Abstract
The giant landrace of maize Jala is a native crop cultured in Nayarit and Jalisco States in the occident of México. In this study, after screening 374 rhizospheric and endophytic bacteria isolated from rhizospheric soil, root, and seed tissues of maize Jala, a total of 16 bacterial strains were selected for their plant-growth-promoting potential and identified by 16S rRNA phylogenetic analysis. The isolates exhibited different combinations of phenotypic traits, including solubilisation of phosphate from hydroxyapatite, production of a broad spectrum of siderophores such as cobalt, iron, molybdenum, vanadium, or zinc (Co2+, Fe3+, Mo2 +, V5+, Zn2+), and nitrogen fixation capabilities, which were detected in both rhizospheric and endophytic strains. Additional traits such as production of 1-aminocyclopropane-1-carboxylate deaminase and a high-rate production of Indoleacetic Acid were exclusively detected on endophytic isolates. Among the selected strains, the rhizospheric Burkholderia sp., and Klebsiella variicola, and the endophytic Pseudomonas protegens significantly improved the growth of maize plants in greenhouse assays and controlled the infection against Fusarium sp. 50 on fresh maize cobs. These results present the first deep approach on handling autochthonous microorganisms from native maize with a potential biotechnological application in sustainable agriculture as biofertilizers or biopesticides.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Not applicable for this section.
Accession Numbers: Uploaded to the National Center for Biotechnology Information database (NCBI): K855127—Achromobacter xylosoxidans Z2K8; MK855134—Achyromobacter xylosoxidans Z3AD5a; MK855132—Burkholderia sp. Z2K9; MK855131—Burkholderia sp. R3J3HD10; MK855133—Chryseobacterium gleum Z1HL3; MK855130—Herbaspirillum seropedicae E2WL3; MK855126—Klebsiella variicola R3J3HD7; MK855128—Kosakonia sp. Z2WD1; MK855135—Pantoea sp. E2K4; MK855136—Pantoea sp. Z2WD2; MK855129—Phytobacter diazotrophicus Z2WL1; MK855121—Pseudomonas protegens E1BL2; MK855122—Pseudomonas protegens E2HL9; MK855125—Pseudomonas alcaligenes Z1K6; MK855123—Pseudomonas japonica Z2K3; MK855124—Rhizobium pusense E2K3.
Code availability
Not applicable for this section.
References
Aguilar A, Peralta H, Mora Y, Díaz R, Vargas-Lagunas C, Girard L, Mora J (2016) Genomic comparison of Agrobacterium pusense strains isolated from bean nodules. Front Microbiol 7:1720. https://doi.org/10.3389/fmicb.2016.01720
Aguilar-Castillo JA, Carballo-Carballo A, Castillo-González F, Santacruz-Varela A, Mejía-Contreras JA, Crossa-Hiriartte J, Baca-Castillo G (2006) Diversidad fenotípica y variantes distintivas de la raza Jala de maíz. Agric Técnica en México 32:57–66. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0568-25172006000100006&lng=es&tlng=es
Aira M, Gómez-Brandón M, Lazcano C, Bååth E, Domínguez J (2010) Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol Biochem 42:2276–2281. https://doi.org/10.1016/j.soilbio.2010.08.029
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389
Arouna O, Deluca F, Camara M, Fall B, Fall B, Ba Diallo A, Docquier JD, Mboup S (2017) Chryseobacterium gleum in a man with prostatectomy in Senegal: a case report and review of the literature. J Med Case Rep 11:1–5. https://doi.org/10.1186/s13256-017-1269-4
Atlas RM (2010) Handbook of microbiological media, 4th edn. CRC Press, Boca Raton
Aujoulat F, Marchandin H, Zorgniotti I, Masnou A, Jumas-Bilak E (2015) Rhizobium pusense is the main human pathogen in the genus Agrobacterium/Rhizobium. Clin Microbiol Infect 21:472.e1–472.e5. https://doi.org/10.1016/j.cmi.2014.12.005
Baldani JI, Reis VM, Videira SS, Boddey LH, Divan Baldani VL (2014) The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists. Plant Soil 384:413–431. https://doi.org/10.1007/s11104-014-2186-6
