Skip to main content
SpringerLink
Log in

Responses of Soil Microbial Communities in the Rhizosphere of Cucumber (Cucumis sativus L.) to Exogenously Applied p-Hydroxybenzoic Acid

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Changes in soil biological properties have been implicated as one of the causes of soil sickness, a phenomenon that occurs in continuous monocropping systems. However, the causes for these changes are not yet clear. The aim of this work was to elucidate the role of p-hydroxybenzoic acid (PHBA), an autotoxin of cucumber (Cucumis sativus L.), in changing soil microbial communities. p-Hydroxybenzoic acid was applied to soil every other day for 10 days in cucumber pot assays. Then, the structures and sizes of bacterial and fungal communities, dehydrogenase activity, and microbial carbon biomass (MCB) were assessed in the rhizosphere soil. Structures and sizes of rhizosphere bacterial and fungal communities were analyzed by polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis (DGGE) and real-time PCR, respectively. p-Hydroxybenzoic acid inhibited cucumber seedling growth and stimulated rhizosphere dehydrogenase activity, MBC content, and bacterial and fungal community sizes. Rhizosphere bacterial and fungal communities responded differently to exogenously applied PHBA. The PHBA decreased the Shannon-Wiener index for the rhizosphere bacterial community but increased that for the rhizosphere fungal community. In addition, the response of the rhizosphere fungal community structure to PHBA acid was concentration dependent, but was not for the rhizosphere bacterial community structure. Our results indicate that PHBA plays a significant role in the chemical interactions between cucumber and soil microorganisms and could account for the changes in soil microbial communities in the continuously monocropped cucumber system.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

REFERENCES

  • Bais, H. P., Park, S. W., Weir, T. L., Callaway, R. M., and Vivanco, J. M. 2004. How plants communicate using the underground information superhighway. Trends Plant Sci. 9:26–32.

    Article  PubMed  CAS  Google Scholar 

  • Batten, K. M., Scow, K. M., and Espeland, E. K. 2008. Soil microbial community associated with an invasive grass differentially impacts native plant performance. Microb. Ecol. 55:220–228.

    Article  PubMed  Google Scholar 

  • Bever, J. D., Dickie, I. A., Facelli, E., Facelli, J. M., Klironomos, J., Moora, M., Rillig, M. C., Stock, W. D., Tibbett, M., and Zobel, M. 2010. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25:468–478.

    Article  PubMed  Google Scholar 

  • Blum, U., Staman, K. L., Flint, L. J., and Shaffer, S. R. 2000. Induction and/or selection of phenolic acid-utilizing bulk-soil and rhizosphere bacteria and their influence on phenolic acid phytotoxicity. J. Chem. Ecol. 26:2059–2078.

    Article  CAS  Google Scholar 

  • Bonanomi, G., Giannino, F., and Mazzoleni, S. 2005. Negative plant-soil feedback and species coexistence. Oikos 111:311–321.

    Article  Google Scholar 

  • Bonanomi, G., Incerti, G., Barile, E., Capodilupo, M., Antignani, V., Mingo, A., Lanzotti, V., Scala, F., and Mazzoleni, S. 2011. Phytotoxicity, not nitrogen immobilization, explains plant litter inhibitory effects: evidence from solid-state 13 C NMR spectroscopy. New Phytol. 191:1018–1030.

    Article  PubMed  CAS  Google Scholar 

  • Brant, J. B., Sulzman, E. W., and Myrold, D. D. 2006. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol. Biochem. 38:2219–2232.

    Article  CAS  Google Scholar 

  • Broeckling, C. D., Broz, A. K., Bergelson, J., Manter, D. K., and Vivanco, J. M. 2008. Root exudates regulate soil fungal community composition and diversity. Appl. Environ. Microbiol. 74:738–744.

    Article  PubMed  CAS  Google Scholar 

  • Cipollini, D., Rigsby, C. M., and Barto, E. K. 2012. Microbes as targets and mediators of allelopathy in plants. J. Chem. Ecol. 38:714–727.

    Article  PubMed  CAS  Google Scholar 

  • de Boer, W., Folman, L. B., Summerbell, R. C., and Boddy, L. 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 29:795–811.

