1Faculty of Agronomy, Vietnam National University of Agriculture, Ha Noi 131000, Vietnam
2Department of Biotechnology, College of Applied Arts and Sciences, National Formosa University, Yunlin 632, Taiwan
3Tetanti AgriBiotech Inc. No. 1, Taichung city 40755, Taiwan
Main Article Content
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.
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.