Plant-microbe interactions before drought influence plant physiological responses to subsequent severe drought

Ulrich, Danielle E. M.; Sevanto, Sanna; Ryan, Max; Albright, Michaeline B. N.; Johansen, Renee B.; Dunbar, John M.

doi:10.1038/s41598-018-36971-3

Plant-microbe interactions before drought influence plant physiological responses to subsequent severe drought

Journal Article · Tue Jan 22 00:00:00 EST 2019 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-018-36971-3· OSTI ID:1619567

; Sevanto, Sanna; Ryan, Max; Albright, Michaeline B. N.; Johansen, Renee B.; Dunbar, John M.

Abstract

We examined the effect of soil microbial communities on plant physiological responses to drought. Bouteloua gracilis seeds were planted in sterilized sand with (inoculated) and without (controls) soil microbial communities. After substantial growth, drought was imposed by completely withholding water. Before soil moisture declined to zero, inoculated plants germinated faster, were significantly taller, and maintained greater soil moisture than controls. The greater soil moisture of the inoculated plants allowed greater photosynthesis but also induced lower tissue drought tolerance (as indicated by turgor loss point) compared to controls. The inoculated plants were more susceptible to severe drought compared to control plants as indicated by significantly lower mean stomatal conductance, as well as marginally significantly greater mean wilting score, for the entire severe drought period after soil moisture declined to zero. Inoculated plants exhibited enhanced growth and photosynthesis and dampened drought stress over short timescales, but also increased susceptibility to drought over long timescales. This work demonstrates (1) an unexpected insight that microbes can have positive initial effects on plant performance, but negative impacts on plant performance during severe drought, and (2) that microbially altered effects on plant function during well-watered and moderate drought conditions can influence plant function under subsequent severe drought.

View Journal Article

Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE; USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1619567

Alternate ID(s):: OSTI ID: 1495170

Report Number(s):: LA-UR--18-31425; LA-UR--19-30513; 249; PII: 36971

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 9; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (64)