    Article  PubMed  Google Scholar 

  • de Graaff, M. A., Classen, A. T., Castro, H. F., and Schadt, C. W. 2010. Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol. 188:1055–1064.

    Article  PubMed  Google Scholar 

  • Eilers, K. G., Lauber, C. L., Knight, R., and Fierer, N. 2010. Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol. Biochem. 42:896–903.

    Article  CAS  Google Scholar 

  • Fierer, N. and Jackson, R. B. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U.S.A. 103:626.

    Article  PubMed  CAS  Google Scholar 

  • Gardes, M. and Bruns, T. D. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhiza and rusts. Mol. Ecol. 2:113–118.

    Article  PubMed  CAS  Google Scholar 

  • Hoshino, Y. T. and Matsumoto, N. 2007. DNA- versus RNA-based denaturing gradient gel electrophoresis profiles of a bacterial community during replenishment after soil fumigation. Soil Biol. Biochem. 39:434–444.

    Article  CAS  Google Scholar 

  • Huang, H. C., Chou, C. H., and Erickson, R. S. 2006. Soil sickness and its control. Allelopathy J. 18:1–21.

    CAS  Google Scholar 

  • Inderjit 2005. Soil microorganisms: An important determinant of allelopathic activity. Plant Soil 274:227–236.

    Article  CAS  Google Scholar 

  • Inderjit and Duke, S. O. 2003. Ecophysiological aspects of allelopathy. Planta 217:529–539.

    Article  PubMed  CAS  Google Scholar 

  • Inderjit and van der Putten, W. H. 2010. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol. Evol. 25:512–519.

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, Kaur, R., Kaur, S., and Callaway, R. M. 2009. Impact of (±)-catechin on soil microbial communities. Commun. Integ. Biol. 2:127–129.

    CAS  Google Scholar 

  • Jilani, G., Mehmood, S., Chaudhry, A. N., Hassan, I., and Akram, M. 2008. Allelochemicals: sources, toxicity and microbial transformation in soil -a review. Ann. Microbiol. 58:351–357.

    Article  CAS  Google Scholar 

  • Kong, C. H., Wang, P., Zhao, H., Xu, X. H., and Zhu, Y. D. 2008. Impact of allelochemical exuded from allelopathic rice on soil microbial community. Soil Biol. Biochem. 40:1862–1869.

    Article  CAS  Google Scholar 

  • Kourtev, P. S., Ehrenfeld, J. G., and Häggblom, M. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166.

    Article  Google Scholar 

  • Kulmatiski, A., Beard, K. H., Stevens, J. R., and Cobbold, S. M. 2008. Plant-soil feedbacks: a meta-analytical review. Ecol. Lett. 11:980–992.

    Article  PubMed  Google Scholar 

  • Li, C., Li, X., Kong, W., Wu, Y., and Wang, J. 2010. Effect of monoculture soybean on soil microbial community in the Northeast China. Plant Soil 330:423–433.

    Article  CAS  Google Scholar 

  • Liu, B., Gumpertz, M. L., Hu, S., and Ristaino, J. B. 2007. Long-term effects of organic and synthetic soil fertility amendments on soil microbial communities and the development of southern blight. Soil Biol. Biochem. 39:2302–2316.

    Article  CAS  Google Scholar 

  • Liu, S., Zhou, X., Liu, B., Pan, K., Liu, S., and Wu, F. 2011. Sugars in watermelon root exudates and their effects on Fusarium oxysporum f.sp. niveum. Allelopathy J. 28:21–28.

    Google Scholar 

  • Mangla, S., Inderjit, and Callaway, R. M. 2008. Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J. Ecol. 96:58–67.

    Google Scholar 

  • Meier, C. L. and Bowman, W. D. 2008. Phenolic-rich leaf carbon fractions differentially influence microbial respiration and plant growth. Oecologia 158:95–107.

    Article  PubMed  Google Scholar 

  • Meier, C. L., Keyserling, K., and Bowman, W. D. 2009. Fine root inputs to soil reduce growth of a neighbouring plant via distinct mechanisms dependent on root carbon chemistry. J. Ecol. 97:941–949.

