The role of abiotic factors modulating the plant-microbe-soil interactions: toward sustainable agriculture. A review

  • Gustavo Santoyo Universidad Michoacana de San Nicolás de Hidalgo, Instituto de Investigaciones Químico Biológicas, Laboratorio de Diversidad Genómica. Morelia, Michoacán http://orcid.org/0000-0002-0374-9661
  • Claudia Hernández-Pacheco Universidad Michoacana de San Nicolás de Hidalgo, Instituto de Investigaciones Químico Biológicas, Laboratorio de Diversidad Genómica. Morelia, Michoacán
  • Julie Hernández-Salmerón Universidad Michoacana de San Nicolás de Hidalgo, Instituto de Investigaciones Químico Biológicas, Laboratorio de Diversidad Genómica. Morelia, Michoacán
  • Rocio Hernández-León Universidad Michoacana de San Nicolás de Hidalgo, Instituto de Investigaciones Químico Biológicas, Laboratorio de Diversidad Genómica. Morelia, Michoacán
Keywords: abiotic interactions, plant growth-promoting rhizobacteria, rhizosphere microbiome, soil

Abstract

Microbial soil communities are active players in the biogeochemical cycles, impacting soil fertility and interacting with aboveground organisms. Although soil microbial diversity has been studied in good detail, the factors that modulate its structure are still relatively unclear, especially the environmental factors. Several abiotic elements may play a key role in modulating the diversity of soil microbes, including those inhabiting the rhizosphere (known as the rhizosphere microbiome). This review summarizes relevant and recent studies that have investigated the abiotic factors at different scales, such as pH, temperature, soil type, and geographic and climatic conditions, that modulate the bulk soil and rhizosphere microbiome, as well as their indirect effects on plant health and development. The plant–microbiome interactions and potential benefits of plant growth-promoting rhizobacteria are also discussed. In the last part of this review, we highlight the impact of climate change on soil microorganisms via global temperature changes and increases in ultraviolet radiation and CO2 production. Finally, we propose the need to understand the function of soil and rhizospheric ecosystems in greater detail, in order to effectively manipulate or engineer the rhizosphere microbiome to improve plant growth in agricultural production.

Downloads

Download data is not yet available.

References

Ahmed Z, Lim BR, Cho J, Song KG, Kim KP, Ahn KH, 2008. Biological nitrogen and phosphorus removal and changes in microbial community structure in a membrane bioreactor: effect of different carbon sources. Water Res 42: 198-210. https://doi.org/10.1016/j.watres.2007.06.062

Alexandre A, Oliveira S, 2013. Response to temperature stress in rhizobia. Crit Rev Microbiol 39: 219-228. https://doi.org/10.3109/1040841X.2012.702097

Andrew DR, Fitak RR, Munguia-Vega A, Racolta A, Martinson VG, Dontsova K, 2012. Abiotic factors shape microbial diversity in Sonoran desert soils. Appl Environ Microbiol 78: 7527-7537. https://doi.org/10.1128/AEM.01459-12

Angel R, Soares, MIM, Ungar ED, Gillor O, 2010. Biogeography of soil archaea and bacteria along a steep precipitation gradient. ISME J 4: 553-563. https://doi.org/10.1038/ismej.2009.136

Arrage AA, Phelps TJ, Benoit RE, White DC, 1993. Survival of subsurface microorganisms exposed to UV radiation and hydrogen peroxide. Appl Environ Microbiol 59: 3545-3550.

