Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Yuan, Zhilin ^a   Druzhinina, Irina S ^b   Labbé, Jessy ^c   Redman, Regina ^d   Qin, Yuan ^a   Rodriguez, Russell ^d,e   Zhang, Chulong ^f   Tuskan, Gerald A ^c   Lin, Fucheng ^f  

^a RESEARCH INSTITUTE OF FORESTRY   (China)

^b VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d Adaptive Symbiotic Technologies   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

BIODIVERSITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HALOPHYTE; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYLOGENY; PLANT ROOT; RHIZOSPHERE; SALINITY;

BIODIVERSITY; MICROBIOTA; PHYLOGENY; PLANT ROOTS; RHIZOSPHERE; RNA, RIBOSOMAL, 16S; SALINITY; SALT-TOLERANT PLANTS; SOIL MICROBIOLOGY;

EID: 84984810747     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32467     Document Type: Article

References (79)

1. Coleman-Derr, D., & Tringe, S. G. Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front. Microbiol. 5, 283 (2014
2. Redman, R. S., Sheehan, K. B., Stout, R. G., Rodriguez, R. J., & Henson, J. M. Thermotolerance generated by plant/fungal symbiosis. Science 298, 1581 (2002
3. Rodriguez, R. J. et al. Stress tolerance in plants via habitat-Adapted symbiosis. ISME J. 2, 404-416 (2008
4. Lucero, M. E., Barrow, J. R., Osuna, P., Reyes, I., & Duke, S. E. Enhancing native grass productivity by cocultivating with endophyteladen calli. Rangeland Ecol. Manage. 61, 124-130 (2008
5. Friesen, M. L. et al. Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42, 23-46 (2011
6. Lebeis, S. L., Rott, M., Dangl, J. L., & Schulze-Lefert, P. 28th New Phytologist Symposium: culturing a plant microbiome community at the cross-Rhodes (meeting report). New Phytol. 196, 341-344 (2012
7. Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren Van Themaat, E., & Schulze-Lefert, P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807-838 (2013
8. Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A., & Dufresne, A. The importance of the microbiome of the plant holobiont. New Phytol. 206, 1196-1206 (2015
9. Badri, D. V., Zolla, G., Bakker, M. G., Manter, D. K., & Vivanco, J. M. Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol. 198, 264-273 (2013
10. Lau, J. A., & Lennon, J. T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl. Acad. Sci. USA 109, 14058-14062 (2012
11. Rolli, E. et al. Improved plant resistance to drought is promoted by the root-Associated microbiome as a water stress-dependent trait. Environ. Microbiol. 17, 316-331 (2015
12. Wagner, M. R. et al. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol. Lett. 17, 717-726 (2014
13. Lucero, M. E., Unc, A., Cooke, P., Dowd, S., & Sun, S. Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. PLoS ONE 6, e17693 (2011
14. Marasco, R. et al. A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS ONE 7, e48479 (2012
15. Kaplan, D. et al. A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivationindependent methods. Am. J. Bot. 100, 1713-1725 (2013
16. De Zelicourt, A., Al-Yousif, M., & Hirt, H. Rhizosphere microbes as essential partners for plant stress tolerance. Mol. Plant 6, 242-245 (2013
17. Ruppel, S., Franken, P., & Witzel, K. Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct. Plant Biol. 40, 940-951 (2013
18. Maciá-Vicente, J. G., Ferraro, V., Burruano, S., & Lopez-Llorca, L. V. Fungal assemblages associated with roots of halophytic and non-halophytic plant species vary differentially along a salinity gradient. Microb. Ecol. 64, 668-679 (2012
19. Mora-Ruiz, M. D., Font-Verdera, F., Orfila, A., Rita, J., & Rosselló-Móra, R. Endophytic microbial diversity of the halophyte Arthrocnemum macrostachyum across plant compartments. FEMS Microbiol. Ecol., doi: 10.1093/femsec/fiw145 (2016
20. Szymanska, S. et al. Metabolic potential and community structure of endophytic and rhizosphere bacteria associated with the roots of the halophyte Aster tripolium L. Microbiol. Res. 182, 68-79 (2016
21. Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90 (2012
22. Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95 (2012
23. Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. USA 110, 6548-6553 (2013
