Symbiotic performance, shoot biomass and water-use efficiency of three groundnut (Arachis hypogaea L.) genotypes in response to phosphorus supply under field conditions in Ethiopia

Abstract

Phosphorus is a key nutrient element involved in energy transfer for cellular metabolism, respiration and photosynthesis and its supply at low levels can affect legume nodulation, N₂ fixation, and C assimilation. A two-year field study was conducted in Ethiopia in 2012 and 2013 to evaluate the effects of P supply on growth, symbiotic N₂ nutrition, grain yield and water-use efficiency of three groundnut genotypes. Supplying P to the genotypes significantly increased their shoot biomass, symbiotic performance, grain yield, and C accumulation. There was, however, no effect on shoot δ¹³C values in either year. Compared to the zero-P control, supplying 40 kg·ha⁻¹ P markedly increased shoot biomass by 77% and 66% in 2012 and 2013, respectively. In both years, groundnut grain yields were much higher at 20 and 30 kg·ha⁻¹ P. Phosphorus supply markedly reduced shoot δ¹⁵N values and increased the %Ndfa and amount of N-fixed, indicating the direct involvement of P in promoting N₂ fixation in nodulated groundnut. The three genotypes differed significantly in δ¹⁵N, %Ndfa, N-fixed, grain yield, C concentration, and δ¹³C. The phosphorus × genotype interaction was also significant for shoot DM, N content, N-fixed and soil N uptake.

Keywords

shoot yield / N-fixed / %Ndfa / δ¹⁵N / δ¹³C / water-use efficiency

References

[1] Sprent J I, Odee D W, Dakora F D. African legumes: a vital but under-utilized resource. Experimental Botany, 2010, 61(5): 1257–1265

[2] Asfaw S, Shiferaw B, Simtowe F, Muricho G, Ferede S. Socio-economic assessment of legume production, farmer technology choice, market linkages, institutions and poverty in rural Ethiopia: institutions, markets, policy and impacts research report No. 3. Field Crops Research, 2010, 36(2): 103–111

[3] Kebede E. Grain legumes production and productivity in Ethiopian smallholder agricultural system, contribution to livelihoods and the way forward. Cogent Food & Agriculture, 2020, 6(1): 1722353

[4] Nelson N O, Janke R R. Phosphorus sources and management in organic production systems. Horticulture Technology, 2007, 17(4): 442–454

[5] Schoninger E L, Gatiboni L C, Ernani P R. Rhizosphere pH and phosphorus forms in an Oxisol cultivated with soybean, brachiaria grass, millet and sorghum. Scientia Agrícola, 2012, 69(4): 259–264

[6] Israel D W. Investigation of the role of phosphorus in symbiotic dinitrogen fixation. Plant Physiology, 1987, 84(3): 835–840

[7] Vance C P, Uhde-Stone C, Allan D L. Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytologist, 2003, 157(3): 423–447

[8] Vance C P, Graham P H, Allan D L. Biological nitrogen fixation: phosphorus—a critical future need? In: Pederosa F O, Hungaria M, Yates M G, Newton W E, eds. Nitrogen fixation from molecules to crop productivity. Dordrecht, the Netherlands: Kluwer Academic publishers, 2000, 509–518

[9] Tang C, Hinsinger P, Drevon J J, Jaillard B. Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L. Annals of Botany, 2001, 88(1): 131–138

[10] Serraj R, Adu-Gyamfi J. Role of symbiotic nitrogen fixation in the improvement of legume productivity under stressed environments. West African Journal of Applied Ecology, 2004, 6(1): 95–109

[11] Clarkson D T, Carvajal M, Henzler T, Waterhouse R N, Smyth A J, Cooke D T, Steudle E. Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany, 2000, 51(342): 61–70

[12] Lovelock C E, Feller I C, Ball M C, Engelbrecht B M J, Ewe M L. Differences in plant function in phosphorus- and nitrogen-limited mangrove ecosystems. New Phytologist, 2006, 172(3): 514–522

[13] Gilbert M E, Zwieniecki M A, Holbrook N M. Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. Journal of Experimental Botany, 2011, 62(8): 2875–2887

[14] Songsri P, Jogloy S, Junjittakarn J, Kesmala T, Vorasoot N, Holbrook C C, Patanothai A. Association of stomatal conductance and root distribution with water use efficiency of peanut under different soil water regimes. Australian Journal of Crop Science, 2013, 7(7): 948–955

