Abstract
Background and aims
In this work we present the development of an easy and feasible in vivo alternative to identify promising Plant Growth Promoting Bacteria (PGPB), using wheat -as a model plant- growing under variable soil and climate conditions.
Methods
The identification of promising strains was carried out by Plant-Assistant Selection (PAS) (compared with the conventional PGPB selection, named in this work as Metabolic Traits Selection or MTS). We validated the ability of the obtained strains by PAS to promote wheat growth, by analyzing biometric and nutrimental parameters, as well as the relative expressions of NRT1.4, GluTR, and 6-SFT1 genes.
Results
Twenty strains were obtained by PAS (170 bacterial strains were originally co-inoculated to plants), of which, twelve strains showed the ability to promote wheat growth mainly by the stem development and the number of leaves. Moreover, thirteen strains up-regulated the 6-SFT1 gene, and three strains up-regulated the GluTR gen. Thus, the strains Enterobacter cloacae TS3, Microbacterium foliorum TS9, Bacillus cereus TS10, Paenibacillus lautus TE8, and Paenibacillus lautus TE10 were identified as promising PGPB, showing strong wheat growth promotion events compared with those strains obtained by MTS.
Conclusions
PAS is an easy and feasible alternative for identification of PGPB. However, ecological and economic factors need to be investigated to use the obtained strains by PAS for commercial microbial inoculants formulations.
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Abbreviations
- 16S rRNA:
-
16S ribosomal RNA
- 18S rRNA:
-
18S ribosomal RNA
- 6-SFT1:
-
Suc:fructan 6-fructosyltransferase
- CFU:
-
Colony forming units
- GAPDH:
-
Glyceraldehyde-3-phosphate dehydrogenase
- GluTR:
-
Glutamyl-tRNA reductase 1
- MTS:
-
Metabolic Traits Selection
- NRT1.4:
-
Nitrate transporter 1.4
- PAS:
-
Plant-Assistant Selection
- PGPB:
-
Plant Growth Promoting Bacteria
References
Alcántar G, Sandoval M (1999) Manual de análisis químico de tejido vegetal. Mexico
Alexander D (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fert Soils 12:39–45
Alvarado M, Beltran MA, Rios P, Martinez M, Amora E, Carreon-Abud (2014) Dinámica estacional de comunidades microbianas en huertas de aguacate con diferente uso de suelo. Biológicas 16:19–24
Ambrosini A, de Souza R, Passaglia L (2016) Ecological role of bacterial inoculants and their potential impact on soil microbial diversity. Plant Soil 400:193–207. https://doi.org/10.1007/s11104-015-2727-7
Arzani A, Ashraf M (2017) Cultivated ancient wheats (Triticum spp.): a potential source of health-beneficial food products. Compr Rev Food Sci Food Saf 16:477–488. https://doi.org/10.1111/1541-4337.12262
Asmelash F, Bekele T, Birhane E (2016) The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7:1–15. https://doi.org/10.3389/fmicb.2016.01095
Barra P, Inostroza N, Acuña J, Mora M, Crowley D, Jorquera M (2016) Formulation of bacterial consortia from avocado (Persea americana mill.) and their effect on growth, biomass and superoxide dismutase activity of wheat seedlings under salt stress. Appl Soil Ecol 102:80–91. https://doi.org/10.1016/j.apsoil.2016.02.014
Berendsen R, Pieterse C, Bakker P (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Bhattacharyya P, Jha D (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. https://doi.org/10.1007/s11274-011-0979-9
Brahmaprakash G, Sahu P (2012) Biofertilizers for sustainability. J Indian Inst Sci 92:37–62
Brouns F, van Buul V, Shewry P (2013) Does wheat make us fat and sick? J Cereal Sci 58:209–215. https://doi.org/10.1016/j.jcs.2013.06.002
Camelo M, Vera S, Bonilla R (2011) Mecanismos de acción de las rizobacterias promotoras del crecimiento vegetal. Revista CORPOICA 12:159–166. https://doi.org/10.21930/rcta.vol12_num2_art:227
Canfora L, Malusà E, Tkaczuk C, Tartanus M, Łabanowska B, Pinzari F (2016) Development of a method for detection and quantification of B. brongniartii and B. bassiana in soil. Sci Rep 6:22933. https://doi.org/10.1038/srep22933
