of Forest Research, Vol. 40, Issue 5 https://doi.org/10.1139/X10-050	journal	May 2010
Climate and annual ring growth of black spruce in some Alberta peatlands Dang, Q. L.; Lieffers, V. J. Canadian Journal of Botany, Vol. 67, Issue 6 https://doi.org/10.1139/b89-239	journal	June 1989
Combined effects of rising [CO ₂ ] and temperature on boreal forests: growth, physiology and limitations Stinziano, Joseph R.; Way, Danielle A. Botany, Vol. 92, Issue 6 https://doi.org/10.1139/cjb-2013-0314	journal	June 2014
Change in photosynthesis and water relations with age and season in Abies amabilis Teskey, R. O.; Grier, C. C.; Hinckley, T. M. Canadian Journal of Forest Research, Vol. 14, Issue 1 https://doi.org/10.1139/x84-015	journal	February 1984
P HOTOSYNTHESIS OF O VERWINTERING E VERGREEN P LANTS Öquist, Gunnar; Huner, Norman P. A. Annual Review of Plant Biology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.arplant.54.072402.115741	journal	June 2003
Photosynthetic Response and Adaptation to Temperature in Higher Plants Berry, J.; Bjorkman, O. Annual Review of Plant Physiology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.pp.31.060180.002423	journal	June 1980
Oak Forest Carbon and Water Simulations: Model Intercomparisons and Evaluations Against Independent data Hanson, P. J.; Amthor, J. S.; Wullschleger, S. D. Ecological Monographs, Vol. 74, Issue 3 https://doi.org/10.1890/03-4049	journal	August 2004

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