Biochemical and physiological characterizations of Rhizobium-Pea (Pisum sativum L.) symbiotic association under abiotic constraints

Authors

  • Khadija Ouerghi
  • Mohamed Bagues
  • Sifi Bouaziz

DOI:

https://doi.org/10.56027/JOASD.102021

Keywords:

Soil, Bacteria, fungui, microbe diversity

Abstract

Pea (Pisum sativum L.) is an important leguminous for the agricultural sector. It is a source of biological nitrogen that efficiently contributes to the soil fertility. In Tunisia, low pea production is due to bad nitrogen management, lack of phosphorus availability and to the abiotic constraints. Thus, in order  to improve the pea production ,a new farming technique involving the rhizobia inoculation was applied. The symbiotic, biochemical, physiological characterization and inoculation trials were performed in both the laboratory, greenhouse and open field. Pea Lincoln variety was used as legume species and fifteen Rhizobium strains isolated from the roots of the nodulated pea were collected from different Tunisian areas. Several physiological and biochemical parameters, i.e. pH, temperature, calcium carbonate and salinity were assessed to characterize the strains nodulating pea. All the rhizobia tests were evaluated on Yeast Extract Mannitol Agar medium (YEMA). Pea nodulation and Gallery API test were carried out under controlled conditions. Significant differences (p<0.01) between the nodules number induced by the different bacterial strains and between strains for the dry matter quantities of aerial and root parts were registered. The pH medium test results showed that among 15 strains only 8 strains having a halo diameter greater than 1 cm at basic pH. The most of isolates are able to grow at both low and high temperatures. The limestone test results qualify these rhizobia as calcifuges. Gallery API test results showed a great diversity of rhizobia assimilation of carbohydrates implying genetic diversity. Our results us to select the most efficient solubilizer Rhizobium strains nodulating pea. In order to confirm the previously cited notions on the diversity of  Rhizobium strains isolated from Pisum sativum roots in Tunisia, inoculation trial with both selected strains in controlled and open field conditions confirmed the capacity of selected strains to fix atmospheric nitrogen and promote plant growth.

References

Abdi N, L’taief B, Hemissi I, Bouraoui M, Maazaoui H and Sifi B. (2014). Nitrogen and Phosphorus fertilization effect on Rhizobia-common bean symbiosis. Annales de l’INRAT, vol 87, pp.31-33.

Abdi, N., Hemissi, I., Bouraoui, M., L'taeif, B. Sifi, B. (2015). Effect of salinity on common bean (Phaesolus vulgaris L.) Sinorhizobium strain symbiosis. Journal of new sciences. Agri Biotechnol, 16, 559-566.

Afzal A. and Bano A. (2008). Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum L.). International Journal of Agriculture and Biology, 10: 85-88.

Ballard RA , Charman N, McInnes A and Davidson J A. (2004). Size, symbiotic effectiveness and genetic diversity of field pea rhizobia (Rhizobium leguminosarum bv. viciae) populations in South Australian soils. Soil Biology and Biochemistry, 13: 1347-1355.

Bargaz A, Drevon JJ, Oufdou, K,Mandri B, Faghire M and Ghoulam C. (2011). Nodule phosphorus requirement and O2 uptake in common bean genotypes under phosphorus deficiency. Soil and Plant Science. 1-10.

Bargaz A, Zaman-Allah M, Farissi M, Lazali M, Drevon JJ, Maougal RT and Carlsson G. (2015). Physiological and Molecular Aspects of Tolerance to Environmental Constraints in Grain and Forage Legumes. International Journal of Molecular Sciences, 16: 18976-19008.

Berraquero FR, Baya AM and Cormenzana AR. (1976). Establishment of indices for the study of phosphate solubilization by soil bacteria. Ars Pharmacéutica, 17: 399-406.

Daimon H, Nobuta K, Ohe M, Harada J and Nakayama Y. (2006). Tricalcium phosphate solubilizing by root nodule bacteria of Sesbania cannabina and Crotalaria juncea. Plant Production Science, 9: 388-389.

Dardanelli M, Angelini J and Fabra A. (2003). A calcium-dependent bacterial surface protein is involved in the attachment of rhizobia to peanut roots. Canadian Journal of Microbiology, 49: 399-405

Delgado MJ, Ligero F and Lluch C. (1994). Effects of salt stress on growth and nitrogen fixation by pea, faba bean and soybean plants. Soil Biology and Biochemistry, 26: 31-376.

