Bacterial communities in the rhizosphere, phyllosphere and endosphere of tomato plants

English version

Autoři: Chun-Juan Dong ^aff001; Ling-Ling Wang ^aff001; Qian Li ^aff001; Qing-Mao Shang ^aff001
Působiště autorů: Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Key Laboratory of Horticultural Crop Biology and Germplasm Innovation, Ministry of Agriculture, Beijing, P.R. China ^aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223847

Souhrn

Plants harbor diverse bacterial communities, which play crucial roles in plant health and growth, in their rhizosphere, phyllosphere and endosphere. Tomato is an important model for studying plant-microbe interactions, but comparison of its associated bacterial community is still lacking. In this study, using Illumina sequencing of 16S rRNA amplicons, we characterized and compared the bacterial size and community from rootzone soil as well as the rhizosphere, phyllosphere and endosphere of roots, stems, leaves, fruits and seeds of tomato plants that were grown in greenhouse conditions. Habitat (soil, phyllospheric, and endophytic) structured the community. The bacterial communities from the soil-type samples (rootzone soil and rhizosphere) showed the highest richness and diversity. The lowest bacterial diversity occurred in the phyllospheric samples, while the lowest richness occurred in the endosphere. Among the endophytic samples, both bacterial diversity and richness varied in different tissues, with the highest values in roots. The most abundant phyla in the tomato-associated community was Proteobacteria, with the exception of the seeds and jelly, where both Proteobacteria and Firmicutes were dominant. At the genus level, the sequences of Pseudomonas and Acinetobacter were prevalent in the rhizosphere, and in the phyllosphere, more than 97% of the sequences were assigned to Acinetobacter. For the endophytes, Acinetobacter, Enterobacter, and Pseudomonas were the abundant genera in the roots, stems and leaves. In the fruits, the bacterial endophytes varied in different compartments, with Enterobacter being enriched in the pericarp and seeds, Acinetobacter in the placenta, and Weissella in the jelly. The present data provide a comprehensive description of the tomato-associated bacterial community and will be useful for better understanding plant-microbe interactions and selecting suitable bacterial taxa for tomato production.

Klíčová slova:

Acinetobacter – Bacteria – Leaves – Pseudomonas – Rhizosphere – Seeds – Tomatoes – Enterobacter

Zdroje

1. Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma LJ. et al. Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol. 2017; 55: 61–83. doi: 10.1146/annurev-phyto-080516-035641 28489497

2. 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. 2013; 64: 807–838. doi: 10.1146/annurev-arplant-050312-120106 23373698

3. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 2009; 321: 341–361.

4. Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E. et al. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci. 2018; 9: 1473. doi: 10.3389/fpls.2018.01473 30405652

5. Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev. 2013; 37: 634–663. doi: 10.1111/1574-6976.12028 23790204

6. Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM. Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 2012; 360: 1–13.

7. Vorholt JA. Microbial life in the phyllosphere. Nat Rev Microbiol. 2012; 10: 828–840. doi: 10.1038/nrmicro2910 23154261

8. Bringel F, Couée I. Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front Microbiol. 2015; 6: 486. doi: 10.3389/fmicb.2015.00486 26052316

9. Afzal I, Shinwari ZK, Sikandar S, Shahzad S. Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiol Res. 2019; 221: 36–49. doi: 10.1016/j.micres.2019.02.001 30825940

10. Rosenblueth M, Martínez-Romero E. Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact. 2006; 19: 827–837. doi: 10.1094/MPMI-19-0827 16903349

11. Singh R, Dubey AK. Diversity and applications of endophytic Actinobacteria of plants in special and other ecological niches. Front Microbiol. 2018; 9: 1767. doi: 10.3389/fmicb.2018.01767 30135681

12. Chaturvedi H, Singh V, Gupta G. Potential of bacterial endophytes as plant growth promoting factors. J Plant Pathol Microbiol. 2016; 7: 2.

13. Müller T, Ruppel S. Progress in cultivation-independent phyllosphere microbiology. FEMS Microbiol Ecol. 2014; 87: 2–17. doi: 10.1111/1574-6941.12198 24003903

14. Bai Y, Kissoudis C, Yan Z, Visser RGF, van der Linden G. Plant behaviour under combined stress: tomato responses to combined salinity and pathogen stress. Plant J. 2018; 93: 781–793. doi: 10.1111/tpj.13800 29237240

15. Karlova R, Chapman N, David K, Angenent GC, Seymour GB, de Maagd RA. Transcriptional control of fleshy fruit development and ripening. J Exp Bot. 2014; 65: 4527–4541. doi: 10.1093/jxb/eru316 25080453

