Photosynthetica 2015, 53(4):562-571 | DOI: 10.1007/s11099-015-0144-z

Assessing the relationship between photosynthetic C accumulation and symbiotic N nutrition in leaves of field-grown nodulated cowpea (Vigna unguiculata L. Walp.) genotypes

A. K. Belane1, F. D. Dakora2,*
1 Department of Crop Sciences, Tshwane University of Technology, Pretoria, South Africa
2 Chemistry Department, Tshwane University of Technology, Pretoria, South Africa

This study evaluated the relationship between photosynthetic carbon accumulation and symbiotic nitrogen nutrition in young fully expanded leaves of 30 nodulated cowpea genotypes grown in the field at Manga, Ghana, in 2005 and 2006. Estimates of fixed-N in photosynthetic leaves revealed greater symbiotic N in genotypes with higher photosynthetic rates and increased leaf transpiration rate/efficiency. There was also greater C accumulation in genotypes with higher symbiotic N and/or total N. Additionally, genotypes with high contents of C per unit of leaf total N exhibited greater C per unit of leaf N-fixed. The C/N and C/Rubisco-N ratios were generally similar in their magnitude when compared to the C/N-fixed ratio due possibly to the fact that Rubisco accounts for a high proportion of photosynthetic leaf N, irrespective of whether the enzyme was formed from soil N or symbiotic N. Cowpea genotypes that relied heavily on soil N for their N nutrition exhibited much higher C/N-fixed ratios, while conversely those that depended more on symbiosis for meeting their N demands showed markedly lower C/N-fixed values. For example, genotypes Omondaw, Bensogla, IT93K-2045-29, and Sanzie, which respectively derived 83.9, 83.1, 82.9, and 76.3% N from fixation, recorded lower C/N-fixed ratios of 10.7, 12.2, 12.1, and 13.0 mg mg-1 in that order in 2005. In contrast, genotypes Botswana White, IT94D-437-1, TVu1509, and Apagbaala, which obtained 14.8, 15.0, 26.4, and 26.0% of their N nutrition from fixation, showed high C/N-fixed values of 84.0, 69.0, 35.2, and 40.6 mg.mg-1, respectively, in 2005. This clearly indicates that genotypes that obtained less N from symbiosis and more N from soil revealed very high C/N-fixed values, an argument that was reinforced by the negative correlations obtained between the three C/N ratios (i.e. C/N, C/Rubisco-N, and C/N-fixed) and leaf N concentration, percentage nitrogen derived from fixation, total N content, amount of N-fixed, and Rubisco N. These data suggest a direct link between photosynthetic C accumulation and symbiotic N assimilation in leaves of nodulated cowpea, and where genotypes derived a large proportion of their N from fixation, photosynthetic C yield substantially increased.

Keywords: N2 fixation; photosynthesis; photosynthetic fixed-N use efficiency; transpiration efficiency; δ15N

Received: July 11, 2014; Accepted: March 25, 2015; Published: December 1, 2015Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Belane, A.K., & Dakora, F.D. (2015). Assessing the relationship between photosynthetic C accumulation and symbiotic N nutrition in leaves of field-grown nodulated cowpea (Vigna unguiculata L. Walp.) genotypes. Photosynthetica53(4), 562-571. doi: 10.1007/s11099-015-0144-z.
Download citation

