Original Article

The plant circadian clock influences rhizosphere community structure and function

  • The ISME Journal volume 12, pages 400410 (2018)
  • doi:10.1038/ismej.2017.172
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Abstract

Plants alter chemical and physical properties of soil, and thereby influence rhizosphere microbial community structure. The structure of microbial communities may in turn affect plant performance. Yet, outside of simple systems with pairwise interacting partners, the plant genetic pathways that influence microbial community structure remain largely unknown, as are the performance feedbacks of microbial communities selected by the host plant genotype. We investigated the role of the plant circadian clock in shaping rhizosphere community structure and function. We performed 16S ribosomal RNA gene sequencing to characterize rhizosphere bacterial communities of Arabidopsis thaliana between day and night time points, and tested for differences in community structure between wild-type (Ws) vs clock mutant (toc1-21, ztl-30) genotypes. We then characterized microbial community function, by growing wild-type plants in soils with an overstory history of Ws, toc1-21 or ztl-30 and measuring plant performance. We observed that rhizosphere community structure varied between day and night time points, and clock misfunction significantly altered rhizosphere communities. Finally, wild-type plants germinated earlier and were larger when inoculated with soils having an overstory history of wild-type in comparison with clock mutant genotypes. Our findings suggest the circadian clock of the plant host influences rhizosphere community structure and function.

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References

  1. , . (2009). Regulation and function of root exudates. Plant Cell Environ 32: 666–681.

  2. , , , , . (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233–266.

  3. . (1998). Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16: 729–770.

  4. , , . (2012). The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478–486.

  5. , , , , , et al. (2012). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10: 57–59.

  6. , , , , . (2016). Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat Plants 2: 15208.

  7. , , , , , et al. (2001). Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and the effects of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33: 1683–1694.

  8. , , , , , et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91–95.

  9. , , , , . (2013). Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64: 807–838.

  10. , . (2009). Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566–3574.

  11. , , . (2001). Effect of N2-fixing bacterial inoculations on yield of sugar beet and barley. J Plant Nutr Soil Sci 164: 527.

  12. , , , , , et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.

  13. , , . (2014). Rhizosphere microbiome assemblage is affected by plant development. ISME J 8: 790–803.

  14. , , , . (2002). Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol Biochem 34: 487–499.

  15. , , , , , et al. (2014). Dynamic succession of soil bacterial community during continuous cropping of peanut (Arachis hypogaea L.). PLoS One 9: e101355.

  16. , , , , . (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9: R130.

  17. , , , , , et al. (2015). Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6: 104.

  18. , , . (2010). Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72: 313–327.

  19. , , . (2004). Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol 162: 63–70.

  20. , , , , , et al. (2005). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science (80-) 309: 630–633.

  21. , . (1997). Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67: 345–366.

  22. . (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.

  23. , . (2002). Root colonization and growth promotion of winter wheat and pea by Cellulomonas spp. at different temperatures. Plant Growth Regul 38: 219–224.

  24. , . (2011). An R companion to applied regression. Sage Publications: Thousand Oaks, CA, USA.

  25. , , , , , et al. (2008). Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J Biol Chem 283: 23073–23083.

  26. , . (2015). Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16: 598–610.

  27. , , , , , et al. (2011). Chimeric 16 S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21: 494–504.

  28. . (2009). The circadian system in higher plants. Annu Rev Plant Biol 60: 357–377.

  29. , , , , , et al. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110–2113.

  30. , . (2007). Context dependence in the coevolution of plant and rhizobial mutualists. Proc Biol Sci 274: 1905–12.

  31. , , , , , . (2016). Root bacterial endophytes alter plant phenotype, but not physiology. PeerJ 4: e2606.

  32. , , , , , et al. (2007). Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ 30: 333–349.

  33. , , , . (1999). Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Can J Bot 77: 1311–1315.

  34. , , , , , et al. (2014). Comparison of brush and biopsy sampling methods of the ileal pouch for assessment of mucosa-associated microbiota of human subjects. Microbiome 2: 5.

  35. , , . (2003). A new approach for the quantification of root-cap mucilage exudation in the soil. Plant Soil 255: 399–407.

  36. , . (1992). Light pulses induce ‘singular’ behavior and shorten the period of the circadian phototaxis rhythm in the CW15 strain of chlamydomonas. J Biol Rhythms 7: 313–327.

  37. , , . (2009). Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321: 5–33.

  38. , , , , , et al. (2006). Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE. Plant Physiol 140: 933–945.

  39. , , . (2016). Acidobacteria strains from subdivision 1 act as plant growth-promoting bacteria. Arch Microbiol 198: 987–993.

  40. , , . (2005). Independent roles for EARLY FLOWERING 3 and ZEITLUPE in the control of circadian timing, hypocotyl length, and flowering time. Plant Physiol 139: 1557–1569.

  41. , , , , . (2008). Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304: 35–44.

  42. , . (2011). Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192: 215–224.

