Abstract
In recent years, the utilization of novel sequencing techniques opened a new field of research into plant microbiota and was used to explore a wide diversity of microorganisms both inside and outside of plant host tissues, i.e., the endosphere and rhizosphere, respectively. An early realization from such research was that species richness and diversity of the plant microbiome are both greater than believed even a few years ago, and soil is likely home to the most abundant and diverse microbial habitats known. In most ecosystems sampled thus far, overall microbial complexity is determined by the combined influences of plant genotype, soil structure and chemistry, and prevailing environmental conditions, as well as the native “bulk soil” microbial populations from which membership is drawn. Beneficial microorganisms, traditionally referring primarily to nitrogen-fixing bacteria, plant growth-promoting rhizobacteria, and mycorrhizal fungi, play a key role in major functions such as plant nutrition acquisition and plant resistance to biotic and abiotic stresses . Utilization of plant-associated microbes in food production is likely to be critical for twenty-first century agriculture, where arable cropland is limited and food, fiber, and feed productivity must be sustained or even improved with fewer chemical inputs and less irrigation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Molden D, Oweis TY, Pasquale S, Kijne JW, Hanjra MA et al (2007) Pathways for increasing agricultural water productivity. In: Water for food, water for life, a comprehensive assessment of water management in agriculture. Earthscan and International Water Management Institute, London, pp 279–310
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 15:151–161
Trenberth KE, Fasullo JT, Branstator G, Phillips AS (2014) Seasonal aspects of the recent pause in surface warming. Nat Clim Chang 4:911–916
Rejeb IB, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress : molecular mechanisms. Plants 3:458–475
Pandey S, Bhandari H, Hardy B (2007) Economic costs of drought and rice farmers’ coping mechanisms. A crosscountry comparative analysis. International Rice Research Institute/World Scientific Publishing, Los Baños, Philippines/Singapore, pp 1–9
Dijk AI, Beck HE, Crosbie RS, Jeu RA, Liu YY et al (2013) The millennium drought in southeast Australia (2001–2009): natural and human causes and implications for water resources, ecosystems, economy, and society. Water Resour Res 49:1040–1057
Ray P, Craven KD (2016) Sebacina vermifera: a unique root symbiont with vast agronomic potential. World J Microbiol Biotechnol 32:1–10
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202
Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122
Sinclair TR (2011) Challenges in breeding for yield increase for drought. Trends Plant Sci 16:289–293
Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F et al (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331
Ngumbi E, Kloepper J (2016) Bacterial-mediated drought tolerance: Current and future prospects. Appl Soil Ecol 105:109–125
Zolla G, Badri DV, Bakker MG, Manter DK, Vivanco JM (2013) Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol 68:1–9
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Rout ME, Southworth D (2013) The root microbiome influences scales from molecules to ecosystems: the unseen majority 1. Am J Bot 100:1689–1691
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624
Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E et al (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–369
Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J et al (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK et al (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920
Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci 110:6548–6553
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J et al (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403
Fierer N, Ladau J, Clemente JC, Leff JW, Owens SM et al (2013) Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342:621–624
Tautges NE, Sullivan TS, Reardon CL, Burke IC (2016) Soil microbial diversity and activity linked to crop yield and quality in a dryland organic wheat production system. Appl Soil Ecol 108:258–268
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803
Lakshmanan V (2015) Root microbiome assemblage is modulated by plant host factors. Adv Bot Res 75:57–79
Wagner MR, Lundberg DS, Tijana G, Tringe SG, Dangl JL et al (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151. doi:10.1038/ncomms12151
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882
Werner GD, Strassmann JE, Ivens AB, Engelmoer DJ, Verbruggen E et al (2014) Evolution of microbial markets. Proc Natl Acad Sci 111:1237–1244
Van Loon LC, Rep M, Pieterse C (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162
Bhattacharyya P, Jha D (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556
Kloepper J, Schroth M (1978) Plant growth-promoting rhizobacteria on radishes. Proceedings of the 4th international conference on pathogenic bacteria, Tours, pp 879–882
Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339
Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312