Avery LM, Lewis Smith RI, West HM, 2003. Response of rhizosphere microbiol communities associated with Antarctic hairgrass (Deschampsia antarctica) to UV radiation. Polar Biol 26: 525-529. https://doi.org/10.1007/s00300-003-0515-y

Bachar A, Al-Ashhab A, Soares MIM, Sklarz MY, Angel R, Ungar ED, Gillor O, 2010. Soil microbial abundance and diversity along a low precipitation gradient. Microb Ecol 60: 453-461. https://doi.org/10.1007/s00248-010-9727-1

Badri DV, Vivanco JM, 2009. Regulation and function of root exudates. Plant Cell Environ 32: 666-681. https://doi.org/10.1111/j.1365-3040.2009.01926.x

Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM, 2013. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288: 4502-4512. https://doi.org/10.1074/jbc.M112.433300

Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM, 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266. https://doi.org/10.1146/annurev.arplant.57.032905.105159

Bardgett RD, Manning P, Morrien E, Vries FT, 2013. Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101: 334-343. https://doi.org/10.1111/1365-2745.12043

Bashan Y, Holguín G, Ferrera-Cerrato R, 1996. Interacciones entre plantas y microorganismos benéficos. Terra 14: 159-194.

Beauregard MS, Hamel C, St-Arnaud M, 2010. Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in Alfalfa. Microb Ecol 59: 379-389. https://doi.org/10.1007/s00248-009-9583-z

Berendsen RL, Pieterse CMJ, Bakker P, 2012. The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486. https://doi.org/10.1016/j.tplants.2012.04.001

Bertin C, Yang X, Weston LA, 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256: 67-83. https://doi.org/10.1023/A:1026290508166

Bhattacharyya PN, Jha DK, 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

Biate DL, Kumari A, Annapurna K, Kumar LV, Ramadoss D, Reddy KK, Naik S, 2015. Legume root exudates: Their role in symbiotic interactions. In: Plant Microbes Symbiosis: Applied Facets; Arora NK (ed), Springer, India, pp: 259-271. https://doi.org/10.1007/978-81-322-2068-8_13

Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A, 2014. Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27: 30-37. https://doi.org/10.1016/j.copbio.2013.09.012

Bronick CJ, Lal R, 2005. Soil structure and management: A review. Geoderma 124: 3-22. https://doi.org/10.1016/j.geoderma.2004.03.005

Caldwell MM, Robberecht R, Nowak RS, 1982. Differencial photosynthetic inhibitory by ultraviolet B radiation in species from the Arctic- alpine lifezone. Arct Alp Res 14: 195-202. https://doi.org/10.2307/1551152

Caldwell MM, Bornman JF, Ballaré CL, Flint SD, Kulandaivelu G, 2007. Terrestrial ecosystems, increased solar ultravioleta radiation, and interactions with oiré climate change factors. Photochem Photobiol Sci 6: 252-266. https://doi.org/10.1039/b700019g

Callaghan TV, Jonasson S, 1995. Arctic terrestrial ecosystems and environmental change. Phi Trans R Soc Lond A 352: 259-276. https://doi.org/10.1098/rsta.1995.0069

Carson JK, Gonzalez-Quinones V, Murphy DV et al., 2010. Low pore connectivity increases bacterial diversity in soil. Appl Environ Microbiol 76: 3936-3942. https://doi.org/10.1128/AEM.03085-09

Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW, 2010. Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76: 999-1007. https://doi.org/10.1128/AEM.02874-09

Cazorla FM, Codina JC, Abad C et al., 2008. 62-kb plasmids harboring rulAB homologues confer UV-tolerance and epiphytic fitness to Pseudomonas syringae pv. syringae mango isolates. Microbial Ecol 56: 283-291. https://doi.org/10.1007/s00248-007-9346-7

Chaparro JM, Sheflin AM, Manter DK, Vivanco JM, 2012. Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fert Soils 48: 489-499. https://doi.org/10.1007/s00374-012-0691-4

Chapin III FS, Matson PA, Vitousek P, 2011. Principles of terrestrial ecosystem ecology. Springer Science and Business Media. https://doi.org/10.1007/978-1-4419-9504-9

Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P, 2010. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12: 2998-3006. https://doi.org/10.1111/j.1462-2920.2010.02277.x

