Salinity-induced changes in the rhizosphere microbiome improve salt tolerance of Hibiscus hamabo

Abstract

Aims

We aimed to assess whether soil salinity changes the microbial community in the rhizosphere of Hibiscus hamabo, and whether these changes in the microbiome feedback on the growth of H. hamabo.

Methods

To test effects of salinity on the rhizosphere microbiome, we first did a greenhouse experiment in which H. hamabo was grown in pots with a sand-soil mixture at different salt concentrations (0, 15, 40 and 90 mM NaCl). Then in another two experiments, we tested effects of the rhizosphere microbiomes on performance of H. hamabo plants by sowing and growing them in pots with a peat-sand-vermiculite mixture inoculated with either soil or root fragments collected from the different salinity treatments (0, 40 and 90 mM NaCl) of the first experiment and crossed with a salinity treatment (0, 40 and 90 mM NaCl).

Results

The bacterial rhizosphere community of H. hamabo was less affected by soil salinities than the fungal community was. Germination and biomass of H. hamabo were highest at a salinity of 40 mM NaCl, and higher in the presence than in the absence of microbial inoculums. Moreover, H. hamabo performed best when the microbial inocula came from the same salinity level, particularly at a salinity of 40 mM NaCl.

Conclusions

Our study provides evidence that salinity-induced changes in rhizosphere microbial communities tend to promote germination and growth of H. hamabo at the respective salinities.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic 109:1–7. https://doi.org/10.1016/j.scienta.2006.02.019

    Article  Google Scholar 

  2. Andronov EE, Petrova SN, Pinaev AG, Pershina EV, Rakhimgalieva SZ, Akhmedenov KM, Gorobets AV, Sergaliev NK (2012) Analysis of the structure of microbial community in soils with different degrees of salinization using T-RFLP and real-time PCR techniques. Eurasian Soil Sci 45:147–156. https://doi.org/10.1134/s1064229312020044

    CAS  Article  Google Scholar 

  3. Aroca R, Ruiz-Lozano JM, Zamarreno AM, Paz JA, Garcia-Mina JM, Pozo MJ, Lopez-Raez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55. https://doi.org/10.1016/j.jplph.2012.08.020

    CAS  Article  PubMed  Google Scholar 

  4. Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schafer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510. https://doi.org/10.1111/j.1469-8137.2008.02583.x

    CAS  Article  PubMed  Google Scholar 

  5. Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants-an economic analogy. Annu. Rev Ecol Systemat 16:363–392. https://doi.org/10.1146/annurev.es.16.110185.002051

    Article  Google Scholar 

  6. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115. https://doi.org/10.1111/j.1461-0248.2007.01130.x

    Article  PubMed  Google Scholar 

  7. Bothe H (2012) Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis 58:7–16. https://doi.org/10.1007/s13199-012-0196-9

    CAS  Article  Google Scholar 

  8. Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456. https://doi.org/10.1111/j.1469-8137.2009.03003.x

    CAS  Article  PubMed  Google Scholar 

  9. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughputcommunity sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428. https://doi.org/10.1093/jxb/ers033

    CAS  Article  PubMed  Google Scholar 

  11. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbialamplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    CAS  Article  PubMed  Google Scholar 

  12. Elhindi K, El Din AS, Abdel-Salam E, Elgorban A (2016) Amelioration of salinity stress in different basil (Ocimum basilicum L.) varieties by vesicular-arbuscular mycorrhizal fungi. Acta Agr Scand B-S P 66:583–592. https://doi.org/10.1080/09064710.2016.1204467

    CAS  Article  Google Scholar 

  13. Enebe MC, Babalola OO (2018) The influence of plant growth-promoting rhizobacteria in plant tolerance to abiotic stress: a survival strategy. Appl Microbiol Biot 102:7821–7835. https://doi.org/10.1007/s00253-018-9214-z

    CAS  Article  Google Scholar 

  14. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280. https://doi.org/10.1093/aob/mcp251

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  16. Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fert Soils 38:170–175. https://doi.org/10.1007/s00374-003-0636-z

    Article  Google Scholar 

  17. Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760. https://doi.org/10.1007/s00248-007-9239-9

    CAS  Article  PubMed  Google Scholar 

  18. Göransson H, Welc M, Bünemann EK, Christl I, Venterink HO (2016) Nitrogen and phosphorus availability at early stages of soil development in the Damma glacier forefield, Switzerland; implications for establishment of N2-fixing plants. Plant Soil 404:251–261. https://doi.org/10.1007/s11104-016-2821-5