Ghimire SR, Craven KD (2011) The ectomycorrhizal fungus Sebacina vermifera, enhances biomass production of switchgrass (Panicum virgatum L.) under drought conditions. Appl Environ Microbiol 77:7063–7067
Ray P, Ishiga T, Decker SR, Turner GB, Craven KD (2015) A novel delivery system for the root symbiotic fungus, Sebacina vermifera, and consequent biomass enhancement of low lignin COMT switchgrass lines. Bioenergy Res 8:922–933
Tringe SG, Von Mering C, Kobayashi A, Salamov AA, Chen K et al (2005) Comparative metagenomics of microbial communities. Science 308:554–557
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci 74:5088–5090
Mullis KB, Erlich HA, Arnheim N, Horn GT, Saiki RK, et al (1987) Process for amplifying, detecting, and/or-cloning nucleic acid sequences. US 4683195 A
Pinto AJ, Raskin L (2012) PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS One 7:e43093
Zhou J, Jiang Y-H, Deng Y, Shi Z, Zhou BY et al (2013) Random sampling process leads to overestimation of β-diversity of microbial communities. MBio 4:e00324–e00313
Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:5428–5433
Aird D, Ross MG, Chen W-S, Danielsson M, Fennell T et al (2011) Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries. Genome Biol 12:R18
Ahn J-H, Kim B-Y, Song J, Weon H-Y (2012) Effects of PCR cycle number and DNA polymerase type on the 16S rRNA gene pyrosequencing analysis of bacterial communities. J Microbiol 50:1071–1074
Kennedy K, Hall MW, Lynch MD, Moreno-Hagelsieb G, Neufeld JD (2014) Evaluating bias of Illumina-based bacterial 16S rRNA gene profiles. Appl Environ Microbiol 80:5717–5722
D’Amore R, Ijaz UZ, Schirmer M, Kenny JG, Gregory R et al (2016) A comprehensive benchmarking study of protocols and sequencing platforms for 16S rRNA community profiling. BMC Genomics 17:55–74
Gohl DM, Vangay P, Garbe J, MacLean A, Hauge A et al (2016) Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat Biotechnol 34:942–949
Yeoh YK, Paungfoo-Lonhienne C, Dennis PG, Robinson N, Ragan MA et al (2015) The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application. Environ Microbiol 18:1338–1351
Marques JM, da Silva TF, Vollu RE, Blank AF, Ding G-C et al (2014) Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. FEMS Microbiol Ecol 88:424–435
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S et al (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811
Köberl M, Dita M, Martinuz A, Staver C, Berg G (2015) Agroforestry leads to shifts within the gammaproteobacterial microbiome of banana plants cultivated in Central America. Front Microbiol 6:91
Zhang K, Shi Y, Jing X, He J-S, Sun R et al (2016) Effects of short-term warming and altered precipitation on soil microbial communities in alpine grassland of the Tibetan plateau. Front Microbiol 7:1032
Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci 111:585–592
Steenwerth K, Drenovsky R, Lambert J-J, Kluepfel D, Scow K et al (2008) Soil morphology, depth and grapevine root frequency influence microbial communities in a Pinot noir vineyard. Soil Biol Biochem 40:1330–1340
Habekost M, Eisenhauer N, Scheu S, Steinbeiss S, Weigelt A et al (2008) Seasonal changes in the soil microbial community in a grassland plant diversity gradient four years after establishment. Soil Biol Biochem 40:2588–2595
Le Roux X, Schmid B, Poly F, Barnard RL, Niklaus PA et al (2013) Soil environmental conditions and microbial build-up mediate the effect of plant diversity on soil nitrifying and denitrifying enzyme activities in temperate grasslands. PLoS One 8:e61069
Nuccio EE, Anderson-Furgeson J, Estera KY, Pett-Ridge J, Valpine P et al (2016) Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. Ecology 97:1307–1318
Lakshmanan V, Selvaraj G, Bais HP (2014) Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 166:689–700
Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ et al (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci 111:13715–13720
Lankau RA (2011) Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions. New Phytol 189:536–548
Breulmann M, Schulz E, Weißhuhn K, Buscot F (2012) Impact of the plant community composition on labile soil organic carbon, soil microbial activity and community structure in semi-natural grassland ecosystems of different productivity. Plant Soil 352:253–265
Lange M, Habekost M, Eisenhauer N, Roscher C, Bessler H et al (2014) Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoS One 9:e96182
Bressan M, Roncato M-A, Bellvert F, Comte G, el Zahar HF et al (2009) Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J 3:1243–1257
Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM et al (2015) Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant-Microbe Interact 28:1049–1058
Qin Y, Druzhinina IS, Pan X, Yuan Z (2016) Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol Adv 34:1245–1259
Kaushal M, Wani SP (2016) Rhizobacterial-plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agric Ecosyst Environ 231:68–78
Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24
Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462
Arzanesh MH, Alikhani H, Khavazi K, Rahimian H, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27:197–205
Armada E, Roldán A, Azcon R (2014) Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil. Microb Ecol 67:410–420
