Abstract

Rhizobium besides its nodule formation characteristic with members of Fabaceae family has been recognized for its great root colonizing ability and growth hormone production potential. In addition to nitrogen fixation in legume plants, rhizobia considered as beneficial tools and act as plant growth promoting rhizobacteria (PGPR) with many non-legumes. Present study was elucidated to determine the comparative role of Rhizbium sp for growth promotion of sunflower. Rhizobia were isolated from five different legumes (mungbean, barseem, lentil, chickpea, and vegetable pea) and checked for their auxin production efficiency. Rhizobial isolates Cp-4 showed maximum auxin potential (5.37 µg mL-1IAA equivalents).Results showed that inoculation of all rhizobial isolates caused significant increase in growth and physiological parameters of sunflower plants. While prominent results were found with inoculation of mungbean rhizobial isolate Mb-2 which increases the chlorophyll a, N, P, fresh and dry matter of sunflower significantly by 8.34, 4.9, 36, 31, and 34%, respectively in comparison to un-inoculated control plants. Hence, present study concluded that Rhizobium sp can be successfully used as PGPR in non-legumes after thorough investigations.

Keywords: Rhizobium sp, PGPR, auxin biosynthesis, growth, sunflower.

References

Adnan, M., Shah, Z., Saleem, N., Basir, A., Inayat-ur-Rahman, Ullah, H., Ibrahim, M., Shah, J. A., Muhammad, Khan, A., Shah, S. R. A., 2016.  Isolation and evaluation of summer legumes Rhizobia as PGPR. Pure and Applied Biology 5(1): 127-133.

Alikhani, H.A., Saleh-Rastin,N., Antoun, H., 2006. Phosphate solubilization activity of rhizobia native to Iranian soils. In: E. Velázquez, C. Rodríguez-Barrueco (Eds.). First international meeting on microbial phosphate solubilization. Volume 102 of the series Developments in Plant and Soil Sciences. Springer. pp. 35-41.

Arnon, D.I., 1949. Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiology 24(1): 1-15.

Barry S.M., Challis, G.L., 2009. Recent advances in siderophore biosynthesis. Current Opinion in Chemical Biology 13(2): 205–215.

Bhattacharyya, P.N., Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology and Biotechnology 28(4): 1327–1350.

Biswas, J.C., Ladha, J.K., Dazzo, F.B., 2000. Rhizobial inoculation improves nutrient uptake and growth of lowland rice. Soil Science Society of America Journal 64(5): 1644-1650.

Bremner, J. M., Mulvaney, C. S., 1982. Nitrogen total. In: Page, A.L. (Ed.). Method of Soil analysis. Part 2: Chemical and microbiological properties. Argonomy No.9, 2nd edition, American Society of Agronomy, Madison, WI, USA. pp. 595-624.

Carson, K.C., Meyer, J.M., Dillworth, M.J., 2000. Hydroxamatesiderophores of root nodule bacteria. Soil Biology and Biochemistry 32(1): 11–21.

Chalk, P.M., 2016. The strategic role of 15N in quantifying the contribution of endophytic N2 fixation to the N nutrition of non-legumes. Symbiosis 69(2): 63–80.

Chen, X., Tang, J.J., Zhi, G.Y., Hu, S.J., 2005. Arbuscular mycorrhizal colonization and phosphorus acquisition of plants: effects of coexisting plant species. Applied Soil Ecology 28(3): 259-269.

Chi, F., Shen, S.-H., Cheng, H.-P., Jing, Y.-X., Yanni, Y. G., Dazzo, F. B., 2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Applied and Environmental Microbiology 71(11): 7271–7278.

Compant, S., Duffy, B., Nowak, J., Clement, C., Barka, E.A., 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology 71(9): 4951–4959. 

Dakora, F.D., Matiru, V., King,M., Phillips, D.A., 2002. Plant growth promotion in legumes and cereals bylumichrome, a rhizobial signal metabolite. In: Finan, T.M., O’Brian, M.R., Layzell, D.B., Vessey, K., Newton, W.E. (Eds.). Nitrogen fixation: global perspectives. CABI Publishing, Wallingford, pp. 321–322.

