Dominant groups of potentially active bacteria shared by barley seeds become less abundant in root associated microbiome

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Yang, Luhua ^a   Danzberger, Jasmin ^a   Schöler, Anne ^a   Schröder, Peter ^a   Schloter, Michael ^a   Radl, Viviane ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

16S rRNA barcoding; Hordeum vulgare L.; Root endophytes; Seed microbiome

Indexed keywords

EID: 85021172906     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.01005     Document Type: Article

References (50)

1. Alm, E. W., Oerther, D. B., Larsen, N., Stahl, D. A., and Raskin, L. (1996). The oligonucleotide probe database. Appl. Environ. Microbiol. 62, 3557-3559.
2. Barba-Espin, G., Diaz-Vivancos, P., Job, D., Belghazi, M., Job, C., and Hernandez, J. A. (2011). Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ. 34, 1907-1919. doi: 10.1111/j.1365-3040.2011.02386.x
3. Berendsen, R. L., Pieterse, C. M. J., and Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478-486. doi: 10.1016/j. tplants.2012.04.001
4. Berg, G., Rybakova, D., Grube, M., and Koberl, M. (2016). The plant microbiome explored: implications for experimental botany. J. Exp. Bot. 67, 995-1002. doi: 10.1093/jxb/erv466
5. Bertrand, H., Nalin, R., Bally, R., and Cleyet-Marel, J. C. (2001). Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biol. Fertil. Soils 33, 152-156. doi: 10.1007/s003740000305
6. Bulgarelli, D., Garrido-Oter, R., Munch, P. C., Weiman, A., Droge, J., Pan, Y., et al. (2015). Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17, 392-403. doi: 10.1016/j.chom. 2015.01.011
7. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95. doi: 10.1038/nature11336
8. Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L., and Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807-838. doi: 10.1146/annurev-arplant-050312-120106
9. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f. 303
10. Coleman-Derr, D., Desgarennes, D., Fonseca-Garcia, C., Gross, S., Clingenpeel, S., Woyke, T., et al. (2016). Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol. 209, 798-811. doi: 10.1111/nph.13697
11. Contesto, C., Milesi, S., Mantelin, S., Zancarini, A., Desbrosses, G., Varoquaux, F., et al. (2010). The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232, 1455-1470. doi: 10.1007/s00425-010-1264-0
12. Cope-Selby, N., Cookson, A., Squance, M., Donnison, I., Flavell, R., and Farrar, K. (2016). Endophytic bacteria in Miscanthus seed: implications for germination, vertical inheritance of endophytes, plant evolution and breeding. GCB Bioenergy 9, 57-77. doi: 10.1111/gcbb.12364
13. de Almeida, C. V., Andreote, F. D., Yara, R., Tanaka, F. A. O., Azevedo, J. L., and de Almeida, M. (2009). Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World J. Microbiol. Biotechnol. 25, 1757-1764. doi: 10.1007/s11274-009-0073-8
14. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072. doi: 10.1128/Aem.03006-05
15. Dorn-In, S., Bassitta, R., Schwaiger, K., Bauer, J., and Holzel, C. S. (2015). Specific amplification of bacterial DNA by optimized so-called universal bacterial primers in samples rich of plant DNA. J. Microbiol. Methods 113, 50-56. doi: 10.1016/j.mimet.2015.04.001
16. Edwards, J., Johnson, C., Santos-Medellin, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., et al. (2015). Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U.S.A. 112, E911-E920. doi: 10.1073/pnas.1414592112