Chang C, Lu J, Zhang H, Ma C, Sun G (2015) Copy number variation of cytokinin oxidase gene Tackx4 associated with grain weight and chlorophyll content of flag leaf in common wheat. PLoS One 10:1–15. https://doi.org/10.1371/journal.pone.0145970
Cherif-silini H, Silini A, Yahiaoui B, Ouzari I (2016) Phylogenetic and plant-growth-promoting characteristics of Bacillus isolated from the wheat rhizosphere. Ann Microbiol 66:1087–1097. https://doi.org/10.1007/s13213-016-1194-6
Chiu C, Lin C, Hsia A, Su LH, Tsay Y (2004) Mutation of a nitrate transporter, AtNRT1: 4, results in a reduced petiole nitrate content and altered leaf development. Plant Cell Physiol 45:1139–1148
Compant S, Reiter B, Nowak J, Sessitsch A, Clément C, Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth- promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693. https://doi.org/10.1128/AEM.71.4.1685
Curci A (2017) Measurement issues in the study of flashbulb memory. In: Luminet O, Curci A (ed) Flashbulb Memories, 2nd. London, pp 27–46
Dal Cortivo C, Barion G, Visioli G, Mattarozzi M, Mosca G, Vamerali T (2017) Increased root growth and nitrogen accumulation in common wheat following PGPR inoculation: assessment of plant-microbe interactions by ESEM. Agric Ecosyst Environ 247:396–408. https://doi.org/10.1016/j.agee.2017.07.006
de los Santos Villalobos S, de Folter S, Délano Frier JP, Gómez Lim MA, Guzmán Ortiz DA, Peña Cabriales JJ (2013) Growth promotion and flowering induction in mango (Mangifera indica L. cv “Ataulfo”) trees by Burkholderia and Rhizobium inoculation: morphometric, biochemical, and molecular events. J Plant Growth Regul 32:615–627. https://doi.org/10.1007/s00344-013-9329-5
de los Santos Villalobos S, Parra Cota F, Herrera Sepúlveda A, Valenzuela Aragón B, Estrada Mora J (2018) Colmena: colección de microorganismos edáficos y endófitos nativos, para contribuir a la seguridad alimentaria nacional. REMEXCA 9:191–202. https://doi.org/10.29312/remexca.v9i1.858
de Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/S1415-475738420150053
Diario Oficial de la Federación (DOF) (2000). Norma Oficial Mexicana NOM-021-RECNAT-2000. In : Diario Oficial de la Federación. Available via DOF http://diariooficial.gob.mx/nota_detalle.php?codigo=717582&fecha=31/12/2002 Accessed 15 Jan 2018
Dohrmann AB, Küting M, Jünemann S, Jaenicke S, Schlüter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt-and conventional maize varieties. ISME J 7:37
FAO (2018) World Food Situation. Available via FAO http://www.fao.org/worldfoodsituation/csdb/en/ Accessed 12 Jan 2018
Fischer RA (2011) Wheat physiology: a review of recent developments. Crop Pasture Sci 62:95–114
Groppa MD, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. BioMetals 20:185–195. https://doi.org/10.1007/s10534-006-9026-y
Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240. https://doi.org/10.1007/s11274-010-0572-7
Guo T, Xuan H, Yang Y, Wang L, Wei L, Wang Y, Kang G (2014) Transcription analysis of genes encoding the wheat root transporter NRT1 and NRT2 families during nitrogen starvation. J Plant Growth Regul 33:837–848
Hassan TU, Bano A (2015) Role of carrier-based biofertilizer in reclamation of saline soil and wheat growth. Arch Agron Soil Sci 61:1719–1731. https://doi.org/10.1080/03650340.2015.1036045
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. https://doi.org/10.1007/s13213-010-0117-1
Hirel B, Tétu T, Lea PJ, Dubois F (2011) Improving nitrogen use efficiency in crops for sustainable agriculture. Sustainability 3:1452–1485. https://doi.org/10.3390/su3091452
Hu P, Wang D, Cassidy MJ, Stanier SA (2014) Predicting the resistance profile of a spudcan penetrating sand overlying clay. Can Geotech J 51:1151–1164. https://doi.org/10.1139/cgj-2013-0374
Ilangumaran G, Smith DL (2017) Plant growth promoting Rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1–14. https://doi.org/10.3389/fpls.2017.01768