Dimkpa, C.O., Merten, D., Svatoš, A., Büchel, G.E., Kothe., 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. Journal of Applied Microbiology 107(5): 1687–1696.

Duncan, D. B., 1955. Multiple range and multiple F-Test. Biometrics 11: 1-42.

Fritsch, C., Heinrich, V., Vogel, R.F., Toelstede, S., 2015. Phenolic acid degradation potential and growth behavior of lactic acid bacteria in sunflower substrates. Food Microbiology 57: 178-186.

Hardoim, P.R., van Overbeek, L.S., van Elsas, J.D., 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology 16(10): 463–471.

Hussain, M.B., Mehboob, I., Zahir, Z.A., Naveed, M., Asghar, H.N., 2009. Potential of Rhizobium spp. for improving growth and yield of rice (Oryza sativa L.).Soil & Environment 28(1): 49-55.

Jiménez-Gómez, A., Menéndez, E., Flores-Félix, J.D.,  García-Fraile, P., Mateos, P.F., Rivas, R., 2016. Effective colonization of spinach root surface by Rhizobium. In: González-Andrés, F., James, E. (Eds). Biological nitrogen fixation and beneficial plant-microbe interaction. Springer. pp. 109-122.

Khalid, A, Arshad, M., Zahir, Z.A., 2006. Phytohormones: microbial production and applications. In: Uphoff, N., Ball, A.S., Fernandes, E., Herren, H., Husson, O., Laing, M., Palm, C., Pretty, J., Sanchez, P., Sanginga, N., Thies, J. (Eds). Biological approaches to sustainable soil systems. Taylor &Francis/CRC, Boca Raton, pp. 207–220.

Kovar, M., Cerny, I., Ernst, D., 2016. Analysis of relations between crop temperature indices and yield of different sunflower hybrids foliar treated by biopreparations. Agriculture 62: 28−40.

Lupwayi, N. Z., Clyton, G.W., Hanson, K.G., Rice, W.A., Biederbeck, V.O., 2004. Endophytic rhizobia in barley, wheat and canola roots. Canadian Journal of Plant Sciences 84(1): 37-45.  

Madhaiyan, M., Poonguzhali, S., Ryu, J.H., Sa, T.M., 2006. Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase containing Methylobacterium fujisawaense. Planta 224(2): 268-278.  

Matiru, V.N., Dakora, F.D., 2004. Potential use of rhizobial bacteria as promoters of plant growth for increased yield in landraces of African cereal crops. African Journal of Biotechnology 3(1): 1-7.

Mehboob , I.,  Naveed, M., Zahir, Z.A., 2009. Rhizobial association with non-legumes: Mechanisms and applications. Critical Reviews in Plant Sciences 28(6): 432-456.

Mehboob, I., Zahir, Z.A., Mahboob, A., Shahzad, S.M., Jawad A., Arshad. M., 2008. Preliminary screening of Rhizobium isolates for improving growth of maize seedlings under axenic conditions. Soil and Environment 27: 64-71.

Mia, M.A.B., Shamsuddin, Z.H., 2010. Rhizobium as a crop enhancer and biofertilizer for increased cereal production. African Journal of Biotechnology 9(37): 6001-6009.

Mullen, M.D., 2005. Phosphorus in soils: biological interactions. In: Hillel, D. (Ed.). Encyclopedia of soils in the environment. Elsevier, Oxford, pp. 210–215.

Naveed, M., Hussain, M.B., Zahir, Z.A., Mitter, B., Sessitsch, A., 2014. Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regulation 73(2): 121-131.

Naveed, M., Mehboob, I., Hussain, M.B., Zahir, Z.A., 2015a. Perspectives of rhizobial inoculation for sustainablecrop production. In: Arora, N.K. (Ed.). Plant Microbes Symbiosis: Applied Facets. pp. 209-239.

Naveed, M., Qureshi, M.A., Zahir, Z.A., Hussain, M.B., Sessitsch, A., Mitter, B., 2015b. L-Tryptophan-dependent biosynthesis of indole-3-acetic acid (IAA) improves plant growth and colonization of maize by Burkholderia phytofirmans PsJN. Annals of Microbiology 65(3): 1381-1389.