Bresson J, Varoquaux F, Bontpart T, Touraine B, Vile D (2013) The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol 200:558–569
Liu F, Xing S, Ma H, Du Z, Ma B (2013) Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164
Hussain MB, Zahir ZA, Asghar HN, Asghar M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat. Int J Agric Biol 16:3–13
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530
Zahir Z, Munir A, Asghar H, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963
Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39
Timmusk S, El-Daim IAA, Copolovici L, Tanilas T, Kännaste A et al (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9:e96086
Amellal N, Burtin G, Bartoli F, Heulin T (1998) Colonization of wheat rhizosphere by EPS producing Pantoea agglomerans and its effect on soil aggregation. Appl Environ Microbiol 64:3740–3747
Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobiumsp. Strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398
Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14
Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R et al (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017
Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269
Murphy B, Martin Nieto L, Doohan F, Hodkinson T (2015) Fungal endophytes enhance agronomically important traits in severely drought-stressed barley. J Agron Crop Sci 201:419–427
Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940
Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416
Bae H, Sicher RC, Kim MS, Kim S-H, Strem MD et al (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117
Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68
Shaharoona B, Arshad M, Zahir Z (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.) Lett Appl Microbiol 42:155–159
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:2535–2554
Bacon C, Hill N (1996) Symptomless grass endophytes: products of coevolutionary symbioses and their role in the ecological adaptations of grasses. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants. American Phytopathologycal Society Press, St Paul, MN, pp 155–178
Marulanda A, Barea J-M, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124
James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM et al (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant-Microbe Interact 15:894–906
Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191
Hahn H, McManus MT, Warnstorff K, Monahan BJ, Young CA et al (2008) Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit. Environ Exp Bot 63:183–199
Augé RM (2000) Stomatal behavior of arbuscular mycorrhizal plants Arbuscular mycorrhizas: physiology and function. Springer, New York, NY, pp 201–237
Duan X, Neuman DS, Reiber JM, Green CD, Saxton AM et al (1996) Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 47:1541–1550
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417
Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM et al (2008) PYK10, a β-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54:428–439
Levitt J (1980) Responses of plants to environmental stresses Volume II Water, radiation, salt, and other stresses. Academic, Cambridge, MA
Aroca R, Vernieri P, Ruiz-Lozano JM (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 59:2029–2041
Subramanian KS, Charest C (1995) Influence of arbuscular mycorrhizae on the metabolism of maize under drought stress. Mycorrhiza 5:273–278
Azcón R, Tobar RM (1998) Activity of nitrate reductase and glutamine synthetase in shoot and root of mycorrhizal Allium cepa: effect of drought stress. Plant Sci 133:1–8
Tarafdar J (1996) The role of vesicular arbuscular mycorrhizal fungi on crop, tree and grasses grown in an arid environment. J Arid Environ 34:197–203
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Huang X-F, Chaparro JM, Reardon KF, Zhang R, Shen Q et al (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–275
Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209–219
Berg G, Grube M, Schloter M, Smalla K (2015) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148
Knief C (2014) Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front Plant Sci 5:216
Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M et al (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258
Acknowledgments
This work was supported by the US Department of Energy, Bioenergy Research Center, through the Office of Biological and Environmental Research in the DOE Office of Science and The Samuel Roberts Noble Foundation. We declare no conflict of interests inherent to this submission.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Science+Business Media LLC
About this protocol
Cite this protocol
Lakshmanan, V., Ray, P., Craven, K.D. (2017). Toward a Resilient, Functional Microbiome: Drought Tolerance-Alleviating Microbes for Sustainable Agriculture. In: Sunkar, R. (eds) Plant Stress Tolerance. Methods in Molecular Biology, vol 1631. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7136-7_4
Download citation
DOI: https://doi.org/10.1007/978-1-4939-7136-7_4
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-7134-3
Online ISBN: 978-1-4939-7136-7
eBook Packages: Springer Protocols