New bacteria genera associated with rice (Oryza sativa L.) in Cuba promote the crop growth
DOI:
https://doi.org/10.15517/am.v33i2.47223Keywords:
bacterial isolation, molecular identification, rhizosphere, grass, plant growth promotionAbstract
Introduction. The rice cultivar INCA LP-7 is one of the eleven principal cultivars in Cuba due to their high yield potential, salinity tolerance, and pathogens resistance. However, there are not reports about the isolation, identification, and characterization of bacteria associated to this cultivar that promote its growth. Objective. To select promising bacteria from the rhizosphere of the INCA LP-7 rice cultivar to promote the crop growth. Materials and methods. The investigation was carried out in 2015 and 2016 at the Instituto Nacional de Ciencias Agropecuarias, Cuba and Instituto de Investigaciones Biologicas Clemente Estable, Uruguay. The 16SrNA gene of bacteria associated with the INCA LP-7 rice cultivar was isolated and identified by sequencing. Characterization was performed as plant growth promoting bacteria and the effect of bacterial inoculation on rice growth was studied. Results. Eleven rizopheric bacteria were isolated from rice plants of the INCA LP-7cultivar. A phylogenetic analysis showed that for the first time in Cuba Pantoea, Acinetobacter, and Mitsuaria genera were reported associated with rice. Rhizobium and Enterobacter genera were also informed as rhizospheric bacteria of INCA LP-7 rice cultivar. Some isolates solubilize inorganic phosphates and potassium, produce siderophores and indolic compound, had exo-celulase and protease activity and formed biofilm. The inoculation of isolates belonging to Pantoea genus produced an increase in height, root length, and biomass of rice plants under greenhouse conditions. Conclusions. Pantoea sp. GG1 and Pantoea sp. GG2 were the most promising strains for the inoculation of the INCA LP-7 rice cultivar. This is the first report in Cuba that focuses on the characterization of the bacterial microbiota part associated to Cuban rice cultivar INCA LP-7 and reports bacteria of the Pantoea genus as crop growth promoters.
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Ansari, F. A., & Ahmad, I. (2018). Biofilm development, plant growth promoting traits and rhizosphere colonization by Pseudomonas entomophila FAP1: a promising PGPR. Advances in Microbiology, 8(3), 235–251. https://doi.org/10.4236/aim.2018.83016
Bakhshandeh, E., Pirdashti, H., & Lendeh, K. S. (2017). Phosphate and potassium-solubilizing bacteria effect on the growth of rice. Ecological Engineering, 103(part A), 164–169. https://doi.org/10.1016/j.ecoleng.2017.03.008
Bellabarba, A., Fagorzi, C., DiCenzo, G. C., Pini, F., Viti, C., & Checcucci. A. (2019). Deciphering the symbiotic plant microbiome: Translating the most recent discoveries on rhizobia for the improvement of agricultural practices in metalcontaminated and high saline lands. Agronomy, 9(9), 529–550. https://doi.org/10.3390/agronomy9090529
Berge, O., Lodhi, A., Brandelet, G., Santaella, C., Roncato, M. A., Christen, R., Heulin, T., & Achouak, W. (2009). Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. International Journal of Systematic and Evolutionary Microbiology, 59(2), 367–372. https://doi.org/10.1099/ijs.0.000521-0
Classen, A. T., Sundqvist, M. K., Henning, J. A., Newman, G. S., Moore, J. A. M., Cregger, M. A., Moorhead, L. C., & Patterson, C. M. (2015). Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere, 6(8), 1–21. https://doi.org/https://doi.org/10.1890/ES15-00217.1
Cui, D., Huang, M. T., Hu, C. Y., Su, J. B., Lin, L. H., Javed, T., Deng, Z. H., & Gao, S. J. (2020). First report of Pantoea stewartii subsp. stewartii causing bacterial leaf wilt of sugarcane in China. Plant Disease, 105(41), 1990–1990. https://doi.org/10.1094/PDIS-09-20-2015-PDN
Das, K., Rajawat, M. V. S., Saxena, A. K., & Prasanna, R. (2017). Development of Mesorhizobium ciceri-based biofilms and analyses of their antifungal and plant growth promoting activity in chickpea challenged by Fusarium wilt. Indian Journal of Microbiology, 57(1), 48–59. https://doi.org/10.1007/s12088-016-0610-8