Chu H, Neufeld JD, Walker VK, Grogan P, 2011. The influence of vegetation type on the dominant soil bacteria, archaea, and fungi in a low arctic tundra landscape. Soil Biol Biochem 75: 1756-1765. https://doi.org/10.2136/sssaj2011.0057

Clark CM, Cleland EE, Collins SL et al., 2007. Environmental and plant community determinants of species loss following nitrogen enrichment. Ecol Lett 10: 596-607. https://doi.org/10.1111/j.1461-0248.2007.01053.x

Clark CM, Tilman D, 2008. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451: 712-715. https://doi.org/10.1038/nature06503

Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR, 2007. Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82: 229-240. https://doi.org/10.1007/s10533-006-9065-z

Compant S, Duffy B, Nowak J, Clément C, Barka EA, 2005. Use of plant growth-promoting rhizobacteria for biocontrol of plant deseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71: 4951-4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005

Coolon JD, Jones KL, Todd TC, Blair JM, Herman MA, 2013. Long-term nitrogen amendment alters the diversity and assemblage of soil bacterial communities in tallgrass prairie. PloS One 8: e67884. https://doi.org/10.1371/journal.pone.0067884

Cutchis P, 1974. Stratospheric ozono depletion and solar ultravioleta radiation on earth. Science 184: 13-19. https://doi.org/10.1126/science.184.4132.13

Das S, Bhattacharyya P, Adhya TK, 2011. Interaction effects of elevated CO2 and temperature on microbial biomass and enzyme activities in tropical rice soils. Environ Monit Assess 182: 555-569. https://doi.org/10.1007/s10661-011-1897-x

Degens BP, Schipper LA, Sparling GP, Vojvodic-Vukovic M, 2000. Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32: 189-196. https://doi.org/10.1016/S0038-0717(99)00141-8

Dohrmann AB, Tebbe CC, 2005. Effect of elevated tropospheric ozone on the structure of bacterial communities inhabiting the rhizosphere of herbaceous plants native to Germany. Appl Environ Microbiol 71: 7750-7758. https://doi.org/10.1128/AEM.71.12.7750-7758.2005

Donnarumma F, Bazzicalupo M, Blažinkov M, Mengoni A, Sikora S, Babić KH, 2014. Biogeography of Sinorhizobium meliloti nodulating alfalfa in different Croatian regions. Res Microbiol 165: 508-516. https://doi.org/10.1016/j.resmic.2014.06.001

Drenovsky RE, Vo D, Graham KJ, Scow KM, 2004. Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microb Ecol 48: 424-430. https://doi.org/10.1007/s00248-003-1063-2

Egamberdiyeva D, 2007. The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36: 184-189. https://doi.org/10.1016/j.apsoil.2007.02.005

Escalante-Lozada A, Gosset-Lagarda G, Martínez-Jiménez A, Bolívar-Zapata F, 2004. Diversidad bacteriana del suelo: métodos de estudio no dependientes del cultivo microbiano e implicaciones biotecnológicas. Agrociencia 38: 583-592.

Fierer N, Jackson RB, 2006. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci 103: 626-631. https://doi.org/10.1073/pnas.0507535103

Formánek P, Rejšek K, Vranová V, 2014. Effect of elevated CO2, O3, and UV radiation on soils. Scientific World J: ID 730149.

