Plant growth-promoting rhizobacteria associated to candelilla rhizosphere (Euphorbia antisyphilitica) and its effects on Arabidopsis thaliana seedlings

  • Maria T. SALAZAR-RAMÍREZ Tecnologico Nacional de México, Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila, 27170 (MX)
  • Jorge SÁENZ-MATA Universidad Juárez del Estado de Durango, Facultad de Ciencias Biológicas, Gómez Palacio, Durango, 35010 (MX)
  • Pablo PRECIADO-RANGEL Tecnologico Nacional de México, Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila, 27170 (MX)
  • Manuel FORTIS-HERNÁNDEZ Tecnologico Nacional de México, Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila, 27170 (MX)
  • Edgar O. RUEDA-PUENTE Universidad de Sonora, Departamento de Agricultura y Ganadería, Boulevard Luis Encinas y Rosales s/n, Colonia Centro, Hermosillo, Sonora C.P. 83000 (MX)
  • Pablo YESCAS-CORONADO Tecnologico Nacional de México, Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila, 27170 (MX)
  • Jorge A. OROZCO-VIDAL Tecnologico Nacional de México, Instituto Tecnológico de Torreón (ITT), Torreón, Coahuila, 27170 (MX)
Keywords: halophilic rhizobateria, Indole-3-acetic acid, phosphates solubilization, salinity, siderophores

Abstract

In the communities of Sierra Mojada and Viesca, Coahuila, Mexico of Coahuila desert, two rhizosphere samplings of candelilla (Euphorbia antisyphilitica Zucc) were collected to isolate, characterize, and identifying plant growth-promoting rhizobacteria (PGPR); 165 rhizobacteria were tested in vitro with Arabidopsis thaliana seedlings to evaluate their potential as plant growth promoters, and obtaining 21 strains with best results in the variables of the number of secondary roots and fresh weight concerning the uninoculated control. Their salinity tolerance was evaluated at concentrations from 0.85 M, 1.7 M and 2.55 M of NaCl. Biochemical tests were accomplishing such as siderophores production, phosphates solubilization, production of Indole-3-acetic acid (IAA), and the activity of the ACC deaminase enzyme. The results obtained from 21 strains selected, high activities were obtained in organic substances like a siderophores since they developed a translucent orange halo around their growth; four rhizobacteria developed a clear halo around the bacterial growth with a thickness between 1.487 mm ± 0.667 mm and 5.267 mm ± 0.704 mm in phosphates solubilization; in the production of Indole-3-acetic acid (IAA), the bacterial strains showed the presence of this phytohormone, with values ​​from 4.444 μg mL-1 to 19.286 μg mL-1; and according to the activity of the ACC deaminase enzyme, values ​​from 0.424 to 1.306 µmol α-KB/h/mg Pr were showed. 16S rRNA sequencing was carried out and genus identified were Bacillus, Staphylococcus, Acinetobacter, Cronobacter and Siccibacter. The results obtained show the potential of the isolated rhizobacteria as growth promoters and the increase in the biomass of the Arabidopsis thaliana seedlings is evident. This is a first indication to proceed to carry out tests in different phenological stages in crops of agricultural importance.

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References

Aguilar X, Valle G, González G, Murillo B (2013). Guía de cultivo de orégano. [Oregano grow guide]. In: La Paz SC (Ed). Centro de Investigaciones Biológicas del Noreste. Baja California Sur, México pp 106.

Altomare C, Tringovska I (2011). Beneficial soil microorganisms, an ecological alternative for soil fertility management. Genetics, biofuels and local farming systems. In: Lichtfouse E (Ed). Sustainable Agriculture Reviews. Springer 7:161-214. https://doi.org/10.1007/978-94-007-1521-9

Angulo VC, Sanfuentes EA, Rodríguez F, Sossa KE (2014). Caracterización de rizobacterias promotoras de crecimiento en plántulas de Eucalyptus nitens. [Characterization of growth-promoting rhizobacteria in seedlings of Eucalyptus nitens]. Revista Argentina de Microbiología 46(4):338-347. https://doi.org/10.1016/S0325-7541(14)70093-8

Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review Plant Biology 57:233-66. https://doi.org/10.1146/annurev.arplant.57.032905.105159

Bakker PAHM, Pieterse CMJ, Loon LC (2007). Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239-243. http://doi.org/10.1094/PHYTO-97-2-0239.

Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiology Biotechnology 28:1327-1350. https://doi.org/10.1007/s11274-011-0979-9

Bric JM, Bostock RM, Silverstone SE (1991). Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Applied and Environmental Microbiology 57:535-538. https://doi.org/10.1128/AEM.57.2.535-538.1991

Carrillo A, Puente M, Castellanos T, Bashan Y (1998). Aplicaciones biotecnológicas de ecología microbiana. Manual de laboratorio. [Biotechnological applications of microbial ecology. Laboratory manual]. Pontifica Universidad Javeriana, Santa Fe de Bogotá Colombia. Investigaciones Biológicas del Noreste. Baja California Sur, México pp 51.

Comisión Nacional Forestal (CONAFOR) (2009). Gerencia de plantaciones forestales comerciales. [National Forestry Commission. Management of the Forest Plantations] http://www.conafor.gob.mx/portal/index.php/temas-forestales/competitividad/estudio-2009

De-Bashan LE, Holguin G, Glick BR, Bashan Y (2007). Bacterias promotoras de crecimiento en plantas para propósitos agrícolas y ambientales. [Growth-promoting bacteria in plants for agricultural and environmental purposes]. Microbiología agrícola. Editorial Trillas, México, D.F., México.

Dellagi A, Rigault M, Segond D, Roux C, Kraepiel Y, Cellier F, … Expert D (2005). Siderophore-mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. The Plant Journal 43:262-272. https://doi.org/10.1111/j.1365-313X.2005.02451.x

Dias ACF, Costa FEC, Andreote FD, Lacava PT, Teixeira MA, Assumpcao LC, … Melo IS (2009). Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World Journal of Microbiology and Biotechnology 25(2):189-195. https://doi.org/1007/s11274-008-9878-0

Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2014). Rhizosphere priming: a nutrient perspective. The Microbial Regulation of Global Biogeochemical Cycles 183. https://doi.org/10.3389/fmicb.2013.00216

Doyle JJ, Doyle JL (1990). Isolation of plant DNA from fresh tissue. Focus 12:13-15.

Esquivel-Cote R, Ramírez-Gama RM, Tsuzuki-Reyes G, Orozco-Segovia A, Huante P (2010). Azospirillum lipoferum containing 1-aminocyclopropane-1-carboxylic acid deaminase improves early growth of tomato seedlings under nitrogen deficiency. Plant and Soil 337:65-75. https://doi.org/10.1007/s11104-010-0499-7

Estrada-González ÁDJ (2017). Aislamiento, caracterización e identificación de bacterias asociadas a Opuntia spp. y su efecto en la germinación y crecimiento de Arabidopsis thaliana L. [Isolation, characterization and identification of bacteria associated with Opuntia spp. and its effect on the germination and growth of Arabidopsis thaliana L.]. Master tesis, Instituto Potosino De Investigación Científica Y Tecnológica, A. C. https://ipicyt.repositorioinstitucional.mx

Faraj-Edbeib M, Abdul-Wahab R, Huyop F (2016). Halophiles: biology, adaptation, and their role in decontamination of hypersaline environments. World Journal Microbiology Biotechnology 32(135):1-24. https://doi.org/10.1007/s11274-016-2081-9

Frommel MI, Nowak J, Lazarovits G (1991). Growth enhancement and development modification of in vitro grown potato (Solanum tuberosum spp. tuberosum) as affected by a non-fluorescent Pseudomonas sp. Plant Physiology 96:928-936. https://doi.org/10.1104/pp.96.3.928

Glick BR (1995). The enhancement of plant growth by free-living bacteria. Canadian Journal of Microbiology 41:109-117. https://doi.org/10.6064/2012/963401

Goldstein AH (1986). Bacterial solubilization of mineral phosphates: historical perspectives and future prospects. American Journal of Alternative Agricultura 1:51-57. http://www.jstor.org/stable/44506926