Balsanelli E, Tadra-Sfeir MZ, Faoro H, Pankievicz VCS, de Baura VA, Pedrosa FO, de Souza EM, Dixon R, Monteiro RA (2016) Molecular adaptations of Herbaspirillum seropedicae during colonization of the maize rhizosphere. Environ Microbiol 18:2343–2356. https://doi.org/10.1111/1462-2920.12887
Barrios-Camacho H, Aguilar-Vera A, Beltran-Rojel M, Aguilar-Vera E, Duran-Bedolla J, Rodriguez-Medina N, Lozano-Aguirre L, Perez-Carrascal OM, Rojas J, Garza-Ramos U (2019) Molecular epidemiology of Klebsiella variicola obtained from different sources. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-46998-9
Bashan Y, Kamnev AA, De-Bashan LE (2013) A proposal for isolating and testing phosphate-solubilizing bacteria that enhance plant growth. Biol Fertil Soils 49:1. https://doi.org/10.1007/s00374-012-0756-4
Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051. https://doi.org/10.1590/S1415-47572012000600020
Bergottini VM, Filippidou S, Junier T, Johnson S, Chain PS, Otegui MB, Zapata PD, Junier P (2015) Genome sequence of Kosakonia radicincitans strain YD4, a plant growth-promoting rhizobacterium isolated from yerba mate (Ilex paraguariensis St. Hill.). Genome Announc. https://doi.org/10.1128/genomeA.00239-15
Bhatti MD, Kalia A, Sahasrabhojane P, Kim J, Greenberg DE, Shelburne SA (2017) Identification and whole genome sequencing of the first case of Kosakonia radicincitans causing a human bloodstream infection. Front Microbiol 8:62. https://doi.org/10.3389/fmicb.2017.00062
Bouffaud ML, Kyselková M, Gouesnard B, Grundmann G, Muller D, Moënne-Loccoz Y (2012) Is diversification history of maize influencing selection of soil bacteria by roots? Mol Ecol 21:195–206. https://doi.org/10.1111/j.1365-294X.2011.05359.x
Brady CL, Goszczynska T, Venter SN, Cleenwerck I, de Vos P, Gitaitis RD, Coutinho TA (2011) Pantoea ananatis sp. nov., isolated from onion plants and seed. Int J Syst Evol Microbiol 61:932–937. https://doi.org/10.1099/ijs.0.022921-0
Bridges JR (1981) Nitrogen-fixing bacteria associated with bark beetles. Microb Ecol 137:131–137. https://doi.org/10.1007/BF02032495
Buckler IV, ES, Stevens NM (2006) Maize origins, domestication, and selection. In Motley TJ, Zerega N, Cross H (ed) Darwin's harvest: New approaches to the origins, evolution, and conservation of crops, Columbia University Press, pp 67–90
Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106
Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BioMed Cent 4:1–4. https://doi.org/10.1186/1471-2105-4-29
Coutinho TA, Venter SN (2009) Pantoea ananatis: an unconventional plant pathogen. Mol Plant Pathol 10:325–335. https://doi.org/10.1111/j.1364-3703.2009.00542.x
Cruz Barrera M, Jakobs-Schoenwandt D, Gómez MI, Becker M, Patel AV, Ruppel S (2019) Salt stress and hydroxyectoine enhance phosphate solubilisation and plant colonisation capacity of Kosakonia radicincitans. J Adv Res 27:91–97. https://doi.org/10.1016/j.jare.2019.03.012
da Fonseca Breda FA, da Silva TFR, Dos Santos SG, Alves GC, Reis VM (2019) Modulation of nitrogen metabolism of maize plants inoculated with Azospirillum brasilense and Herbaspirillum seropedicae. Arch Microbiol 201:547–558. https://doi.org/10.1007/s00203-018-1594-z
Dall’Asta P, Velho AC, Pereira TP, Stadnik MJ, Arisi ACM (2019) Herbaspirillum seropedicae promotes maize growth but fails to control the maize leaf anthracnose. Physiol Mol Biol Plants 25:167–176. https://doi.org/10.1007/s12298-018-0616-2
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Desnoues N, Lin M, Guo X, Ma L, Carreño-Lopez R, Elmerich C (2003) Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice. Microbiology 149:2251–2262. https://doi.org/10.1099/mic.0.26270-0
Douriet-Gámez NR, Maldonado-Mendoza IE, Ibarra-Laclette E, Blom J, Calderón-Vázquez CL (2018) Genomic analysis of Bacillus sp. strain B25, a biocontrol agent of maize pathogen Fusarium verticillioides. Curr Microbiol 75:247–255. https://doi.org/10.1007/s00284-017-1372-1
