Potential seed germination-enhancing plant growth-promoting rhizobacteria for restoration of Pinus chiapensis ecosystems

Abstract

Rhizosphere soil samples of three Pinus chiapensis sites were analyzed for their physicochemical properties, soil bacteria isolated and screened in vitro for growth-promoting abilities. Nine isolates that showed promise were identified to five genera Dyella, Luteimonas, Enterobacter, Paraburkholderia and Bacillus based on the sequences of 16S rRNA gene. All the strains were isolated from non-disturbed stands. These bacteria significantly decreased germination time and increased sprout sizes. Indole acetic acid and gibberellin production and phosphate solubilisation were detected. Results indicate that these biochemicals could be essential for P. chiapensis distribution and suggest the possibility that PGPR inoculation on P. chiapensis seeds prior to planting could improve germination and possibly seedling development.

Keywords

Pinus chiapensis / Plant growth-promoting rhizobacteria / Dyella / Luteimonas / Enterobacter

References

[1] Abbas R, Rasul S, Aslam K, Baber M, Shahid M, Mubeen F, Naqqash T. Halotolerant PGPR: a hope for cultivation of saline soils. J King Saud Univ Sci, 2019, 31(4): 1195-1201.

[2] Alba LMP, González EM, Ramírez MN, Castillo SMA. Determinantes de la distribución de Pinus spp. en la altiplanicie central de Chiapas. México Bol Soc Bot Mex, 2003, 73: 7-15.

[3] Anand R, Grayston S, Chanway C. N2-fixation and seedling growth promotion of lodgepole pine by endophytic Paenibacillus polymyxa. Microb Ecol, 2013, 66(2): 369-374.

[4] Andreolli M, Lampis S, Poli M, Gullner G, Biró B, Vallini G. Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons. Chemosphere, 2013, 92(6): 688-694.

[5] Angulo VC, Sanfuentes EA, Rodríguez F, Sossa KE. Characterization of growth-promoting rhizobacteria in Eucalyptus nitens seedlings. Rev Argent Microbiol, 2014, 46(4): 338-347.

[6] Barriuso J, Ramos SB, Santamaría C, Daza A, Gutiérrez MFJ. Effect of inoculation with putative plant growth-promoting rhizobacteria isolated from Pinus spp. on Pinus pinea growth, mycorrhization and rhizosphere microbial communities. J Appl Microbiol, 2008, 105: 1298-1309.

[7] Birgit K, Marc AC, Gerhard LM. Plant hormone interactions during seed dormancy release and germination. Seed Sci Res, 2005, 15: 281-307.

[8] Candau R, Avalos J, Cerda-Olmedo E. Regulation of gibberellin biosynthesis in Gibberella fujikuroi. Plant Physiol, 1992, 100(3): 1184-1188.

[9] Chakraborty P, Sarker RK, Roy R, Ghosh A, Maiti D, Tribedi P. Bioaugmentation of soil with Enterobacter cloacae AKS7 enhances soil nitrogen content and boosts soil microbial functional-diversity. 3 Biotech, 2019, 9: 253.

[10] Cheng J, Zhang MY, Wang WX, Manikprabhu D, Salam N, Zhang TY, Wu YY, Li WJ, Zhang YX. Luteimonas notoginsengisoli sp. nov., isolated from rhizosphere. Int J Syst Evol Microbiol, 2016, 66(2): 946-950.

[11] Contreras M, Loeza PD, Villegas J, Farias R, Santoyo G. A glimpse of the endophytic bacterial diversity in roots of blackberry plants (Rubus fruticosus). Genet Mol Res, 2016, 15(3): 1-10.

[12] Das A, Osborne JW. Monitoring the stress resistance of Pennisetum purpureum in Pb (II) contaminated soil bioaugmented with Enterobacter cloacae as defence strategy. Chemosphere, 2018, 210: 495-502.

[13] Del Castillo RF, Acosta S. Ethnobotanical notes on Pinus strobus var. chiapensis. Anales del instituto Biología. Serie Botánica, 2002, 73(2): 319-327.

[14] Del Castillo RF, Trujillo AS, Sáenz RC. Pinus chiapensis, a keystone: genetics, ecology and conservation. For Ecol Manag, 2009, 257: 2201-2208.

[15] Dixon JB. Roles of clays in soils. Appl Clay Sci, 1991, 5(5–6): 489-503.

[16] Donahue JK, Dvorak WS, Gutierrez EA. The Distribution, ecology, and gene conservation of Pinus ayacahuite and Pinus chiapensis in Mexico and Central America, 1991, College of Forest Resources No: North Carolina State University 8

[17] Dvorak WS, Donahue JK, Vasquez JA. Provenance and progeny results for the tropical white pine, Pinus chiapensis, at five and eight years of age. New For, 1996, 12: 125-140.