16. Singh VK, Singh AK, Kumar A. Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech. 2017; 7: 255. doi: 10.1007/s13205-017-0896-1 28730550

17. Raza W, Ling N, Zhang R, Huang Q, Xu Y, Shen Q. Success evaluation of the biological control of Fusarium wilts of cucumber, banana, and tomato since 2000 and future research strategies. Crit Rev Biotechnol. 2017; 37: 202–212. doi: 10.3109/07388551.2015.1130683 26810104

18. Romero FM, Marina M, Pieckenstain FL. Novel components of leaf bacterial communities of field-grown tomato plants and their potential for plant growth promotion and biocontrol of tomato diseases. Res Microbiol. 2016; 167: 222–233. doi: 10.1016/j.resmic.2015.11.001 26654914

19. de Lamo FJ, Constantin ME, Fresno DH, Boeren S, Rep M, Takken FLW. Xylem sap proteomics reveals distinct differences between R gene- and endophyte-mediated resistance against Fusarium wilt disease in tomato. Front Microbiol. 2018; 9: 2977. doi: 10.3389/fmicb.2018.02977 30564219

20. Marquez-Santacruz H, Hernandez-Leon R, Orozco-Mosqueda M, Velazquez-Sepulveda I, Santoyo G. Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalisixocarpa) and their detection in the rhizosphere. Genet Mol Res. 2010; 9: 2372–2380. doi: 10.4238/vol9-4gmr921 21157706

21. Ottesen AR, González Peña A, White JR, Pettengill JB, Li C, Allard S, et al. Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiol. 2013; 13: 114. doi: 10.1186/1471-2180-13-114 23705801

22. Romero FM, Marina M, Pieckenstain FL. The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS Micorbiol Lett. 2015; 351: 187–194.

23. Allard SM, Walsh CS, Wallis AE, Ottesen AR, Brown EW, Micallef SA. Solanum lycopersicum (tomato) hosts robust phyllosphere and rhizosphere bacterial communities when grown in soil amended with various organic and synthetic fertilizers. Sci Total Environ. 2016; 573: 555–563. doi: 10.1016/j.scitotenv.2016.08.157 27580466

24. Tian BY, Cao Y, Zhang KQ. Metagenomic insights into communities, functions of endophytes, and their associates with infection by root-knot nematode, Meloidogyne incognita, in tomato roots. Sci Rep. 2015; 5: 17087. doi: 10.1038/srep17087 26603211

25. Toju H, Okayasu K, Notaguchi M. Leaf-associated microbiomes of grafted tomato plants. Sci Rep. 2019; 9: 1787. doi: 10.1038/s41598-018-38344-2 30741982

26. Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, et al. Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res. 2014; 21: 217–227. doi: 10.1093/dnares/dst052 24277737

27. Tremblay J, Singh K, Fern A, Kirton ES, He S, Woyke T, et al. Primer and platform effects on 16S rRNA tag sequencing. Front Microbiol. 2015; 6: 771. doi: 10.3389/fmicb.2015.00771 26300854

28. Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, et al. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol. 2016; 209: 798–811. doi: 10.1111/nph.13697 26467257

29. Rezki S, Campion C, Iacomi-Vasilescu B, Preveaux A, Toualbia Y, Bonneau S, et al. Differences in stability of seed-associated microbial assemblages in response to invasion by phytopathogenic microorganisms. Peer J. 2016; 4: e1923. doi: 10.7717/peerj.1923 27077013

30. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011; 27: 2194–2200. doi: 10.1093/bioinformatics/btr381 21700674

31. Bodenhausen N, Horton MW, Bergelson J. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 2013; 8: e56329. doi: 10.1371/journal.pone.0056329 23457551

32. Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada HR, et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 2013; 7: 1344–1353. doi: 10.1038/ismej.2013.16 23486247

33. Schloss PD, Gevers D, Westcott SL. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 2011; 6: e27310. doi: 10.1371/journal.pone.0027310 22194782

34. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005; 71: 8228–8235. doi: 10.1128/AEM.71.12.8228-8235.2005 16332807

35. Yashiro E, McManus PS. Effect of streptomycin treatment on bacterial community structure in the apple phyllosphere. PLoS ONE 2012; 7: e37131. doi: 10.1371/journal.pone.0037131 22629357

36. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, et al. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA. 2009; 106: 16428–16433. doi: 10.1073/pnas.0905240106 19805315

37. Knief C, Delmotte N, Chaffron S, Stark M, Inn erebner G, et al. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 2012; 6:1378–1390. doi: 10.1038/ismej.2011.192 22189496