24. Edwards, J. et al. Structure, variation and assembly of the root-Associated microbiomes of rice. Proc. Natl. Acad. Sci. USA 112, E911-E920 (2015
25. Gottel, N. R. et al. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl. Environ. Microbiol. 77, 5934-5944 (2011
26. Hacquard, S., & Schadt, C. W. Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytol. 205, 1424-1230 (2015
27. Guttman, D. S., McHardy, A. C., & Schulze-Lefert, P. Microbial genome-enabled insights into plant-microorganism interactions. Nat. Rev. Genet. 15, 797-813 (2014
28. Van der Heijden, M. G. A., & Schlaeppi, K. Root surface as a frontier for plant microbiome research. Proc. Natl. Acad. Sci. USA 112, 2299-2300 (2015
29. Mahé, S. et al. PHYMYCO-DB: a curated database for analyses of fungal diversity and evolution. PLoS ONE 7, e43117 (2012
30. DeAngelis, K. M., & Firestone, M. K. Phylogenetic clustering of soil microbial communities by 16S rRNA but not 16S rRNA genes. Appl. Environ. Microbiol. 78, 2459-2461 (2012
31. Meuser, J. E. et al. Contrasting patterns of community assembly in the stratified water column of Great Salt Lake, Utah. Microb. Ecol. 66, 268-280 (2013
32. Horner-Devine, M. C., & Bohannan, B. J. Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87, S100-S108 (2006
33. Placella, S. A., Brodie, E. L., & Firestone, M. K. Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc. Natl. Acad. Sci. USA 109, 10931-10936 (2012
34. Pajares, S., Souza, V., & Eguiarte, L. E. Multivariate and phylogenetic analyses assessing the response of bacterial mat communities from an ancient oligotrophic aquatic ecosystem to different scenarios of long-Term environmental disturbance. PLoS ONE 10, e0119741 (2015
35. Shade, A., & Handelsman, J. Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4-12 (2012
36. Poisot, T., Péquin, B., & Gravel, D. High-Throughput sequencing: a roadmap toward community ecology. Ecol. Evol. 3, 1125-1139 (2013
37. Dekkers, L. C. et al. A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365. Mol. Plant-Microbe Interact. 11, 45-56 (1998
38. Dekkers, L., Phoelich, C. C., Van der Fits, L., & Lugtenberg, B. J. A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365. Proc. Natl. Acad. Sci. USA 95, 7051-7056 (1998
39. Davidson, A. L., Dassa, E., Orelle, C., & Chen, J. Structure, function and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364 (2008
40. Bruto, M., Prigent-Combaret, C., Muller, D., & Mo?nne-Loccoz, Y. Analysis of genes contributing to plant-beneficial functions in plant growth-promoting rhizobacteria and related Proteobacteria. Sci. Rep. 4, 6261 (2014
41. Eastman, A. W., Heinrichs, D. E., & Yuan, Z. C. Comparative and genetic analysis of the four sequenced Paenibacillus polymyxa genomes reveals a diverse metabolism and conservation of genes relevant to plant-growth promotion and competitiveness. BMC Genomics 15, 851 (2014
42. Becker, E. A. et al. Phylogenetically driven sequencing of extremely halophilic archaea reveals strategies for static and dynamic osmo-response. PLoS Genet. 10, e1004784 (2014
43. Mohammadipanah, F., Hamedi, J., & Dehhaghi M. Halophilic bacteria: potentials and applications in biotechnology. In Halophiles: biodiversity and sustainable exploitation. (eds. Maheshwari, D. K., & Saraf, M. 277-321 (Springer, 2015
44. Camacho Carvajal, M. M., Wijfjes, A. H. M., Mulders, I. H. M., Lugtenberg, B. J. J., & Bloemberg, G. V. Characterization of NADH dehydrogenases of Pseudomonas fluorescens WCS365 and their role in competitive root colonization. Mol. Plant-Microbe Interact. 15, 662-671 (2002
45. Cleary, D. F., de Voogd, N. J., Polónia, A. R., Freitas, R., & Gomes, N. C. Composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in the Spermonde Archipelago, Indonesia. Microb. Ecol. 70, 889-903 (2015
46. Mercado-Blanco, J., & Bakker, P. A. Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92, 367-389 (2007
47. Bashan, Y. Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol. Adv. 16, 729-770 (1998
48. Lakshmanan, V., Selvaraj, G., & Bais, H. P. Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol. 166, 689-700 (2014