Olsen, S. R., Sommers, L. E., 1982. Phosphorus. In: Page, A.L. (Ed.). Method of Soil analysis. Part 2: Chemical and microbiological properties. Argonomy No.9, 2nd edition, American Society of Agronomy, Madison, WI, USA. pp. 403-430.

Paungfoo-Lonhienne, C., Lonhienne, T.G.A., Yeoh, Y.K., Webb, R.I., Lakshmanan, P., Chan, C.X., Lim, P.E., Ragan, M.A., Schmidt, S., Hugenholtz, P., 2014. A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microbial Biotechnology 7(2): 142– 154.

Perrine-Walker, F.M., Gartner, E., Hocart, C.H., Becker, A., Rolfe, B.G., 2007. Rhizobium-inhibited rice growth inhibition caused by nitric oxide accumulation. Molecular Plant Microbe Interactions 20(3): 283–292.

Qureshi, M. A., Shahzad, H., Imran, Z., Mushtaq, M., Akhtar, N., Ali M.A., Mujeeb, F., 2013. Potential of Rhizobium species to enhance growth and fodder yield of maize in the presence and absence of L-tryptophan. The Journal of Animal & Plant Sciences 23(5): 1448-145.

Roy, M., Basu, P.S., 2004. Studies on root nodules of leguminous plants bioproduction of indole acetic acid by a Rhizobium sp. from a twiner Clitoria ternatea L. Acta Biotechnology 12(6): 453-460.

Russell, A.D., Hugo, W.B., Ayliffo, G.A.J., 1982. Principles and practices of disinfection, preservation and sterilization. Blackwell Scientific Publications, London, UK.

Sachdev, D.P., Chaudhari,H.G., Kasture, V.M., Dhavale, D.D., Chopade, B.A., 2009. Isolation and characterization of Indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum) and their effect on plant growth. Indian Journal of Experimental Biology 47(12): 993-1000.

Sarwar, M., Martens D.A., Arshad M., Frankenberger Jr., W.T., 1992. Tryptophan dependent biosynthesis of auxins in soil. Plant and Soil 147(2): 207-215.

Sessitsch, A., Howieson, J.G., Perret, X., Antoun, H., Martínez-Romero, E., 2002. Advances in Rhizobium research. Critical Reviews in Plant Sciences 21(4): 323-387.

Shah, N.A., Shah, H., Akmal, N., 2005. Sunflower area and production variability in Pakistan: opportunities and constraints. Helia 28(43): 165- 178.

Shahid, M., Hameed, S., Imran, A., Ali, S., van Elsas, J.D., 2012. Root colonization and growth promotion of sunflower (Helianthus annuus L.) by phosphate solubilizing Enterobacter sp. Fs-11. World Journal of Microbiology and Biotechnology 28(8): 2749–2758.

Shahid, M., Hameed, S., Tariq, M., Zafar, M., Ali, A., Ahmad, N., 2015. Characterization of mineral phosphate-solubilizing bacteria for enhanced sunflower growth and yield-attributing traits. Annual Microbiology 65(3): 1525–1536.

Steel, R.G.D., Torrie, J.H., Dickey, D.A., 1997. Principles and procedures of statistics. McGraw Hill Co. Inc. New York. USA.

Vincent, J.M., 1970. A manual for the practical study of root-nodule bacteria. IBP Handbook Number 15, Blackwell, Oxford.

Yang, J., Kloepper, J.W., Ryu, C.M., 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends in Plant Science 14(1): 1–4.

Yanni, Y.G., Rizk, R.Y., Abd El-Fattah, F.K., Squartini, A., Corich, V., Giacomini, A., de Bruijn, F., Rademaker, J., Maya-Flores, J., Ostrom, P., Vega-Hernandez, M., Hollingsworth, R.I., Martinez-Molina, E., Mateos, P., Velazquez, E., Wopereis, J., Triplett, E., Umali-Garcia, M., Anarna, A.J., Rolfe, B.G., Ladha, J.K., Hill, J., Mujoo, R., Ng, P.K., Dazzo, F.B., 2001. The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Functional Plant Biology 28(9): 845-870.