Gage DJ, 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68: 280-300. https://doi.org/10.1128/MMBR.68.2.280-300.2004

Gaiero JR, McCall CA, Thompson KA et al., 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

Geiger F, Bengtsson, J, Berendse F et al., 2010. Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11: 97-105. https://doi.org/10.1016/j.baae.2009.12.001

Geyer KM, Altrichter AE, Takacs-Vesbatch CD, Van Horn DJ, Gooseff MN, Barret JE, 2014. Bacterial community composition of divergent soil habitats in a polar desert. FEMS Microbiol Ecol 89: 490-494. https://doi.org/10.1111/1574-6941.12306

Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS, 2003. Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69: 1800-1809. https://doi.org/10.1128/AEM.69.3.1800-1809.2003

Glick BR, 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012: article ID 963401. https://doi.org/10.6064/2012/963401

Glick BR, 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169: 30-39. https://doi.org/10.1016/j.micres.2013.09.009

Handelsman J, 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68: 669-685. https://doi.org/10.1128/MMBR.68.4.669-685.2004

Hättenschwiler S, Tiunov AV, Scheu S, 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Ann Rev Ecol Evol System 36: 191-218. https://doi.org/10.1146/annurev.ecolsys.36.112904.151932

Hernández-León R, Velázquez-Sepúlveda I, Orozco-Mosqueda MC, Santoyo G, 2010. Metagenómica de suelos: grandes desafíos y nuevas oportunidades biotecnológicas. Phyton 79: 133-139.

Hernández-León R, Rojas-Solís D, Contreras-Pérez M et al., 2015. Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol Cont 81: 83-92. https://doi.org/10.1016/j.biocontrol.2014.11.011

Hernández-Salmerón JE, Valencia-Cantero E, Santoyo G, 2013. Genome-wide analysis of long, exact DNA repeats in rhizobia. Genes Genom 35: 441-449. https://doi.org/10.1007/s13258-012-0052-6

Hiltner L, 1904. Uber neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter bessonderer Berucksichtigung der Grundung und Brache. Arb Dtsch Landwirtsch Ges Berl 98: 59-78.

Hu S, Chapin FS, Firestone MK et al., 2001. Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409: 188-191. https://doi.org/10.1038/35051576

Hugenholtz P, Goebel BM, Pace NR, 1998. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765-4774.

Joergensen RG, Emmerling C, 2006. Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. J Plant Nut Soil Sci 169: 295-309. https://doi.org/10.1002/jpln.200521941

Johnson D, Campbell CD, Lee JA, Callaghan TV, Gwynn-Jones D, 2002. Arctic microorganisms respond more to elevated UV-B radiation than CO2. Lett Nature 416: 82-83. https://doi.org/10.1038/416082a

Kado CI, 1992. Plant pathogenic bacteria. In: The prokaryotes; Balows A et al. (eds). Springer-Verlag, NY. pp: 660-662.

Kang SM, Khan AL, Waqas M et al., 2014. Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9: 673-682. https://doi.org/10.1080/17429145.2014.894587

Kerkhoff AJ, Enquist BJ, Green JL, Bryant JA, Lamanna C, 2008. Microbes on mountainsides : Contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci 105: 11505-11511. https://doi.org/10.1073/pnas.0801920105

Koch M, Delmotte N, Rehrauer H, Vorholt JA, Pessi G, Hennecke H, 2010. Rhizobial adaptations to hosts, a new facet in the legume root-nodule symbiosis. Mol Plant-Microbe Interact 23: 784-790. https://doi.org/10.1094/MPMI-23-6-0784

Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ, 2004. Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microbe Interact 17: 6-15. https://doi.org/10.1094/MPMI.2004.17.1.6

Lauber CL, Hamady M, Knight R, Fierer N, 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75: 5111-5120. https://doi.org/10.1128/AEM.00335-09

Liu X, Lindemann WC, Whitford WG, Steiner RL, 2000. Microbial diversity anti activity of disturbed soil in the northern Chihuahuan desert. Biol Fert Soils 32: 243-249. https://doi.org/10.1007/s003740000242

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

Lynch JM, 1990. The rhizosphere. Wiley, NY.

