Root endophyte bacteria in drought-tolerant and drought-susceptible maize lines

Alma Sánchez-Bautista, Carlos De León-García de Alba, Sergio Aranda-Ocampo, Emma Zavaleta-Mejía, Cristian Nava-Díaz, Paul H. Goodwin, Santos G. Leyva-Mir

Abstract


Maize (Zea mays) ranks second as food in the world and drought limits its productivity. Plants harbor endophytic bacteria that influence health and drought tolerance. The goal of this research was to estimate the density and diversity of cultivable endophyte bacteria from the root system of seven homozygous maize drought-tolerant and seven drought-susceptible lines in three locations of Mexico during three crop cycles. The density and diversity of bacterial populations was assessed by direct counting on plates and identified by PCR. The results identified three groups of endophytic bacteria: 1) highly frequent (Bacillus subtilis, Bacillus megaterium y Pseudomonas geniculata), 2) frequent (Bacillus firmus, Pseudomonas hibiscola y Sinorhizobium meliloti) y 3) low frequency (Acinetobacter soli, Stenotrophomonas maltophila y Burkholderia gladioli.  The analysis of variance (ANOVA) showed significant differences (p?0.05) in density (Log10 CFU g-1 root) of population by location, crop cycle, days after sowing and maize lines. The density of Bacillus subtilis, Pseudomonas hibiscola in the locality of El Batán and Bacillus megaterium, Sinorhizobium meliloti in Tlaltizapán, were significantly higher in drought-tolerant maize lines compared to drought-susceptible lines.

Keywords


Zea mays; endophytic bacteria; bacterial diversity; 16S rADN

Full Text:

PDF (Español)

References


Albareda M, Dardanelli MS, Sousa C, Megías M, Temprano F and Rodríguez D. 2006 Factors affecting the attachment of rhizospheric bacteria to bean and soybean roots. FEMS Microbiology Letters 259:67-73. https://doi.org/10.1111/j.1574-6968.2006.00244.x

Anzai Y, Kim H, Park JY, Wakabayashi H and Oyaizu H. 2000. Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. International Journal of Systematic and Evolutionary Microbiology 50:1563-1589. DOI: 10.1099/00207713-50-4-1563

Baudoin E, Benizri E and Guckert A., 2003. Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biology and Biochemistry 35:1183-1192. https://doi.org/10.1016/S0038-0717(03)00179-2

Bodenhausen N, Horton MW and Bergelson J. 2013. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLOS ONE 8:e56329. https://doi.org/10.1371/journal.pone.0056329

Canbolat M, Bilen S, Çakmakçi R, Sahin F and Aydi A. 2006. Effect of plant growth promoting bacteria and soil compaction on barley seeding growth, nutrient uptake, soil properties and rhizosphere microflora. Biology and Fertility of Soils 42:350-357. https://link.springer.com/article/10.1007/s00374-005-0034-9

Cavaglieri L, Orlando J and Etcheverry M. 2009. Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiological Research 164:391-399. https://doi.org/10.1016/j.micres.2007.03.006

Chi F, Yang P, Han F, Jing Y and Shen S. 2010. Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861-1874. http://onlinelibrary.wiley.com/doi/10.1002/pmic.200900694/full

Cochran, W. G. Técnicas de muestreo. México: Compañía Editorial Continental, 1982. 513 p.

Dimpka C. Weinand T and Asch F. 2009. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell and Environment 32:1682-1694. DOI: 10.1111/j.1365-3040.2009.02028.x

Fan X, Hu H, Huang G, Huang F, Li Y and Palta J. 2015. Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize. Plant Soil 390:337-349. https://doi.org/10.1007/s11104-015-2410-z

Farag MA, Zhang H and Ryu CM. 2013. Dynamic chemical communication between plants and bacteria through airborne signals: induced resistance by bacterial volatiles. Journal of Chemical Ecology 39:1007-1018. https://link.springer.com/article/10.1007/s10886-013-0317-9

FAO. 2016. Disponible en línea: http://www.fao.org/docrep/003/x7650s/x7650s10.html (Consulta, marzo 2016)

FIRA, Fideicomisos Instituidos en Relación con la Agricultura. 2016. Disponible en línea: https://www.gob.mx/cms/uploads/attachment/file/61952/Panorama_Agroalimentario_Ma_z_2015.pdf (Consulta, febrero 2016)

Galkiewicz JP and Kellogg CA. 2008. Cross-Kingdom amplification using Bacteria-specific primers: complications for studies of coral microbial ecology. Applied Environmental Microbiology 74:7828-7831. Disponible en línea: http://aem.asm.org/content/74/24/7828.short

Gond SK, Bergen MS, Torres MS, White JF and Kharwar RF. 2015. Effect of bacterial endophyte on expression of defense in Indian popcorn against Fusarium moniliforme. Symbiosis 66:133-140. https://doi.org/10.1007/s13199-015-0348-9