    CAS  Article  Google Scholar 

  19. Hashem A, Abd Allah EF, Alqarawi AA, Ai-Huqail AA, Wirth S, Egamberdieva D (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089. https://doi.org/10.3389/fmicb.2016.01089

    Article  PubMed  PubMed Central  Google Scholar 

  20. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53. https://doi.org/10.1007/s00248-007-9249-7

    Article  PubMed  Google Scholar 

  21. Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379. https://doi.org/10.1007/s00572-006-0046-9

    CAS  Article  PubMed  Google Scholar 

  22. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  23. Lastochkina O, Pusenkova L, Yuldashev R, Babaev M, Garipova S, Blagova D, Khairullin R, Aliniaeifard S (2017) Effects of Bacillus subtilis on some physiological and biochemical parameters of Triticum aestivum L. (wheat) under salinity. Plant Physiol Bioch 121:80–88. https://doi.org/10.1016/j.plaphy.2017.10.020

    CAS  Article  Google Scholar 

  24. Lau JA, Lennon JT (2011) Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224. https://doi.org/10.1111/j.1469-8137.2011.03790.x

    Article  PubMed  Google Scholar 

  25. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109:14058–14062. https://doi.org/10.1073/pnas.1202319109

    Article  PubMed  Google Scholar 

  26. Li HY (2008) Three dimensional variability and visualization of soil electrical conductivity in coastal saline land. PhD Thesis. Zhejiang University

  27. Li JM, Liao JJ, Guan M, Wang EF, Zhang J (2012) Salt tolerance of Hibiscus hamabo seedlings: a candidate halophyte for reclamation areas. Acta Physiol Plant 34:1747–1755. https://doi.org/10.1007/s11738-012-0971-5

    CAS  Article  Google Scholar 

  28. Li HS, Lei P, Pang X, Li S, Xu H, Xu ZQ, Feng XH (2017) Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl Soil Ecol 119:26–34. https://doi.org/10.1016/j.apsoil.2017.05.033

    CAS  Article  Google Scholar 

  29. Lin X, Feng Y, Zhang H, Chen R, Wang J, Zhang J, Chu H (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity inan arable soil in North China revealed by 454 pyrosequencing. Environ SciTechnol 46:5764–5771. https://doi.org/10.1021/es3001695

    CAS  Article  Google Scholar 

  30. Mohamed DJ, Martiny JBH (2011) Patterns of fungal diversity and composition along a salinity gradient. Isme J 5:379–388. https://doi.org/10.1038/ismej.2010.137

    Article  PubMed  Google Scholar 

  31. Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  32. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692. https://doi.org/10.1016/j.tplants.2010.09.008

    CAS  Article  PubMed  Google Scholar 

  33. Oduor AMO, Leimu R, van Kleunen M (2016) Invasive plant species are locally adapted just as frequently and at least as strongly as native plant species. J Ecol 104:957–968. https://doi.org/10.1111/1365-2745.12578

    Article  Google Scholar 

  34. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P (2011) The vegan package: community ecology package. R package version 2.0--2. Available: http://www.R-project.org. Accessed on 3.2.2015

  35. Pankhurst CE, Yu S, Hawke BG, Harch BD (2001) Capacity of fatty acid profiles and substrate utilization patterns to describe differences in soil microbial communities associated with increased salinity or alkalinity at three locations in South Australia. Biol Fert Soils 33:204–217. https://doi.org/10.1007/s003740000309

    CAS  Article  Google Scholar 

  36. Patel S, Jinal HN, Amaresan N (2017) Isolation and characterization of drought resistance bacteria for plant growth promoting properties and their effect on chilli (Capsicum annuum) seedling under salt stress. Biocatal Agric Biotechnol 12:85–89. https://doi.org/10.1016/j.bcab.2017.09.002

    Article  Google Scholar 

  37. Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200. https://doi.org/10.1007/s13593-011-0029-x

    CAS  Article  Google Scholar 

  38. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. Accessed on 3.2.2015

  39. Rath KM, Rousk J (2015) Salt effects on the soil microbial decomposer community and their role in organic carbon cycling: a review. Soil Biol Biochem 81:108–123. https://doi.org/10.1016/j.soilbio.2014.11.001

