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Effects of elevated CO2 on leaf area dynamics in nodulating and non-nodulating soybean stands

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Abstract

Aims

The effects of elevated CO2 on leaf area index (LAI) vary among studies. We hypothesized that the interactive effects of CO2 and nitrogen on leaf area loss have important roles in LAI regulation.

Methods

We studied the leaf area production and loss using nodulating soybean and its non-nodulating isogenic line in CO2-controlled greenhouse systems.

Results

Leaf area production increased with elevated CO2 levels in the nodulating soybean stand and to a lesser extent in the non-nodulating line. Elevated CO2 levels accelerated leaf area loss only in nodulating plants. Consequently, both plants exhibited a similar stimulation of peak LAI with CO2 elevation. The accelerated leaf loss in nodulating plants may have been caused by newly produced leaves shading the lower leaves. The nodulating plants acquired N throughout the growth phase, whereas non-nodulating plants did not acquire N after flowering due to the depletion of soil N. N retranslocation to new organs and subsequent leaf loss were faster in non-nodulating plants compared with nodulating plants, irrespective of the CO2 levels.

Conclusion

LAI regulation in soybean involved various factors, such as light availability within the canopy, N acquisition and N demands in new organs. These effects varied among the growth stages and CO2 levels.

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References

  • Ackerly DD, Coleman JS, Morse SR, Bazzaz FA (1992) CO2 and temperature effects on leaf area production in two annual plant species. Ecology 73:1260–1269

    Article  Google Scholar 

  • Ainsworth EA, Long SP (2004) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372

    Article  Google Scholar 

  • Anten NPR (2002) Evolutionarily stable leaf area production in plant populations. J Theor Biol 217:15–32

    Article  PubMed  Google Scholar 

  • Anten NPR (2005) Optimal photosynthetic characteristics of individual plants in vegetation stands and implications for species coexistence. Ann Bot 95:495–506

    Article  PubMed  CAS  Google Scholar 

  • Anten NPR, During H (2011) Is analyzing the nitrogen use at the plant canopy level a matter of choosing the right optimization criterion? Oecologia 167:293–303

    Article  PubMed  Google Scholar 

  • Anten NPR, Schieving F, Medina E, Werger MJA, Schuffelen P (1995) Optimal leaf area indices in C3 and C4 mono- and dicotyledonous species at low and high nitrogen availability. Physiol Plant 95:541–550

    Article  CAS  Google Scholar 

  • Anten NPR, Hirose T, Onoda Y, Kinugasa T, Kim HY, Okada M, Kobayashi K (2004) Elevated CO2 and nitrogen availability have interactive effects on canopy carbon gain in rice. New Phytol 161:459–471

    Article  Google Scholar 

  • Cowling SA, Field CB (2003) Environmental control of leaf area production: Implications for vegetation and land-surface modeling. Global Biogeochem Cycles 17:1–14

    Article  Google Scholar 

  • Craine JM, Reich PB (2001) Elevated CO2 and nitrogen supply alter leaf longevity of grassland species. New Phytol 150:397–403

    Article  CAS  Google Scholar 

  • Curtis PS, Vogel CS, Pregitzer KS, Zak DR, Teeri JA (1995) Interacting effects of soil fertility and atmospheric CO2 on leaf area growth and carbon gain physiology in Populus x euramericana (Dode) Guinier. New Phytol 129:253–263

    Article  Google Scholar 

  • Dermody O, Long SP, DeLucia EH (2006) How does elevated CO2 or ozone affect the leaf-area index of soybean when applied independently? New Phytol 169:145–155

    Article  PubMed  CAS  Google Scholar 

  • Dermody O, Long SP, McConnaughay KY, DeLucia EH (2008) How elevated CO2 and O3 affect the interception and utilization of radiation by a soybean canopy? Global Change Biol 14:556–564

    Article  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Drake BJ, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Ann Rev Plant Physiol Plant Mol Biol 48:609–639