Marquez-Santacruz HA, Hernandez-Leon R, Orozco-Mosqueda MC, Velazquez-Sepulveda I, Santoyo G, 2010. Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Gen Mol Res 9: 2372-2380. https://doi.org/10.4238/vol9-4gmr921

Marschner P, Crowley D, Yang CH, 2004. Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261: 199-208. https://doi.org/10.1023/B:PLSO.0000035569.80747.c5

Martínez-Absalón S, Rojas-Solís D, Orozco-Mosqueda MC et al., 2014. Potential use and mode of action of the new strain Bacillus thuringiensis UM96 for the biological control of the grey mould phytopathogen Botrytis cinerea. Biocon Sci Technol 24: 1349-1362. https://doi.org/10.1080/09583157.2014.940846

Mosier AC, Li Z, Thomas BC, Hettich RL, Pan C, Banfield JF, 2015. Elevated temperature alters proteomic responses of individual organisms within a biofilm community. ISME J 9: 180-194. https://doi.org/10.1038/ismej.2014.113

Müller R, Crutzen PJ, Grooß JU, Bürhl C, Russell JM, Gernandt H, McKenna DS, Tuck AF, 1997. Severe chemical ozone loss in the Arctic Turing the winter of 1995-96. Nature 398: 709-712. https://doi.org/10.1038/39564

Mummey D, Holben W, Six J, Stahl P, 2006. Spatial stratification of soil bacterial populations in aggregates of diverse soils. Microb Ecol 51: 404-411. https://doi.org/10.1007/s00248-006-9020-5

Newman LA, Reynolds CM, 2005. Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23: 6-8. https://doi.org/10.1016/j.tibtech.2004.11.010

Niederbacher B, Winkler JB, Schnitzler JP, 2015. Volatile organic compounds as non-invasive markers for plant phenotyping. J Exp Bot 66 (18): 5403-5416. https://doi.org/10.1093/jxb/erv219

Owen D, Williams AP, Griffith GW, Withers PJA, 2015. Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl Soil Ecol 86: 41-54. https://doi.org/10.1016/j.apsoil.2014.09.012

Rashid S, Charles TC, Glick BR, 2012. Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61: 217-224. https://doi.org/10.1016/j.apsoil.2011.09.011

Raymond J, Siefert JL, Staples CR, Blankenship RE, 2004. The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554. https://doi.org/10.1093/molbev/msh047

Reich PB, Oleksyn J, 2004. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Nat Acad Sci 101: 11001-11006. https://doi.org/10.1073/pnas.0403588101

Rinnan R, Keinänen MM, Kasurinen A et al., 2005. Ambient ultravioleta radiation in the Arctic reduces root biomass and alters microbiol community composition but has no effects on microbiol biomass. Global Change Biol 11: 564-574. https://doi.org/10.1111/j.1365-2486.2005.00933.x

Robson TM, Pancotto VA, Scopel AL, Flint SD, Caldwell MM, 2005. Solar UV-B influences microfaunal community composition in a Tierra del Fuego peatland. Soil Biol Biochem 37: 2205-2215. https://doi.org/10.1016/j.soilbio.2005.04.002

Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Triplett EW, 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1: 283-290. https://doi.org/10.1038/ismej.2007.53

Rolli E, Marasco R, Vigani G et al., 2014. Improved plant resistance to drought is promoted by the root‐associated microbiome as a water stress‐dependent trait. Environ Microbiol 17: 316-331. https://doi.org/10.1111/1462-2920.12439

Rousk J, Baath E, Brookes PC et al., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4: 1340-1351. https://doi.org/10.1038/ismej.2010.58

Ruamps LS, Nunan N, Chenu C, 2011. Microbial biogeography at the soil pore scale. Soil Biol Biochem 43: 280-286. https://doi.org/10.1016/j.soilbio.2010.10.010

Ruamps LS, Nunan N, Pouteau V, Leloup J, Raynaud X, Roy V, Chenu C, 2013. Regulation of soil organic C mineralization at the pore scale. FEMS Microb Ecol 86: 26-35. https://doi.org/10.1111/1574-6941.12078

