Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Improved grain yield of cowpea (Vigna unguiculata) under water deficit after inoculation with Bradyrhizobium elkanii and Rhizophagus irregularis

Rui S. Oliveira A B H , Patrícia Carvalho B , Guilhermina Marques C , Luís Ferreira D , Sandra Pereira C , Mafalda Nunes B , Inês Rocha A , Ying Ma A , Maria F. Carvalho E , Miroslav Vosátka F G and Helena Freitas A
+ Author Affiliations
- Author Affiliations

A Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal.

B Department of Environmental Health, Research Centre on Health and Environment, School of Allied Health Sciences, Polytechnic Institute of Porto, Rua Dr António Bernardino de Almeida, 400, 4200-072, Porto, Portugal.

C University of Trás-os-Montes e Alto Douro, Centre for the Research and Technology of Agro-Environmental and Biological Sciences (UTAD-CITAB), Quinta de Prados, 5000-801 Vila Real, Portugal.

D Animal and Veterinary Research Centre (CECAV), University of Trás-os-Montes and Alto Douro (UTAD), Quinta de Prados, 5000-801 Vila Real, Portugal.

E CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenuenida General Norton de Matos, 4450-208 Matosinhos, Portugal.

F Institute of Botany, Academy of Sciences of the Czech Republic, Zámek 1, 252 43 Průhonice, Czech Republic.

G Department of Experimental Plant Biology, Charles University, Faculty of Science, Viničná 5, Praha 2, Czech Republic.

H Corresponding author. Email: rsoliveira@uc.pt

Crop and Pasture Science - https://doi.org/10.1071/CP17087
Submitted: 18 February 2017  Accepted: 6 June 2017   Published online: 17 July 2017

Abstract

Cowpea (Vigna unguiculata (L.) Walp.), a plant broadly cultivated for human consumption and animal feed, is among the most nutritious grain legumes. Most of the areas where cowpea is grown are drought-prone, and there is a need to address this issue, with water scarcity becoming a major concern in agriculture. Cowpea is known to form mutualistic associations with nitrogen-fixing (NF) bacteria and arbuscular mycorrhizal (AM) fungi. These beneficial soil microorganisms have the capacity to benefit plants by reducing the effects of environmental stresses, including drought. Our aim was to study the effect of inoculation with Bradyrhizobium elkanii and Rhizophagus irregularis on the growth and grain yield of cowpea under water-deficit conditions. Under moderate water deficit, grain yield was increased by 63%, 55% and 84% in plants inoculated with B. elkanii, R. irregularis and B. elkanii + R. irregularis, respectively. Under severe water deficit, inoculation with B. elkanii and B. elkanii + R. irregularis resulted in grain-yield enhancement of 45% and 42%, respectively. The use of cowpea inoculated with NF bacteria and AM fungi has great potential for sustainable agricultural production under drought conditions.

Additional keywords: plant-microbe interactions, pulses, rhizobia, sustainable agriculture, tripartite symbiosis, water stress.


References

Ames RN, Thiagarajan TR, Ahmad MH, McLaughlin WA (1991) Co-selection of compatible rhizobia and vesicular-arbuscular mycorrhizal fungi for cowpea in sterilized and non-sterilized soils. Biology and Fertility of Soils 12, 112–116.
Co-selection of compatible rhizobia and vesicular-arbuscular mycorrhizal fungi for cowpea in sterilized and non-sterilized soils.CrossRef |

Association of Official Analytical Chemists (2006) ‘Official methods of analysis.’ 18th edn (Association of Official Analytical Chemists: Gaithersburg, MD, USA)

Augé RM, Kubikova E, Moore JL (2001) Foliar dehydration tolerance of mycorrhizal cowpea, soybean and bush bean. New Phytologist 151, 535–541.
Foliar dehydration tolerance of mycorrhizal cowpea, soybean and bush bean.CrossRef |

Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25, 13–24.
Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis.CrossRef |

Bagayoko M, George E, Römheld V, Buerkert A (2000) Effects of mycorrhizae and phosphorus on growth and nutrient uptake of millet, cowpea and sorghum on a West African soil. The Journal of Agricultural Science 135, 399–407.
Effects of mycorrhizae and phosphorus on growth and nutrient uptake of millet, cowpea and sorghum on a West African soil.CrossRef |

Baláz M, Vosátka M (2001) A novel inserted membrane technique for studies of mycorrhizal extraradical mycelium. Mycorrhiza 11, 291–296.
A novel inserted membrane technique for studies of mycorrhizal extraradical mycelium.CrossRef |