Spatial Variability in seed Production of the Perennial Bunchgrass Bouteloua Gracilis (Gramineae) Coffin, Debra P.; Lauenroth, William K. American Journal of Botany, Vol. 79, Issue 3 https://doi.org/10.1002/j.1537-2197.1992.tb14558.x	journal	March 1992
Differential sensitivity to regional-scale drought in six central US grasslands Knapp, Alan K.; Carroll, Charles J. W.; Denton, Elsie M. Oecologia, Vol. 177, Issue 4 https://doi.org/10.1007/s00442-015-3233-6	journal	February 2015
Soil microbial communities buffer physiological responses to drought stress in three hardwood species Kannenberg, Steven A.; Phillips, Richard P. Oecologia, Vol. 183, Issue 3 https://doi.org/10.1007/s00442-016-3783-2	journal	November 2016
Photosynthetic pathway and ontogeny affect water relations and the impact of CO 2 on Bouteloua gracilis (C 4 ) and Pascopyrum smithii (C 3 ) Morgan, J. A.; LeCain, D. R.; Read, J. J. Oecologia, Vol. 114, Issue 4 https://doi.org/10.1007/s004420050472	journal	May 1998
Microwave-assisted technology for the clearing and staining of arbuscular mycorrhizal fungi in roots Dalpé, Yolande; Séguin, Sylvie Marie Mycorrhiza, Vol. 23, Issue 4 https://doi.org/10.1007/s00572-012-0472-9	journal	January 2013
Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis Augé, Robert M. Mycorrhiza, Vol. 11, Issue 1 https://doi.org/10.1007/s005720100097	journal	May 2001
Plant root-microbe communication in shaping root microbiomes Lareen, Andrew; Burton, Frances; Schäfer, Patrick Plant Molecular Biology, Vol. 90, Issue 6 https://doi.org/10.1007/s11103-015-0417-8	journal	January 2016
Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland Porras-Alfaro, Andrea; Herrera, Jose; Natvig, Donald O. Plant and Soil, Vol. 296, Issue 1-2 https://doi.org/10.1007/s11104-007-9290-9	journal	June 2007
Diffusion of glucose in microbial extracellular polysaccharide as affected by water potential Chenu, C.; Roberson, E. B. Soil Biology and Biochemistry, Vol. 28, Issue 7 https://doi.org/10.1016/0038-0717(96)00070-3	journal	July 1996
Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review Or, D.; Smets, B. F.; Wraith, J. M. Advances in Water Resources, Vol. 30, Issue 6-7 https://doi.org/10.1016/j.advwatres.2006.05.025	journal	June 2007
A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland Khidir, H. H.; Eudy, D. M.; Porras-Alfaro, A. Journal of Arid Environments, Vol. 74, Issue 1 https://doi.org/10.1016/j.jaridenv.2009.07.014	journal	January 2010
Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: Effectiveness of autochthonous or allochthonous strains Ortiz, N.; Armada, E.; Duque, E. Journal of Plant Physiology, Vol. 174 https://doi.org/10.1016/j.jplph.2014.08.019	journal	February 2015
Understanding and exploiting plant beneficial microbes Finkel, Omri M.; Castrillo, Gabriel; Herrera Paredes, Sur Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.018	journal	August 2017
Isolation and identification of an EPS-producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure Kaci, Yahia; Heyraud, Alain; Barakat, Mohamed Research in Microbiology, Vol. 156, Issue 4 https://doi.org/10.1016/j.resmic.2005.01.012	journal	May 2005
Quantifying the impact of microbes on soil structural development and behaviour in wet soils Helliwell, J. R.; Miller, A. J.; Whalley, W. R. Soil Biology and Biochemistry, Vol. 74 https://doi.org/10.1016/j.soilbio.2014.03.009	journal	July 2014
Rhizosphere bacteria help plants tolerate abiotic stress Yang, Jungwook; Kloepper, Joseph W.; Ryu, Choong-Min Trends in Plant Science, Vol. 14, Issue 1 https://doi.org/10.1016/j.tplants.2008.10.004	journal	January 2009
Visual assessment of wilting as a measure of leaf water potential and seedling drought survival Engelbrecht, Bettina M. J.; Tyree, Melvin T.; Kursar, Thomas A. Journal of Tropical Ecology, Vol. 23, Issue 4 https://doi.org/10.1017/S026646740700421X	journal	July 2007
Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants Shabat, Sheerli Kruger Ben; Sasson, Goor; Doron-Faigenboim, Adi The ISME Journal, Vol. 10, Issue 12 https://doi.org/10.1038/ismej.2016.62	journal	May 2016
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis Bonfante, Paola; Genre, Andrea Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1046	journal	July 2010
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Evidence for the Existence of Three Primary Strategies in Plants and Its Relevance to Ecological and Evolutionary Theory Grime, J. P. The American Naturalist, Vol. 111, Issue 982 https://doi.org/10.1086/283244	journal	November 1977
Regulation of Photosynthesis of C3 Plants in Response to Progressive Drought: Stomatal Conductance as a Reference Parameter Medrano, H. Annals of Botany, Vol. 89, Issue 7 https://doi.org/10.1093/aob/mcf079	journal	June 2002
