Skip to main content
Log in

Soil microbes alleviate allelopathy of invasive plants

  • Article
  • Life & Medical Sciences
  • Published:
Science Bulletin

Abstract

Soil microbes are one of the most important determinants of allelopathic effects in the field. However, most studies testing the role of allelopathy in biological invasions did not consider the roles of soil microbes. Here we tested the hypothesis that soil microbes which can degrade allelochemicals may accumulate in soils over time by adaptation and therefore increase the degradation of allelochemicals and alleviate the allelopathic effects in biological invasions. As expected, soil microbes significantly decreased the allelopathic effects of leaf leachates of eight in the nine invasive plant species studied. In addition, Ageratina adenophora showed lower allelopathic effects in soil with long or intermediately invasion history than those in soil with short invasion history. The two main allelochemicals of the invader were degraded more rapidly with increasing invasion history in the soil. Correspondingly, biomass and activity of the soil microbes were higher in the soils with long invasion history than in that with short invasion history. Our results indicate that soil microbes may gradually adapt to the allelochemicals of Ageratina and alleviate its allelopathic effects and thus support the above hypothesis. It is necessary to consider the effects of soil microbes when testing the roles of allelopathy or the novel weapons hypothesis in biological invasions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Callaway RM, Ridenour W (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  2. Murrell C, Gerber E, Krebs C et al (2011) Invasive knotweed affects native plants through allelopathy. Am J Bot 98:38–43

    Article  Google Scholar 

  3. Smith LM, Reynolds HL (2014) Light, allelopathy, and post-mortem invasive impact on native forest understory species. Biol Invasions 16:1131–1144

    Article  Google Scholar 

  4. Zheng L, Feng YL (2005) Allelopathic effects of Eupatorium adenophorum Spreng. on seed germination and seedling growth in ten herbaceous species. Acta Ecol Sin 25:2782–2787

    Google Scholar 

  5. Zheng YL, Feng YL, Zhang LK et al (2015) Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol 205:1350–1359

    Article  Google Scholar 

  6. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  Google Scholar 

  7. Inderjit, Evans H, Crocoll C (2011) Volatile chemicals from leaf litter are associated with invasiveness of a neotropical weed in Asia. Ecology 92:316–324

    Article  Google Scholar 

  8. Qin RM, Zheng YL, Valiente-Banuet A (2013) The evolution of increased competitive ability, innate competitive advantages, and novel biochemical weapons act in concert for a tropical invader. New Phytol 197:979–988

    Article  Google Scholar 

  9. Inderjit, Nilsen ET (2003) Bioassays and field studies for allelopathy in terrestrial plants: progress and problems. Crit Rev Plant Sci 22:231–238

    Article  Google Scholar 

  10. Tharayil N, Bhowmik P, Alpert P et al (2009) Dual purpose secondary compounds: phytotoxin of Centaurea diffusa also facilitates nutrient uptake. New Phytol 181:424–434

    Article  Google Scholar 

  11. Metlen KL, Aschehoug ET, Callaway RM (2013) Competitive outcomes between two exotic invaders are modified by direct and indirect effects of a native conifer. Oikos 122:632–640

    Article  Google Scholar 

  12. Asaduzzaman M, An M, Pratley JE et al (2014) Canola (Brassica napus) germplasm shows variable allelopathic effects against annual ryegrass (Lolium rigidum). Plant Soil 380:47–56

    Article  Google Scholar 

  13. Blair A, Hanson B, Brunk G et al (2005) New techniques and findings in the study of a candidate allelochemical implicated in invasion success. Ecol Lett 8:1039–1047

    Article  Google Scholar 

  14. Callaway RM, Cipollini D, Barto K et al (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055

    Article  Google Scholar 

  15. Weidenhamer J, Romeo J (2004) Allelochemicals of Polygonella myriophylla: chemistry and soil degradation. J Chem Ecol 30:1067–1082

    Article  Google Scholar 

  16. Inderjit (2005) Soil microorganisms: an important determinant of allelopathic activity. Plant Soil 274:227–236

    Article  Google Scholar 

  17. Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727

    Article  Google Scholar 

  18. Ehlers BK (2011) Soil microorganisms alleviate the allelochemical effects of a Thyme Monoterpene on the performance of an associated grass species. PLoS One 6:e26321

    Article  Google Scholar 

  19. Blum U (1998) Effects of microbial utilization of phenolic acids and their phenolic acid breakdown products on allelopathic interactions. J Chem Ecol 24:685–708

    Article  Google Scholar 

  20. Chen L, Yang X, Raza W et al (2011) Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Appl Microbiol Biotechnol 89:1653–1663

    Article  Google Scholar 

  21. Arbeli Z, Fuentes CL (2007) Accelerated biodegradation of pesticides: an overview of the phenomenon, its basis and possible solutions, and a discussion on the tropical dimension. Crop Prot 26:1733–1746