de los Santos, M. C., Taulé, C., Mareque, C., Beracochea, M., & Battistoni, F. (2015). Identification and characterization of the part of the bacterial community associated with field-grown tall fescue (Festuca arundinacea) cv. SFRO Don Tomás in Uruguay. Annals of Microbiology, 66, 329–342. https://doi.org/10.1007/s13213-015-1113-2
Fahad, S., Adnan, M., Noor, M., Arif, M., Alam, M., Ali Khan, I., Ullah, H., Wahid, F., Mian, I. A., Jamal, Y., Basir, A., Hassan, S., Saud, S., Riaz, A. M., Wu, Ch., Khan, M. A., & Wang, D. (2019). Major constraints for global rice production. In M. Hasanuzzaman, M. Fujita, K. Nahar, & J. K. Biswas (Eds.), Major Constraints for Global Rice Production. Advances in rice research for abiotic stress tolerance (Chapter 1, pp. 1–22). Woodhead Publishing. https://doi.org/10.1016/B978-0-12-814332-2.00001-0
Fan, X., Cai, K., Wen, F., & Cai, Y. (2016). Effects of silicon on morphology, ultrastructure and exudates of rice root under heavy metal stress. Acta Physiologiae Plantarum, 38, Article 197. https://doi.org/10.1007/s11738-016-2221-8
Fang, K., Wang, Y. Z., & Zhang, H. B. (2019). Differential effects of plant growth-promoting bacteria on invasive and native plants. South African Journal of Botany, 124, 94–101. https://doi.org/10.1016/j.sajb.2019.04.007
Fernández, L., Ortega, E., Kleiner, D., Ortega-Rodés, P., Rodes, R., & Dong, Z. (2004). A putative new endophytic nitrogen-fixing bacterium Pantoea sp. from sugarcane. Journal of Applied Microbiology, 97(3), 504–511. https://doi.org/10.1111/j.1365-2672.2004.02329.x
Ferreira, C. M., Vilas-Boas, Â., Sousa, C. A., Soares, H. M., & Soares, E. V. (2019). Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions. AMB Express, 9, Article 78. https://doi.org/10.1186/s13568-019-0796-3
Food and Agriculture Organization. (2019). Food outlook biannual report on global food markets. Retrieved January 22, 2021, from http://www.fao.org/economic/est/est-commodities/oilcrops/oilcrop-policies/en/
Gandhi, A., & Muralidharan, G. (2016). Assessment of zinc solubilizing potentiality of Acinetobacter sp. isolated from rice rhizosphere. European Journal of Soil Biology, 76, 1–8. https://doi.org/10.1016/j.ejsobi.2016.06.006
García, J. C., Hernández, A., Acebo, Y., & Rives, N. (2008). Obtención de un nuevo método de desinfección de semillas de arroz. Cultivos Tropicales, 29, 55–59.
García, F., Muñoz, H., Carreño, C., & Mendoza, G. (2010). Caracterización de cepas nativas de Azospirillum spp. y su efecto en el desarrollo de Oryza sativa L. en Lambayeque. Scientia Agropecuaria, 1(2), 107–116. https://doi.org/10.17268/sci.agropecu.2010.02.01
Gholamalizadeh, R., Khodakaramian, G., & Ebadi, A. A. (2017). Assessment of rice associated bacterial ability to enhance rice seed germination and rice growth promotion. Brazilian Archives of Biology and Technology, 60, Article e17160410. https://doi.org/10.1590/1678-4324-2017160410
Gómez Padilla, E., Ruiz-Díez, B., Fajardo, S., Eichler-Loebermann, B., Samson, R., van Damme, P., López R., & Fernández-Pascual, M. (2017). Caracterización de rizobios aislados de nódulos de frijol Caupí, en suelos salinos de Cuba. Cultivos Tropicales, 38(4), 39–49.
Groth, M., Takeda, N., Perry, J., Uchida, H., Dräxl, S., Brachmann, A., Sato S., Tabata, S, Kawaguchi M., Wang T. L., & Parniske, M. (2010). NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell, 22(7), 2509–2526. https://doi.org/10.1105/tpc.109.069807
Heracle BioSoft SRL. (2020). Automatic DNA sequence assembler [Data set]. http://www.dnabaser.com/
Hernández Forte, I., & Nápoles García, M. C. (2017). Rizobios residentes en la rizosfera de plantas de arroz (Oryza sativa L.) cultivar INCA LP-5. Cultivos Tropicales, 38(1), 39–49.
Hernández-Jiménez, A., Pérez-Jiménez, J. M., Bosch-Infante, D., & Castro Speck, N. (2015). Clasificación de los suelos de Cuba. Ediciones INCA.