International Maize and Wheat Improvement Center (CIMMYT) (2018) Wheat Atlas by CIMMYT. Available via CIMMYT http://wheatatlas.org/visualizations. Accessed 14 Jan 2018
Jarošová J, Kundu JK (2010) Validation of reference genes as internal control for studying viral infections in cereals by quantitative real-time RT-PCR. BMC Plant Biol 10:146
Kibblewhite M, Ritz K, Swift M (2008) Soil health in agricultural systems. Philos Trans R Soc Lond Ser B Biol Sci 363:685–701. https://doi.org/10.1098/rstb.2007.2178
Lares-orozco MF, Robles-morúa A, Yepez EA, Handler RM (2016) Global warming potential of intensive wheat production in the Yaqui Valley, Mexico : a resource for the design of localized mitigation strategies. J Clean Prod 127:522–532. https://doi.org/10.1016/j.jclepro.2016.03.128
Livak K, Schimttgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCt method. Methods 25:402–408
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63:541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918
Mahmood S, Ahmad M, Ahmad Z, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448. https://doi.org/10.1016/j.biotechadv.2013.12.005
Meisner CA, Acevedo E, Flores D, Sayre KD, Ortiz-Monasterio I, Byerlee D (1992) Wheat production and grower practices in the Yaqui Valley. Sonora, CIMMYT Wheat Special Report (WPSR)
Meléndez MG, Camargo GZ, Meza Contreras JJ, Sepúlveda AH, de los Santos Villalobos S, Parra Cota FI (2017) Abiotic stress tolerance of microorganisms associated with oregano (Origanum vulgare L.) in the Yaqui Valley, Sonora. Open Agriculture 2:260–265. https://doi.org/10.1515/opag-2017-0029
Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, Van Vuuren DP, Carter T, Emori S, Kainuma M, Kram T, Meehl G, Mitchell J, Nakicenovic N, Riahi K, Smith S, Stouffer R, Thomson A, Weyant J, Wilbanks TJ (2010) The next generation of scenarios for climate change research and assessment. Nature 463:747–756. https://doi.org/10.1038/nature08823
Onyia CE, Anyanwu CU (2013) Comparative study on solubilization of tricalcium phosphate (TCP) by phosphate solubilizing fungi (PSF) isolated from Nsukka pepper plant rhizosphere and root free soil. J Yeast Fungal Res 4:52–57
Philippot L, Raaijmakers JM, Lemanceau P, Van Der WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. https://doi.org/10.1038/nrmicro3109
Raeder U, Broda P (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1:17–20
Rao AN (2013). Food, Agriculture and Education: Science and Technology Education and Future Human Needs (Vol. 6). Elsevier, United Kingdom
Red de estaciones meteorológicas automatizadas de Sonora (REMAS) (2018) Available via REMAS http://www.siafeson.com/remas/ Accessed 17 Nov 2018
Reynolds MP, Borlaug NE (2006) Impacts of breeding on international collaborative wheat improvement. J Agric Sci 144(3). https://doi.org/10.1017/S0021859606005867
Rojas-Solís D, Zetter-Salmón E, Contreras-Pérez M, Rocha-Granados MC, Macías-Rodríguez L, Santoyo G (2018) Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. World Res J Agric Biotechnol 13:46–52. https://doi.org/10.1016/j.bcab.2017.11.007
Ruuska SA, Rebetzke GJ, van Herwaarden AF, Richards RA, Fettell NA, Tabe L, Jenkins CL (2006) Genotypic variation in water-soluble carbohydrate accumulation in wheat. Funct Plant Biol 33:799–809
Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008
Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29. https://doi.org/10.1016/j.micres.2013.08.009
Servicio de Información Agroalimentaria y Pesquera (SIAP) (2018) Avance de siembras y cosechas. Available via SIAP http://infosiap.siap.gob.mx:8080/agricola_siap_gobmx/ResumenDelegacion.do. Accessed 12 Jan 2018
Sharip Z, Schooler SS, Hipsey MR, Hobbs RJ (2012) Eutrophication, agriculture and water level control shift aquatic plant communities from floating-leaved to submerged macrophytes in Lake Chini. Malaysia Biol Invasions 14:1029–1044. https://doi.org/10.1007/s10530-011-0137-1