49. Lebeis, S. L. The potential for give and take in plant-microbiome relationships. Front. Plant Sci. 5, 287 (2014
50. Bodenhausen, N., Bortfeld-Miller, M., Ackermann, M., & Vorholt, J. A. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet. 10, e1004283 (2014
51. Santhanam, R., Luu, V. T., Weinhold, A., Goldberg, J., Oh, Y., & Baldwin, I. T. Native root-Associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc. Natl. Acad. Sci. USA 112, 5013-5020 (2015
52. De Roy, K., Marzorati, M., Van den Abbeele, P., Van de Wiele, T., & Boon, N. Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities. Environ. Microbiol. 16, 1472-1481 (2014
53. Bashan, Y., Holguin, G., & Lifshitz, R. Isolation and characterization of plant growth-promoting rhizobacteria. In Methods in Plant Molecular Biology and Biotechnology 331-345 (CRC Press, 1993
54. Sarma, B. K., Yadav, S. K., Singh, S., & Singh, H. B. Microbial consortium-mediated plant defense against phytopathogens: readdressing for enhancing efficacy. Soil Biol. Biochem. 87, 25-33 (2015
55. White, J. F. et al. Collaboration between grass seedlings and rhizobacteria to scavenge organic nitrogen in soils. AoB Plants doi: 10.1093/aobpla/plu093 (2015
56. Newsham, K. K. A meta-Analysis of plant responses to dark septate root endophytes. New Phytol. 190, 783-793 (2011
57. Mandyam, K., & Jumpponen, A. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud. Mycol. 53, 173-189 (2005
58. Xu, X. H. et al. The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte. Sci. Rep. 4, 5783 (2014
59. Yuan, Z. L., Zhang, C. L., Lin, F. C., & Kubicek, C. P. Identity, diversity and molecular phylogeny of the endophytic mycobiota in rare wild rice roots (Oryza granulate) from a nature reserve in Yunnan, China. Appl. Environ. Microbiol. 76, 1642-1652 (2010
60. Bodenhausen, N., Horton, M. W., & Bergelson, J. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8, e56329 (2013
61. Winsley, T., Van Dorst, J. M., Brown, M. V., & Ferrari, B. C. Capturing greater 16S rRNA gene sequence diversity within the domain Bacteria. Appl. Environ. Microbiol. 78, 5938-5941 (2012
62. Cordier, T. et al. The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica) varies significantly along an elevation gradient. New Phytol. 196, 510-519 (2012
63. Ihrmark, K. et al. New primers to amplify the fungal ITS2 region-evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol. Ecol. 82, 666-677 (2012
64. Zimmerman, N. B., & Vitousek, P. M. Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc. Natl. Acad. Sci. USA 109, 13022-130227 (2012
65. Martin, K. J., & Rygiewicz, P. T. Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol. 5, 28 (2005
66. Schloss, P. D. et al. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009
67. Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267 (2007
68. Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196 (2007
69. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004
70. Librado, P., & Rozas, J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452 (2009
71. Webb, C. O., Ackerly, D. D., & Kembel, S. W. Phylocom: software for the analysis of phylogenetic community structure and character evolution. Bioinformatics 24, 2098-2100 (2008
72. Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1-10 (1992
73. Webb, C. O., Ackerly, D. D., Mcpeek, M. A., & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Evol. Syst. 33, 475-505 (2002
74. Rao, C. R. Diversity and dissimilarity coefficients: a unified approach. Theor. Popul. Biol. 21, 24-43 (1982
75. Printzen, C., Fernández-Mendoza, F., Muggia, L., Berg, G., & Grube, M. Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata. FEMS Microbiol. Ecol. 82, 316-325 (2012
76. Sharpton, T. J. An introduction to the analysis of shotgun metagenomic data. Front. Plant Sci. 5, 209 (2014
77. Langille, M. G. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814-821 (2013
78. Parks, D. H., Tyson, G. W., Hugenholtz, P., & Beiko, R. G. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123-3124 (2014
79. Mahmoud, R. S., & Narisawa, K. A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS ONE 8, e78746 (2013