Gouws LM, Botes E and Wiese AJ, Trenkamp S, Torres-Jerez I, Tang J, Hills NP, Usadel B, Lloyd RJ, Fernie RA, Kossmann J and van der Merwe M. 2012. The plant growth promoting substance, lumichrome, mimics starch, and ethylene-associated symbiotic responses in lotus and tomato roots. Front Plant Science 120:1-20. https://dx.doi.org/10.3389%2Ffpls.2012.00120

Grover M, Ali SZ, Sandhya V, Rasul A and Venkateswarlu B. 2010. Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World Journal of Microbiology and Biotechnology 27:1231-1240. https://doi.org/10.1007/s11274-010-0572-7

Gutiérrez-Zamora ML and Martinez-Romero E. 2001. Natural endophytic association between Rhizobium etli and maize (Zea mays L.). Journal of Biotechnology 91:117-126. https://doi.org/10.1016/S0168-1656(01)00332-7

Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T and Achouak W. 2008. Plant host habitat and root exudates shape soil bacterial community structure. The ISME Journal 2:1221-1230. Disponible en línea: http://www.abdn.ac.uk/staffpages/uploads/mbi010/ISME%20Journal%2012,%201221-1230_1.pdf

Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M and Sessitsch A. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79:293-320. Disponible en línea: http://mmbr.asm.org/content/79/3/293.short

Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD and Lutzoni F. 2007. Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Molecular Phylogenetics and Evolution 42:543-555. https://doi.org/10.1016/j.ympev.2006.07.012

Ikeda CA, Bassani LL, Adamoski D, Stringari D, Cordeiro VK, Glienke C, Steffens MBR, Hungria M and Galli-Terasawa LV. 2013. Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microbial Ecology 65:154-160. DOI: 10.1007/s00248-012-0104-0

Johnston-Monje D and Raizada MN. 2011. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6: e20396. https://doi.org/10.1371/journal.pone.0020396

Kasim WA, Osman ME, Omar MN, Abd El-Daim IA, Bejai S and Meijer J. 2013. Control of drought stress in wheat using plant-growth- promoting bacteria. Journal of Plant Growth Regulation 32:122-130. Disponible en línea: https://link.springer.com/article/10.1007/s00344-012-9283-7

Kamara YA, Menkir A, Badu-Apraku B and Ibikunle O. 2003. The influence of drought stress on growth, yield and yield components of selected maize genotypes. Journal of Agricultural Science 141:43-50. https://doi.org/10.1017/S0021859603003423

Kavamura VN, Santos SN, Silva JL, Parma MM, Avila LA, Visconti A, Zucchi TD, Taketani RG, Andreote FD and Melo IS. 2013. Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiological Research 168:183-191. http://dx.doi.org/10.1016/j.micres.2012.12.002

Kim YC, Glick BR., Bashan Y and Ryu CM. 2012. Enhancement of plant drought tolerance by microbes. In: Aroca R. (eds) Plant responses to drought stress. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32653-0_15

Li X, Rui J, Maoa Y, Yannarell A and Mackie R. 2014. Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biology and Biochemistry 68: 392-401. https://doi.org/10.1016/j.soilbio.2013.10.017

Liu Y, Zuo S, Zou YY, Wang JH and Song W. 2013. Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Annals of Microbiology 63:71-79. Disponible en línea: https://link.springer.com/article/10.1007/s13213-012-0446-3

Mahuku GS. 2004. A simple extraction method suitable for PCR based analysis of plant, fungal and bacterial DNA. Plant Molecular Biology Reporter 22:71-81. Disponible en línea: https://link.springer.com/article/10.1007%2FBF02773351?LI=true

Marulanda A, Barea JM and Azcón R. 2006. An indigenous drought- tolerant strain of Glomus intraradices associated with a native bacterium improves water transport and root development in Retama sphaerocarpa. Microbial Ecology 52:670-678. Disponible en línea: https://link.springer.com/article/10.1007/s00248-006-9078-0

Marulanda A, Barea JM and Azco?n R. 2009. Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. Journal of Plant Growth Regulation 28:115-124. Disponible en línea: https://link.springer.com/article/10.1007/s00344-009-9079-6

McInroy JA and Kloepper JW. 1995. Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant and Soil 173:337-342. Disponible en línea: https://link.springer.com/article/10.1007%2FBF00011472?LI=true

Mehnaz S, Kowalik T, Reynolds B and Lazarovits G. 2010. Growth promoting effects of corn (Zea mays) bacterial isolates under greenhouse and field conditions. Soil Biology and Biochemistry 42:1848-1856. https://doi.org/10.1016/j.soilbio.2010.07.003

Montañez A, Blanco RA, Barlocco C, Beracochea M and Sicardi M. 2012. Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Applied Soil Ecology 58:21-28. https://doi.org/10.1016/j.apsoil.2012.02.009