Ryan J, Sommer R, 2012. Soil fertility and crop nutrition research at an international center in the Mediterranean region: achievements and future perspective. Arch Agron Soil Sci 58: S41-S54. https://doi.org/10.1080/03650340.2012.693601

Ryan PR, Dessaux Y, Thomashow LS, Weller DM, 2009. Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321: 363-383. https://doi.org/10.1007/s11104-009-0001-6

Santoyo G, Romero D, 2005. Gene conversion and concerted evolution in bacterial genomes. FEMS Microbiol Rev 29: 169-183. https://doi.org/10.1016/j.fmrre.2004.10.004

Santoyo G, Orozco-Mosqueda MC, Govindappa M, 2012. Mechanisms of biocontrol and plant growth-promoting activity in soil bacterial species of Bacillus and Pseudomonas: A review. Biocon Sci Technol 22: 855-872. https://doi.org/10.1080/09583157.2012.694413

Shi R, Zhang Y, Chen X et al., 2010. Influence of long-term nitrogen fertilization on micronutrient density in grain of winter wheat (Triticum aestivum L.). J Cereal Sci 51: 165-170. https://doi.org/10.1016/j.jcs.2009.11.008

Singh B, Dawson LA, McDonald CA, Buckland SM, 2009. Impact of biotic and abiotic interaction on soil microbial communities and functions: a field study. Appl Soil Ecol 41: 239-248. https://doi.org/10.1016/j.apsoil.2008.10.003

Singh D, Shi L, Adams JM, 2013. Bacterial diversity in the mountains of South-West China: Climate dominates over soil parameters. J Microbiol 51: 439-447. https://doi.org/10.1007/s12275-013-2446-9

Sinha RP, Klisch M, Häder D, 1999. Induction of a mycosporine-like amino acid (MAA) in the rice-field cyanobacterium Anabaena sp. by UV radiation. J Photochem Photobiol 52: 59-64. https://doi.org/10.1016/S1011-1344(99)00103-7

Stomeo F, Makhalanyane TP, Valverde A et al., 2012. Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiol Ecol 82: 326-340. https://doi.org/10.1111/j.1574-6941.2012.01360.x

Suding KN, Collins SL, Gough L et al., 2005. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Nat Acad Sci 102: 4387-4392. https://doi.org/10.1073/pnas.0408648102

Sundin GW, Jacobs JL, 1999. Ultraviolet radiation (UVR) sensitivity analysis and UVR survival strategies of a bacterial community from the phyllosphere of field-grown peanut (Arachis hypogeae L.). Microb Ecol 38: 27-38. https://doi.org/10.1007/s002489900152

Thummes K, Schäfer J, Käampfer P, Jäckel U, 2007. Thermophilic methanogenic Archea in composta material: occurrence, persistence and possible mechanisms for their distribution to other environments. Syst Appl Microbiol 30: 634-643. https://doi.org/10.1016/j.syapm.2007.08.001

Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S, 2002. Agricultural sustainability and intensive production practices. Nature 418: 671-677. https://doi.org/10.1038/nature01014

Tisdall JM, 1996. Formation of soil aggregates and accumulation of soil organic matter. In: Structure and organic matter storage in agricultural soils; Carter MR, Stewart BA (eds), pp: 57-96. CRC Press, Boca Raton.

Turner CL, Blair JM, Schartz RJ, Neel JC, 1997. Soil N and plant responses to fire, topography, and supplemental N in tallgrass prairie. Ecology 78: 1832-1843. https://doi.org/10.1890/0012-9658(1997)078[1832:SNAPRT]2.0.CO;2

Uroz S, Calvaruso C, Turpault M-P, Frey-Klett P, 2009. The microbial weathering of soil minerals: Ecology, actors and mechanisms. Trends Microbiol 17: 378-387. https://doi.org/10.1016/j.tim.2009.05.004

