Host genotype and age shape the leaf and root microbiomes of a wild perennial plant

Nature Communications

Volumn 7, Issue , 2016, Pages

  Wagner, Maggie R ^a,e   Lundberg, Derek S ^b,f   Del Rio, Tijana G ^c   Tringe, Susannah G ^c   Dangl, Jeffery L ^b,d   Mitchell Olds, Thomas ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c DOE JOINT GENOME INSTITUTE   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

^f MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGE STRUCTURE; BIOME; GENOTYPE-ENVIRONMENT INTERACTION; HERB; HOST; LEAF MORPHOLOGY; RHIZOSPHERE; SOIL MICROORGANISM; WILD POPULATION;

BRASSICACEAE; FIELD EXPERIMENT; GENETIC REGULATION; GENOTYPE ENVIRONMENT INTERACTION; INOCULATION; MICROBIAL COMMUNITY; MICROBIOME; MUSTARD; PERENNIAL PLANT; PLANT LEAF; SOIL; GENETICS; GENOTYPE; MICROBIOLOGY; MICROFLORA; PLANT ROOT;

BACTERIA (MICROORGANISMS); BOECHERA STRICTA; BRASSICACEAE;

RNA 16S;

BRASSICACEAE; GENE-ENVIRONMENT INTERACTION; GENOTYPE; MICROBIOTA; PLANT LEAVES; PLANT ROOTS; RNA, RIBOSOMAL, 16S; SOIL; SOIL MICROBIOLOGY;

EID: 84978378801     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12151     Document Type: Article

References (70)