    Article  Google Scholar 

  • Muscolo, A. and Sidari, M. 2006. Seasonal fluctuations in soil phenolics of a coniferous forest: effects on seed germination of different coniferous species. Plant Soil 284:305–318.

    Article  CAS  Google Scholar 

  • 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 encoding for 16S rRNA. Appl. Environ. Microbiol. 59:695–700.

    PubMed  CAS  Google Scholar 

  • Nayyar, A., Hamel, C., Lafond, G., Gossen, B. D., Hanson, K., and Germida, J. 2009. Soil microbial quality associated with yield reduction in continuous-pea. Appl. Soil Ecol. 43:115–121.

    Article  Google Scholar 

  • Nijjer, S., Rogers, W. E., and Siemann, E. 2007. Negative plant-soil feedbacks may limit persistence of an invasive tree due to rapid accumulation of soil pathogens. Proc. R. Soc. B 274:2621–2627.

    Article  PubMed  Google Scholar 

  • Politycka, B., Wójcik-Wojtkowiak, D., and Pudelski, T. 1984. Phenolic compounds as a cause of phytotoxicity in greenhouse substrates used in cucumber growing. Acta Hort. 156:89–94.

    Google Scholar 

  • Pollock, J. L., Kogan, L. A., Thorpe, A. S., and Holben, W. E. 2011. (±)-Catechin, a root exudate of the invasive Centaurea Stoebe Lam. (Spotted Knapweed) exhibits bacteriostatic activity against multiple soil bacterial populations. J. Chem. Ecol. 37:1044–1053.

    Article  PubMed  CAS  Google Scholar 

  • Pramanik, M. H. R., Nagai, M., Asao, T., and Matsui, Y. 2000. Effects of temperature and photoperiod on phytotoxic root exudates of cucumber (Cucumis sativus) in hydroponic culture. J. Chem. Ecol. 26:1953–1967.

    Article  CAS  Google Scholar 

  • Qu, X. H. and Wang, J. G. 2008. Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl. Soil Ecol. 39:172–179.

    Article  Google Scholar 

  • Reinhart, K. O. and Callaway, R. M. 2006. Soil biota and invasive plants. New Phytol. 170:445–457.

    Article  PubMed  Google Scholar 

  • Rinnan, R. and Bååth, E. 2009. Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Appl. Environ. Microbiol. 75:3611–3620.

    Article  PubMed  CAS  Google Scholar 

  • Shafer, S. R. and Blum, U. 1991. Influence of phenolic acids on microbial populations in the rhizosphere of cucumber. J. Chem. Ecol. 17:369–389.

    Article  CAS  Google Scholar 

  • Sharma, S., Aneja, M. K., Mayer, J., Schloter, M., and Munch, J. C. 2004. RNA fingerprinting of microbial community in the rhizosphere soil of grain legumes. FEMS Microbiol. Lett. 240:181–186.

    Article  PubMed  CAS  Google Scholar 

  • Shi, S., Richardson, A. E., O'Callaghan, M., Deangelis, K. M., Jones, E. E., Stewart, A., Firestone, M. K., and Condron, L. M. 2011. Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol. Ecol. 77:600–610.

    Article  PubMed  CAS  Google Scholar 

  • Singh, H. P., Batish, D. R., and Kohli, R. K. 1999. Autotoxicity: concept, organisms and ecological significance. Crit. Rev. Plant Sci. 18:757–772.

    Article  CAS  Google Scholar 

  • Souto, X. C., Chiapusio, G., and Pellissier, F. 2000. Relationships between phenolics and soil microorganisms in spruce forests: significance for natural regeneration. J. Chem. Ecol. 26:2025–2034.

    Article  CAS  Google Scholar 

  • Tabatabai, M. A. 1994. Soil enzymes. pp. 775-833, in R. W. Weaver, J. R. Angle, and P. S. Bottomley (eds.), Methods of Soil Analysis. Soil Society of America, Madison.

    Google Scholar 

  • Vance, E. D., Brookes, P. C., and Jenkinson, D. S. 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19:703–707.