  43. , , , , , et al. (2015). Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science (80-) 349: 860–864.

  44. , . (2009). Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541–556.

  45. , , , , , et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86–90.

  46. , , , , , . (2014). Soil sterilization effects on root growth and formation of rhizosheaths in wheat seedlings. Pedobiologia (Jena) 57: 123–130.

  47. , , . (2014). Do hydraulic redistribution and nocturnal transpiration facilitate nutrient acquisition in Aspalathus linearis? Oecologia 175: 1129–1142.

  48. . (1998). Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am Nat 151: 20–28.

  49. . (2006). Plant circadian rhythms. Plant Cell 18: 792–803.

  50. , , , , , et al. (2012). An improved green genes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6: 610–8.

  51. , , , , . (2014). Waste not, want not: why rarefying microbiome data is inadmissible McHardy AC (ed). PLoS Comput Biol 10: e1003531.

  52. , , . (2013). The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37: 634–663.

  53. , , , , , et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science (80-), 332 1097–100.

  54. . (2016). agricolae: Statistical Procedures for Agricultural Research .

  55. , , , , . (1995). Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267: 1161–1163.

  56. , , , , , et al. (2015). Natural diversity in daily rhythms of gene expression contributes to phenotypic variation. Proc Natl Acad Sci USA 112: 905–910.

  57. , , , , , et al. (2014). Analysis, Optimization and Verification of Illumina-Generated 16S rRNA Gene Amplicon Surveys. PLoS One 9: e94249.

  58. , , , , . (2014). Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9: 980–989.

  59. , , , , , et al. (2013). Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110: 6548–6553.

  60. , , . (2016). Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol 90: 635–644.

  61. R Core Team. (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.

  62. , , , . (2009). Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321: 305–339.

  63. , . (2011). Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156: 989–996.

  64. , , . (2016). Nicotiana roots recruit rare rhizosphere taxa as major root-inhabiting microbes. Microb Ecol 71: 469–472.

  65. , , , , , . (2016). Variation in circadian rhythms is maintained among and within populations in Boechera stricta. Plant Cell Environ 39: 1293–1303.

  66. , , , , , et al. (2011). Metagenomic biomarker discovery and explanation. Genome Biol 12: R60.

  67. , , , . (1998). Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant, Cell Environ 21: 347–359.

  68. , , , , , et al. (2014). Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci USA 111: 6341–6346.

  69. , . (2010). Elucidation of a diurnal pattern of catechin exudation by centaurea stoebe. J Chem Ecol 36: 200–204.

  70. , , , , . (2004). Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labelling. Physiol Plant 120: 434–441.

  71. , , , , , . (1997). The influence of functional diversity and composition on ecosystem processes. Science (80-) 277: 1300–1302.

  72. . (1996). Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26: 53–59.

  73. , , . (2012). Soil inoculation method determines the strength of plant–soil interactions. Soil Biol Biochem 55: 1–6.

  74. , , , , , . (2014). Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol Lett 17: 717–26.

  75. , , , , , et al. (2016). Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7: 12151.

  76. , . (1999). Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120: 705–716.

  77. , , , , , et al. (2011). PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa. FEMS Microbiol Ecol 75: 497–506.

  78. . (2009) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York: New York.

  79. , . (2009). Evidence for the adaptive significance of circadian rhythms. Ecol Lett 12: 970–981.

  80. , , , , . (2013). Soil microbiomes vary in their ability to confer drought tolerance to ArabidopsisAppl Soil Ecol 68: 1–9.

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Acknowledgements

This work was supported by the National Science Foundation grants IOS-1444571 to CW, BEE, LM and OIA-1655726 to CW and BEE, and a Wyoming INBRE sequencing and bioinformatics award to CH and CW. We thank the Powells’ for allowing us to collect soil from their property and Lindsay Leverett for collecting soil from the Catsburg site.

Author information

Affiliations

  1. Department of Botany, University of Wyoming, Laramie, WY, USA

    • Charley J Hubbard
    • , Marcus T Brock
    • , Brent E Ewers
    •  & Cynthia Weinig
  2. Program in Ecology, University of Wyoming, Laramie, WY, USA

    • Charley J Hubbard
    • , Linda TA van Diepen
    • , Brent E Ewers
    •  & Cynthia Weinig
  3. Ecosystem Science and Management, University of Wyoming, Laramie, WY, USA

    • Linda TA van Diepen
  4. Marine Biological Laboratory, Josephine Bay Paul Center, Woods Hole, MA, USA

    • Loïs Maignien
  5. Laboratory of Microbiology of Extreme Environments, UMR 6197, Institut Européen de la Mer, Université de Bretagne Occidentale, Plouzane, France

    • Loïs Maignien
  6. Department of Molecular Biology, University of Wyoming, Laramie, WY, USA

    • Cynthia Weinig

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Competing interests

The authors declare no conflict of interest.

Corresponding author

Correspondence to Cynthia Weinig.

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