Host Genotype and Edaphic Factors Cumulatively Influence the Occurrence of Siderophore-producing Bacteria Associated with Rice (Oryza sativa L.)

Date Received: Apr 05, 2021

Date Published: Mar 30, 2022

Views

1325

Download

300

How to Cite:

Thuy, P., Chung, W.-C., & Young, L.-S. (2022). Host Genotype and Edaphic Factors Cumulatively Influence the Occurrence of Siderophore-producing Bacteria Associated with Rice (Oryza sativa L.). Vietnam Journal of Agricultural Sciences, 5(1), 1313–1325. https://doi.org/10.31817/vjas.2022.5.1.01

Host Genotype and Edaphic Factors Cumulatively Influence the Occurrence of Siderophore-producing Bacteria Associated with Rice (Oryza sativa L.)

Phan Thi Thuy (*) 1 , Chung Wei-Ching 2   , Young Li-Sen 3

  • Corresponding author: ptthuy.hua.edu@gmail.com
  • 1 Faculty of Agronomy, Vietnam National University of Agriculture, Ha Noi 131000, Vietnam
  • 2 Department of Biotechnology, College of Applied Arts and Sciences, National Formosa University, Yunlin 632, Taiwan
  • 3 Tetanti AgriBiotech Inc. No. 1, Taichung city 40755, Taiwan
  • Keywords

    Seed endosphere, rhizosphere, dissemination, siderophore, Fe sequestration

    Abstract


    Seed-borne rice endophytes are capable of disseminating into host plant tissues as well as to their rhizosphere. Here, we investigated the occurrence of siderophore-producing bacteria (SPB) in the seed endospheres of two distinct rice (Oryza sativa L.) cultivars, TK8 (ssp. japonica) and TCN1 (ssp. indica), and their dissemination into the rhizospheres through culture-dependent methods. Their patterns of occurrence in the rhizospheres as well as in the root and shoot tissues of 30 day-old cultivars grown in three different kinds of soils were tested. The significance of SPB on Fe sequestration of TCN1 was studied using Enterobacter sp. LS-756. TK8 seeds were found to be not only abundant in endopsheric SPB (> 10-fold), but also exhibited enhanced SPB dissemination into the rhizosphere (1.3-fold) as compared to TCN1. The proportion of endophytic SPB was consistently higher in roots than in shoots, and it was found to decline with decreasing soil pH. A similar declining trend was further evident through the analysis of SPB composition in the rhizospheric and bulk soils. LS-756-inoculated TCN1 seedlings under low availability of Fe showed 32%, 178%, and 368% increases in Fe, chlorophyll, and chlorophyll b contents as compared to the uninoculated controls. Thus, the occurrence of seed-borne endophytic SPB and their dissemination into the rhizosphere vary significantly according to the rice genotype. Higher co-occurrence of SPB in the rhizosphere and internal root tissues of rice plants grown under Fe-limited conditions and the enhanced Fe uptake due to SPB inoculation substantiated their potential involvement in Fe sequestration.

    References

    Ahmad F. & Ahmad I. (2013). Assessment of microbial assortment in agricultural soil of district Aligarh, Uttar Pradesh, India. World Journal of Applied Sciences and Research. 3: 1-8.

    Ahmed E. & Holmström S. J. M. (2014). Siderophores in environmental research: roles and applications. Microbial Biotechnology. 7: 196-208.

    Andreote F. D., Gumiere T. & Durrer A. (2014). Exploring interactions of plant microbiomes. Scientia Agricola. 71: 528-539.

    Aznar A., Chen N. W. G., Thomine S. & Dellagi A. (2015). Immunity to plant pathogens and iron homeostasis. Plant Science. 240: 90-97.

    Barraquio W. L., Revilla L. & Ladha J. K. (1997). Isolation of endophytic diazotrophic bacteria from wetland rice. Plant Soil. 194: 15-24.

    Belkhodja R., Morales F., Quilez F., Lopez-Millan A. F., Abadia A. & Abadia J. (1998). Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the photosystem II acceptor side. Photosynthesis Research. 56: 265-276.

    Boopathi E. & Sankara R. K. (1999). A siderophore from Pseudomonas putida type A1: structural and biological characterization. Biochimica et Biophysica Acta. 1435: 30-40.

    Botta A. L., Santacecilia A., Ercole C., Cacchio P. & Del Gallo M. (2013). In vitro and in vivo inoculation of four endophytic bacteria on Lycopersicon esculentum. New Biotechnology. 30: 666-674.

    Bremner J. M. & Mulvaney C. S. (1982). Nitrogen total. In: Page A. L., Miller R. H. & Kenney D. R. (Eds.) Methods of soil analysis. Part 2 – microbiological and biochemical properties. New York: Soil Science Society of America (SSA book series, 5). 595-624.