Shewry PR, Hey SJ (2015) The contribution of wheat to human diet and health. Food Energy Secur 4:178–202. https://doi.org/10.1002/FES3.64
Smith CR, Blair PL, Boyd C, Cody B, Hazel A, Hedrick A, Kathuria H, Khurana P, Kramer B, Muterspaw K, Peck C, Sells E, Skinner J, Tegeler C, Wolfe Z (2016) Microbial community responses to soil tillage and crop rotation in a corn/soybean agroecosystem. Ecol Evol 6:8075–8084. https://doi.org/10.1002/ece3.2553
Stephenson TJ, McIntyre CL, Collet C, Xue GP (2011) TaNF-YB3 is involved in the regulation of photosynthesis genes in Triticum aestivum. Funct Integr Genomics 11:327–340
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671
Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson A (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:1–10. https://doi.org/10.3389/fpls.2017.00049
Trabelsi D, Mhamdi R (2013) Microbial Inoculants and Their Impact on Soil Microbial Communities : A Review BioMed Res Int
Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21(5):573
Velten S, Leventon J, Jager N, Newig J (2015) What is sustainable agriculture? A Syst Rev Sustain 7:7833–7865. https://doi.org/10.3390/su7067833
Villarreal-Delgado MF, Villa-Rodríguez ED, Cira-Chávez LA, Estrada-Alvarado MI, Parra-Cota FI, de los Santos-Villalobos S (2018) The genus Bacillus as a biological control agent and its implications in the agricultural biosecurity. Mex J Phytopathol 36:95–130. https://doi.org/10.18781/R.MEX.FIT.1706-5
Wang Y, Liu S, Zhang H, Zhao Y, Zhao H, Liu H (2014) Glycine betaine application in grain filling wheat plants alleviates heat and high light-induced photoinhibition by enhancing the psbA transcription and stomatal conductance. Acta Physiol Plant 36:2195–2202. https://doi.org/10.1007/s11738-014-1596-7
Weinberg ZG, Muck RE, Weimer PJ (2003) The survival of silage inoculant lactic acid bacteria in rumen fluid. J Appl Microbiol 94:1066–1071. https://doi.org/10.1046/j.1365-2672.2003.01942.x
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 6S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Xue GP, McIntyre CL, Jenkins CL, Glassop D, van Herwaarden AF, Shorter R (2008) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 146:441–454
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14(6):415–421
Zhen Z, Liu H, Wang N, Guo L, Meng J, Ding N, Wu G, Jiang G (2014) Effects of manure compost application on soil microbial community diversity and soil microenvironments in a temperate cropland in China. PLoS One 9:e108555
Zhou C, Li F, Xie Y, Zhu L, Xiao X, Ma Z, Wang J (2017) Involvement of abscisic acid in microbe-induced saline-alkaline resistance in plants. Plant Signal Behav 2324. https://doi.org/10.1080/15592324.2017.1367465
Acknowledgements
The authors acknowledge support by the Cátedras CONACyT Program through Project 1774 “Alternativas agrobiotecnológicas para incrementar la competitividad del cultivo de trigo en el Valle del Yaqui: desde su ecología microbiana hasta su adaptabilidad al cambio climático”; CONACyT Project 253663 “Fortalecimiento de la infraestructura del Laboratorio de Biotecnología del Recurso Microbiano del ITSON para la creación de COLMENA: COLección de Microrganismos Edáficos y Endófitos NAtivos, para contribuir a la seguridad alimentaria regional y nacional”; and CONACyT Project 257246 “Interacción trigo x microorganismos promotores del crecimiento vegetal: identificando genes con potencial agro-biotecnológico”, and scholarship 703393 (Brenda Valenzuela Aragon).
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Valenzuela-Aragon, B., Parra-Cota, F.I., Santoyo, G. et al. Plant-assisted selection: a promising alternative for in vivo identification of wheat (Triticum turgidum L. subsp. Durum) growth promoting bacteria. Plant Soil 435, 367–384 (2019). https://doi.org/10.1007/s11104-018-03901-1
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DOI: https://doi.org/10.1007/s11104-018-03901-1