17. Goggin, D. E., Emery, R. J. N., Kurepin, L. V., and Powles, S. B. (2015). A potential role for endogenous microflora in dormancy release, cytokinin metabolism and the response to fluridone in Lolium rigidum seeds. Ann. Bot. 115, 293-301. doi: 10.1093/aob/mcu231
18. Griffiths, R. I., Whiteley, A. S., O’Donnell, A. G., and Bailey, M. J. (2000). Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl. Environ. Microbiol. 66, 5488-5491. doi: 10.1128/Aem.66.12. 5488-5491.2000
19. Han, S. C., Li, D., Trost, E., Mayer, K. F., Vlot, A. C., Heller, W., et al. (2016). Systemic Responses of barley to the 3-hydroxy-decanoyl-homoserine lactone producing plant beneficial endophyte acidovorax radicis N35. Front. Plant Sci. 7:1868. doi: 10.3389/Fpls.2016.01868
20. Hardoim, P. R., Hardoim, C. C. P., van Overbeek, L. S., and van Elsas, J. D. (2012). Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7:e30438. doi: 10.1371/journal.pone.0030438
21. Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttila, A. M., Compant, S., Campisano, A., et al. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79, 293-320. doi: 10.1128/Mmbr.00050-14
22. Hardoim, P. R., van Overbeek, L. S., and van Elsas, J. D. (2008). Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463-471. doi: 10.1016/j.tim.2008.07.008
23. Hood, M. A., van Dijk, K. V., and Nelson, E. B. (1998). Factors affecting attachment of Enterobacter cloacae to germinating cotton seed. Microb. Ecol. 36, 101-110. doi: 10.1007/s002489900097
24. Kaul, S., Sharma, T., and Dhar, M. K. (2016). “Omics” tools for better understanding the plant-endophyte interactions. Front. Plant Sci. 7:955. doi: 10.3389/Fpls.2016.00955
25. Kechid, M., Desbrosses, G., Rokhsi, W., Varoquaux, F., Djekoun, A., and Touraine, B. (2013). The NRT2.5 and NRT2.6 genes are involved in growth promotion of Arabidopsis by the plant growth-promoting rhizobacterium (PGPR) strain Phyllobacterium brassicacearum STM196. New Phytol. 198, 514-524. doi: 10.1111/nph.12158
26. Kefela, T., Gachomo, E. W., and Kotchoni, S. O. (2015). Paenibacillus polymyxa, Bacillus licheniformis and Bradyrhizobium japonicum IRAT FA3 promote faster seed germination rate, growth and disease resistance under pathogenic pressure. J. Plant Biochem. Physiol. 3:145. doi: 10.4172/2329-9029.1000145
27. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., et al. (2013). Evaluationofgeneral 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1. doi: 10.1093/Nar/Gks808
28. Kristin, A., and Miranda, H. (2013). The root microbiota-a fingerprint in the soil? Plant Soil 370, 671-686. doi: 10.1007/s11104-013-1647-7
29. Kumar, M., Agnihotri, R. K., Vamil, R., and Sharma, R. (2014). Effect of phytohormones on seed germination and seedling growth of Coriandrum sativum L. Pak. J. Biol. Sci. 17, 594-596. doi: 10.3923/pjbs.2014.594.596
30. Kutter, S., Hartmann, A., and Schmid, M. (2006). Colonization of barley (Hordeum vulgare) with Salmonella enterica and Listeria spp. FEMS Microbiol. Ecol. 56, 262-271. doi: 10.1111/j.1574-6941.2005.00053.x
31. Lindgreen, S. (2012). AdapterRemoval: easy cleaning of next-generation sequencing reads. BMC Res. Notes 5:337. doi: 10.1186/1756-05 00-5-337
32. Lopez-Lopez, A., Rogel, M. A., Ormeno-Orrillo, E., Martinez-Romero, J., and Martinez-Romero, E. (2010). Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst. Appl. Microbiol. 33, 322-327. doi: 10.1016/j.syapm.2010. 07.005
33. Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-92. doi: 10.1038/Nature11237