Hernández-Rodríguez, A., Rives-Rodríguez, N., Díaz de la Osa, A., de la Fe-Pérez, Y., Pijeira-Fernández, G., & Divan-Baldani, V. L. (2016). Caracterización de bacterias diazotróficas asociativas con actividad promotora del crecimiento vegetal en Oryza sativa L. Revista Cubana de Ciencias Biológicas, 5(2), 1–9. http://www.rccb.uh.cu/index.php/RCCB/article/view/157/266
Islam, A., & Muttaleb, A. (2016). Effect of potassium fertilization on yield and potassium nutrition of boro rice in a wetland ecosystem of Bangladesh. Archives of Agronomy and Soil Science, 62(11), 1530–1540. https://doi.org/10.1080/24749508.2017.1361145
Jayasekara, S., & Ratnayake, R. (2019). Microbial cellulases: an overview and applications. In A. Rodríguez Pascual, & M. E. Eugenio Martin (Eds.), Cellulose. IntechOpen. https://doi.org/10.5772/intechopen.84531
Jiang, Z., Zhang, X., Wang, Z., Cao, B., Deng, S., Bi, M., & Zang, Y. (2019). Enhanced biodegradation of atrazine by Arthrobacter sp. DNS10 during co-culture with a P solubilizing bacteria: Enterobacter sp. P1. Ecotoxicology Environmental Safety, 172, 159–166. https://doi.org/10.1016/j.ecoenv.2019.01.070
Kaminsky, L. M., Trexler, R. V., Malik, R. J., Hockett, K. L., & Bell, T. H. (2019). The inherent conflicts in developing soil microbial inoculants. Trends in Biotechnology, 37(2), 140–151. https://doi.org/10.1016/j.tibtech.2018.11.011
Kim, S. J., Lee, C. M., Han, B. R., Kim, M. Y., Yeo, Y. S., Yoon, S. H., Koo, B. S., & Jun, H. K. (2008). Characterization of a gene encoding cellulase from uncultured soil bacteria. FEMS Microbiology Letters, 282(1), 44–51. https://doi.org/10.1111/j.1574-6968.2008.01097.x
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
Liu, H., Zhang, C., Yang, J., Yu, N., & Wang, E. (2018). Hormone modulation of legume-rhizobial symbiosis. Journal of Integrative Plant Biology, 60(8), 632–648. https://doi.org/10.1111/jipb.12653
Mahato, S., & Kafle, A. (2018). Comparative study of Azotobacter with or without other fertilizers on growth and yield of wheat in Western hills of Nepal. Annals of Agrarian Science, 16(3), 250–256. https://doi.org/10.1016/j.aasci.2018.04.004
Marag, P. S., & Suman, A. (2018). Growth stage and tissue specific colonization of endophytic bacteria having plant growth promoting traits in hybrid and composite maize (Zea mays L.). Microbiological Research, 214, 101–113. https://doi.org/10.1016/j.micres.2018.05.016
Mareque, C., Taulé, C., Beracochea, M., & Battistoni, F. (2015). Isolation, characterization and plant growth promotion effects of putative bacterial endophytes associated with sweet sorghum (Sorghum bicolor (L) Moench). Annals of Microbiology, 65(2), 1057–1067. https://doi.org/10.1007/s13213-014-0951-7
Martínez-Rosales, C., & Castro-Sowinski, S. (2011). Antartic bacterial isolates that produce cold-active extracellular proteases at low temperature but are active and stable at high temperature. Polar Reserch, 30(1), 7123–7131. https://doi.org/10.3402/polar.v30i0.7123
Megías, E., Megías, M., Ollero, F.J., & Hungria, M. (2016). Draft genome sequence of Pantoea ananatis strain AMG521, a rice plant growth-promoting bacterial endophyte isolated from the Guadalquivir marshes in southern Spain. Genome Announcements, 4(1), Article e01681-15. https://doi.org/10.1128/genomeA.01681-15
Paula, A. J., Hwang, G., & Koo, H. (2020). Dynamics of bacterial population growth in biofilms resemble spatial and structural aspects of urbanization. Nature Commun, 11(1), Article 1354. https://doi.org/10.1038/s41467-020-15165-4
Peeters, E., Nelis, H. J., & Coenye, T. (2008). Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods, 72(2), 157–165. https://doi.org/10.1016/j.mimet.2007.11.010
Pérez, N. J., González Cepero, M. C., Cristo Valdés, E., Díaz Solís, S. H., Díaz Valdés, E. C., & Blanco Reinoso, G. (2015). Cultivares cubanos de arroz. GeoTech. http://repositorio.geotech.cu/jspui/bitstream/1234/1477/1/Cultivares%20cubanos%20de%20arroz.pdf
Rajeswari, P., & Kapoor, R. (2017). Combined application of different species of Trichoderma and Pseudomonas fluorescens on the cellulolytic enzymes of Fusarium oxysporum for the control of Fusarium Wilt diseasei Arachis hypogaea. L. Bioscience Biotechnology Research Asia, 14(3), 1169–1176. https://doi.org/10.13005/bbra/2557
Rives, N., Acebo, Y., & Hernández, A. (2007). Bacterias promotoras del crecimiento vegetal en el cultivo del arroz (Oryza sativa L.). Perspectivas de su uso en Cuba. Cultivos Tropicales, 28(2), 29–38.