Bell LW, Lawrence J, Johnson B, Peoples MB (2017) New ley legumes increase nitrogen fixation and availability and grain crop yields in subtropical cropping systems. Crop & Pasture Science 68, 11–26.
New ley legumes increase nitrogen fixation and availability and grain crop yields in subtropical cropping systems.CrossRef |

Brundrett M, Melville L, Peterson RL (1994) ‘Practical methods in mycorrhizal research.’ (Mycologue Publications: Waterloo, ON, Canada)

Chalk PM, Souza RF, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biology & Biochemistry 38, 2944–2951.
The role of arbuscular mycorrhiza in legume symbiotic performance.CrossRef | 1:CAS:528:DC%2BD28XotFKju7Y%3D&md5=fca34a67eeb0c2893def63a6fd390d0eCAS |

Diallo AT, Samb PI, Roy-Macauley H (2001) Water status and stomatal behaviour of cowpea, Vigna unguiculata (L.) Walp, plants inoculated with two Glomus species at low soil moisture levels. European Journal of Soil Biology 37, 187–196.
Water status and stomatal behaviour of cowpea, Vigna unguiculata (L.) Walp, plants inoculated with two Glomus species at low soil moisture levels.CrossRef |

Ehlers JD, Hall AE (1997) Cowpea (Vigna unguiculata L. Walp.). Field Crops Research 53, 187–204.
Cowpea (Vigna unguiculata L. Walp.).CrossRef |

Elowad HOA, Hall AE (1987) Influences of early and late nitrogen fertilization on yield and nitrogen fixation of cowpea under well-watered and dry field conditions. Field Crops Research 15, 229–244.
Influences of early and late nitrogen fertilization on yield and nitrogen fixation of cowpea under well-watered and dry field conditions.CrossRef |

FAO (2003) ‘Food energy—methods of analysis and conversion factors.’ (Food and Agriculture Organization of the United Nations: Rome) Available at: www.fao.org/uploads/media/FAO_2003_Food_Energy_02.pdf (accessed 10 February 2017)

FAOSTAT (2017) Statistics Division. Food and Agriculture Organization of the United Nations, Rome. Available at: www.fao.org/faostat/en/#home (accessed 10 February 2017).

Fery RL (2002) New opportunities in Vigna. In ‘Trends in new crops and new uses’. (Eds J Janick, A Whipkey) pp. 424–428. (ASHS Press: Alexandria, VA, USA)

Figueiredo MVB, Burity HA, de França FP (1998) Water deficit stress effects on N2 fixation in cowpea inoculated with different Bradyrhizobium strains. Canadian Journal of Plant Science 78, 577–582.
Water deficit stress effects on N2 fixation in cowpea inoculated with different Bradyrhizobium strains.CrossRef |

Figueiredo MVB, Vilar JJ, Burity HA, de França FP (1999) Alleviation of water stress effects in cowpea by Bradyrhizobium spp. inoculation. Plant and Soil 207, 67–75.
Alleviation of water stress effects in cowpea by Bradyrhizobium spp. inoculation.CrossRef |

Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots.CrossRef |

Grewal KS, Buchan GD, Tonkin PJ (1990) Estimation of field capacity and wilting point of some New Zealand soils from their saturation percentages. New Zealand Journal of Crop and Horticultural Science 18, 241–246.
Estimation of field capacity and wilting point of some New Zealand soils from their saturation percentages.CrossRef |

Halilou O, Hamidou F, Taya BK, Mahamane S, Vadez V (2015) Water use, transpiration efficiency and yield in cowpea (Vigna unguiculata) and peanut (Arachis hypogaea) across water regimes. Crop & Pasture Science 66, 715–728.
Water use, transpiration efficiency and yield in cowpea (Vigna unguiculata) and peanut (Arachis hypogaea) across water regimes.CrossRef | 1:CAS:528:DC%2BC2MXhtV2murbL&md5=59f9203099695c21b43b8b1b1cdf842dCAS |

Hall AE (2012) Phenotyping cowpeas for adaptation to drought. Frontiers in Physiology 3, 155

Iqbal MA (2015) Evaluation of forage cowpea and hey as a feed resource for ruminant production: a mini-review. Global Veterinaria 14, 747–751.

Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biology & Biochemistry 42, 125–127.
Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses.CrossRef | 1:CAS:528:DC%2BD1MXhsVGrtLfE&md5=54acf5d2f2c60f27604fedcc2ee739baCAS |

Koide RT, Li M (1989) Appropriate controls for vesicular–arbuscular mycorrhiza research. New Phytologist 111, 35–44.
Appropriate controls for vesicular–arbuscular mycorrhiza research.CrossRef |

Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147, 981–993.
Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts.CrossRef | 1:CAS:528:DC%2BD3MXjtVeisb8%3D&md5=f0083b3534d745d3d26de0a2b7a6eb20CAS |

Ngakou A, Tamò M, Parh IA, Nwaga D, Ntonifor NN, Korie S, Nebane CLN (2008) Management of cowpea flower thrips, Megalurothrips sjostedti (Thysanoptera, Thripidae), in Cameroon. Crop Protection 27, 481–488.
Management of cowpea flower thrips, Megalurothrips sjostedti (Thysanoptera, Thripidae), in Cameroon.CrossRef | 1:CAS:528:DC%2BD1cXhslGmtrg%3D&md5=322575d19f052280bbf10c0ad9675bfaCAS |

Nielsen SS, Brandt WE, Singh BB (1993) Genetic variability for nutritional composition and cooking time of improved cowpea lines. Crop Science 33, 469–472.
Genetic variability for nutritional composition and cooking time of improved cowpea lines.CrossRef | 1:CAS:528:DyaK2cXis1yltLk%3D&md5=ee0f210378b7bfee31dcd6b9ec894469CAS |

Oliveira RS, Castro PML, Dodd JC, Vosátka M (2005a) Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 60, 1462–1470.
Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment.CrossRef | 1:CAS:528:DC%2BD2MXmvFSjt7c%3D&md5=f4a43efaa0de6d4a22446d80e79f8518CAS |

Oliveira RS, Vosátka M, Dodd JC, Castro PML (2005b) Studies on the diversity of arbuscular mycorrhizal fungi and the efficacy of two native isolates in a highly alkaline anthropogenic sediment. Mycorrhiza 16, 23–31.
Studies on the diversity of arbuscular mycorrhizal fungi and the efficacy of two native isolates in a highly alkaline anthropogenic sediment.CrossRef | 1:CAS:528:DC%2BD2MXht1SqtLzJ&md5=f02f89319cb3787d29f45266a354f519CAS |

Oliveira RS, Castro PML, Dodd JC, Vosátka M (2006) Different native arbuscular mycorrhizal fungi influence the coexistence of two plant species in a highly alkaline anthropogenic sediment. Plant and Soil 287, 209–221.
Different native arbuscular mycorrhizal fungi influence the coexistence of two plant species in a highly alkaline anthropogenic sediment.CrossRef | 1:CAS:528:DC%2BD28XhtVCntb%2FF&md5=d4b481aadf25ecc2c695f25c87875d52CAS |

Oliveira RS, Boyer LR, Carvalho MF, Jeffries P, Vosátka M, Castro PML, Dodd JC (2010) Genetic, phenotypic and functional variation within a Glomus geosporum isolate cultivated with or without the stress of a highly alkaline anthropogenic sediment. Applied Soil Ecology 45, 39–48.
Genetic, phenotypic and functional variation within a Glomus geosporum isolate cultivated with or without the stress of a highly alkaline anthropogenic sediment.CrossRef |

Oliveira RS, Ma Y, Rocha I, Carvalho MF, Vosátka M, Freitas H (2016a) Arbuscular mycorrhizal fungi are an alternative to the application of chemical fertilizer in the production of the medicinal and aromatic plant Coriandrum sativum L. Journal of Toxicology and Environmental Health. Part A. 79, 320–328.
Arbuscular mycorrhizal fungi are an alternative to the application of chemical fertilizer in the production of the medicinal and aromatic plant Coriandrum sativum L.CrossRef | 1:CAS:528:DC%2BC28XmtFejur8%3D&md5=73bc76988367ef1a3106979482a39ae8CAS |

Oliveira RS, Rocha I, Ma Y, Vosátka M, Freitas H (2016b) Seed coating with arbuscular mycorrhizal fungi as an ecotechnological approach for sustainable agricultural production of common wheat (Triticum aestivum L.). Journal of Toxicology and Environmental Health. Part A. 79, 329–337.
Seed coating with arbuscular mycorrhizal fungi as an ecotechnological approach for sustainable agricultural production of common wheat (Triticum aestivum L.).CrossRef | 1:CAS:528:DC%2BC28XmtFejur0%3D&md5=31e231feb37cc7f62bfd489dc6ec2059CAS |

Omirou M, Fasoula DA, Ioannides IM (2016) Bradyrhizobium inoculation alters indigenous AMF community assemblages and interacts positively with AMF inoculum to improve cowpea performance. Applied Soil Ecology 108, 381–389.
Bradyrhizobium inoculation alters indigenous AMF community assemblages and interacts positively with AMF inoculum to improve cowpea performance.CrossRef |