[18] Eberl L, Vandamme P. Members of the genus Burkholderia: good and bad guys. F1000Res, 2016, 5: 1007.

[19] Esmaeel Q, Vilanova ML, Rondeau M, Leclère V, Clément C, Jacquard C, Sanchez L, Ait BE. Paraburkholderia phytofirmans PsJN-Plants interaction: from perception to the induced mechanisms. Front Microbiol, 2018, 9: 2093.

[20] Finkmann W, Altendorf K, Stackebrandt E, Lipski A. Characterization of N₂O-producing Xanthomonas-like isolates from biofilters as Stenotrophomonas nitritireducens sp. nov., Luteimonas mephitis gen. nov., sp. nov. and Pseudoxanthomonas broegbernensis gen. nov., sp. nov. Int J Syst Evol Microbiol, 2000, 5(1): 273-282.

[21] Glickmann E, Deessaux Y. A critical examination of the specificity of the Salkosky reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol, 1995, 61(2): 793-796.

[22] Habib SH, Kausar H, Saud HM. Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Res Int, 2016, 2016: 1-10.

[23] Hoseini M, Rahimzadeh-Khoei F, Mirshekari B. Seed priming techniques improve germination and yield in two landraces of lemon balm in laboratory experiment and field study. Int J Indigen Med Plants, 2013, 29(1): 1144-1150.

[24] Iasur-Kruh L, Zahavi T, Barkai R, Freilich S, Zchori-Fein E, Naor V. Dyella-like bacterium isolated from an insect as a potential biocontrol agent against grapevine yellows. Phytopathology, 2018, 108(3): 336-341.

[25] Jukes TH, Cantor CR. Munro HN. Evolution of protein molecules. Mammalian protein metabolism, 1969, New York: Academic Press 21

[26] Kumar P, Dubey RC, Maheshwari DK. Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res, 2012, 167(8): 493-499.

[27] Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol, 2016, 33(7): 1870-1874.

[28] Ljung K, Östin A, Lioussanne L, Sandberg G. Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings. Plant Physiol, 2001, 125: 464-475.

[29] Madmony A, Chernin L, Pleban S, Peleg E, Riov J. Enterobacter cloacae, an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbial, 2005, 50(3): 209-216.

[30] Martínez AL, De los Santos PHM, Fierros GAM, Fierros MR, Pérez MR, Hernández RA, Hernández R. Expansion factors and system partition of aerial biomass for Pinus chiapensis (Martínez) Andresen. Rev mex de cienc forestales, 2018, 10(51): 107-132.

[31] Mu Y, Pan Y, Shi W, Liu L, Jiang Z, Luo X, Zeng XC, Li WJ. Luteimonas arsenica sp. Nov., an arsenic-tolerant bacterium isolated from arsenic-contaminated soil. Int J Syst Evol Microbiol, 2016, 66(6): 2291-2296.

[32] Muñoz-Flores H, Hernández-Zaragoza J, Hernández-Zaragoza O, García-Magaña PJ, Barrera Ramírez JR. Growth comparison of Pinus chiapensis (Martínez) Andresen, Pinus greggii Engelm and Pinus patula Schl. et Cham in commercial plantation established in Hueyapan, Puebla. Foresta Veracruzana, 2015, 17(1): 1-8.

[33] Muñoz-Rojas J, Fuentes-Ramírez LE, Caballero-Mellado J. Antagonism among Gluconacetobacter diazotrophicus strains in culture media and in endophytic association. FEMS Microbiol Ecol, 2005, 54: 57-66.

[34] Murphy J, Riley JP. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta, 1962, 27: 31-36.

[35] Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A. Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul, 2014, 73: 121-131.

[36] Ngo HT, Yin CS. Luteimonas terrae sp. Nov., isolated from rhizosphere soil of Radix ophiopogonis. Int J Syst Evol Microbiol, 2016, 66(5): 1920-1925.

[37] Nicholas KB, Nicholas HB. GeneDoc: a tool for editing and annotating multiple sequence alignments. Embnew News, 1997, 4: 14.

[38] Ou FH, Gao ZH, Chen MH, Bi JY, Qiu LH. Dyella dinghuensis sp. nov and Dyella choica sp. Nov., isolated from forest soil. Int J Syst Evol Microbiol, 2019, 69(5): 1496-1503.

[39] Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils, 2010, 46: 807-816.

[40] Pramanik K, Mitra S, Sarkar A, Maiti TK. Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain Enterobacter aerogenes MCC 3092. J Hazard Mater, 2018, 351: 317-329.

[41] Probanza A, Mateos JL, Garcia JAL, Ramos B, De Felipe MR, Gutiérrez MFJ. Effects of inoculation with PGPR Bacillus and Pisolithus tinctorius on Pinus pinea L. growth, bacterial rhizosphere colonization, and mycorrhizal infection. Microb Ecol, 2001, 41: 140-148.