Denison RF and Kiers ET. (2004). Why are most rhizobia beneficial to their plant hosts, rather than parasitic?. Clinical Microbiology and Infection, 6:1235-1239

Dumont E, Bahrman N, Goulas E, Valot B, Sellier H and Hilbert JL. (2011). A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Science, 180: 86–98.

Farissi M, Faghire M, Bouizgaren A, Bargaz A, Makoudi B and Ghoulam C. (2014). Growth, nutrients concentrations and enzymes involved in plants nutrition of alfalfa populations under saline conditions. Journal of Agriculture Science and Technology, 16: 301–314.

Fitouri-Dhane S, Trabelsi D, Saïdi S, Zribi K, Ben Jeddi F and M’hamdi R. (2012). Diversity of rhizobia nodulating sulla (Hedysarum coronarium L.) and selection of inoculant strains for semi-arid Tunisia. Annals of Microbiology, 62 : (1)77-84.

Gobat JM, Aragno M and Matthey W. (1998). Le sol vivant. Bases de pédologie, biologie des sols. Presses polytechniques et universitaires romandes, pp 458-463.

Gomes NCM, Heuer H, Schoenfeld J, Costa R, Mendoca-Hagler L, Smalla K. (2001). Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant and Soil, 232: 167-180.

Graham A. 1992. The current status of the legume fossil record in the Caribbean Region. In Herendeen, P.S., Dilcher, D.L. (eds.), Advances in Legume Systematics: Part 4, The Fossil Record. The Royal Botanic Gardens, Kew., pp. 161–167

Graham PH, Sadowsky MJ, Keyser HH, Barnet YM, Bradley RS, Cooper JE, Deley DJ, Jarvis BDW, RoslyCcky EB, Strijdom BW and Young JPW. (1991). Proposed minimal standards for the description of new genera and species of root-and stemnodulating bacteria. International Journal of Systematic Bacteriology, 41:582-587.

Hachana A, Hemissi I, Cherif H, Hlel D, Bouraoui M, Abdi N, Maazaoui H, Cherif A and Sifi B. (2017). Diagnosis of Biodiversity of RhizobiumLeguminosarum Nodulating Pea (Pisum Sativum L.) in Differents Soils of Tunisia. Recent Advances in Environmental Science from the Euro-Mediterranean and surrunding regions. Conference for Environmental Integration (EMCEI-1), Tunisia.

He Y, Guo L, Zhang H and Huang G. (2011). Symbiotic effectiveness of pea-rhizobia associations and the implications for farming systems inthe western Loess Plateau, China. African Journal of Biotechnology, 10: (18): 3540-3548.

Hemissi I, Abdi N, Bargaz A, Bouraoui M, Mabrouk Y, Saidi M and Sifi B. (2015). Inoculationwith Phosphate solubilizing Mezorhizobium strains improves the Performance of chickpea (Cicer aritenium L.) under Phosphorus deficiency. Journal of Plant Nutrition, 38: 1656-1671.

Hemissi I, Mabrouk Y, Abdi N, Bouraoui M, Saidi M and Sifi B. (2011). Effects of some Rhizobium strains on chickpea growth and biological control of Rhizoctonia solani. African Journal of Microbiology Research, 5: (24): 4080-4090.

Hemissi I, Mabrouk Y, Abdi N, Bouraoui M, Saidi M and Sifi B. (2013). Growth promotion and protection against Orobanche foetida of chickpea (Cicer aerietinum) by two Rhizobium strains under greenhouse conditions. African Journal of Biotechnology, Vol. 12: (12) 1371-1377.

Henault C and Revellin C. (2011). Inoculants of leguminous crops for mitigating soil emissions of the greenhouse gas nitrous oxide. Plant and Soil, 346(1-2):289-296.

Huang J, Afshar RK, Tao A and Chen C. (2017). Efficacy of starter N fertilizer and rhizobia inoculant in dry pea (Pisum sativum L.) production in a semi-arid temperate. Soil Science and Plant Nutrition, 63, 3: 248–253

Hussain M, Asgher Z, Tahir M, Ijaz M, Shahid M, Ali H and Sattar A. (2016). Bacteria in combination with fertilizers improve growth, productivity and net returns of wheat (Triticum aestivum L.). Pakistan Journal of Agriculture Sciences, 53: 633-645.

Kersters K, Hinz KH, Hertle A, Segers P, Lievens A, Siegmann Oand De Ley J. (1984). Bordetella avium sp. nov., isolated from the respiratory tracts of turkeys and other birds. International Journal of Systematic Bacteriology, 34: 56–70.