González-Mancilla A, Almaraz-Suárez JJ, Ferrera-Cerrato R, Rodríguez-Guzmán MDP, Gaytán T, Rey O, Arteaga-Garibay RI (2017). Caracterización y selección de rizobacterias promotoras de crecimiento en plántulas de chile Poblano (Capsicum annuum L.). [Characterization and selection of growth-promoting

rhizobacteria in Poblano pepper seedlings]. Revista Internacional de Contaminación Ambiental 33(3):463-474. https://doi.org/10.20937/RICA.2017.33.03.09

Hariprasad P, Niranjana SR (2009). Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant and Soil 316(1):13-24. https://doi.org/10.1007/s11104-008-9754-6

Jha B, Gontia I, Hartmann A (2011). The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant and Soil 356:265-277. https://doi.org/10.1007/s11104-011-0877-9

Johansson JF, Paul LR, Finlay RD (2004). Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiology Ecology 48:1-13. https://doi.org/10.1016/j.femsec.2003.11.012

Kanekar P, Kanekar S, Kelkar A, Dhakephalkar P (2011). Halophiles - taxonomy, diversity, physiology and applications. Satyanarayana NT, Narain B, Prakash JA (Eds). Microorganisms in Environmental Management 1-34. https://doi.org/10.1007/978-94-007-2229-3_1

Kloepper JW, Lifshitz R, Schroth MN (1988). Pseudomonas inoculants to benefit plant production. ISI Atlas of Science. Animal and Plant Sciences 1:60-64.

López-Bucio J, Campos-Cuevas C, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez I, Valencia-Cantero E (2007). Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 20:207-217. https://doi.org/10.1094/MPMI-20-2-0207

MacFaddin J (2000). Biochemical tests for identification of medical bacteria. Lippicott Williams & Wilkins, Philadelphia pp 912.

Asif M, Mughal AH, Bisma R, Mehdi Z, Saima S, Ajaz M, ... Sidique S (2018). Application of different strains of biofertilizers for raising quality forest nursery. International Journal of Current Microbiology and Applied Sciences 7(10):3680-3686. https://doi.org/10.20546/ijcmas.2018.710.425

Meziane H, Van der Sluis I, Van Loon LC, Höfte M, Bakker PAHM (2005). Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Molecular Plant Pathology 6:177-185. https://doi.org/10.1111/j.1364-3703.2005.00276.x

Nawangsih AA, Damayanti I, Wiyono S, Kartika JG (2011). Selection and characterization of endophytic bacteria as biocontrol agents of tomato bacterial wilt disease. Hayati Journal of Biosciences 18(2):66-70. https://doi.org/10.4308/hjb.18.2.66

Oren A (2008). Microbial life at high salt concentrations: phylogenetic and metabolic diversity in saline systems. Saline Systems 4(2):1-13. https://doi.org/10.1186/1746-1448-4-2

Palacio-Rodríguez R, Coria-Arellano JL, López-Bucio J, Sánchez-Salas J, Muro-Pérez G, Castañeda-Gaytán G, Sáenz-Mata J (2017). Halophilic rhizobacteria from Distichlis spicata promote growth and improve salt tolerance in heterologous plant hosts. Symbiosis 73(3):179-189. https://doi.org/10.1007/s13199-017-0481-8

Palacio-Rodríguez R, Ramos BP, Coria-Arellano JL, Reyes BN, Sáenz-Mata J (2016). Mecanismos de las PGPR para mitigar el estrés abiótico de plantas. [Mechanisms of PGPR to mitigate abiotic stress in plants]. Arido-Ciencia 1(1):5-12 http://aridociencia.mx/numeros/2016/VIN1/articulo2.pdf

Penrose DM, Glick BR (2003). Methods for isolating and characterizing ACC deaminase containing plant growth-promoting rhizobacteria. Physiologia Plantarum 118:10-15. https://doi.org/10.1034/j.1399-3054.2003.00086.x

Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Möenne-Loccoz Y (2009). The rhizosphere: a playground and battlefield for sailborne pathogens and beneficial microorganisms. Plant and Soil 321:341-361. https://doi.org/10.1007/s11104-008-9568-6

Ramos-Acosta BP (2015). Aislamiento y caracterización de PGPR´s de mezquite (Prosopis spp.). [Insolationa and characterization of PGPR of mesquite]. Master Thesis, Universidad Autónoma Agraria Antonio Narro. Unidad Laguna. http://repositorio.uaaan.mx:8080/xmlui/handle/123456789/42377

