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Plant and Soil

, Volume 330, Issue 1–2, pp 163–172 | Cite as

Interactions between elevated CO2 and N2-fixation determine soybean yield—a test using a non-nodulated mutant

  • Shimpei Oikawa
  • Kay-May Miyagi
  • Kouki Hikosaka
  • Masumi Okada
  • Toshinori Matsunami
  • Makie Kokubun
  • Toshihiko Kinugasa
  • Tadaki Hirose
Regular Article

Abstract

Elevated CO2 increases seed production more in plant species that form a symbiotic association with N2–fixing bacteria than in species without such association. We studied the mechanism of the increase of seed production with elevated CO2 using nodulated soybean (Glycine max cv. Enrei) and its non-nodulated isogenic line (cv. En1282). Increase in seed production with elevated CO2 was observed in nodulated Enrei but was not in non-nodulated En1282. The increase in seed production in Enrei was explained by the increase in the rate of dry mass production during the reproductive period. This increase was associated with the increase in N assimilation in the reproductive period and the seed N concentration that remained the same as that at ambient CO2. Dry mass production and nitrogen assimilation did not increase in the vegetative phase in both lines. These results accorded with the amount of nodules in Enrei that increased at elevated CO2 especially after flowering. We conclude that the increase in N assimilation in the reproductive period would be the key for increasing soybean yield in the future high-CO2 world.

Keywords

Glycine max Elevated carbon dioxide concentration Non-nodulated isogenic line Symbiosis Seed production Nitrogen 

Notes

Acknowledgements

We thank Kazumasa Ishikawa, Chiho Kamiyama and Yosuke Matsumoto of Tohoku University, and Meguru Inoue, Teruo Saito, Yukichi Satoh and other members of NARCT for technical assistance. We are also grateful to Shoichiro Akao for allowing us to use En1282. David Lawlor provided valuable comments on an earlier version of this paper. This work was supported in part by Grant-in-aid from the Japan Ministry of Education, Science and Culture.