Drehe I, Simonetti E, Ruiz JA (2018) Contribution of the siderophores pyoverdine and enantio-pyochelin to fitness in soil of Pseudomonas protegens Pf-5. Curr Microbiol 75:1560–1565. https://doi.org/10.1007/s00284-018-1560-7
Eberl L, Vandamme P (2016) Members of the genus Burkholderia: good and bad guys. Research. https://doi.org/10.12688/f1000research.8221.1
Esmaeel Q, Sanchez L, Robineau M, Dorey S, Clément C, Jacquard C, Barka EA (2018) Draft genome sequence of plant growth-promoting Burkholderia sp. strain BE12, isolated from the rhizosphere of maize. Genome Announc 6:e00299-e318. https://doi.org/10.1128/AEM.67.11.5285-5293.2001
Faoro H, Oliveira WK, Weiss VA, Tadra-Sfeir MZ, Cardoso RL, Balsanelli E, Brusamarello-Santos LCC, Camilios-Neto D, Cruz LM, Raittz RT, Marques ACQ, LiPuma J, Fadel-Picheth CMT, Souza EM, Pedrosa FO (2019) Genome comparison between clinical and environmental strains of Herbaspirillum seropedicae reveals a potential new emerging bacterium adapted to human hosts. BMC Genomics 20:630. https://doi.org/10.1186/s12864-019-5982-9
Figuerola ELM, Guerrero LD, Türkowsky D, Wall LG, Erijman L (2015) Crop monoculture rather than agriculture reduces the spatial turnover of soil bacterial communities at a regional scale. Environ Microbiol 17:678–688. https://doi.org/10.1111/1462-2920.12497
Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. https://doi.org/10.3732/ajb.1200572
Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics 12:543–548. https://doi.org/10.1093/bioinformatics/12.6.543
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195. https://doi.org/10.1104/pp.26.1.192
Haahtela K, Kari K, Sundman V (1983) Nitrogenase activity (acetylene reduction) of root-associated, cold-climate Azospirillum, Enterobacter, Klebsiella, and Pseudomonas species during growth on various carbon sources and at various partial pressures of oxygen. Appl Environ Microbiol 45:563–570. https://doi.org/10.1128/AEM.45.2.563-570.1983
He Z, Honeycutt CW (2005) A modified molybdenum blue method for orthophosphate determination suitable for investigating enzymatic hydrolysis of organic phosphates. Commun Soil Sci Plant Anal 36:9–10. https://doi.org/10.1081/CSS-200056954
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. College of Agriculture, University of California, Circular, p 347
Hoffman CS, Winston F (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57:267–272. https://doi.org/10.1016/0378-1119(87)90131-4
Ikeda AC, Bassani LL, Adamoski D, Stringari D, Cordeiro VK, Glienke C, Steffens MB, Hungria M, Galli-Terasawa LV (2013) Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microb Ecol 65:154–160. https://doi.org/10.1007/s00248-012-0104-0
Ji SH, Gururani MA, Chun S-C (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169:83–98. https://doi.org/10.1016/j.micres.2013.06.003
Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6:e20396
Kämpfer P, McInroy JA, Doijad S, Chakraborty T, Glaeser SP (2016) Kosakonia pseudosacchari sp. nov., an endophyte of Zea mays. Syst Appl Microbiol 39:1–7. https://doi.org/10.1371/journal.pone.0020396
Karimi B, Dequiedt S, Terrat S, Jolivet C, Arrouays D, Wincker P, Cruaud C, Bispo A, Chemidlin N, Prévost-Bouré NC, Ranjard L (2019) Biogeography of soil bacterial networks along a gradient of cropping intensity. Sci Rep 9:3812. https://doi.org/10.1038/s41598-019-40422-y
Kempton JH (1924) Jala maize, a giant variety from Mexico. J Hered 15:337–344
Kim M, Oh H-S, Park S-C, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
Leveau JHJ, Lindow SE (2005) Utilization of the plant hormone indole-3-acetic acid for growth by utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Appl Environ Microbiol 71:2365–2371. https://doi.org/10.1128/AEM.71.5.2365-2371.2005
Lin L, Wei C, Chen M, Wang H, Li Y, Li Y, Yang L, An Q (2015) Complete genome sequence of endophytic nitrogen-fixing Klebsiella variicola strain DX120E. Stand Genomic Sci 10:22. https://doi.org/10.1186/s40793-015-0004-2