Morales Y, Juárez D, Aragón C, Mascarua M, Bustillos M, Fuentes L, Martínez R and Muñoz J. 2011. Growth response of maize plantlets inoculated with Enterobacter spp., as a model for alternative agriculture. Revista Argentina de Microbiología 43:287-293. Disponible en línea: http://www.scielo.org.ar/pdf/ram/v43n4/v43n4a09.pdf

Nacamulli C, Bevivino A, Dalmastri C, Tabacchioni S and Chiarini L. 1997. Perturbation of maize rhizosphere microflora following seed bacterization with Burkholderia cepacia MCI 7. FEMS Microbiology Ecology. 23:183-193. https://doi.org/10.1111/j.1574-6941.1997.tb00401.x

Naseem H and Bano A. 2014. Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance in maize. Journal of Plant Interactions. 9:689-701. https://doi.org/10.1080/17429145.2014.902125

Naveed M. Mitter B, Reichenauer TG, Wieczorek K and Sessitsch A. 2014. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD 17. Environmental and Experimental Botany 97:30-39. https://doi.org/10.1016/j.envexpbot.2013.09.014

Oliveira ALM, Stoels M, Schmid M, Reis VM, Baldani JI and Hartmann A. 2009. Colonization of sugarcane plantlets by mixed inoculations with diazotrophic bacteria. European Journal of Soil Biology 45:106-113. https://doi.org/10.1016/j.ejsobi.2008.09.004

Pereira P, Ibáñez F, Rosenblueth M, Etcheverry M and Martínez-Romero E. 2011. Analysis of the bacterial diversity associated with the roots of maize (Zea mays L.) through culture-dependent and culture-independent methods. International Scholarly Research Network 2011:1-10. DOI:10.5402/2011/938546

Rai R, Prasanta K, Dash BM, Prasanna AS. 2007. Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World Journal Microbiology and Biotechnology 23:853-858. DOI:10.1007/s11274-006-9309-z

Rosenblueth M and Martinez-Romero E. 2006. Bacterial endophytes and their interaction with hosts. Molecular Plant-Microbe Interactions 19:827-837. Disponible en línea: http://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI-19-0827

Roumiansteva ML and Muntyan VS. 2015. Root nodule bacteria Sinorhizobium meliloti: Tolerance to salinity and bacterial genetic determinants. Microbiology 84:303-318. DOI: 10.1134/S0026261715030170

Saravanakumar D, Kavino M, Raguchander T, Subbian P and Samiyappan R. 2011. Plant growth promoting bacteria enhance water stress resistance in green gram plants. Acta Physiology Plant 33:203-209. Disponible en línea: https://link.springer.com/content/pdf/10.1007%2Fs11738-010-0539-1.pdf

Shehata HR, Lyons EM, Jordan KS and Raizada MN. 2016. Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. Journal of Applied Microbiology 120:756-769. Disponible en línea: http://onlinelibrary.wiley.com/doi/10.1111/jam.13050/epdf

Somers E, Vanderleyden J and Srinivasan M. 2004. Rhizosphere bacterial signalling: A love parade beneath our feet. Critical Reviews in Microbiology: 30:205-240. DOI: 10.1080/10408410490468786

Timmusk S, Islam A, Abd El D, Lucian C, Tanilas T and Kannaste A, Behers L, Nevo E, Seisenbaeva G, Stenströ E and Niinemets Ü. 2014. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: Enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9:1-13. https://doi.org/10.1371/journal.pone.0096086

Toledo I, Lloret L and Martínez-Romero E. 2003. Sinorhizobium americanum sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Systematic and Applied Microbiology 26:54-64. Disponible en línea: http://www.sciencedirect.com/science/article/pii/S0723202004701599

Wang E, Tan ZY, Willems A, Fernández-López M, Reinhold-Hurek B and Martínez-Romero E. 2002. Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. International Journal of Systematic and Evolutionary Microbiology 52:1687-1693. http://dx.doi.org/10.1099/00207713-52-5-1687

Wilkinson S and Davies WJ. 2010. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell & Environment 33:510-525. Disponible en línea: http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2009.02052.x/full

Whitehead AN, Barnard LMA, Slater H, Natalie JL, Simpson G and Salmond PC .2001. Quorum-sensing in Gram-negative bacteria. FEMS Microbiology Reviews 25:365-404. https://doi.org/10.1111/j.1574-6976.2001.tb00583.x

Yang J, Kloepper JW and Ryu C. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends in Plant Science 14:1-4. https://doi.org/10.1016/j.tplants.2008.10.004

Yasmin H, Bano A and Samiullah A. 2013. Screening of PGPR isolates from semi-arid region and their implication to alleviate drought stress. Pakistan Journal Botany 45: 51-58. Disponible en línea: https://www.scopus.com/record/display.uri?eid=2-s2.0-84873424619&origin=inward&txGid=f67ad4b109d3d368731a8b22a1f14cfa

Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS and Pare PW. 2007. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839-851. Disponible línea: https://link.springer.com/content/pdf/10.1007%2Fs00425-007-0530-2.pdf




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.1710-3

Refbacks

  • There are currently no refbacks.