Ran LX, Li ZN, Wu GJ, Van Loon LC, Bakker PAHM (2005). Induction of systemic resistance against bacterial wilt in Eucalyptus urophylla by fluorescent Pseudomonas spp. European Journal of Plant Pathology 113:59-70. https://doi.org/10.1007/s10658-005-0623-3

Reinold B, Hurek T, Fendrik I, Pot B, Gillis M, Kersters K, Thielmans S, De Ley J (1987). Azospirillum halopraeferens sp. nov. A nitrogen-fixing organism associated whit roots of Kallar grass (Leptochloa fusca (L.) Kunth). International Journal of Systematic Bacteriology 37:43.51. https://doi.org/10.1099/00207713-37-1-43

Ribaudo CM (2013). Mecanismos bioquímicos y moleculares desencadenados en la interacción bacterias promotoras de crecimiento vegetal y plantas de interés agronómico [Biochemical and molecular mechanisms triggered in the interaction of plant growth promoting bacteria and plants of agronomic interest]. Ph. D. Thesis Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. https://bibliotecadigital.exactas.uba.ar/collection/tesis/document/tesis_n5372_Ribaudo

Sandhya V, Ali SZ, Venkateswarlu B, Reddy G, Grover M (2010). Effect of osmotic stress on plant growth promoting Pseudomonas spp. Archives of Microbiology 192(10):867-876. https://doi.org/10.1007/s00203-010-0613-5

Saraf M, Kumar JC, Patel D (2011). The role of ACC deaminase producing PGPR in sustainable agriculture. In: Maheshwari DK (Ed). Plant Growth and Health Promoting Bacteria. Springer Berlin Heidelberg, Microbiology Monographs 18:365-385. https://doi.org/10.1007/978-3-642-13612-2_16

Schwyn B, Neilands JB (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry 160:47-56. https://doi.org/10.1016/0003-2697(87)90612-9

Sharma A, Pathak A, Sahgal M, Meyer JM, Wray V, Johri BN (2007). Molecular characterization of plant growth promoting rhizobacteria that enhance peroxidase and phenylalanine ammonia-lyase activities in chile (Capsicum annuum L.) and tomato (Lycopersicon esculentum Mill.). Archives of Microbiology 188(5):483-494. https://doi.org/10.1007/s00203-007-0270-5

Singh G, Mukerji KG (2006). Root exudates as determinant of rhizospheric microbial biodiversity. In: Microbial Activity in the Rhizoshere. Springer Berlin Heidelberg, pp 39-53. https://doi.org/10.1007/3-540-29420-1_3

Stafford WH, Baker GC, Brown SA, Burton SG, Cowan DA (2005). Bacterial diversity in the rizhosphere of Proteaceae species. Environmental Microbiology 7:1755-1768. https://doi.org/10.1111/j.1462-2920.2005.00929.x

Tejera-Hernández B, Rojas-Badia M, Heydrich-Pérez M (2011). Potencialidades del género Bacillus en la promoción del crecimiento vegetal y el control biológico de hongos fitopatógenos. [Potentialities of the genus Bacillus in the promotion of plant growth and the biological control of phytopathogenic fungi]. Revista CENIC Ciencias Biológicas Redalyc 42:131-138. https://www.redalyc.org/articulo.oa?id=181222321004

Weisburg W, Barns S, Pelletier D, David P, Gene L (1991). 16s ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173(2):697-703. https://doi.org/10.1128/jb.173.2.697-703.1991

Zahir ZA, Arshad M, Frankenberger WTJr (2004). Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Advances in Agronomy 81:97-168. https://doi.org/10.1016/S0065-2113(03)81003-9

Published
2021-04-29
How to Cite
SALAZAR-RAMÍREZ, M. T., SÁENZ-MATA, J., PRECIADO-RANGEL, P., FORTIS-HERNÁNDEZ, M., RUEDA-PUENTE, E. O., YESCAS-CORONADO, P., & OROZCO-VIDAL, J. A. (2021). Plant growth-promoting rhizobacteria associated to candelilla rhizosphere (Euphorbia antisyphilitica) and its effects on Arabidopsis thaliana seedlings. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(2), 12294. https://doi.org/10.15835/nbha49212294
Section
Research Articles
CITATION
DOI: 10.15835/nbha49212294