Madhaiyan M, Poongushali S, Lee JS, Saravanan VS, Lee KC, Santhanakrishnan P (2010) Enterobacter arachidis sp. nov., a plant-growth-promoting diazotrophic bacterium isolated from rhizosphere soil from groundnut. Int J Syst Evol Microbiol 60:1559–1564. https://doi.org/10.1099/ijs.0.013664-0
Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56. https://doi.org/10.1007/s002840010259
Mertschnigg T, Patz S, Becker M, Feierl G, Ruppel S, Bunk B, Spröer C, Overmann J, Zarfel G (2020) First report of Kosakonia radicincitans bacteraemia from Europe (Austria)—Identification and whole-genome sequencing of strain DSM 107547. Sci Rep 10:1948. https://doi.org/10.1038/s41598-020-58689-x
Michavila G, Adler C, De Gregorio PR, Lami MJ, Caram Di Santo MC, Zenoff AM, de Cristobal RE, Vincent PA (2017) Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biol 19:608–617. https://doi.org/10.1111/plb.12556
Molina-Romero D, Baez A, Quintero-Hernández V, Castañeda-Lucio M, Fuentes-Ramírez LE, Bustillos-CristalesRodríguez-Andrade MRO, Morales-García YE, Munive A, Muñoz-Rojas J (2017) Compatible bacterial mixture, tolerant to desiccation, improves maize plant growth. PLoS One 12:e0187913. https://doi.org/10.1371/journal.pone.0187913
Montañez A, Abreu C, Gill PR, Hardarson G, Sicardi M (2009) Biological nitrogen fixation in maize (Zea mays L.) by 15N isotope-dilution and identification of associated culturable diazotrophs. Biol Fertil Soils 45:253–263. https://doi.org/10.1007/s00374-008-0322-2
Morales-Jiménez J, Vera-Ponce de León A, García-Domínguez A, Martínez-Romero E, Zúñiga G, Hernández-Rodríguez C (2013) Nitrogen-fixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microb Ecol 66:200–210. https://doi.org/10.1007/s00248-013-0206-3
Panday D, Schumann P, Das SK (2011) Rhizobium pusense sp. nov., isolated from the rhizosphere of chickpea (Cicer arietinum L.). Int J Syst Evol Microbiol 61:2632–2639. https://doi.org/10.1099/ijs.0.028407-0
Pande A, Pandey P, Mehra S, Singh M, Kaushik S (2017) Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. J Genet Eng Biotechnol 15:379–391. https://doi.org/10.1016/j.jgeb.2017.06.005
Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220. https://doi.org/10.1139/m96-032
Peng G, Zhang W, Luo H, Xie H, Lai W, Tan Z (2009) Enterobacter oryzae sp. nov., a nitrogen-fixing bacterium isolated from the wild rice species Oryza latifolia. Int J Syst Evol Microbiol 59:1650–1655. https://doi.org/10.1099/ijs.0.005967-0
Pereira SIA, Castro PML (2014) Diversity and characterization of culturable bacterial endophytes from Zea mays and their potential as plant growth-promoting agents in metal-degraded soils. Environ Sci Pollut Res 21:14110–14123. https://doi.org/10.1007/s11356-014-3309-6
Pérez-Montaño F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336. https://doi.org/10.1016/j.micres.2013.09.011
Pillonetto M, Arend L, Gomes SMT, Oliveira MAA, Timm LN, Martins AF, Barth AL, Mazzetti A, Hersemann L, Smits THM, Mira MT, Rezzonico F (2018) Molecular investigation of isolates from a multistate polymicrobial outbreak associated with contaminated total parenteral nutrition in Brazil. BMC Infect Dis 18:397. https://doi.org/10.1186/s12879-018-3287-2
Prasanna BM (2012) Diversity in global maize germplasm: characterization and utilization. J Biosci 37:843–855. https://doi.org/10.1007/s12038-012-9227-1
Rao VR (1978) Effect of carbon sources on asymbiotic nitrogen fixation in a paddy soil. Soil Biol Biochem 10:319–321. https://doi.org/10.1016/0038-0717(78)90029-9
Raven JA (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol 109:279–287. https://doi.org/10.1111/j.1469-8137.1988.tb04196.x
Reis VM, Estrada-de los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VLD, Schmid M, Baldani JI, Balandreau J, Hartmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162. https://doi.org/10.1099/ijs.0.02879-0