Kishinevsky BD, Nandasena KG, Yates RJ, Nemas C, Howieson JG. (2003). Phenotypic and genetic diversity among rhizobia isolated from three Hedysarum species: H. spinosissimum, H. coronarium and H. flexuosum. Plant and Soil, 251:143–153.

Kouki S, Abdi N, Hemissi I, Bouraoui M, Sifi B. (2016). Phosphorus fertilization effect on common bean (Phaseolus vulgaris L.) -rhizobia symbiosis. Journal of new sciences, Agri Biotech, 25(1):1130-1137.

Kumar Meena R, Kumar Singh R, Pal Singh N, Kumari Meena S, Singh Meena V. (2015). Isolation of low temperature surviving plant growth –promoting rhizobacteria (PGPR) from pea (Pisum sativum L.) and documentation of their plant growth promoting traits. Biocatalysis and Agricultural Biotechnology, (4)4: 471-479.

L’taief B, Sifi B, Zaman-Allah M, Drevon JJ, Lachaal M. (2007). Effect of salinity on root –nodule conductance to the oxygen diffusion in the cicer arietinum-Mesorhizobium cicer symbiosis. Plant physiology, 164: 1028-1036.

Lynch DH, Smith DL. (1993). Soybean (Glycine max) nodulation and N2 fixation as affected by exposure to a low root-zone temperature. Physiologia Plantarum, 88: 212–220.

Maatallah J, Berraho EB, Sanjuan J and Lluch C. (2002). Phenotypic characterization of rhizobia isolated from chickpea (Cicer arietinum) growing in Maroccan soils. Agronomy, 22: 321-329.

Maazaoui H, Drevon JJ, SIFi B. (2016). Uptake and nitrogen fixation in a Tunisian multi local field test. Journal of new sciences. Agricultural and Biotechnology, 30(10): 1806-1811

Mahdhi M, Mars M. (2006). Genotypic diversity of rhizobia isolated from Retama raetam in arid regions of Tunisia. Annals of Microbiology, 56: 305–311.

Mahdhi M, Nzoué A, de Lajudie P, Mars M. (2008). Characterization of Retama raetam root nodules bacteria in arid Tunisian soils. Progress in Natural Science, 18: 43–49.

Mahdhi M, Nzoué A, Gueye F, Merabet C, de Lajudie P, Mars M. (2007). Phenotypic and genotypic diversity of Genista saharae microsymbionts from the infra-arid region of Tunisia. Letters in Applied Microbiology. 45: 604–609.

ManivannanM, Ganesh P, Kumar RS, Tharmaraj K and Ramya BS. (2012). Isolation, screening, characterization and antagonism assay of PGPR isolates from rhizosphere of rice plants in Cuddalore District. International Journal of Pharmaceutical and Biological Archive, 3: 179-185.

Marra LM, Maria de Oliveira S, Fonsêca Sousa Soares CR and Moreira FMS. (2011). Solubilisation of inorganic phosphates by inoculant strains from tropical legumes. Scientia Agricola, 68: 603-609.

Moawad HA, Beck DP. (1991). Some characteristics of Rhizobium leguminosarum isolates from un-inoculated field-grown lentil. Soil Biology and Biochemistry. 23: 933–937.

Muniz AW, Dalla Costa M, Saccol de Sá EL, Fiuza AB and Bros E. (2017). Symbiotic efficiency of pea (Pisum sativum) rhizobia association under field conditions. African Journal of Agricultural Research. Vol. 12(32):2582-2585.

Parkinson JA and Allen SE. (1975). A wet oxidation process suitable for the determination of nitrogen and mineral nutrients in biological material. Communications in Soil Science and Plant Analysis, 6: 1–11.

Pikovskaya RI. (1948). Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Microbiology, 17: 362-370.

Prosperi JM. (1993). Selection of annual medics for French Mediterranean regions. Introducing Ley Farming to the Mediterranean Basin: Christiansen, S., Materon, L., Falcinelli, M., Cocks, P. (Eds.), Proceedings of an International Workshop, Perugia, Italy. pp. 173–191

Qureshi MA, Ahmad ZA, Akhtar N, Iqbal A, Mujeeb F and Shakir MA. (2012). Role of phosphate solubilizing bacteria (PSB) in enhancing P-availability and promoting cotton growth. Journal of Animal and Plant Sciences, 22: 204–210.

Rani S, Kumar P, Kumar A, Kumar A and Sewhag M. (2016). Effect of biofertilizers on nodulation, nutrient uptake, yield and energy use efficiency of field pea (Pisum sativum L.). Journal of Agricultural Meteorology, 18(2):330-332.

