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Geographical and Temporal Changes of Foliar Fungal Endophytes Associated with the Invasive Plant Ageratina adenophora

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Abstract

Endophytes may gradually accumulate in the new geographic range of a non-native plant, just as pathogens do. To test this hypothesis, the dynamics of colonization and diversity of foliar fungal endophytes of non-native Ageratina adenophora were investigated. Previous reports showed that the time since the initial introduction (1930s) of A. adenophora into China varied among populations. Endophytes were sampled in three provinces of Southwest China in 21 sites that varied from 20 to 70 years since the introduction of A. adenophora from its native Central America. Endophyte isolation frequencies varied from 1.87 % to 60.23 % overall in a total of 4,032 leaf fragments. Based on ITS sequence variations, 463 fungal endophytes were distinguished as 112 operational taxonomic units (OTUs) belonging to the Sordariomycetes (77 OTUs, 373 isolates), Dothideomycetes (18 OTUs, 38 isolates), and Agaricomycetes (17 OTUs, 52 strains) classes. Colletotrichum (28.51 %), Nemania (14.90 %), Phomopsis (13.17 %), and Xylaria (4.97 %) were the most abundant genera. Both endophyte diversity and overall isolation frequency increased with time since introduction. The genetic differentiation of the fungus Colletotrichum gloeosporioides indicated that the dispersal of endophytes was likely affected by a combination of geographic factors and the invasion history of the host A. adenophora.

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References

  1. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66

    Article  Google Scholar 

  2. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206

    Article  CAS  PubMed  Google Scholar 

  3. Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398

    Article  PubMed  Google Scholar 

  4. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549

    Article  PubMed  Google Scholar 

  5. Andonian K, Hierro JL (2011) Species interactions contribute to the success of a global plant invader. Biol Invasions 13:2957–2965

    Article  Google Scholar 

  6. Aschehoug ET, Metlen KL, Callaway RM, Newcombe G (2012) Fungal endophytes directly increase the competitive effects of an invasive forb. Ecology 93:3–8

    Article  PubMed  Google Scholar 

  7. Callaway RM, Maron JL (2006) What have exotic plant invasions taught us over the past 20 years? Trends Ecol Evol 21:369–374

    Article  PubMed  Google Scholar 

  8. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733

    Article  CAS  PubMed  Google Scholar 

  9. Ding J, Mack RN, Lu P, Ren M, Huang H (2008) China's booming economy is sparking and accelerating biological invasions. Bioscience 58:317–324

    Article  Google Scholar 

  10. Duan H, Qiang S, Su X, Wu H, Zhu Y, Liu L (2005) Genetic diversity of Eupatorium adenophorum determined by AFLP marker. Acta Ecol Sin 25:2109–2114

    CAS  Google Scholar 

  11. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    Article  CAS  Google Scholar 

  12. Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101:607–613

    Article  Google Scholar 

  13. Gui F, Wan F, Guo J (2009) Determination of the population genetic structure of the invasive weed Ageratina adenophora using ISSR-PCR markers. Rus J Plant Physiol 56:410–416

    Article  CAS  Google Scholar 

  14. Higgins KL, Coley PD, Kursar TA, Arnold AE (2011) Culturing and direct PCR suggest prevalent host generalism among diverse fungal endophytes of tropical forest grasses. Mycologia 103:247–260

    Article  PubMed  Google Scholar 

  15. Huang W, Guo J, Wan F, Gao B, Xie B (2007) AFLP Analysis on genetic diversity and genetic structure of Eupatorium adenophorum populations in China. J Agric Biotechnol 15:992–1000

    CAS  Google Scholar 

  16. Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H (2009) Colletotrichum: a catalogue of confusion. Fungal Divers 39:1–17

    Google Scholar 

  17. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

    Google Scholar 

  18. Jiang H, Shi Y, Zhou Z, Yang C, Chen Y, Chen L, Yang M, Zhang H (2011) Leaf chemistry and co-occurring species interactions affecting the endophytic fungal composition of Eupatorium adenophorum. Ann Microbiol 61:655–662