    Article  CAS  Google Scholar 

  • Escudero A, Mediavilla S (2003) Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span. J Ecol 91:880–889

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Falster DS, Westoby M (2003) Plant height and evolutionary games. Trends Ecol Evol 18:337–343

    Article  Google Scholar 

  • Fangmeier A, Chrost B, Högy P, Krupinska K (2000) CO2 enrichment enhances flag leaf senescence in barley due to a greater grain nitrogen sink capacity. Environ Exp Biol 44:151–164

    Article  CAS  Google Scholar 

  • Francisco PB Jr, Akao S (1993) Autoregulation and nitrate inhibition of nodule formation in soybean cv. Enrei and its nodulation mutants. J Exp Bot 44:547–553

    Article  CAS  Google Scholar 

  • Franklin O, Ågren GI (2002) Leaf senescence and resorption as mechanisms of maximizing photosynthetic production during canopy development at N limitation. Funct Ecol 16:727–733

    Article  Google Scholar 

  • Givnish TJ (1982) On the adaptive significance of leaf height in forest herbs. Am Nat 120:353–381

    Article  Google Scholar 

  • Gray SB, Dermody O, DeLucia EH (2010) Spectral reflectance from soybean canopy exposed to elevated CO2 and O3. J Exp Bot 61:4413–4422

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka K (2003) A model of dynamics of leaves and nitrogen in a canopy: an integration of canopy photosynthesis, leaf life-span, and nitrogen use efficiency. Am Nat 162:149–164

    Article  PubMed  Google Scholar 

  • Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Ann Bot 95:521–533

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka K, Anten NPR (2012) An evolutionary game of leaf dynamics and its consequence for canopy structure. Funct Ecol 26:1024–1032

    Article  Google Scholar 

  • Hikosaka K, Terashima I, Katoh S (1994) Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97:451–457

    Article  Google Scholar 

  • Hikosaka K, Kawauchi Y, Kurosawa T (2010) Why does Viola hondensis (Violaceae) shed its winter leaves in spring? Ame J Bot 97:1944–1950

    Article  Google Scholar 

  • Hikosaka K, Kinugasa T, Oikawa S, Onoda Y, Hirose T (2011) Effects of elevated CO2 concentration on seed production in C3 annual plants. J Exp Bot 62:1523–1530

    Article  PubMed  CAS  Google Scholar 

  • Hirose T (1971) Nitrogen turnover and dry-matter production of a Solidago altissima population. Jpn J Ecol 21:18–32

    Google Scholar 

  • Hirose T, Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72:520–526

    Article  Google Scholar 

  • Hirose T, Ackerly DD, Traw MB, Bazzaz FA (1996) Effects of CO2 elevation on canopy development in the stands of two co-occurring annuals. Oecologia 108:215–223

    Google Scholar 

  • Hirose T, Ackerly DD, Traw MB, Ramseier D, Bazzaz FA (1997) CO2 elevation, canopy photosynthesis, and optimal leaf area index. Ecology 78:2339–2350

    Google Scholar 

  • Jones P, Allen LH Jr, Jones JW, Boote KJ, Campbell WJ (1984) Soybean canopy growth, photosynthesis, and transpiration responses to whole-season carbon dioxide enrichment. Agr J 76:633–637

    Article  CAS  Google Scholar 

  • Killingbeck (1993) Inefficient nitrogen resorption in genets of the actinorhizal nitrogen-fixing shrub Comptonia peregrine: physiological ineptitude or evolutionary trade-off? Oecologia 94:542–549

  • Killingbeck (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

  • Kim H-Y, Lieffering M, Kobayashi K, Okada M, Miura S (2003) Seasonal changes in the effects of elevated CO2 on rice at three levels of nitrogen supply: a free air CO2 enrichment (FACE) experiment. Global Change Biol 9:826–837

    Article  Google Scholar 

  • Kimball BA, Kobayashi K, Bindi (2002) Responses of agricultural crops to free-air CO2 enrichment. Adv Agr 77:293–368