Rao DLN, Giller KE, Yeo AR and Flowers TJ. (2002). The effects of salinity and sodicity upon nodulation and nitrogen fixation in chickpea (Cicer arietinum L.). Annals of Botany, 89(5): 563-570.

Rejili M, Mahdhi M, Fterich A, Dhaoui S, Guefrachi I, Abdeddayem R and Mars M. (2012). Symbiotic nitrogen fixation of wild legumes in Tunisia: Soil fertility dynamics, field nodulation and nodules effectiveness. Agriculture, Ecosystems and Environment, 157: 60– 69.

Rice WA, Clayton GW, Olsen PE and Lupwayi NZ. (2000). Rhizobial inoculant formulations and soil pH influence field pea nodulation and nitrogen fixation. Canadian Journal of Soil Science, 395-400

Roldan A, Garcia-Orenes F and Albaladejo J. (1994). Microbial populations in the rhizosphere of the Brachypodium retusum and their relationship with stable aggregates in a semiarid soil of southeastern Spain. Arid Soil Research and Rehabilitation, 8:105–114.

Singh JS, Pandey VC and Singh DP. (2011). Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agriculture, Ecosystems and Environment, 140: 339-353.

Singh NP, Singh RK, Meena VS, Meena RK. (2015). Can we use maize (Zea mays) rhizobacteria as plant growth promoter. Vegetos, 28 (1): 86–99

Singh S, Kumar V, Sidhu GK, Daljeet SD, Singh D, Koul B, Singh HJ, Singh J. (2019). Plant growth promoting rhizobacteria from heavy metal contaminated soil promote growth attributes of Pisum sativum L. Biocatalysis and Agricultural Biotechnology, 17: 665–671.

Van Rhijn R and Vanderleyden J. (1995). The Rhizobium-plant symbiosis. Microbiology and Molecular Biology Reviews, 59(1):124-142.

Van-Rossum D, Schurmans FP, Gillis M, Muyotcha A, Van Verseveld HW, Stouthamer AH and Boogerd FC. (1995). Genetic and phenotypic analysis of Bradyrhizobium strains nodulating peanut (Arachis hypogea L.) roots. Applied and Environmental Microbiology, 61: 1599-1609.

Verma JP, Yadav J, Tiwari KN and Jaiswal DK. (2014). Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum L.) in India. Soil Biology and Biochemistry, 70: 33–37.

Vincent JM. (1970). A Manual for the Practical Study of Root Nodule Bacteria. Oxford: Blackwell Scientific.

Walpola BC, Yoon MH. (2012). Prospectus of phosphate solubilizing microorganisms and phosphorus availability in agricultural soils: a review. African Journal of Microbiology Research, 6: 6600–6605

Wei HC, Rollins J, Fabian L, Hayes M, Polevoy G, Bazinet C and Brill JA. (2008). Depletion of plasma membrane PtdIns (4,5) P2 reveals essential roles for phosphoinositides in flagellar biogenesis. Journal of Cell Science, 121 (7): 1076--1084.

West SA, Toby Kiers E, Simms Ellen L and Denison FR. (2002). Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proceeding of the Royal Society of London B, 269: 685- 694.

Yang C, Bueckert R, Schoenau J, Diederichsen A, Zakeri H and Warkentin T. (2017). Symbiosis of selected Rhizobium leguminosarum bv. viciae strains with diverse pea genotypes: effects on biological nitrogen fixation. Canadian Journal of Microbiology, 63(11):909-919.

Yanni YG, Rizk R.Y, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G., De Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK and Dazzo F.B. (1997). Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant and Soil, 194: 99–114

Zahran H. (2001). Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. Journal of Biotechnology, 91 : 143–153.

Zaman-Allah M, Sifi B, Issoufou M, EL Aouni MH.2005. Salt tolerance of a common bean (Phaseolus vulgaris L.) cultivar as affected by rhizobia. Symbiosis, 40:17-22.

Zeppenfeld T, Balkenhol N, Kóvacs K, Carminati A. (2017). Rhizosphere hydrophobicity: A positive trait in the competition for water. Plos One, 7 (12).

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Published

2021-12-01

How to Cite

Ouerghi, K., Bagues, M., & Bouaziz, S. (2021). Biochemical and physiological characterizations of Rhizobium-Pea (Pisum sativum L.) symbiotic association under abiotic constraints. JOURNAL OF OASIS AGRICULTURE AND SUSTAINABLE DEVELOPMENT, 3(2), 30–45. https://doi.org/10.56027/JOASD.102021

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