    Article  Google Scholar 

  19. Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190

    Article  Google Scholar 

  20. Ko Ko TW, Stephenson SL, Bahkali LH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120

    Article  Google Scholar 

  21. Li X (2004) Distribution, damage and control of Eupatorium adenophorum. Guangxi Plant Prot 17:18–19

    Google Scholar 

  22. Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572

    Article  PubMed  Google Scholar 

  23. Lu P, San W, Ma K (2005) Advance in the invasive species Eupatorium adenophorum. Acta Phytoecol Sin 29:1029–1037

    Google Scholar 

  24. Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456

    Article  PubMed  Google Scholar 

  25. Newcombe G, Shipunov A, Eigenbrode SD, Raghavendra AKH, Ding H, Anderson CL, Menjivar R, Crawford M, Schwarzländer M (2009) Endophytes influence protection and growth of an invasive plant. Commun Integr Biol 2:29–31

    Article  PubMed Central  PubMed  Google Scholar 

  26. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  27. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  CAS  PubMed  Google Scholar 

  28. van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37

    Article  PubMed  Google Scholar 

  29. Rudgers JA, Mattingly WB, Koslow JM (2005) Mutualistic fungus promotes plant invasion into diverse communities. Oecologia 144:463–471

    Article  PubMed  Google Scholar 

  30. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  31. Saikkonen K, Wali P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. 2004. Trends Plant Sci 9:275–180

    Article  CAS  PubMed  Google Scholar 

  32. Spellerberg IF, Fedor PJ (2003) A tribute to clarde Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon–Wiener’ index. Glob Ecol Biogeogr 12:177–179

    Article  Google Scholar 

  33. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4(5):e140. doi:10.1371/journal.pbio.0040140

    Article  PubMed Central  PubMed  Google Scholar 

  34. Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651

    Article  PubMed  Google Scholar 

  35. Shipunov A, Newcombe G, Raghavendra AKH, Anderson CL (2008) Hidden diversity of endophytic fungi in an invasive plant. Am J Bot 95:1096–1108

    Article  PubMed  Google Scholar 

  36. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2006) Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 22:120–126

    Article  PubMed  Google Scholar 

  38. Vilá M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708

    Article  PubMed  Google Scholar 

  39. Wang R, Wang Y (2006) Invasion dynamics and potential spread of the invasive alien plant species Ageratina adenophora (Asteraceae) in China. Divers Distrib 12:397–408

    Article  Google Scholar 

  40. Wang R, Wang J-F, Qiu Z-J, Meng B, Wan F-H, Wang Y-Z (2011) Multiple mechanisms underlie rapid expansion of an invasive alien plant. New Phytol 191:828–839

    Article  PubMed  Google Scholar 

  41. Williamson M (1996) Biological invasions. Chapman and Hall, London

    Google Scholar 

  42. Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J Ecol 96:777–783

    Article  Google Scholar 

  44. Wu Z, Qin G, Deng T (2006) Invasion and establishment of Eupatorium adenophorum Spreng and its risk appraisal in some areas of Guangxi. Southwest China J Agric Sci 17:469–471

    Google Scholar 

  45. Zhou S, Tang C, Hou T, Li M, Jiang H (2006) Study on the transmission of Eupatorium adenophorum. Sichuan Anim Vet Sci 5:30–31

    Google Scholar 

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Acknowledgments

We particularly thank three anonymous reviewers for the detailed and constructive suggestions for our paper. We also thank Huan Jiang, Zhen-Xin Zhou, Yun-Jiao Chen, Chen Yang, Yun-Tao Shi, and Li-Min Chen at Yunnan University for partially sampling, isolating, and identifying the endophytes; Susan Straight at the Center for Intercultural Education, New Mexico, USA, and Kelly Gorman, University of Victoria, Canada, for helping us with the English language. This project was financially supported by the National Basic Research Program of China (973 Program) (2013CD127500) and the National Science Foundation of China (Nos. 30960077, 31360153).

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Correspondence to Han-Bo Zhang.

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L. Mei and M. Zhu contributed equally to this work.

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Mei, L., Zhu, M., Zhang, DZ. et al. Geographical and Temporal Changes of Foliar Fungal Endophytes Associated with the Invasive Plant Ageratina adenophora . Microb Ecol 67, 402–409 (2014). https://doi.org/10.1007/s00248-013-0319-8

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