    CAS  Article  Google Scholar 

  40. Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Systemat 18:209–235. https://doi.org/10.1146/annurev.ecolsys.18.1.209

    Article  Google Scholar 

  41. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. Isme J 2:404–416. https://doi.org/10.1038/ismej.2007.106

    Article  PubMed  Google Scholar 

  42. Ruiz-Lozano JM, Porcel R, Azcon C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044. https://doi.org/10.1093/jxb/ers126

    CAS  Article  PubMed  Google Scholar 

  43. Sardinha M, Muller T, Schmeisky H, Joergensen RG (2003) Microbial performance in soils along a salinity gradient under acidic conditions. Appl Soil Ecol 23:237–244. https://doi.org/10.1016/s0929-1393(03)00027-1

    Article  Google Scholar 

  44. Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S, Mondal MH, Maiti TK (2018) A halotolerant Enterobacter sp displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol 169:20–32. https://doi.org/10.1016/j.resmic.2017.08.005

    CAS  Article  PubMed  Google Scholar 

  45. Sedlacek JF, Bossdorf O, Cortes AJ, Wheeler JA, van Kleunen M (2014) What role do plant-soil interactions play in the habitat suitability and potential range expansion of the alpine dwarf shrub Salix herbacea? Basic Appl Ecol 15:305–315. https://doi.org/10.1016/j.baae.2014.05.006

    Article  Google Scholar 

  46. Sheng M, Tang M, Chen H, Yang BW, Zhang FF, Huang YH (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296. https://doi.org/10.1007/s00572-008-0180-7

    CAS  Article  PubMed  Google Scholar 

  47. Soares MA, Li HY, Kowalski KP, Bergen M, Torres MS, White JF (2016) Evaluation of the functional roles of fungal endophytes of Phragmites australis from high saline and low saline habitats. Biol Invasions 18:2689–2702. https://doi.org/10.1007/s10530-016-1160-z

    Article  Google Scholar 

  48. Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS One 9. https://doi.org/10.1371/journal.pone.0105592

    Article  Google Scholar 

  49. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527. https://doi.org/10.1093/aob/mcg058

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Walsh DA, Papke RT, Doolittle WF (2005) Archaeal diversity along a soil salinity gradient prone to disturbance. Environ Microbiol 7:1655–1666. https://doi.org/10.1111/j.1462-2920.2005.00864.x

    CAS  Article  PubMed  Google Scholar 

  51. Wang XL (2010) Study of the mechanisms of salt tolerance in Hibiscus hamabo. Shanghai Jiaotong University, Master Thesis

    Google Scholar 

  52. Yan N, Marschner P, Cao WH, Zuo CQ, Qin W (2015) Influence of salinity and water content on soil microorganisms. Int Soil Water Conserv Res 3:316–323. https://doi.org/10.1016/j.iswer.2015.11.003

    Article  Google Scholar 

  53. Yang H, Du G, Wang K (2008) Study on the physiological characteristics of Hibiscus hamabo under stress. J Zhejiang Forest Sci Technol 28:43–47

    Google Scholar 

  54. Yuan BC, Xu XG, Li ZZ, Gao TP, Gao M, Fan XW, Deng HM (2007) Microbial biomass and activity in alkalized magnesic soils under arid conditions. Soil Biol Biochem 39:3004–3013. https://doi.org/10.1016/j.soilbio.2007.05.034

    CAS  Article  Google Scholar 

  55. Zhou H, Li H, Shao X, Fang C, Ye X, Wu M (2013) Physiological properties changes of Hibiscus hamabo seedlings under different salinity water logging. J Zhejiang Forest Sci Technol 33:41–45

    Google Scholar 

Download references

Acknowledgments

This study was funded by Taizhou Afforestation Project [2015[3]], and Project entrusted by Taizhou Forest Bureau [H2015-122].

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Junmin Li or Zexin Jin.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Matthew G. Bakker.

Electronic supplementary material

ESM 1

(DOCX 873 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yuan, Y., Brunel, C., van Kleunen, M. et al. Salinity-induced changes in the rhizosphere microbiome improve salt tolerance of Hibiscus hamabo. Plant Soil 443, 525–537 (2019). https://doi.org/10.1007/s11104-019-04258-9

Download citation

Keywords

  • Hibiscus hamabo
  • Local adaptation
  • Plant tolerance
  • Salt stress
  • Soil microbial community