Ossler JN, Zielinski CA, Heath KD (2015) Tripartite mutualism: facilitation or trade-offs between rhizobial and mycorrhizal symbionts of legume hosts. American Journal of Botany 102, 1332–1341.
Tripartite mutualism: facilitation or trade-offs between rhizobial and mycorrhizal symbionts of legume hosts.CrossRef | 1:CAS:528:DC%2BC28XnsFehsb4%3D&md5=f7830ab1cd517e6bf79fff9b6117f76fCAS |

Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.CrossRef |

Porter W (1979) The “most probable number” method for enumerating infective propagules of vesicular arbuscular mycorrhizal fungi in soil. Australian Journal of Soil Research 17, 515–519.
The “most probable number” method for enumerating infective propagules of vesicular arbuscular mycorrhizal fungi in soil.CrossRef |

Rangel A, Saraiva K, Schwengber P, Narciso MS, Domont GB, Ferreira ST, Pedrosa C (2004) Biological evaluation of a protein isolate from cowpea (Vigna unguiculata) seeds. Food Chemistry 87, 491–499.
Biological evaluation of a protein isolate from cowpea (Vigna unguiculata) seeds.CrossRef | 1:CAS:528:DC%2BD2cXkslKmsL8%3D&md5=e161548170312f55964ab28fad8d49b4CAS |

Schakel KA, Hall AE (1979) Reversible leaflet movements in relation to drought adaptation of cowpeas, Vigna unguiculata (L.) Walp. Australian Journal of Plant Physiology 6, 265–276.
Reversible leaflet movements in relation to drought adaptation of cowpeas, Vigna unguiculata (L.) Walp.CrossRef |

Sikora S, Redzepovic S, Bradic M (2002) Genomic fingerprinting of Bradyrhizobium japonicum isolates by RAPD and rep-PCR. Microbiological Research 157, 213–219.
Genomic fingerprinting of Bradyrhizobium japonicum isolates by RAPD and rep-PCR.CrossRef | 1:CAS:528:DC%2BD38XovFagu74%3D&md5=140323343691ce37d4292705b127852eCAS |

Singh BB, Ehlers JD, Sharma B, Freire Filho FR (2002) Recent progress in cowpea breeding. In ‘Challenges and opportunities for enhancing sustainable cowpea production’. (Eds CA Fatokun, SA Tarawali, BB Singh, PM Kormawa, M Tamo) pp. 22–40. (International Institute of Tropical Agriculture: Ibadan, Nigeria)

Somasegaran P, Hoben HJ (1985) ‘Methods in legume–Rhizobium technology.’ (Department of Agronomy and Soil Science, University of Hawaii, Hawaii Institute of Tropical Agriculture and Human Resources: Manoa, HI, USA)

Taiwo LB, Osonubi O, Akano MJ (2001) Growth and nodulation of cowpea (Vigna unguiculata) in response to compost and inoculation with Glomus etunicatum and Bradyrhizobium. Tropical Agricultural Research and Extension 4, 101–107.

Timko MP, Singh BB (2008) Cowpea, a multifunctional legume. In ‘Genomics of tropical crop plants’. Ch. 10. (Eds PH Moore, R Ming) pp. 227–258. (Springer Science + Business Media LLC: New York)

Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173, 697–703.
16S ribosomal DNA amplification for phylogenetic study.CrossRef | 1:CAS:528:DyaK3MXhsl2lurY%3D&md5=a014edb25bf1ce0a431d3ad8ce4c82d1CAS |

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.CrossRef | 1:CAS:528:DyaK2cXmsFShsbY%3D&md5=9b57c922c4bcfc1432fab3d0e2099d3dCAS |

Wilson BAL, Ash GJ, Harper JDI (2012) Arbuscular mycorrhizal fungi improve the growth and nodulation of the annual legume messina (Melilotus siculus) under saline and non-saline conditions. Crop & Pasture Science 63, 164–178.
Arbuscular mycorrhizal fungi improve the growth and nodulation of the annual legume messina (Melilotus siculus) under saline and non-saline conditions.CrossRef |

Zhang YF, Wang ET, Tian CF, Wang FQ, Han LL, Chen WF, Chen WX (2008) Bradyrhizobium elkanii, Bradyrhizobium yuanmingense and Bradyrhizobium japonicum are the main rhizobia associated with Vigna unguiculata and Vigna radiata in the subtropical region of China. FEMS Microbiology Letters 285, 146–154.
Bradyrhizobium elkanii, Bradyrhizobium yuanmingense and Bradyrhizobium japonicum are the main rhizobia associated with Vigna unguiculata and Vigna radiata in the subtropical region of China.CrossRef | 1:CAS:528:DC%2BD1cXhtVers7fN&md5=5a99ebcd9e5284fe495d5b1d5a6a909eCAS |



Export Citation

View Altmetrics