[42] Reeuwijk LPV (2002) Procedures for soil analysis. Technical paper 9. International Soil Reference and Information Centre, ISRIC and Food and Agriculture Organization of the United Nations. https://www.isric.online/sites/default/files/ISRIC_TechPap09.pdf

[43] Reyes C, Ávalos J, Cerdá-Olmedo E. Gibberellins and Carotenoids in the Wild Type and Mutants of Gibberella fujikuroi. Appl Environ Microbiol, 1991, 57: 3378-3382.

[44] Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S, Mondal MH, Maiti TK. A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol, 2018, 169(1): 20-32.

[45] Secretaria del medio Ambiente y Recursos Naturales. Norma Oficial Mexicana NOM-059-ECOL (2001) Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. https://www.biodiversidad.gob.mx/pdf/NOM-059-ECOL-2001.pdf

[46] Sethuraman P, Balasubramanian N. Removal of Cr (VI) from aqueous solution using Bacillus subtilis, Pseudomonas aeruginosa and Enterobacter cloacae. Int J Eng Sci Technol, 2010, 2(6): 1811-1825.

[47] Shahid M, Hameed S, Zafar M, Tahir M, Ijaz M, Tariq M, Hussain K, Ali A. Enterobacter sp. strain Fs-11 adapted to diverse ecological conditions and promoted sunflower achene yield, nutrient uptake, and oil contents. Braz J Microbiol, 2019, 50(2): 459-469.

[48] Smithers B. Soil preferences in germination and survival of Limber Pine in the Great Basin White Mountains. Forests, 2017 8 11 423

[49] Sun ZB, Zhang H, Yuan XF, Wang YX, Feng DM, Wang YH, Feng YJ. Luteimonas cucumeris sp., nov., isolated a from a cucumber leaf. Int J Syst Evol Microbiol, 2012, 62: 2916-2920.

[50] Tak HI, Ahmad F, Babalola OO, Inam A. Growth, photosynthesis and yield of chickpea as influenced by urban wastewater and different levels of phosphorus. Int J Plant Res, 2012, 2: 6-13.

[51] Thomas P, Farjon A (2013) Pinus strobus var. chiapensis. The IUCN Red List of Threatened Species 2013: e.T32499A2820834. https://dx.doi.org/https://doi.org/10.2305/IUCN.UK.2013-1.RLTS.T32499A2820834.en. Downloaded on 02 October 2020

[52] Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 1997, 25(24): 4876-4882.

[53] Upadhyay SK, Singh JS, Singh DP. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere, 2011, 21(2): 214-222.

[54] USDA–NRCS United States Department of Agriculture (2020) Natural Resources Conservation Servicehttps://www.nrcs.usda.gov/Internet/FSE_DOCUMENTS/nrcs142p2_053254.pdf

[55] Wang Q, Little CH, Odén PC. Control of longitudinal and cambial growth by gibberellins and indole-3-acetic acid in current-year shoots of Pinus sylvestris. Tree Physiol, 1997, 17(11): 715-721.

[56] Wani PA, Khan MS, Zaidi A. Co-inoculation of nitrogen fixing and phosphate solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agron Hung, 2007, 55(3): 315-323.

[57] Xin G, Glawe D, Doty SL. Characterization of three endophytic, indole-3-acetic acid-producing yeasts occurring in Populus trees. Mycol Res, 2009, 113(9): 973-980.

[58] Xin Y, Cao X, Wu P, Xue S. Luteimonas dalianensis sp. nov., an obligate marine bacterium isolated from seawater. J Microbiol, 2014, 52: 729-733.

[59] Zamora SC, Velasco VF. Pinus strobus var. chiapensis, una especie en peligro de extinción en el estado de Chiapas. Ciencia forestal, 1977, 2: 3-23.

[60] Zhang DC, Liu HC, Xin YH, Zhou YG, Schinner F, Margesin R. Luteimonas terricola sp. nov., a psychrophilic bacterium isolated from soil. Int J Syst Evol Microbiol, 2010, 60: 1581-1584.

[61] Zhao G, Jiang X. Roles of Gibberellin and auxin in promoting seed germination and seedling vigor in Pinus massoniana. Fort Sci, 2014, 60(2): 367-373.

[62] Zhou H, Qu Y, Kong C, Wu Y, Zhu K, Yang J, Zhou J. Promiscuous esterase activities of the C-C hydrolases from Dyella ginsengisoli. Biotechnol Lett, 2012, 34: 1107-1113.

[63] Zhou XY, Gao ZH, Chen MH, Jian MQ, Qiu LH. Dyella monticola sp. nov. and Dyella psychrodurans sp. nov., isolated from monsoon evergreen broad-leaved forest soil of Dinghu Mountain, China. Int J Syst Evol Microbiol, 2019, 69(4): 1016-1023.