Selection on soil microbiomes reveals reproducible impacts on plant function

ISME Journal

Volumn 9, Issue , 2015, Pages 980-989

  Panke Buisse, Kevin ^a   Poole, Angela C ^a   Goodrich, Julia K ^a   Ley, Ruth E ^a   Kao Kniffin, Jenny ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; DICOTYLEDON; ENZYME ACTIVITY; HOST PLANT; MICROBIAL COMMUNITY; PHENOTYPE; RHIZOSPHERE; SOIL MICROORGANISM; SPECIES DIVERSITY;

ARABIDOPSIS THALIANA; BRASSICA RAPA;

SOIL;

ARABIDOPSIS; BIOMASS; BRASSICA RAPA; CHEMISTRY; FLOWER; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MICROFLORA; REPRODUCIBILITY; SOIL;

ARABIDOPSIS; BIOMASS; BRASSICA RAPA; FLOWERS; GENOTYPE; MICROBIOTA; REPRODUCIBILITY OF RESULTS; SOIL; SOIL MICROBIOLOGY;

EID: 84925144072     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.196     Document Type: Article

References (48)

1. Agrawal AA, Johnson MTJ, Hastings AP, Maron JL. (2013). A field experiment demonstrating plant life-history evolution and its eco-evolutionary feedback to seed predator populations. Am Nat 181: S35-S45.
2. Allison SD. (2005). Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol Lett 8: 626-635.
3. Allison SD, Vitousek PM. (2005). Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37: 937-944.
4. Altman J, Lawlor S. (1966). The effects of some chlorinated hydrocarbons on certain soil bacteria. J Appl Microbiol 29: 260-265.
5. Amasino R. (2010). Seasonal and developmental timing of flowering. Plant J 61: 1001-1013.
6. Bainard LD, Koch AM, Gordon AM, Klironomos JN. (2013). Growth response of crops to soil microbial communities from conventional monocropping and tree-based intercropping systems. Plant Soil 363: 345-356.
7. Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel JC. (2000). Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Microbiol 46: 229-236.
8. Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91-95.
9. Burns RG. (1982). Enzyme activity in soil-location and a possible role in microbial ecology. Soil Biol Biochem 14: 423-427.
10. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. (2010a). PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267.
11. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
12. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621-1624.
13. Dodds PN, Rathjen JP. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548.
14. Eddy R, Hahn DT, Aschenbeck L. (2008). 101 ways to try to grow Arabidopsis: What fertilizer strength and frequency was required? Purdue Methods for Arabidopsis Growth. Paper 10. http://docs.lib.purdue. edu/pmag/10.
15. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
16. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD. (2011). Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43: 1387-1397.
17. Haichar F, el Z, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J et al. (2008). Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2: 1221-1230.
18. Kerr B, Godfrey-Smith P. (2002). Individualist and multi-level perspectives on selection in structured populations. Biol Philos 17: 477-517.
19. Kiers ET, Hutton MG, Denison RF. (2007). Human selection and the relaxation of legume defences against ineffective rhizobia. Proc R Soc B-Biological Sci 274: 3119-3126.
20. Kinkel LL, Bakker MG, Schlatter DC. (2011). A coevolu-tionary framework for managing disease-suppressive soils. Annual Review of Phytopathology 49: 47-67.
21. Kurahashi M, Fukunaga Y, Sakiyama Y, Harayama S, Yokota A. (2009). Lamia majanohamensis gen. Nov., sp nov., an Actinobacterium isolated from sea cucumber Holothuria edulis, and proposal of Lamiaceae fam. Nov. Int J. Syst Evol Microbiol 59: 869-873.
22. Lan Y, Wang Q, Cole JR, Rosen GL. (2012). Using the RDP classifier to predict taxonomic novelty and reduce the search space for finding novel organisms. PLoS One 7: e32491.
23. Lau JA, Lennon JT. (2011). Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192: 215-224.
24. Lau JA, Lennon JT. (2012). Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci USA 109: 14058-14062.
25. Lozupone C, Lladser ME, Knights D, Stombaugh J et al. (2011). UniFrac: an effective distance metric for microbial community comparison. ISME J 5: 169.
26. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86.
27. Mazzola M. (2004). Assessment and management of soil microbial community structure for disease suppression. Annu Rev Phytopathol 42: 35-59.
28. McLellan CA, Turbyville TJ, Wijeratne EK, Kerschen A, Vierling E, Queitsch C et al. (2007). A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol 145: 174-182.
29. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM et al. (2011). Deciphering the rhizo-sphere microbiome for disease-suppressive bacteria. Science 332: 1097-1100.
30. Michaels SD, Amasino RM. (2001). Loss of FLOWERING LOCUS C activity eliminates the late-flowering phe-notype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13: 935-941.
31. Nord EA, Lynch JP. (2008). Delayed reproduction in Arabidopsis thaliana improves fitness in soil with suboptimal phosphorus availability. Plant Cell Environ 31: 1432-1441.
32. Okasha S. (2009). Individuals, groups, fitness and utility: multi-level selection meets social choice theory. Biol Philos 24: 561-584.
33. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL et al. (2013). Diversity and heritability of the maize rhizo-sphere microbiome under field conditions. Proc Natl Acad Sci USA 110: 6548-6553.
34. Da Rocha UN, Plugge CM, George I, van Elsas JD, van Overbeek LS. (2013). The rhizosphere selects for particular groups of acidobacteria and verrucomicrobia. PLoS One 8: e82443.
35. Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A, Pardesi KR, Zinjarde S et al. (2011). Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetum glaucum. J Microbiol Biotechnol 21: 556-566.
36. Saiya-Cork KR, Sinsabaugh RL, Zak DR. (2002). The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34: 1309-1315.
37. Sarkar SF, Guttman DS. (2004). Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol 70: 1999-2012.
38. Schimel JP, Bennett J. (2004). Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85: 591-602.
39. Sherameti I, Tripathi S, Varma A, Oelmüller R. (2008). The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant Microbe Interact 21: 799-807.
40. Simpson GG, Dean C. (2002). Flowering-Arabidopsis, the rosetta stone of flowering time? Science 296: 285-289.
41. Sinsabaugh RL. (1994). Enzymatic analysis of microbial pattern and process. Biol Fertil Soils 17: 69-74.
42. Sinsabaugh RL. (2010). Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42: 391-404.
43. Sugiyama A, Bakker MG, Badri D V, Manter DK, Vivanco JM. (2013). Relationships between Arabidopsis genotype-specific biomass accumulation and associated soil microbial communities. Botany-Botanique 91: 123-126.
44. Swenson W, Wilson DS, Elias R. (2000). Artificial ecosystem selection. Proc Natl Acad Sci USA 97: 9110-9114.
45. Tibshirani R, Hastie T, Narasimhan B, Chu G. (2002). Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci USA 99: 6567-6572.
46. Wilson DS. (1975). Theory of group selection. Proc Natl Acad Sci USA 72: 143-146.
47. Xia Y, Kong YH, Thomsen TR, Nielsen PH. (2008). Identification and ecophysiological characterization of epiphytic protein-hydrolyzing Saprospira-ceae ('Candidatus epiflobacter' spp.) in activated sludge. Appl Environ Microbiol 74: 2229-2238.
48. Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA. (2012). Natural enemies drive geographic variation in plant defenses. Science 338: 116-119.