    Carvalhais L. C., Muzzi F., Tan C. H., Hsien-Choo J. & Schenk P. M. (2013). Plant growth in Arabidopsis is assisted by compost soil-derived microbial communities. Frontiers Plant Science. 4. DOI: 10.3389/fpls.2013.00235.

    Chaudhary H. J., Peng G. X., Hu M., He Y. M., Yang L. J., Luo Y. & Tan Z. Y. (2012). Genetic diversity of endophytic diazotrophs of the wild rice, Oryza alta and identification of the new diazotroph, Acinetobacter oryzae sp. nov. Microbial Ecology. 63: 813-821.

    Compant S., Christophe C. & Sessitsch A. (2010). Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biology & Biochemistry. 42: 669-678.

    Costa R., Gotz M., Mrotzek N., Lottmann J., Berg G. & Smalla K. (2006). Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiology Ecology. 56: 236-249.

    Edwards U., Rogall T., Blocker H., Emde M. & Bottger E. C. (1989). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research. 17: 7843-7853.

    Elbeltagy A., Nishioka K., Suzuki H., Sato T., Sato Y. I. & Morisaki H. (2000). Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Science and Plant Nutrition. 46: 617-629.

    Engelhard M., Hurek T. & Reinhold-Hurek B. (2000). Preferential occurrence of diazotrophic endophytes, Azoarcus spp., in wild rice species and landraces of Oryza sativa in comparison with modern races. Environmental Microbiology. 2: 131-141.

    Fujii T., Huang Y. D., Higashitani A., Nishimura Y., Iyama S., Hirota Y., Yoneyama Y. & Dixon R. A. (1987). Effect of inoculation with Klebsiella oxytoca and Enterobacter cloacae on dinitrogen fixation by rice-bacteria associations. Plant and Soil. 103: 221-226.

    Gaonkar T. & Bhosle S. (2013). Effect of metals on a siderophore producing bacterial isolate and its implications on microbial assisted bioremediation of metal contaminated soils. Chemosphere. 93: 1835-1843.

    Gunes A., Alpaslan M. & Inal A. (2008). Critical nutrient concentrations and antagonistic and synergistic relationships among the nutrients of NFT-grown young tomato plants. Journal of Plant Nutrition. 21: 2035-2047.

    Hallmann J., Quadt-Hallmann A., Mahaffee W. F. & Kleopper J. W. (1997). Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology. 43: 895-914.

    Hameed A., Yeh M. W., Hsieh Y. T., Chung W. C., Lo C. T. & Young L. S. (2015). Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant and Soil. 394: 177-197.

    Hansch R. & Mendel R. R. (2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology. 12: 259-266.

    Hardoim P. R., Hardoim C. C., van Overbeek L. S. & van Elsas J. D. (2012). Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7: e30438.

    Jones J. B. (2001). Laboratory guide for conducting soil tests and plant analysis. CRC, Boca Raton. 363.

    Joseph B., Ranjan Patra R. & Lawrence R. (2007). Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). International Journal of Plant Production. 2: 141-152.

    Joshi P., Tyagi V. & Bhatt A. B. (2011). Characterization of rhizobacteria diversity isolated from Oryza sativa cultivated at different altitudes in North Himalaya. Advances in Applied Science Research. 2: 208-216.

    Kaga H., Mano H., Tanaka F., Watanabe A., Kaneko S. & Morisaki H. (2009). Rice seeds as sources of endophytic bacteria. Microbes Environment. 24: 154-162.

    Katiyar V. & Goel R. (2004). Siderophore mediated plant growth promotion at low temperature by mutant of fluorescent pseudomonad. Plant Growth Regulation. 42: 239-244.

    Kumar U., Vithal kumar L. & Annapurna K. (2013). Antagonistic potential and functional diversity of endo and rhizospheric bacteria of basmati rice. Oryza. 50: 162-168.

    Liu H. W., Carvalhais L. C., Crawford M., Singh E., Dennis P. G., Pieterse C. M. J. & Schenk P. M. (2017). Inner plant values: diversity, colonization and benefits from endophytic bacteria. Frontiers in Microbiology. 8. DOI: 10.3389/fmicb.2017.02552.

    Loaces I., Ferrando L. & Scavino A. F. (2011). Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microbial Ecology. 61: 606-618.

    Lucena J. J. (2006). Synthetic iron chelates to correct iron deficiency in plants. In: Barton L. L. & Abadía J. (Eds.). Iron Nutrition in Plants and Rhizospheric Microorganisms. Springer, Netherlands. 103-128.

    Lynch J. M. (1995). Microbial activity in acid soils. Plant-Soil Interactions at Low pH: Principles and Management. Developments in Plant and Soil Science. 64: 167-172.

    Mano H., Tanaka F., Watanabe A., Kaga H., Okunishi S. & Morisaki H. (2006). Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environment. 21: 86-100.

    Mano H., Tanaka F., Nakamura C., Kaga H. & Morisaki H. (2007). Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environment. 22: 175-185.