[15] Alkhader A M F, Abu Rayyan A M. Improving water use efficiency of lettuce (Lactuca sativa L.) using phosphorous fertilizers. SpringerPlus, 2013, 2(1): 563

[16] Songsri P, Jogloy S, Holbrook C C, Kesmala T, Vorasoot N, Akkasaeng C, Patanothai A. Association of root, specific leaf area and SPAD chlorophyll meter reading to water use efficiency of peanut under different available soil water. Agricultural Water Management, 2009, 96(5): 790–798

[17] Payne W A, Hossner L R, Onken A B, Wendt C W. Nitrogen and phosphorus uptake in pearl millet and its relation to nutrient and transpiration efficiency. Agronomy Journal, 1995, 87(3): 425–431

[18] Ali S, Munir A, Hayat R, Ijaz S S. Enhancing water use efficiency, nitrogen fixation capacity of mash bean and soil profile nitrate content with phosphorous and potassium application. Journal of Agronomy, 2005, 4(4): 340–344

[19] Kröbel R, Campbell C A, Zentner R P, Lemke R, Steppuhn H, Desjardins R L, De Jong R. Nitrogen and phosphorus effects on water use efficiency of spring wheat grown in a semi-arid region of the Canadian prairies. Canadian Journal of Soil Science, 2012, 92(4): 573–587

[20] Pandey R, Meena S K, Krishnapriya V, Ahmad A, Kishora N. Root carboxylate exudation capacity under phosphorus stress does not improve grain yield in green gram. Plant Cell Reports, 2014, 33(6): 919–928

[21] Hossain M A, Hamid A. Influence of N and P fertilizer application on root growth, leaf photosynthesis and yield performance of groundnut. Bangladesh Journal of Agricultural Research, 2007, 32(3): 369–374

[22] Bouyoucos G J. Hydrometer method improved for making particle size analyses of soils. Agronomy Journal, 1962, 54(5): 464–465

[23] Bray R H, Kurtz L T. Determination of total, organic, and available forms of phosphorus in soils. Soil Science, 1945, 59(1): 39–46

[24] Walkley A, Black I A. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 1934, 37(1): 29–38

[25] Mariotti A, Germon J C, Hubert P, Kaiser P, Letolle R, Tardieux A, Tardieux P. Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant and Soil, 1981, 62(3): 413–430

[26] Pausch R C, Mulchi C L, Lee E H, Meisinger J J. Use of ¹³C and ¹⁵N isotopes to investigate O₃ effects on C and N metabolism in soybeans. Part II. Nitrogen uptake, fixation, and partitioning. Agriculture, Ecosystems & Environment, 1996, 60(1): 61–69

[27] Shearer G, Kohl D H. N₂-fixation in field settings: estimations based on natural ¹⁵N abundance. Functional Plant Biology, 1986, 13(6): 699–756

[28] Nyemba R C, Dakora F D. Evaluating N₂ fixation by food grain legumes in farmers’ fields in three agro-ecological zones of Zambia, using ¹⁵N natural abundance. Biology and Fertility of Soils, 2010, 46(5): 461–470

[29] Unkovich M, Herridge D A, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P. Measuring plant-associated nitrogen fixation in agricultural systems. Australian Centre for International Agricultural Research (ACIAR), 2008

[30] Farquhar G D, Hubick K T, Condon A G, Richards R A. Carbon isotope fractionation and plant water-use efficiency. In: Rundel P W, Ehleringer J R, Nagy K A, eds. Stable isotope in Ecological Research. New York: Springer-Verlag, 1989, 21–40

[31] Craig H. Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochimica et Cosmochimica Acta, 1957, 12(1–2): 133–149

[32] Food and Agricultural Organization of the United Nations (FAO). Plant Nutrition for Food Security. A Guide for Integrated Nutrient Management. Rome: FAO, 2006

[33] Tadesse T, Haque I, Aduayi E A. Soil, plant, water, fertilizer, animal manure and compost analysis. Working Document No. 13. International Livestock Research Center for Africa. CGSpace Home International Livestock Research Institute (ILRI), ILRI project reports, papers and documents, 1991

[34] Rao S S, Shaktawat M S. Residual effect of organic manure, phosphorus and gypsum application in preceding groundnut (Arachis hypogaea) on soil fertility and productivity of Indian mustard (Brassica juncea). Indian Journal of Agronomy, 2002, 47(4): 487–494