    Article  Google Scholar 

  • Kinugasa T, Sato T, Oikawa S, Hirose T (2011) Demand and supply of N in seed production of soybean (Glycine max) at different N fertilization levels after flowering. J Plant Res 125:275–281

    Article  PubMed  Google Scholar 

  • Koike T (1995) Effects of CO2 in interaction with temperature and soil fertility on the foliar phenology of alder, birch, and maple seedlings. Can J Bot 73:149–157

    Article  Google Scholar 

  • Körner C, Asshoff R, Bignucolo O, Hättenchwiler KSG, Paláez-Riedl S, Pepin S, Siegwolf RTW, Zotz G (2005) Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–1362

    Article  PubMed  Google Scholar 

  • Leadley PW, Reynolds JF (1989) Effect of carbon dioxide enrichment on development of the first six main stem leaves in soybean. Am J Bot 76:1551–1555

    Article  Google Scholar 

  • Mae T, Ohira K (1981) The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22:1067–1074

    CAS  Google Scholar 

  • Matsunami T, Otera M, Amemiya S, Kokubun M, Okada M (2009) Effect of CO2 concentration, temperature and N fertilization on biomass production of soybean genotypes differing in N fixation capacity. Plant Prod Sci 12:156–167

    Article  CAS  Google Scholar 

  • McCarthy HR, Oren R, Finzi AC, Johnsen KH (2006) Canopy leaf area constrains [CO2]-induced enhancement of productivity and partitioning among aboveground carbon pools. Proc Natl Acad Sci USA 104:19356–19361

    Article  Google Scholar 

  • Miglietta F, Raschi A, Resti R, Badiani M (1993) Growth and onto-morphogenesis of soybean (Glycine max Merril) in an open, naturally CO2-enriched environment. Plant Cell Environ 16:909–918

    Article  CAS  Google Scholar 

  • Miyagi K-M, Kinugasa T, Hirose T, Hikosaka K (2007) Elevated CO2 concentration, nitrogen use, and seed production in annual plants. Global Change Biol 13:2161–2170

    Article  Google Scholar 

  • Newberry RM, Wolfenden J (1996) Effects of elevated CO2 and nutrient supply on the seasonal growth and morphology of Agrostis capillaries. New Phytol 132:403–411

    Article  Google Scholar 

  • Norby RJ, Sholtis JD, Gunderson CA, Jawdy SS (2003) Leaf dynamics of a deciduous forest canopy: no response to elevated CO2. Oecologia 136:574–584

    Article  PubMed  Google Scholar 

  • Oikawa S, Hikosaka K, Hirose T (2005) Dynamics of leaf area and nitrogen in a canopy of an annual herb, Xanthium canadense. Oecologia 143:517–526

    Article  PubMed  Google Scholar 

  • Oikawa S, Hikosaka K, Hirose T (2006) Leaf lifespan and lifetime carbon balance of individual leaves in a stand of an annual herb, Xanthium canadense. New Phytol 172:104–116

    Article  PubMed  CAS  Google Scholar 

  • Oikawa S, Hikosaka K, Hirose T (2008) Does leaf shedding increase the whole-plant carbon gain despite some nitrogen being lost with shedding? New Phytol 178:617–624

    Article  PubMed  CAS  Google Scholar 

  • Oikawa S, Miyagi K-M, Hikosaka K, Okada M, Matsunami T, Kokubun M, Kinugasa T, Hirose T (2010) Interaction between elevated CO2 and N2-fixation determine soybean yield-a test using non-nodulated mutant. Plant Soil 330:163–172

    Article  CAS  Google Scholar 

  • Okada M, Hamasaki T, Sameshima R (2000) Pre-air-conditioned temperature gradient chambers for research on temperature stress in plants. Biotronics 29:43–55