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
A new fungal large subunit ribosomal RNA primer for high throughput sequencing surveys Mueller, Rebecca C.; Gallegos-Graves, La Verne; Kuske, Cheryl R. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fiv153	journal	December 2015
Functional convergence in hydraulic architecture and water relations of tropical savanna trees: from leaf to whole plant Bucci, S. J.; Goldstein, G.; Meinzer, F. C. Tree Physiology, Vol. 24, Issue 8 https://doi.org/10.1093/treephys/24.8.891	journal	August 2004
Leaf turgor loss point is correlated with drought tolerance and leaf carbon economics traits Zhu, Shi-Dan; Chen, Ya-Jun; Ye, Qing Tree Physiology, Vol. 38, Issue 5 https://doi.org/10.1093/treephys/tpy013	journal	February 2018
Root Exudation and Rhizosphere Biology: Fig. 1. Walker, Travis S.; Bais, Harsh Pal; Grotewold, Erich Plant Physiology, Vol. 132, Issue 1 https://doi.org/10.1104/pp.102.019661	journal	May 2003
Drought tolerance as predicted by leaf water potential at turgor loss point varies strongly across species within an Amazonian forest Maréchaux, Isabelle; Bartlett, Megan K.; Sack, Lawren Functional Ecology, Vol. 29, Issue 10 https://doi.org/10.1111/1365-2435.12452	journal	April 2015
Where, when and how plant-soil feedback matters in a changing world van der Putten, Wim H.; Bradford, Mark A.; Pernilla Brinkman, E. Functional Ecology, Vol. 30, Issue 7 https://doi.org/10.1111/1365-2435.12657	journal	April 2016
Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait: Root bacteria protect plants from drought Rolli, Eleonora; Marasco, Ramona; Vigani, Gianpiero Environmental Microbiology, Vol. 17, Issue 2 https://doi.org/10.1111/1462-2920.12439	journal	March 2014
The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms Mendes, Rodrigo; Garbeva, Paolina; Raaijmakers, Jos M. FEMS Microbiology Reviews, Vol. 37, Issue 5 https://doi.org/10.1111/1574-6976.12028	journal	September 2013
Global analysis of plasticity in turgor loss point, a key drought tolerance trait Bartlett, Megan K.; Zhang, Ya; Kreidler, Nissa Ecology Letters, Vol. 17, Issue 12 https://doi.org/10.1111/ele.12374	journal	October 2014
Top 10 plant pathogenic bacteria in molecular plant pathology: Top 10 plant pathogenic bacteria Mansfield, John; Genin, Stephane; Magori, Shimpei Molecular Plant Pathology, Vol. 13, Issue 6 https://doi.org/10.1111/j.1364-3703.2012.00804.x	journal	June 2012
Demography of perennial grassland plants: survival, life expectancy and life span: Demography of grassland plants Lauenroth, William K.; Adler, Peter B. Journal of Ecology, Vol. 96, Issue 5 https://doi.org/10.1111/j.1365-2745.2008.01415.x	journal	July 2008
Seasonal, diurnal and rehydration-induced variation of pressure-volume relationships in Pseudotsuga menziesii Kubiske, Mark E.; Abrams, Marc D. Physiologia Plantarum, Vol. 83, Issue 1 https://doi.org/10.1111/j.1399-3054.1991.tb01288.x	journal	November 1991
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi Hoeksema, Jason D.; Chaudhary, V. Bala; Gehring, Catherine A. Ecology Letters, Vol. 13, Issue 3 https://doi.org/10.1111/j.1461-0248.2009.01430.x	journal	March 2010
The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis: Drivers of plant drought tolerance Bartlett, Megan K.; Scoffoni, Christine; Sack, Lawren Ecology Letters, Vol. 15, Issue 5 https://doi.org/10.1111/j.1461-0248.2012.01751.x	journal	March 2012
Comparative Water Relations and Photosynthesis of Mycorrhizal and Non-Mycorrhizal Bouteloua Gracilis H.B.K. lag ex Steud. Allen, Michael F.; Smith, William K.; Moore, Thomas S. New Phytologist, Vol. 88, Issue 4 https://doi.org/10.1111/j.1469-8137.1981.tb01745.x	journal	August 1981
Variation in moisture contents between bulk soil and the rhizosheath of wheat (Triticum aestivum L. cv. Wembley) Young, I. M. New Phytologist, Vol. 130, Issue 1 https://doi.org/10.1111/j.1469-8137.1995.tb01823.x	journal	May 1995
Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms Blackman, Christopher J.; Brodribb, Tim J.; Jordan, Gregory J. New Phytologist, Vol. 188, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03439.x	journal	August 2010
Developing microbe-plant interactions for applications in plant-growth promotion and disease control, production of useful compounds, remediation and carbon sequestration Wu, Cindy H.; Bernard, Stéphanie M.; Andersen, Gary L. Microbial Biotechnology, Vol. 2, Issue 4 https://doi.org/10.1111/j.1751-7915.2009.00109.x	journal	July 2009
Understanding and engineering beneficial plant-microbe interactions: plant growth promotion in energy crops Farrar, Kerrie; Bryant, David; Cope-Selby, Naomi Plant Biotechnology Journal, Vol. 12, Issue 9 https://doi.org/10.1111/pbi.12279	journal	November 2014
Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions: Auxin, plant roots and plant-microbe interaction Sukumar, Poornima; LeguÉ, ValÉRie; VayssiÈRes, Alice Plant, Cell & Environment, Vol. 36, Issue 5 https://doi.org/10.1111/pce.12036	journal	December 2012
Dynamics of leaf water relations components in co-occurring iso- and anisohydric conifer species: Dynamics of leaf water relations components Meinzer, Frederick C.; Woodruff, David R.; Marias, Danielle E. Plant, Cell & Environment, Vol. 37, Issue 11 https://doi.org/10.1111/pce.12327	journal	April 2014
Thermotolerance Generated by Plant/Fungal Symbiosis Redman, R. S. Science, Vol. 298, Issue 5598 https://doi.org/10.1126/science.1072191	journal	November 2002
Variation Among Biomes in Temporal Dynamics of Aboveground Primary Production Knapp, A. K. Science, Vol. 291, Issue 5503 https://doi.org/10.1126/science.291.5503.481	journal	January 2001
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Novel Root Fungal Consortium Associated with a Dominant Desert Grass Porras-Alfaro, A.; Herrera, J.; Sinsabaugh, R. L. Applied and Environmental Microbiology, Vol. 74, Issue 9 https://doi.org/10.1128/AEM.02769-07	journal	March 2008
Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp Roberson, Emily B.; Firestone, Mary K. Applied and Environmental Microbiology, Vol. 58, Issue 4 https://doi.org/10.1128/aem.58.4.1284-1291.1992	journal	January 1992
Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Vilgalys, R.; Hester, M. Journal of Bacteriology, Vol. 172, Issue 8 https://doi.org/10.1128/jb.172.8.4238-4246.1990	journal	August 1990
Rhizosphere interactions: root exudates, microbes, and microbial communities Huang, Xing-Feng; Chaparro, Jacqueline M.; Reardon, Kenneth F. Botany, Vol. 92, Issue 4 https://doi.org/10.1139/cjb-2013-0225	journal	April 2014
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105159	journal	June 2006
The Mineral Nutrition of Wild Plants Chapin, F. S. Annual Review of Ecology and Systematics, Vol. 11, Issue 1 https://doi.org/10.1146/annurev.es.11.110180.001313	journal	November 1980
Research priorities for harnessing plant microbiomes in sustainable agriculture Busby, Posy E.; Soman, Chinmay; Wagner, Maggie R. PLOS Biology, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pbio.2001793	journal	March 2017
Microbiome Profiling by Illumina Sequencing of Combinatorial Sequence-Tagged PCR Products Gloor, Gregory B.; Hummelen, Ruben; Macklaim, Jean M. PLoS ONE, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pone.0015406	journal	October 2010
Plantecophys - An R Package for Analysing and Modelling Leaf Gas Exchange Data Duursma, Remko A. PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0143346	journal	November 2015
Responses of soil microbial communities to water stress: results from a meta-analysis Manzoni, Stefano; Schimel, Joshua P.; Porporato, Amilcare Ecology, Vol. 93, Issue 4 https://doi.org/10.1890/11-0026.1	journal	April 2012
Important Species of the Major Forage Types in Colorado and Wyoming Costello, David F. Ecological Monographs, Vol. 14, Issue 1 https://doi.org/10.2307/1961633	journal	January 1944
Growth Characteristics of Blue Grama in Northeastern Colorado Turner, G. T.; Klipple, G. E. Journal of Range Management, Vol. 5, Issue 1 https://doi.org/10.2307/3893982	journal	January 1952
Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland Mueller, Rebecca C.; Belnap, Jayne; Kuske, Cheryl R. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00891	journal	September 2015
Phytohormones and Beneficial Microbes: Essential Components for Plants to Balance Stress and Fitness Egamberdieva, Dilfuza; Wirth, Stephan J.; Alqarawi, Abdulaziz A. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02104	journal	October 2017
Root traits contributing to plant productivity under drought Comas, Louise H.; Becker, Steven R.; Cruz, Von Mark V. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00442	journal	January 2013
Enhanced Drought Stress Tolerance by the Arbuscular Mycorrhizal Symbiosis in a Drought-Sensitive Maize Cultivar Is Related to a Broader and Differential Regulation of Host Plant Aquaporins than in a Drought-Tolerant Cultivar Quiroga, Gabriela; Erice, Gorka; Aroca, Ricardo Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01056	journal	June 2017

Similar Records

Related Subjects

58 GEOSCIENCES
59 BASIC BIOLOGICAL SCIENCES
Biological Science
Earth Sciences

Plant-microbe interactions before drought influence plant physiological responses to subsequent severe drought

Citation Formats

References (64)

Similar Records

Related Subjects