1. Ritpitakphong, U. et al. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol. 210, 1033-1043 (2016).
2. Santhanam, R. et al. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc. Natl Acad. Sci. USA 112, E5013-E5020 (2015).
3. Busby, P. E., Peay, K. G. & Newcombe, G. Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol. 209, 1681-1692 (2015).
4. 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).
5. Lau, J. A. & Lennon, J. T. Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytol. 192, 215-224 (2011).
6. 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).
7. Berendsen, R. L., Pieterse, C. M. & Bakker, P. A. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478-486 (2012).
8. Schlaeppi, K. & Bulgarelli, D. The plant microbiome at work. Mol. Plant Microbe Interact. 28, 212-217 (2015).
9. Whitham, T. G. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7, 510-523 (2006).
10. Whitham, T. G. et al. Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84, 559-573 (2003).
11. Dawkins, R. in The Extended Phenotype (WH Freeman, 1982).
12. Bordenstein, S. R. & Theis, K. R. host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLOS Biol. 13, e1002226 (2015).
13. Falconer, D. & Mackay, T. in Introduction to Quantitative Genetics (Pearson Education Limited, 1996).
14. Moran, N. A. & Sloan, D. B. The hologenome concept: helpful or hollow? PLoS Biol. 13, e1002311 (2015).
15. Bressan, M. et al. Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J. 3, 1243-1257 (2009).
16. Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90 (2012).
17. Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95 (2012).
18. Lebeis, S. L. et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860-864 (2015).
19. 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).
20. Horton, M. W. et al. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun. 5, 5320 (2014).
21. Anderson, J. T., Wagner, M. R., Rushworth, C. A., Prasad, K. V. & Mitchell-Olds, T. The evolution of quantitative traits in complex environments. Heredity (Edinb.) 112, 4-12 (2014).
22. Balint-Kurti, P., Simmons, S. J., Blum, J. E., Ballaré, C. L. & Stapleton, A. E. Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol. Plant Microbe Interact. 23, 473-484 (2010).
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. Boege, K., Dirzo, R., Siemens, D. & Brown, P. Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol. Lett. 10, 177-187 (2007).
25. Pongrac, P. et al. Glucosinolate profiles change during the life cycle and mycorrhizal colonization in a Cd/Zn Hyperaccumulator Thlaspi praecox (Brassicaceae). J. Chem. Ecol. 34, 1038-1044 (2008).
26. Copeland, J. K., Yuan, L., Layeghifard, M., Wang, P. W. & Guttman, D. S. Seasonal community succession of the phyllosphere microbiome. Mol. Plant Microbe Interact. 28, 274-285 (2015).
27. Redford, A. J. & Fierer, N. Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb. Ecol. 58, 189-198 (2009).
28. Maignien, L., DeForce, E. A., Chafee, M. E., Eren, A. M. & Simmons, S. L. Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. mBio 5, e00682-13-e00682-13 (2014).
29. Jackson, C. R. & Denney, W. C. Annual and seasonal variation in the phyllosphere bacterial community associated with leaves of the southern magnolia (Magnolia grandiflora). Microb. Ecol. 61, 113-122 (2011).
30. Rushworth, C. A., Song, B.-H., Lee, C.-R. & Mitchell-Olds, T. Boechera, a model system for ecological genomics. Mol. Ecol. 20, 4843-4857 (2011).
31. Song, B. H., Clauss, M. J., Pepper, A. & Mitchell-Olds, T. Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Mol. Ecol. 15, 357-369 (2006).
32. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
33. McMurdie, P. J. & Holmes, S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 10, e1003531 (2014).
34. Kembel, S. W., Wu, M., Eisen, J. A. & Green, J. L. Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput. Biol. 8, e1002743 (2012).
35. Lozupone, C. A., Hamady, M., Kelley, S. T. & Knight, R. Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576-1585 (2007).
36. Shakya, M. et al. A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS ONE 8, e76382 (2013).
37. Edwards, J. et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl Acad. Sci. USA 112, E911-E920 (2015).
38. Bonito, G. et al. Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol. Ecol. 23, 3356-3370 (2014).
39. Coleman-Derr, D. et al. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol. 209, 798-811 (2016).
40. Redford, A. J., Bowers, R. M., Knight, R., Linhart, Y. & Fierer, N. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves: biogeography of phyllosphere bacterial communities. Environ. Microbiol. 12, 2885-2893 (2010).
41. Vorholt, J. A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828-840 (2012).
42. Lindow, S. E. & Brandl, M. T. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69, 1875-1883 (2003).
43. Kosma, D. & Jenks, M. in Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops (eds Jenks, M., Hasegawa, P. & Jain, S. M.) 91-120 (Springer Netherlands, 2007).
44. Timm, C. M. et al. Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment. Front. Microbiol. 6, 1118 (2015).
45. Bradshaw, A. D. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13, 115-155 (1965).
46. Hoffmann, A. A. & Schiffer, M. Changes in the heritability of five morphological traits under combined environmental stresses in Drosophila melanogaster. Evolution 52, 1207 (1998).
47. Paaby, A. B. & Rockman, M. V. Cryptic genetic variation: evolution's hidden substrate. Nat. Rev. Genet. 15, 247-258 (2014).
48. Holloway, G. J., Povey, S. R. & Sibly, R. M. The effect of new environment on adapted genetic architecture. Heredity 64, 323-330 (1990).
49. Gavrilets, S. & Scheiner, S. M. The genetics of phenotypic plasticity. V. Evolution of reaction norm shape. J. Evol. Biol. 6, 31-48 (1993).
50. Hoffmann, A. & Merliä, J. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14, 96-101 (1999).
51. Falconer, D. The problem of environment and selection. Am. Nat. 86, 293-298 (1952).
52. Zarraonaindia, I. et al. The soil microbiome influences grapevine-associated microbiota. mBio 6, e02527-14 (2015).
53. Bodenhausen, N., Horton, M. W. & Bergelson, J. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8, e56329 (2013).
54. Kim, M. et al. Distinctive phyllosphere bacterial communities in tropical trees. Microb. Ecol. 63, 674-681 (2012).
55. Bai, Y. et al. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528, 364-369 (2015).
56. Tremblay, J. et al. Primer and platform effects on 16S rRNA tag sequencing. Front. Microbiol. 6, 771 (2015).
57. Lundberg, D. S., Yourstone, S., Mieczkowski, P., Jones, C. D. & Dangl, J. L. Practical innovations for high-throughput amplicon sequencing. Nat. Methods 10, 999-1002 (2013).
58. Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963 (2011).
59. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996-998 (2013).
60. DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072 (2006).
61. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
62. Wang, Q., Garrity, G., Tiedje, J. M. & Cole, J. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267 (2007).
63. McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).
64. Wickham, H. in ggplot2: Elegant Graphics For Data Analysis (Springer, 2009).
65. Oksanen, J. F. et al. vegan: community Ecology Package. R package version 2.3-4. https://CRAN.R-project.org/package=vegan.
66. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48 (2015).
67. Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest: Tests in Linear Mixed Effects Models R package version 2.0-30. https://CRAN.R-project. org/package=lmerTest (2016).
68. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300 (1995).
69. Wagner, M. R. et al. Data from: Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Dryad Digit. Reposit. doi:10.5061/ dryad.g60r3 (2016).
70. Becker, R., Wilks, A. & Brownrigg, R. maps: Draw Geographical Maps. R package version 3.1.0. http://CRAN.R-project.org/package=maps (2016).