References

  1. Ainsworth E.A., Rogers A., Blum H. et al.: Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to free-air CO2 enrichment (FACE). - J. Exp. Bot. 54: 2769-2774, 2003. Go to original source...
  2. Ainsworth E.A., Rogers A., Nelson R., Long S.P.: Testing the "source-sink" hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. - Agr. Forest. Meteorol. 122: 85-94, 2004. Go to original source...
  3. Anyia A.O., Herzog H.: Water-use efficiency, leaf area and leaf gas exchange of cowpeas under mid-season drought. - Eur. J. Agron. 20: 327-339, 2004. Go to original source...
  4. Ayisi K.K., Nkgapele R.J., Dakora F.D.: Nodule formation and function in six varieties of cowpea (Vigna unguiculata L. Walp) grown in a nitrogen-rich field soil in South Africa. - Symbiosis 28: 17-31, 2000.
  5. Belane A.K., Dakora F.D.: Measurement of N2 fixation in 30 cowpea (Vigna unguiculata L. Walp.) genotypes under field conditions in Ghana, using the 15N natural abundance technique. - Symbiosis 48: 47-56, 2009. Go to original source...
  6. Cheng L., Fuchigami L.H.: Rubisco activation state decreases with increasing nitrogen content in apple leaves. - J. Exp. Bot. 51: 1687-1694, 2000. Go to original source...
  7. Dakora F.D., Atkins C.A., Pate J.S.: Effect of nitrate on nitrogen fixation and nitrogenous solutes of xylem in two nodulated West African geocarpic legumes, Kersting's bean (Macrotyloma geocarpum L.) and Bambara groundnut (Vigna subterranea L.). - Plant Soil 140: 255-262, 1992. Go to original source...
  8. Dakora F.D.: Nodule function in symbiotic Bambara groundnut (Vigna subterranea L.) and Kersting's bean (Macrotyloma geocarpum L.) is tolerant of nitrate in the root medium. - Ann. Bot.-London 82: 687-690, 1998. Go to original source...
  9. Dordas C.A., Sioulas C.: Safflower yield, chlorophyll content, photosynthesis, and water use efficiency response to nitrogen fertilization under rainfed conditions. - Indust. Crops Prod. 27: 75-85, 2008. Go to original source...
  10. Drake B.G., Gonzàlez-Meler M.A., Long S.P.: More efficient plants: a consequence of rising atmospheric CO2? - Annu. Rev. Plant Phys. 48: 609-639, 1997. Go to original source...
  11. Driessen P., Deckers J., Spaargaren O.: FAO: World Soil Resources Reports 60. FAO-UNESCO Soil Map of the World-Revised Legend. Pp. 146. ISRIC, Wageningen 1990.
  12. Elowad H.O.A., Hall A.E.: Influences of early and late nitrogen fertilization on yield and nitrogen fixation of cowpea under well-watered and dry field conditions. - Field Crop. Res. 15: 229-244, 1987. Go to original source...
  13. Evans J.R.: Photosynthesis and nitrogen relationships in leaves of C3 plants. - Oecologia 78: 9-19, 1989. Go to original source...
  14. Field C., Mooney H.A.: The photosynthesis-nitrogen relationship in wild plants. - In: Givinish T.J. (ed.): On the Economy of Form and Function. Pp. 25-55. Cambridge University Press, Cambridge 1986.
  15. Hamid A., Agata W., Kawamitsu Y.: Photosynthesis, transpiration and water-use efficiency in four cultivars of mungbean, Vigna radiata (L.) Wilczek. - Photosynthetica 24: 96-101, 1990.
  16. Heineke D., Kauder F., Frommer W. et al.: Application of transgenic plants in understanding responses to atmospheric change. - Plant Cell Environ. 22: 623-628, 1999. Go to original source...
  17. Hikosaka K., Terashima I.: A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. - Plant Cell Environ. 18: 605-618, 1995. Go to original source...
  18. Isopp H., Frehner M., Almeida J.P.F. et al.: Nitrogen plays a major role in leaves when source-sink relations change: C and N metabolism in Lolium perenne growing under free air CO2 enrichment. - Aust. J. Plant Physiol. 27: 851-858, 2000. Go to original source...
  19. Junk G., Svec H.: The absolute abundance of the nitrogen isotopes in the atmosphere and compressed gas from various sources. - Geochim. Cosmochim. Ac. 14: 134-243, 1958. Go to original source...