    Google Scholar 

  • Ono K, Terashima I, Watanabe A (1996) Interaction between nitrogen deficit of a plant and nitrogen content in the old leaves. Plant Cell Physiol 37:1083–1089

    Article  CAS  Google Scholar 

  • Parker GAJ, Maynard-Smith J (1990) Optimality theory in evolutionary biology. Nature 348:27–33

    Article  Google Scholar 

  • Pornon A, Marty C, Winterton P, Lamaze T (2011) The intriguing paradox of leaf lifespan responses to nitrogen availability. Func Ecol 25:796–801

    Article  Google Scholar 

  • Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Global Change Biol 5:807–837

    Article  Google Scholar 

  • Reich PB, Falster DS, Ellsworth DS, Wright IJ, Westoby M, Oleksyn J, Lee TD (2009) Controls on declining carbon balance with leaf age among 10 woody species in Australian woodland: do leaves have zero daily net carbon balances when they die? New Phytol 183:153–166

    Article  PubMed  CAS  Google Scholar 

  • Rogers A, Fischer BU, Bryant J, Frehner M, Blum H, Raines CA, Long SP (1998) Acclimation of photosynthesis to elevated CO2 under low-nitrogen nutrition is affected by the capacity for assimilate utilization. Perennial ryegrass under free-air CO2 enrichment. Plant Physiol 118:683–689

    Article  PubMed  CAS  Google Scholar 

  • Sigurdsson BD (2001) Elevated [CO The intriguing paradox of leaf lifespan responses to nitrogen availability] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study. Trees 15:403–413

    Article  Google Scholar 

  • Sinclair TR, de Wit CT (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189:565–567

    Article  PubMed  CAS  Google Scholar 

  • Sinclair TR, de Wit CT (1976) Analysis of carbon and nitrogen limitation to soybean yield. Agr J 68:319–324

    Article  CAS  Google Scholar 

  • Smart CM (1994) Gene expression during leaf senescence. New Physol 126:419–448

    Article  CAS  Google Scholar 

  • Thomas H, Stoddart JL (1980) Leaf senescence. Ann Rev Plant Physiol 31:83–111

    Article  CAS  Google Scholar 

  • Yasumura Y, Hikosaka K, Hirose T (2007) Nitrogen resorption and protein degradation during leaf senescence in Chenopodium album grown in different light and nitrogen conditions. Funct Plant Biol 34:409–417

    Google Scholar 

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Acknowledgments

We thank Meguru Inoue, Teruo Saito, Yukichi Satoh, and other members of NARCT, Chiho Kamiyama and Kay-May Miyagi of Tohoku University for technical assistance. Shoichiro Akao allowed us to use En1282. Makie Kokubun provided the seeds. We are also grateful to Elizabeth Ainsworth, Toshihiko Kinugasa and Toshinori Matsunami for comments. This work was supported by KAKENHI, a Grant-in-Aid for Young Scientists by Japan Society for the Promotion of Sciences (No. 23770027) and a Grant-in Aid for Scientific Research on Innovative Areas from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 21114001).

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Authors and Affiliations

  1. College of Science, Ibaraki University, Mito, 310-0056, Japan

    Shimpei Oikawa

  2. Faculty of Agriculture, Iwate University, Morioka, 020-8550, Japan

    Masumi Okada

  3. Graduate School of Life Sciences, Tohoku University, Sendai, 980-8578, Japan

    Kouki Hikosaka

  4. CREST, JST, Chiyoda, Tokyo, 102-0076, Japan

    Kouki Hikosaka

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  1. Shimpei Oikawa
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  2. Masumi Okada
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  3. Kouki Hikosaka
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Correspondence to Shimpei Oikawa.

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Repsonsible Editor: Euan K. James.

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Oikawa, S., Okada, M. & Hikosaka, K. Effects of elevated CO2 on leaf area dynamics in nodulating and non-nodulating soybean stands. Plant Soil 373, 627–639 (2013). https://doi.org/10.1007/s11104-013-1826-6

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