References

  1. Ackerly DD, Bazzaz FA (1995) Plant growth and reproduction along CO2 gradients: non-linear responses and implications for community change. Global Change Biol 1:199–207CrossRefGoogle Scholar
  2. Ainsworth EA, Long SP (2005) 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 165:351–372CrossRefPubMedGoogle Scholar
  3. Ainsworth EA, Davey PA, Bernacchi CJ, Dermody OR, Heaton EA, Moore DJ, Morgan PB, Naidu SL, Ra H-SY, Zhu X-G, Curtis PS, Long SP (2002) A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield. Global Change Biol 8:695–709CrossRefGoogle Scholar
  4. Ainsworth EA, Rogers A, Nelson R, Long SP (2004) Testing the ‘source-sink’ hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agricultural Forest Meteorol 122:85–94CrossRefGoogle Scholar
  5. Ainsworth EA, Rogers A, Leakey ADB (2008) Targets for crop biotechnology in a future high-CO2 and high-O3 world. Plant Physiol 147:13–19CrossRefPubMedGoogle Scholar
  6. BassiriRad H, Griffin KL, Reynolds JF, Strain BR (1997) Changes in root NH4+ and NO3- absorption rates of loblolly and ponderosa pine in response to CO2 enrichment. Plant Soil 190:1–9CrossRefGoogle Scholar
  7. Cure JD, Israel DW, Rufty TW (1988) Nitrogen stress effects on growth and seed yield of nonnodulated soybean during acclimation to elevated CO2. Crop Sci 28:671–677CrossRefGoogle Scholar
  8. Francisco PB Jr, Akao S (1993) Autoregulation and nitrate inhibition of nodule formation in soybean cv. Enrei and its nodulation mutants. J Exp Bot 44:547–553Google Scholar
  9. Hardarson G, Atkins C (2003) Optimising biological N2 fixation by legumes in farming systems. Plant Soil 252:41–54CrossRefGoogle Scholar
  10. Hardy RWF, Havelka UD (1976) Photosynthate as a major factor limiting nitrogen fixation by field-grown legumes with emphasis on soybeans. In: Nutman PS (ed) Symbiotic nitrogen fixation. Cambridge University Press, Cambridge, pp 421–439Google Scholar
  11. Hikosaka K, Onoda Y, Kinugasa T, Nagashima H, Anten NPR, Hirose T (2005) Plant responses to elevated CO2 concentration at different scales: leaf, whole plant, canopy, and population. Eco Res 20:243–253CrossRefGoogle Scholar
  12. Hirose T, Kinugasa T, Shitaka Y (2005) Time of flowering, costs of reproduction, and reproductive output in annuals. In: Reekie EG, Bazzaz FA (eds) Reproductive allocation in plants. Elsevier Academic Press, San Diego, pp 159–188CrossRefGoogle Scholar
  13. Hungate BA, Dijkstra P, Johnson DW, Hinkle CR, Krake BG (1999) Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Global Change Biol 5:781–789CrossRefGoogle Scholar
  14. Jablonski LM, Wand X, Curtis PS (2002) Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol 156:9–26CrossRefGoogle Scholar
  15. Kim H-Y, Liffering M, Miura S, Kobayashi K, Okada M (2001) Growth and nitrogen uptake of CO2–enriched rice under field conditions. New Phytol 150:223–229CrossRefGoogle Scholar
  16. Kimball BA, Kobayashi K, Bindi M (2002) Responses of agricultural crops to free-air CO2 enrichment. Adv Agron 77:293–368CrossRefGoogle Scholar
  17. Kinugasa T, Hikosaka K, Hirose T (2003) Reproductive allocation of an annual Xanthium canadense growing in elevated CO2. Oecologia 137:1–9CrossRefPubMedGoogle Scholar
  18. Larigauderie A, Reynolds JF, Strain BR (1994) Root response to CO2 enrichment and nitrogen supply in loblolly pine. Plant Soil 165:21–32CrossRefGoogle Scholar
  19. Lüscher A, Hendrey GR, Nösberger J (1998) Longterm responsiveness to free air CO2 enrichment of functional types, species and genotypes of permanent grassland. Oecologia 113:37–45Google Scholar
  20. Lüscher A, Hartwig UA, Suter D, Nösberger J (2000) Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Global Change Biol 6:655–662CrossRefGoogle Scholar
  21. 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 12:156–167CrossRefGoogle Scholar
  22. Minchin FR, Summerfield RJ, Hadley P, Roberts EH, Rawsthorne S (1981) Carbon and nitrogen nutrition of nodulated roots of grain legumes. Plant Cell Environ 4:5–26CrossRefGoogle Scholar
  23. Miyagi K-M, Kinugasa T, Hirose T, Hikosaka K (2007) Elevated CO2 concentration, nitrogen use, and seed production in annual plants. Global Change Biol 13:2161–2170CrossRefGoogle Scholar
  24. Morgan PB, Bollero GA, Nelson RL, Dohleman FG, Long SP (2005) Smaller than predicted increase in aboveground net primary production and yield of field-grown soybean under fully open-air [CO2] elevation. Global Change Biol 11:1856–1865CrossRefGoogle Scholar
  25. Nakamura T, Koike T, Lei T, Ohashi K, Shinano T, Tadano T (1999) The effect of CO2 enrichment on the growth of nodulated and non-nodulated isogenic types of soybean raised under two nitrogen concentrations. Photosynthetica 37:61–70CrossRefGoogle Scholar
  26. Navas M-L, Sonie L, Richarte J, Roy J (1997) The influence of elevated CO2 on species phenology, growth and reproduction in a Mediterranean old-field community. Global Change Biol 3:523–530CrossRefGoogle Scholar
  27. Norby RJ (1994) Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide. Plant Soil 165:9–20CrossRefGoogle Scholar
  28. Okada M, Hamasaki T, Sameshima R (2000) Pre-air-conditioned temperature gradient chambers for research on temperature stress in plants. Biotronics 29:43–55Google Scholar
  29. R Development Core Team (2006) R: a language and environment for statistical computing. Vienna, Austria: Royal Foundation for Statistical Computing, http://www.R-project.org
  30. Rogers A, Allen DJ, Davey PA, Morgan PB, Ainsworth EA, Bernacchi CJ, Cornic G, Dermody O, Dohleman FG, Heaton EA, Mahoney J, Zhu X-G, Delucia EH, Ort DR, Long SP (2004) Leaf photosynthesis and carbohydrate dynamics of soybeans grown throughout their life-cycle under Free-Air Carbon dioxide Enrichment. Plant Cell Environ 27:449–458CrossRefGoogle Scholar
  31. Rogers A, Gibon Y, Stitt M, Morgan PB, Bernacchi CJ, Ort DR, Long SP (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant, Cell Environ 29:1651–1658CrossRefGoogle Scholar
  32. Shitaka Y, Hirose T (1998) Effects of shift in flowering time on the reproductive output of Xanthium canadense in a seasonal environment. Oecologia 114:361–367Google Scholar
  33. Sinclair TR, de Wit CT (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189:565–567CrossRefPubMedGoogle Scholar
  34. Soussana JF, Hartwig UA (1996) The effects of elevated CO2 on symbiotic N2 fixation: a link between the carbon and nitrogen cycles. Plant Soil 18:101–114CrossRefGoogle Scholar
  35. Streeter J, Wong PP (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23CrossRefGoogle Scholar
  36. Takahashi Y (2005) Stable increasing technique of soybean yield by nitrogen fertilizer application. In: Japanese Society of Soil Science and Plant Nutrition (ed) Improvement of Production and Quality of Soybean in Relation to Plant Nutrition and Physiology. Hakuyusha Co, LTD, Tokyo, pp 12–38 In JapaneseGoogle Scholar
  37. Taub DR, Miller B, Allen H (2008) Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis. Global Change Biol 14:565–575CrossRefGoogle Scholar
  38. West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530CrossRefPubMedGoogle Scholar
  39. Ziska LH, Bunce JA (2007) Predicting the impact of changing CO2 on crop yields: some thoughts on food. New Phytol 175:607–618CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Shimpei Oikawa
    • 1
    • 2
  • Kay-May Miyagi
    • 3
  • Kouki Hikosaka
    • 3
  • Masumi Okada
    • 4
  • Toshinori Matsunami
    • 5
  • Makie Kokubun
    • 6
  • Toshihiko Kinugasa
    • 7
  • Tadaki Hirose
    • 8
  1. 1.Center for Bioresource Field ScienceKyoto Institute of TechnologyKyotoJapan
  2. 2.Department of Plant BiologyUniversity of IllinoisUrbanaUSA
  3. 3.Graduate School of Life SciencesTohoku UniversityMiyagiJapan
  4. 4.Faculty of AgricultureIwate UniversityIwateJapan
  5. 5.Akita Prefectural AgricultureForestry and Fisheries Research CenterAkitaJapan
  6. 6.Graduate School of Agricultural ScienceTohoku UniversityMiyagiJapan
  7. 7.Faculty of AgricultureTottori UniversityTottoriJapan
  8. 8.Department of International Agricultural DevelopmentTokyo University of AgricultureTokyoJapan

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