Relman DA (1993) Universal bacterial 16S rRNA amplification and sequencing. In: Persing DH, Smith TF, Tenover FC, White TJ (eds) Diagnostic molecular microbiology: principles and applications. ASM Press, Washington, pp 489–495
Reyna-Flores F, Barrios-Camacho H, Dantan-Gonzalez E, Ramírez-Trujillo JA, Beltrán FLA, Rodríguez-Medina N, Garza-Ramos U, Suárez-Rodríguez R (2018) Draft genome sequences of endophytic isolates of Klebsiella variicola and Klebsiella pneumoniae obtained from the same sugarcane plant. Genome Announc. https://doi.org/10.1128/genomeA.00147-18
Rice E (2007) Conservation in a changing world: in situ conservation of the giant maize of Jala. Genet Resourc Crop Evol 54:701–713. https://doi.org/10.1007/s10722-006-0023-3
Rodríguez-Medina N, Barrios-Camacho H, Duran-Bedolla J, Garza-Ramos U (2019) Klebsiella variicola: an emerging pathogen in humans. Emerg Microbes Infect 8:973–988. https://doi.org/10.1080/22221751.2019.1634981
Rosenblueth M, Ormeño-Orrillo E, López-López A, Rogel MA, Reyes-Hernández BJ, Martínez-Romero JC, Reddy PM, Martínez-Romero E (2018) Nitrogen fixation in cereals. Front Microbiol 9:1794. https://doi.org/10.3389/fmicb.2018.01794
Ruiz JA, Bernar EM, Jung K (2015) Production of siderophores increases resistance to fusaric acid in Pseudomonas protegens Pf-5. PLoS One 10:e0117040. https://doi.org/10.1371/journal.pone.0117040
Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648. https://doi.org/10.1007/s10295-007-0240-6
Salha Y, Sudalaimuthuasari N, Kundu B, AlMaskari RS, Alkaabi AS, Hazzouri KM, AbuQamar SF, El-Tarabily KA, Amiri KMA (2020) Complete genome sequence of Phytobacter diazotrophicus strain UAEU22, a plant growth-promoting bacterium isolated from the date palm rhizosphere. Microbiol Resour Announc. https://doi.org/10.1128/MRA.00499-20
Scholten H, Pierik R (1998) Agar as a gelling agent: chemical and physical analysis. Plant Cell Rep 17:230–235. https://doi.org/10.1007/s002990050384
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophore. Anal Biochem 160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158:243–248. https://doi.org/10.1078/0944-5013-00197
Suhaimi NS, Yap KP, Ajam N, Thong KL (2014) Genome sequence of Kosakonia radicincitans UMEnt01/12, a bacterium associated with bacterial wilt diseased banana plant. FEMS Microbiol Lett 358:11–13. https://doi.org/10.1111/1574-6968.12537
Swenson CE, Sadikot RT (2015) Achromobacter respiratory infections. Ann Am Thorac Soc 12:252–258. https://doi.org/10.1513/AnnalsATS.201406-288FR
Szkop M, Sikora P, Orzechowski S (2012) A novel, simple, and sensitive colorimetric method to determine aromatic amino acid aminotransferase activity using the Salkowski reagent. Folia Microbiol 57:1–4. https://doi.org/10.1007/s12223-011-0089-y
Tagele SB, Kim SW, Lee HG, Kim HS, Lee YS (2018) Effectiveness of multi-trait Burkholderia contaminans KNU17BI1 in growth promotion and management of banded leaf and sheath blight in maize seedling. Microbiol Res 214:8–18. https://doi.org/10.1016/j.micres.2018.05.004
Tagele SB, Kim SW, Lee HG, Lee YS (2019) Potential of novel sequence type of Burkholderia cenocepacia for biological control of root rot of maize (Zea mays L.) caused by Fusarium temperatum. Int J Mol Sci 20:1005. https://doi.org/10.3390/ijms20051005
Wang Y, Xu X, Liu T, Wang H, Yang Y, Chen X, Zhu S (2020) Analysis of bacterial and fungal communities in continuous-cropping ramie (Boehmeria nivea L. Gaud) fields in different areas in China. Sci Rep 10:3264. https://doi.org/10.1038/s41598-020-58608-0
Weber NF, Herrmann I, Hochholdinger F, Ludewig U, Neumann G (2018) PGPR-Induced growth stimulation and nutrient acquisition in maize: Do root hairs matter? Sci Agric Bohem 49:164–172. https://doi.org/10.2478/sab-2018-0022
Wei CY, Lin L, Luo LJ, Xing YX, Hu CJ, Yang LT, Li YR, An Q (2014) Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol Fertil Soils 50:657–666. https://doi.org/10.1007/s00374-013-0878-3