    Article  Google Scholar 

  22. Lawrence JG, Ochman H (2002) Reconciling the many faces of lateral gene transfer. Trends Microbiol 10:1–4

    Article  Google Scholar 

  23. Top EM, Springael D, Boon N (2002) Catabolic mobile genetic elements and their potential use in bioaugmentation of polluted soils and waters. FEMS Microbiol Ecol 42:199–208

    Article  Google Scholar 

  24. Aelion CM, Swindoll CM, Pfaender FK (1987) Adaptation to and biodegradation of xenobiotic compounds by microbial communities from a pristine aquifer. Appl Environ Microbiol 53:2212–2217

    Google Scholar 

  25. Gray RA, Joo GK (1985) Reduction in weed control after repeated application of thiocarbamate and other herbicides. Weed Sci 33:698–702

    Google Scholar 

  26. Karpouzas DG, Hatziapostolou P, Papadopoulou-Mourkidou E et al (2004) The enhanced biodegradation of fenamiphos in soils from previously treated sites and the effect of soil fumigants. Environ Toxicol Chem 23:2099–2107

    Article  Google Scholar 

  27. Perry LG, Thelen GC, Ridenour WM et al (2005) Dual role for an allelochemical: (±)-catechin from Centaurea maculosa root exudates regulates conspecific seedling establishment. J Ecol 93:1126–1135

    Article  Google Scholar 

  28. Perry LG, Thelen GC, Ridenour WM et al (2007) Concentrations of the allelochemical (±)-catechin in Centaurea maculosa soils. J Chem Ecol 33:2337–2344

    Article  Google Scholar 

  29. Inderjit, Pollock JL, Callaway RM et al (2008) Phytotoxic effects of (±)-catechin in vitro, in soil, and in the field. PLoS One 3:e2536

  30. Kaur H, Kaur R, Kaur S et al (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS One 4:e4700

  31. Vance ED, Brookes PC, Jenkinson DS (1987) Microbial biomass measurements in forest soils: determination of kC values and tests of hypotheses to explain the failure of the chloroform fumigation-incubation method in acid soils. Soil Biol Biochem 19:689–696

    Article  Google Scholar 

  32. Yang G, Wan F, Liu W et al (2008) Influence of two allelochemicals from Ageratina adenophora Sprengel on ABA, IAA and ZR contents in roots of upland rice seedlings. Allelopathy J 21:253

    Google Scholar 

  33. Williamson B, Richardson D (1988) Bioassays for allelopathy: measuring treatment responses with independent controls. J Chem Ecol 14:181–187

    Article  Google Scholar 

  34. Li ZG, Luo YM, Teng Y (2008) Methods of analysis soil and environment microbes. Science Press, Beijing

    Google Scholar 

  35. Lankau RA (2010) Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol Invasions 12:2059–2068

    Article  Google Scholar 

  36. Zhu X, Zhang J, Ma KP (2011) Soil biota reduce allelopathic effects of the invasive Eupatorium adenophorum. PLoS One 6:e25393

    Article  Google Scholar 

  37. Meiners SJ, Kong CH, Ladwig LM et al (2012) Developing an ecological context for allelopathy. Plant Ecol 213:1861–1867

    Article  Google Scholar 

  38. Hole SJ, McClure NC, Powles SB (2001) Rapid degradation of carbetamide upon repeated application to Australian soils. Soil Biol Bioch 33:739–745

    Article  Google Scholar 

  39. Lau JA (2006) Evolutionary responses of native plants to novel community members. Evolution 60:56–63

    Article  Google Scholar 

  40. Kong CH, Xu XH, Chen JJ et al (2002) Allelopathy of Ageratum conyzoides IX. Transformation of main allelochemical in the soil. Acta Ecol Sin 8:1189–1195

    Google Scholar 

  41. Lalljee B, Facknath S (2000) Allelopathic interactions in soil. In: Narwal SS et al (eds) Allelopathy in ecological agriculture and forestry. Kluwer Academic Publishers, Dordrecht, pp 47–58

  42. Karban R (2007) Experimental clipping of sagebrush inhibits seed germination of neighbours. Ecol Lett 10:791–797

    Article  Google Scholar 

  43. Rasher DB, Hay ME (2014) Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed. Proc R Soc B 281:20132615

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Da-Wen Li and Ailaoshan Station for Subtropical Forest Ecosystem Studies, Chinese Academy of Sciences for field assistance. This work was supported by the National Natural Science Foundation of China (31100410, 31470575 and 30830027), the National Key Technology R&D Program of China (2011BAD30B00), and Chinese Academy Science 135 Program (XTBG-T01, F01).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yang-Ping Li or Yu-Long Feng.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 612 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, YP., Feng, YL., Chen, YJ. et al. Soil microbes alleviate allelopathy of invasive plants. Sci. Bull. 60, 1083–1091 (2015). https://doi.org/10.1007/s11434-015-0819-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11434-015-0819-7

Keywords

Navigation