Uroz S, Ioannidis P, Lengelle J, Cébron A, Morin E, Buée M, Martin F, 2013. Functional assays and metagenomic analyses reveals differences between the microbial communities inhabiting the soil horizons of a Norway spruce plantation. Plos ONE 8: e55929. https://doi.org/10.1371/journal.pone.0055929

Van Ginkel JH, Gorissen A, Polci D, 2000. Elevated atmospheric carbon dioxide concentration: effects of increased carbon input in a Lolium perenne soil on microorganisms and decomposition. Soil Biol Biochem 32: 449-456. https://doi.org/10.1016/S0038-0717(99)00097-8

Van Horn DJ, Van Horn ML, Barrett JE et al., 2013. Factors controlling soil microbial biomass and bacterial diversity and community composition in a cold desert ecosystem: Role of geographic scale. PLoS ONE 8: e66103. https://doi.org/10.1371/journal.pone.0066103

Van Rhijn P, Vanderleyden J, 1995. The Rhizobium-plant symbiosis. Microbiol Rev 59: 124-142.

Vassilev N, Vassileva M, Nicolaeva I, 2006. Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71: 137-144. https://doi.org/10.1007/s00253-006-0380-z

Verville JH, Hobbie SE, Chapin FS, Hooper DU, 1998. Response of tundra CH4 and CO2 flux to manipulation of temperature and vegetation. Biogeochemistry 41: 215-235. https://doi.org/10.1023/A:1005984701775

Wang J, Cao P, Hu H, Li J, Han L, 2014. Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb Ecol 69: 135-145. https://doi.org/10.1007/s00248-014-0465-7

Wardle DA, Bardgett RD, Klironomos JN et al., 2004. Ecological linkages between aboveground and belowground biota. Science 304: 1629-1633. https://doi.org/10.1126/science.1094875

Whipps JM, Hand P, Pink D, Bending GD, 2008. Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105: 1744-1755. https://doi.org/10.1111/j.1365-2672.2008.03906.x

Wit DR, Bouvier T, 2006. Everything is everywhere, but, the environment selects´; what did Baas Becking and Beijerinck really say? Environ Microbiol 8: 755-758. https://doi.org/10.1111/j.1462-2920.2006.01017.x

Yang CH, Crowley DE, 2000. Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66: 345-351. https://doi.org/10.1128/AEM.66.1.345-351.2000

Yergeau E, Bokhorst S, Huiskes AHL et al., 2007. Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiol Ecol 59: 436-451. https://doi.org/10.1111/j.1574-6941.2006.00200.x

Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A et al., 2014. Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69: 395-406. https://doi.org/10.1007/s00248-014-0530-2

Zhang XF, Zhao L, Xu SJ et al., 2013. Soil moisture effect on bacterial and fungal community in Beilu River (Tibetan Plateau) permafrost soils with different vegetation types. J Appl Microbiol 114: 1054-1065. https://doi.org/10.1111/jam.12106

Zhang Y, Cong J, Lu H, Li G, Qu Y, Su X, Zhou J, Li D, 2014. Community structure and elevational diversity patterns of soil Acidobacteria. J Environ Sci 26: 1717-1724. https://doi.org/10.1016/j.jes.2014.06.012

Zhuang X, Chen J, Shim H, Bai Z, 2007. New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33: 403-413. https://doi.org/10.1016/j.envint.2006.12.005

Zogg GP, Zak DR, Ringelberg et al., 1997. Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Amer J 61: 475-481. https://doi.org/10.2136/sssaj1997.03615995006100020015x

Published
2017-04-20
How to Cite
Santoyo, G., Hernández-Pacheco, C., Hernández-Salmerón, J., & Hernández-León, R. (2017). The role of abiotic factors modulating the plant-microbe-soil interactions: toward sustainable agriculture. A review. Spanish Journal of Agricultural Research, 15(1), e03R01. https://doi.org/10.5424/sjar/2017151-9990
Section
Agricultural environment and ecology