Weller-Stuart T, De Maayer P, Coutinho T (2017) Pantoea ananatis: genomic insights into a versatile pathogen. Mol Plant Pathol 18:1191–1198. https://doi.org/10.1111/mpp.12517
Witzel K, Gwinn-Giglio M, Nadendla S, Shefchek K, Ruppel S (2012) Genome sequence of Enterobacter radicincitans DSM16656(T), a plant growth-promoting endophyte. J Bacteriol 194:5469. https://doi.org/10.1128/JB.01193-12
Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, Lu W, Zhang W, Yao Z, Li H, Liu W, He S, Geng L, Zhang X, Yang F, Yu H, Zhan Y, Li D, Lin Z, Wang Y, Elmerich C, Lin M, Jin Q (2008) Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci USA 105:7564–7569. https://doi.org/10.1073/pnas.0801093105
You M, Fang S, MacDonald J, Xu J, Yuan ZC (2020) Isolation and characterization of Burkholderia cenocepacia CR318, a phosphate solubilizing bacterium promoting corn growth. Microbiol Res 233:126395. https://doi.org/10.1016/j.micres.2019.126395
Zhang GX, Peng GX, Wang ET, Yan H, Yuan QH, Zhang W, Lou X, Wu H, Tan ZY (2008) Diverse endophytic nitrogen-fixing bacteria isolated from wild rice Oryza rufipogon and description of Phytobacter diazotrophicus gen. nov. sp. nov. Arch Microbiol 189:431–439. https://doi.org/10.1007/s00203-007-0333-7
Zhang J, Wang X-J, Wang J-P, Wang W-X (2014) Carbon and nitrogen contents in typical plants and soil profiles in Yanqi Basin of Northwest China. J Integr Agric 13:648–656. https://doi.org/10.1016/S2095-3119(13)60723-6
Zhao K, Penttinen P, Zhang X, Ao X, Liu M, Yu X, Chen Q (2014) Maize rhizosphere in Sichuan, China, hosts plant growth promoting Burkholderia cepacia with phosphate solubilizing and antifungal abilities. Microbiol Res 169:76–82. https://doi.org/10.1016/j.micres.2013.07.003
Zhou WP, Shen WJ, Li YE, Hui DF (2017) Interactive effects of temperature and moisture on composition of the soil microbial community. Eur J Soil Sci 68:909–918. https://doi.org/10.1111/ejss.12488
Zhu B, Zhou Q, Lin L, Hu C, Shen P, Yang L, An Q, Xie G, Li Y (2013) Enterobacter sacchari sp. nov., a nitrogen-fixing bacterium associated with sugar cane (Saccharum officinarum L.). Int J Syst Evol Microbiol 63:2577–2582. https://doi.org/10.1099/ijs.0.045500-0
Acknowledgements
All the authors would like to thank Proof-Reading-Service.com Ltd. for review of the English version of the manuscript. B.R.G., E.D.U.C., and J.E.G.C. are grateful to the Consejo Nacional de Ciencia y Tecnología (CONACYT) and PIFI/BEIFI-IPN for the scholarships. L.V.T. and C.H.R. are fellows of EDI-IPN, COFAA-IPN, and SNI-CONACYT. This work was supported by the Secretaría de Investigación y Posgrado-IPN (SIP-20181779, 20195643, 20200782) and the project 16131431995 “Estudio de la diversidad microbiana asociada a suelo rizosférico de 10 variedades de maíz” by the Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP).
Author information
Authors and Affiliations
Contributions
BRG, CVG and JEGC performed the isolation and bacterial characterization; BRG, NMJ and EVC performed greenhouse experiments; RIAG, LVT and CHHR provided the samples, designed, and coordinated the study; BRG wrote the first draft manuscript; EVC RIAG, NMJ and CHHR contributed to manuscript editing. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in the publication.
Ethics approval
Not applicable for this section.
Consent to participate
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent for publication
Not applicable for this section.
Rights and permissions
About this article
Cite this article
Rios-Galicia, B., Villagómez-Garfias, C., De la Vega-Camarillo, E. et al. The Mexican giant maize of Jala landrace harbour plant-growth-promoting rhizospheric and endophytic bacteria. 3 Biotech 11, 447 (2021). https://doi.org/10.1007/s13205-021-02983-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-021-02983-6