38. Lindow SE, Leveau JH. Phyllosphere microbiology. Curr Opin Biotechnol. 2002; 13: 238–243. doi: 10.1016/s0958-1669(02)00313-0 12180099

39. Rastogi G, Coaker GL, Leveau JHJ. New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett. 2013; 348: 1–10. doi: 10.1111/1574-6968.12225 23895412

40. Hardoim PR, van Overbeek LS, van Elsas JD. Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 2008; 16: 463–471. doi: 10.1016/j.tim.2008.07.008 18789693

41. Andreote FD, Pereira E Silva MC. Microbial communities associated with plants: learning from nature to apply it in agriculture. Curr Opin Microbiol. 2017; 37: 29–34. doi: 10.1016/j.mib.2017.03.011 28437663

42. Czajkowski R, de Boer WJ, Velvis H, van der Wolf JM. Systemic colonization of potato plants by a soilborne, green fluorescent protein-tagged strain of Dickeya sp. biovar 3. Phytopathology 2010; 100: 134–142. doi: 10.1094/PHYTO-100-2-0134 20055647

43. Wang W, Zhai Y, Cao L, Tan H, Zhang R. Endophytic bacterial and fungal microbiota in sprouts, roots and stems of rice (Oryza sativa L.). Microbiol Res. 2016; 188–189: 1–8. doi: 10.1016/j.micres.2016.04.009 27296957

44. Gans J, Wolinsky M, Dunbar J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 2005; 309:1387–1390. doi: 10.1126/science.1112665 16123304

45. Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD. Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol. 2011; 77: 154–164. doi: 10.1111/j.1574-6941.2011.01092.x 21426364

46. Tian XY, Zhang CS. Illumina-based analysis of endophytic and rhizosphere bacterial diversity of the coastal halophyte Messerschmidia sibirica. Front Microbiol. 2017; 8: 2288. doi: 10.3389/fmicb.2017.02288 29209296

47. Lee SA, Park J, Chu B, Kim JM, Joa JH, Sang MK, et al. Comparative analysis of bacterial diversity in the rhizosphere of tomato by culture-dependent and -independent approaches. J Microbiol. 2016; 54: 823–831. doi: 10.1007/s12275-016-6410-3 27888459

48. Magnucka EG, Pietr SJ. Various effects of fluorescent bacteria of the genus Pseudomonas containing ACC deaminase on wheat seedling growth. Microbiol Res. 2015; 181: 112–119. doi: 10.1016/j.micres.2015.04.005 25983132

49. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JH. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 2012; 6:1812–1822. doi: 10.1038/ismej.2012.32 22534606

50. Manter DK, Delgado JA, Holm DG, Stong RA. Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol. 2010; 60: 157–166. doi: 10.1007/s00248-010-9658-x 20414647

51. Lopez-Velasco G, Tydings HA, Boyer RR, Falkinham JO 3rd, Ponder MA. Characterization of interactions between Escherichia coli O157:H7 with epiphytic bacteria in vitro and on spinach leaf surfaces. Int J Food Microbiol. 2012; 153: 351–357. doi: 10.1016/j.ijfoodmicro.2011.11.026 22177225

52. Compant S, Kaplan H, Sessitsch A, Nowak J, Barka EA, Clement C. Endophytic colonization of Vitis vinifera L. by Burkholderia phytofiimans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol. 2008; 63: 84–93. doi: 10.1111/j.1574-6941.2007.00410.x 18081592

53. Zhao J, Xu Y, Ding Q, Huang X, Zhang Y, Zou Z, et al. Association mapping of main tomato fruit sugars and organic acids. Front Plant Sci. 2016; 7: 1286. doi: 10.3389/fpls.2016.01286 27617019

54. Amari M, Arango LF, Gabriel V, Robert H, Morel S, Moulis C, et al. Characterization of a novel dextransucrase from Weissella confusa isolated from sourdough. Appl Microbiol Biotechnol. 2013; 97: 5413–5422. doi: 10.1007/s00253-012-4447-8 23053097

55. Porter NT, Luis AS, Martens EC. Bacteroides thetaiotaomicron. Trends Microbiol. 2018; 26: 966–967. doi: 10.1016/j.tim.2018.08.005 30193959

56. Halpern M, Fridman S, Atamna-Ismaeel N, Izhaki I. Rosenbergiella nectarea gen. nov., sp. nov., in the family Enterobacteriaceae, isolated from floral nectar. Int J Syst Evol Microbiol. 2013; 63: 4259–4265. doi: 10.1099/ijs.0.052217-0 23832968

Bacterial communities in the rhizosphere, phyllosphere and endosphere of tomato plants

Souhrn

Klíčová slova:

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