Rives, N., Hernández, A., Acebo, Y., & Heydrich, M. (2006). Caracterización de algunos géneros bacterianos asociados al cultivo del arroz variedad J-104. Revista Cubana del Arroz, 2, 7–13.
Rives, N., Vega, M., Díaz, A., Acebo, Y., Muñiz, O., & Hernández, A. (2010). Aislamiento y caracterización molecular de bacterias endófitas fijadoras de nitrógeno asociadas a 4 variedades comerciales de arroz. Revista Cubana del Arroz, 12, 68–82.
Schwyn, B., & Neilands, J. B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160(1), 47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Shahzad, R., Waqas, M., Khan, A. L., Al-Hosni, K., Kang, S. M., Seo, C. W., & Lee, I. J. (2017). Indoleacetic acid production and plant growth promoting potential of bacterial endophytes isolated from rice (Oryza sativa L.) seeds. Acta Biologica Hungarica, 68(2), 175–186. https://doi.org/10.1556/018.68.2017.2.5
Singh, H., Jaiswal, V., Singh, S., Tiwari, S. P., Singh, B., & Katiyar, D. (2017). Antagonistic compounds producing plant growth promoting rhizobacteria: a tool for management of plant disease. Journal of Advances of Microbiology Research, 3(4), 1–12. https://doi.org/10.9734/JAMB/2017/33368
Suman, A., Yadav, A. N., & Verma, P. (2016). Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In D. P. Singh, H. B. Singh, & R. Prabba (Eds.) Microbial inoculants in sustainable agricultural productivity (pp. 117–144). Springer. https://doi.org/10.1007/978-81-322-2647-5_7
Tahir, M., Naeem, M. A., Shahid, M., Khalid, U., Farooq, A. B. U., Ahmad, N., Ahmad, I., Arshad, M., & Waqar, A. (2020). Inoculation of pqqE gene inhabiting Pantoea and Pseudomonas strains improves the growth and grain yield of wheat with a reduced amount of chemical fertilizer. Journal of Applied Microbiology, 129(3), 575–589. https://doi.org/10.1111/jam.14630
Taulé, C., Mareque, C., Barlocco, C., Hackembruch, F., Reis, V. M., Sicardi, M., & Battistoni, F. (2011). The contribution of nitrogen fixation to sugarcane (Saccharum officinarum L.), and the identification and characterization of part of the associated diazotrophic bacterial community. Plant Soil, 356(1–2), 35–49. https://doi.org/10.1007/s11104-011-1023-4
Tejera-Hernández, B., Heydrich-Pérez, M., & Rojas-Badía, M. M. (2013). Aislamiento de Bacillus solubilizadores de fosfatos asociados al cultivo del arroz. Agronomía Mesoamericana, 24(2), 357–364. https://doi.org/10.15517/AM.V24I2.12535
Vejan, P., Abdullah, R., Khadiran, T., Ismail, S., & Nasrulhaq-Boyce, A. (2016). Role of plant growth promoting rhizobacteria in agricultural sustainability: a review. Molecules, 21(5), Article 573. https://doi.org/10.3390/molecules21050573
Velazco, A., & Castro, R. (1999). Estudio de la inoculación de Azospirillum brasilense en el cultivo del arroz (Variedad A´82) en condiciones de macetas. Cultivos Tropicales, 20(1), 5–9. https://ftp.inca.edu.cu/revista/1999/1/CT20101.pdf
Vincent, J. M. (1970). A manual for the practical study of root-nodule bacteria. International Programme Handbook.
Walitang, D. I., Kim, K., Kim, Y., Kang, Y. K., & Kim, S. T. (2018). The influence of host genotype and salt stress on the seed endophytic community of salt-sensitive and salt-tolerant rice cultivars. BMC Plant Biology, 18, Article 51. https://doi.org/10.1186/s12870-018-1261-1
Yanni, Y. G., & Dazzo, F. B. (2015). Occurrence and ecophysiology of the natural endophytic Rhizobium–rice association and translational assessment of within the Egypt Nile delta. In F. J. de Bruijn (Ed), Biological nitrogen fixation (Vol 2, pp. 1125–1142), John Wiley & Sons Inc. Published.
Zhang, J., Zhang, C., Yang, J., Zhang, R., Gao, J., Zhao, X., Zhao, J., Zhao, D., & Zhang, X. (2018). Insights into Endophytic Bacterial Community Structures of Seeds Among Various Oryza sativa L. Rice Genotypes. Journal of Plant Growth Regulation, 38(1), 93–102. https://doi.org/10.1007/s00344-018-9812-0
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