[35] Nwokwu G N. Influence of phosphorus and plant spacing on the growth and yield of groundnut (Arachis hypogea L.). International Science Research Journal, 2011, 3: 97–103

[36] Doley K, Jite P K. Response of groundnut (‘JL-24’) cultivar to mycorrhiza inoculation and phosphorous application. Notulae Scientia Biologicae, 2012, 4(3): 118–125

[37] Unkovich M J, Pate J S, Sanford P, Amstrong E L. Potential precision of the d¹⁵N natural abundance method in field estimation of nitrogen fixation by crop and pasture legumes in South-west Australia. Australian Journal of Agricultural Research, 1994, 45(1): 119–132

[38] Yakubu H, Kwari J D, Sandabe M K. Effect of phosphorus fertilizer on nitrogen fixation by some grain legume varieties in Sudano–Sahelian Zone of North Eastern Nigeria. Nigerian Journal of Basic and Applied Sciences, 2010, 18(1): 19–26

[39] Mohamed S S, Abdalla A S. Growth and yield response of groundnut (Arachis hypogaea L.) to microbial and phosphorus fertilizers. Journal Agri-Food Applied Science, 2013, 1(3): 78–85

[40] Graham P H, Vance C P. Nitrogen fixation in perspective: an overview of research and extension needs. Field Crops Research, 2000, 65(2–3): 93–106

[41] Herridge D F, Bergersen F J, Peoples M B. Measurement of nitrogen fixation by soybean in the field using the ureide and natural N abundance methods. Plant Physiology, 1990, 93(2): 708–716

[42] Peoples M B, Herridge D F, Ladha J K. Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production. Plant and Soil, 1995, 174(1–2): 3–28

[43] Zahran H H. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiology and Molecular Biology, 1999, 63(4): 968–989

[44] Mokgehle S N, Dakora F D, Mathews C. Variation in N₂ fixation and N contribution by 25 groundnut (Arachis hypogaea L.) varieties grown in different agro-ecologies, measured using ¹⁵N natural abundance. Agriculture, Ecosystems & Environment, 2014, 195: 161–172

[45] Belane A K, Asiwe J, Dakora F D. Assessment of N₂ fixation in 32 cowpea (Vigna unguiculata L. Walp) genotypes grown in the field at Taung in South Africa, using ¹⁵N natural abundance. African Journal of Biotechnology, 2011, 10(55): 11450–11458

[46] Brück H, Payne W A, Sattelmacher B. Effect of phosphorus and water supply on yield, transpirational water-use efficiency, and carbon isotope discrimination of pearl millet. Crop Science, 2000, 40(1): 120–125

[47] Sawwan J, Shibli R A, Swaidat I, Tahat M. Phosphorus regulates osmotic potential and growth of African violet under in vitro-induced water deficit. Journal of Plant Nutrition, 2000, 23(6): 759–771

[48] Lovelock C E, Feller I C, Ball M C, Engelbrecht B M J, Ewe M L. Differences in plant function in phosphorus- and nitrogen-limited mangrove ecosystems. New Phytologist, 2006, 172(3): 514–522

[49] Kohn M J. Carbon isotope compositions of terrestrial C₃ plants as indicators of (paleo)ecology and (paleo)climate. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(46): 19691–19695

[50] Ma J Y, Sun W, Liu X N, Chen F H. Variation in the stable carbon and nitrogen isotope composition of plants and soil along a precipitation gradient in northern China. PLoS One, 2012, 7(12): e51894

[51] Liu W G, Feng X H, Ning Y F, Zhang Q L, Cao Y N, An Z S. d¹³C variation of C₃ and C₄ plants across an Asian monsoon rainfall gradient in arid northwest China. Global Change Biology, 2005, 11(7): 1094–1100

[52] Hartman G, Danin A. Isotopic values of plants in relation to water availability in the Eastern Mediterranean region. Oecologia, 2010, 162(4): 837–852

Acknowledgements

We are grateful to the Bill and Melinda Gates Foundation, the NRF, the South African Research Chair in Agrochemurgy and Plant Symbioses, and Tshwane University of Technology for financial support to FDD’s research and bursary to SKM.

Compliance with ethics guidelines

Sofiya K. Muhaba and Felix D. Dakora declare that they have no conflicts of interest or financial conflicts to disclose.

This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2020. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)