  20. Kaschuk G., Kuyper T.W., Leffelaar P.A. et al.: Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mychorrizal symbioses? - Soil Biol. Biochem. 41: 1233-1244, 2009. Go to original source...
  21. Khan W., Prithiviraj B., Smith D.L.: Nod factor [Nod Bj V (C18:1, MeFuc)] and lumichrome enhance photosynthesis and growth of corn and soybean. - J. Plant Physiol. 165: 1342-1351, 2008. Go to original source...
  22. Lawson T.: Guard cell photosynthesis and stomatal function. - New Phytol. 181: 13-34, 2009. Go to original source...
  23. Mächler F., Oberson A., Grub A. et al.: Regulation of photosynthesis in nitrogen deficient wheat seedlings. - Plant Physiol. 87: 46-49, 1988. Go to original source...
  24. Makoi J.H.J.R., Chimphango S.B.M., Dakora F.D.: Effect of legume density and mixed culture on symbiotic N2 fixation in five cowpea (Vigna unguiculata L. Walp.) genotypes in South Africa. - Symbiosis 48: 57-67, 2009. Go to original source...
  25. Makoi J.H.J.R., Chimphango S.B.M., Dakora F.D.: Photosynthesis, water-use efficiency and ∂13C of five cowpea (Vigna unguiculata L. Walp.) genotypes grown in mixed culture and at different densities with sorghum (Sorghum bicolor L.). - Photosynthetica 48: 143-155, 2010. Go to original source...
  26. Mariotti A., Germon J.C., Hubert P. et al.: Experimental determination of nitrogen kinetic isotope fraction: some principle; illustrations for the denitrification and nitrification processes. - Plant Soil 62: 413-430, 1981. Go to original source...
  27. Maskey S.L., Bhattarai S., Peoples M.B., Herridge D.F.: On-farm measurements of nitrogen fixation by winter and summer legumes in the Hill and Terai regions of Nepal. - Field Crop. Res. 70: 209-221, 2001. Go to original source...
  28. Moore B.D., Cheng S.H., Sims D. et al.: The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. - Plant Cell Environ. 22: 567-582, 1999. Go to original source...
  29. Morison J.I.L., Baker N.R., Mullineaux P.M. et al.: Improving water use in crop production. - Philos. T. R. Soc. B 363: 639-658, 2007.
  30. Pule-Meulenberg F., Belane A.K., Krasova-Wade T., Dakora F.D.: Symbiotic functioning and bradyrhizobial biodiversity of cowpea (Vigna unguiculata L. Walp.) in Africa. - BMC Microbiol 10: 89, 2010. Go to original source...
  31. Robertson M.J., Carberry P.S., Huth N.I. et al.: Simulation of growth and development of diverse legume species in APSIM. - Aust. J. Agric. Res. 53: 429-446, 2002. Go to original source...
  32. Rosenzweig C., Parry M.L.: Potential impact of climate change on world food supply. - Nature 367: 133-8, 1994. Go to original source...
  33. Shearer G., Kohl D.H.: N2-fixation in field settings: Estimations based on natural 15N abundance. - Aust. J. Plant Physiol. 13: 699-756, 1986. Go to original source...
  34. Streeter J., Wong P.P.: Inhibition of legume nodule formation and N2 fixation by nitrate. - Crit. Rev. Plant Sci. 7: 1-23, 1988. Go to original source...
  35. Tubiello F.N., Rosenzweig C., Kimball B.A. et al.: Testing CERES wheat with free-air carbon dioxide enrichment (FACE) experimental data: CO2 and water interactions. - Agron. J. 91: 247-255, 1999. Go to original source...
  36. Unkovich M.J., Herridge D., Peoples M. et al.: 15N natural abundance method. - In: Unkovich M.J., Herridge D., Peoples M. et al. (ed.): Measuring plant-associated nitrogen fixation in agricultural systems. Pp. 131-132. Australian Centre for International Agricultural Research (ACIAR), Monograph No. 136, Canberra 2008.
  37. Wang H., Ngwenyama N., Liu Y. et al.: Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. - Plant Cell 19: 63-73, 2007. Go to original source...
  38. Xu L.K., Hsiao T.C.: Predicted versus measured photosynthetic water-use efficiency of crop stands under dynamically changing field environments. - J. Exp. Bot. 55: 2395-2411, 2004. Go to original source...
  39. Zelitch I.,: The close relationship between net photosynthesis and crop yield. - BioScience 32: 796-802, 1982. Go to original source...