    Article  CAS  Google Scholar 

  • Waldrop, M. P. and Firestone, M. K. 2004. Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284.

    Article  PubMed  Google Scholar 

  • Wang, M. L., Gu, Y., and Kong, C. H. 2008. Effects of rice phenolic acids on microorganisms and enzyme activities of non-flooded and flooded paddy soils. Allelopathy J. 22:311–319.

    Google Scholar 

  • Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setälä, H., Van Der Putten, W. H., and Wall, D. H. 2004. Ecological linkages between aboveground and belowground biota. Science 304:1629–1633.

    Article  PubMed  CAS  Google Scholar 

  • Welbaum, G. E., Sturz, A. V., Dong, Z., and Nowak, J. 2004. Managing soil microorganisms to improve productivity of agro-ecosystems. Crit. Rev. Plant Sci. 23:175–193.

    Article  CAS  Google Scholar 

  • White, T. J., Buns, T. D., Lee, S., and Taylor, J. 1990. Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. pp. 315-322, in M. A. Innis, D. H. Gefland, J. J. Sninsky, and T. J. White (eds.), PCR Protocols: A Guide to Methods and Applications. Academic, New York.

    Google Scholar 

  • Wolfe, B. E. and Klironomos, J. N. 2005. Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487.

    Article  Google Scholar 

  • Wu, F. Z. and Wang, X. Z. 2006. Effect of p-hydroxybenzoic and cinnamic acids on soil fungi (Fusarium oxysporum f.sp. cucumerinum) growth and microbial population. Allelopathy J 18:129–140.

    Google Scholar 

  • Wu, F., Wang, X., and Xue, C. 2009a. Effect of cinnamic acid on soil microbial characteristics in the cucumber rhizosphere. Eur. J. Soil Biol. 45:356–362.

    Article  CAS  Google Scholar 

  • Wu, H., Shen, S., Han, J., Liu, Y., and Liu, S. 2009b. The effect in vitro of exogenously applied p-hydroxybenzoic acid on Fusarium oxysporum f. sp. niveum. Phytopathol. Mediterr. 48:439–446.

    CAS  Google Scholar 

  • Zhang, S., Jin, Y., Zhu, W., Tang, J., Hu, S., Zhou, T., and Chen, X. 2010. Baicalin released from Scutellaria baicalensis induces autotoxicity and promotes soil-born pathogens. J. Chem. Ecol. 36:329–338.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, X. and Wu, F. 2012. Dynamics of the diversity of fungal and Fusarium communities during continuous cropping of cucumber in the greenhouse. FEMS Microbiol. Ecol. 80:469–478.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, X., Yu, G., and Wu, F. 2011. Effects of intercropping cucumber with onion or garlic on soil enzyme activities, microbial communities and cucumber yield. Eur. J. Soil Biol. 47:279–287.

    Article  CAS  Google Scholar 

  • Zhou, X., Yu, G., and Wu, F. 2012. Soil phenolics in a continuously mono-cropped cucumber (Cucumis sativus L.) system and their effects on cucumber seedling growth and soil microbial communities. Eur. J. Soil Sci. 63:332–340.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Basic Research Program of China (2009CB119004-05) and the National Staple Vegetable Industrial Technology Systems of China (CARS-25-08) and the National Natural Science Foundation of China (30971998).

Author information

Authors and Affiliations

  1. Department of Horticulture, Northeast Agricultural University, Mucai 59, Xiangfang, Harbin, 150030, People’s Republic of China

    Xingang Zhou & Fengzhi Wu

  2. Department of Horticulture, Zhejiang University, Yuhangtang Road 886, Hangzhou, 310058, People’s Republic of China

    Gaobo Yu

Authors
  1. Xingang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gaobo Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fengzhi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fengzhi Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, X., Yu, G. & Wu, F. Responses of Soil Microbial Communities in the Rhizosphere of Cucumber (Cucumis sativus L.) to Exogenously Applied p-Hydroxybenzoic Acid. J Chem Ecol 38, 975–983 (2012). https://doi.org/10.1007/s10886-012-0156-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0156-0

Keywords

Search

Navigation