34. Mantelin, S., Fischer-Le Saux, M., Zakhia, F., Bena, G., Bonneau, S., Jeder, H., et al. (2006). Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots: Phyllobacterium bourgognense sp nov., Phyllobacterium ifriqiyense sp nov., Phyllobacterium leguminum sp nov and Phyllobacterium brassicacearum sp nov. Int. J. Syst. Evol. Microbiol. 56, 827-839. doi: 10.1099/ijs.0.63911-0
35. Muyzer, G., de Waal, E. C., and Uitterlinden, A. G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695-700.
36. Oracz, K., El-Maarouf-Bouteau, H., Bogatek, R., Corbineau, F., and Bailly, C. (2008). Release of sunflower seed dormancy by cyanide: cross-talk with ethylene signalling pathway. J. Exp. Bot. 59, 2241-2251. doi: 10.1093/jxb/ern089
37. Palaniyandi, S. A., Yang, S. H., Zhang, L. X., and Suh, J. W. (2013). Effects of actinobacteria on plant disease suppression and growth promotion. Appl. Microbiol. Biotechnol. 97, 9621-9636. doi: 10.1007/s00253-013-5206-1
38. Peiffer, J. A., Spor, A., Koren, O., Jin, Z., Tringe, S. G., Dangl, J. L., et al. (2013). Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. U.S.A. 110, 6548-6553. doi: 10.1073/pnas. 1302837110
39. Pitzschke, A. (2016). Developmental peculiarities and seed-borne endophytes in quinoa: omnipresent, robust bacilli contribute to plant fitness. Front. Microbiol. 7:2. doi: 10.3389/fmicb.2016.00002
40. Puente, M. E., Li, C. Y., and Bashan, Y. (2009). Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ. Exp. Bot. 66, 402-408. doi: 10.1016/j.envexpbot.2009.04.007
41. Reinhold-Hurek, B., Bunger, W., Burbano, C. S., Sabale, M., and Hurek, T. (2015). Roots shaping their microbiome: global hotspots for microbial activity. Annu. Rev. Phytopathol. 53, 403-424. doi: 10.1146/annurev-phyto-082712-102342
42. Reiter, B., Wermbter, N., Gyamfi, S., Schwab, H., and Sessitsch, A. (2003). Endophytic Pseudomonas spp. populations of pathogen-infected potato plants analysed by 16S rDNA- and 16S rRNA-based denaturating gradient gel electrophoresis. Plant Soil 257, 397-405. doi: 10.1023/A:1027382232391
43. Rodrigues, A. C., Bonifacio, A., Antunes, J. E. L., da Silveira, J. A. G., and Figueiredo, M. D. B. (2013). Minimization of oxidative stress in cowpea nodules by the interrelationship between Bradyrhizobium sp and plant growth-promoting bacteria. Appl. Soil Ecol. 64, 245-251. doi: 10.1016/j.apsoi1.2012. 12.018
44. Schmieder, R., and Edwards, R. (2011). Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE 6:e17288. doi: 10.1371/journal.pone.0017288
45. Spohn, M., Treichel, N. S., Cormann, M., Schloter, M., and Fischer, D. (2015). Distribution of phosphatase activity and various bacterial phyla in the rhizosphere of Hordeum vulgare L. depending on P availability. Soil Biol. Biochem. 89, 44-51. doi: 10.1016/j.soilbio.2015.06.018
46. Sultan, A., Andersen, B., Svensson, B., and Finnie, C. (2016). Exploring the plant-microbe interface by profiling the surface-associated proteins of barley grains. J. Proteome Res. 15, 1151-1167. doi: 10.1021/acs.jproteome.5b01042
47. Timmusk, S., and Wagner, E. G. H. (1999). The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant Microbe Interact. 12, 951-959. doi: 10.1094/MPMI.1999. 12.11.951
48. Truyens, S., Weyens, N., Cuypers, A., and Vangronsveld, J. (2015). Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ. Microbiol. Rep. 7, 40-50. doi: 10.1111/1758-2229.12181
49. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267. doi: 10.1128/Aem. 00062-07
50. Zadoks, J. C., Chang, T. T., and Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Res. 14, 415-421. doi: 10.1111/j.1365-3180.1974. tb01084.x