    Mano H. & Morisaki H. (2008). Endophytic bacteria in the rice plant. Microbes Environment. 23: 109-117.

    Miethke M. & Marahiel M. A. (2007). Siderophore-based iron acquisition and pathogen control. Microbiology and Molecular Biology Reviews. 71: 413-451.

    Mori S., Nishizawa N., Hayashi H., Chino M., Yoshimura E. & Ishihara J. (1991). Why are young rice plants highly susceptible to iron deficiency? Plant and Soil. 130: 143-156.

    Naureen Z., Hafeez F. Y., Hussain J., Harrasi A. A., Bouqellah N. & Roberts M. R. (2015). Suppression of incidence of Rhizoctonia solani in rice by siderophore producing rhizobacterial strains based on competition for iron. European Scientific Journal. 11: 186-207.

    Neilands J. B. (1995). Siderophore: Structure and function of microbial iron transport compounds. The Journal of Biological Chemistry. 270: 26723-26726.

    Okunishi S., Sako K., Mano H., Imamura A. & Morisaki H. (2005). Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environment. 20: 168-177.

    Prakamhang J., Minamisawa K., Teamtaisong K., Boonkerd N. & Teaumroong N. (2009). The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Applied Soil Ecology. 42: 141-149.

    Prasad P. V. V. (2003). Plant nutrition: iron chlorosis. In: Thomas B., Murray B. G. & Murphy D. J. (Eds.). Encyclopedia of Applied Plant Sciences. London, UK, Elsevier. 649-656.

    Radzki W., Gutierrez Manero F. J., Algar E., Lucas Garcia J. A., Garcia-Villaraco A. & Ramos S. B. (2013). Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Antonie Van Leeuwenhoek. 104: 321-330.

    Rajkumar M., Ae N., Prasad M.N.V. & Freitas H. (2010). Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnology. 28: 142-149.

    Rungin S., Indananda C., Suttiviriya P., Kruasuwan W., Jaemsaeng R. & Thamchaipenet A. (2012). Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek. 102: 463-472.

    Schmidt W. (1999). Mechanisms and regulation of reduction-based iron uptake in plants. New Phytologist. 141: 1-26.

    Schwyn B. & Neilands J. B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry. 160: 47-56.

    Sessitsch A., Hardoim P., Doring J., et al. (2012). Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Molecular Plant-Microbe Interactions. 25: 28-36.

    Sharma A. & Johri B. N. (2003). Growth promoting influence of siderophore-producing Pseudomonas strains GRP3Aand PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiological Research. 158: 243-248.

    Sullivan T. S., Ramkissoon S., Garrison V. H., Ramsubhag A. & Thies J. E. (2012). Siderophore production of African dust microorganisms over Trinidad and Tobago. Aerobiologia. 28: 391-401.

    Sun L., Qiu F. B., Zhang X. X., Dai X., Dong X. Z. & Song W. (2008). Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microbial Ecology. 55: 415-424.

    Verma V. C., Singh S. K. & Prakash S. (2011). Bio-control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss. Journal of Basic Microbiology. 51: 550-556.

    Vieire F. C. S. & Nahas E. (2005). Comparison of microbial numbers in soils by using various culture media and temperatures. Microbiological Research. 160: 197-202.

    Walitang D., Kim K., Madhaiyan M., Kim Y. K., Kang Y. & Sa T. (2017). Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of Rice. BMC Microbiology. 17. DOI: 10.1186/s12866-017-1117-0.

    Wang M., Eyre A. W., Thon M. R., Oh Y. & Dean R. A. (2020). Dynamic changes in the microbiome of rice during shoot and root growth derived from seeds. Frontiers in Microbiology. 11. DOI: 10.3389/fmicb.2020.559728.

    Wilson M., He Z. & Yang X. (2004). The Red Soils of China: Their Nature, Management and Utilization. DOI:10.1007/978-1-4020-2138-1.

    Yasmin H., Bano A., Samiullah, Naz R., Farooq U., Nosheen A. & Fahad S. (2012). Growth promotion by P-solubilizing, siderophore and bacteriocin producing rhizobacteria in Zea mays L. Journal of Medicinal Plants Research. 6: 553-559.

    Young L. S., Hameed A., Peng S. Y., Shan Y. H. & Wu S. P. (2013). Endophytic establishment of the soil isolate Burkholderia sp. CC-Al74 enhances growth and P-utilization rate in maize (Zea mays L.). Applied Soil Ecology. 66: 40-47.

    Yu S., Teng C., Bai X., Liang J., Song T., Dong L., Jin Y. & Qu J. (2017). Optimization of siderophore production by Bacillus sp. PZ-1 and its potential enhancement of phytoextration of Pb from soil. Journal of Microbiology and Biotechnology. 27: 1500-1512.

    Yu X., Ai C., Xin L. & Zhou G. (2011). The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. European Journal of Soil Biology. 47: 138-145.