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Endophytic and Epiphytic Phyllosphere Fungal Communities Are Shaped by Different Environmental Factors in a Mediterranean Ecosystem

Microbial Ecology volume 76, pages 668–679 (2018)Cite this article

Abstract

The diversity and factors influencing fungal assemblages in phyllosphere of Mediterranean tree species have been barely studied, especially when endophytic and epiphytic communities are simultaneously considered. In this work, the endophytic and epiphytic fungal communities from olive tree phyllosphere were studied. This tree species is natural from the Mediterranean region and adapted to grow under adverse climatic conditions. The main objectives were to determine whether there are differences between both fungal communities and to examine whether different abiotic (climate-related) and biotic (plant organs) factors play a pivotal role in structuring these communities. Both communities differed in size and composition, with epiphytic community being richer and more abundant, displaying also a dominance of melanized fungi. Season was the major driver of community composition, especially of epiphytes. Other drivers shaping epiphytes were wind speed and temperature, while plant organ, rainfall, and temperature were the major drivers for endophytic composition. In contrast, canopy orientation caused slight variations in community composition of fungi, but with distinct effects in spring and autumn seasons. In conclusion, epiphytic and endophytic communities are not driven by the same factors. Several sources of variation undergo complex interactions to form and maintain phyllosphere fungal community in Mediterranean climates. Climatic parameters have influence on these fungal communities, suggesting that they are likely to be affected by climate changes in a near future.

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References

  1. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148

    PubMed  PubMed Central  Google Scholar 

  3. Moricca S, Ragazzi A (2008) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology 98:380–386

    Article  PubMed  CAS  Google Scholar 

  4. Collado J, Platas G, González I, Peláez F (1999) Geographical and seasonal influences on the distribution of fungal endophytes in Quercus ilex. New Phytol 144:525–532

    Article  Google Scholar 

  5. Linaldeddu BT, Sirca C, Spano D, Franceschini A (2011) Variation of endophytic cork oak-associated fungal communities in relation to plant health and water stress. For Pathol 41:193–201

    Article  Google Scholar 

  6. Martinez-Alvarez P, Martin-Garcia J, Rodriguez-Ceinos S, Diez JJ (2012) Monitoring endophyte populations in pine plantations and native oak forests in Northern Spain. For Syst 21:373–382

    Google Scholar 

  7. Moricca S, Ginetti B, Ragazzi A (2012) Species- and organ-specificity in endophytes colonizing healthy and declining Mediterranean oaks. Phytopathol Mediterr 51:587–598

    Google Scholar 

  8. Botella L, Santamaría O, Díez JJ (2010) Fungi associated with the decline of Pinus halepensis in Spain. Fungal Divers 40:1–11

    Article  Google Scholar 

  9. Martín-García J, Espiga E, Pando V, Diez JJ (2011) Factors influencing endophytic communities in poplar plantations. Silva Fenn 45:169–180

    Article  Google Scholar 

  10. Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  12. Rastogi G, Coaker GL, Leveau JH (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10

    Article  PubMed  CAS  Google Scholar 

  13. Osono T (2007) Endophytic and epiphytic phyllosphere fungi of red-osier dogwood (Cornus stolonifera) in British Columbia. Mycoscience 48:47–52

    Article  Google Scholar 

  14. Santamaria J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microb Ecol 50:1–8

    Article  PubMed  Google Scholar 

  15. Osono T (2008) Endophytic and epiphytic phyllosphere fungi of Camellia japonica: seasonal and leaf age-dependent variations. Mycologia 100:387–391

    Article  PubMed  Google Scholar 

  16. Loumou A, Giourga C (2003) Olive groves: “the life and identity of the Mediterranean”. Agric Hum Values 20:87–95

    Article  Google Scholar 

  17. SNIRH (2016) http://snirh.apambiente.pt. Accessed 22 Aug 2016

  18. Malavolta C, Perdikis D (2012) Guidelines for integrated production of olives. IOBC technical guideline III, vol 77. 2nd edn, pp 1–19

    Google Scholar 

  19. Martins F, Pereira JA, Bota P, Bento A, Baptista P (2016) Fungal endophyte communities in above- and belowground olive tree organs and the effect of season and geographic location on their structures. Fungal Ecol 20:193–201

    Article  Google Scholar 

  20. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  21. Oliveira I, Pereira JA, Lino-Neto T, Bento A, Baptista P (2012) Fungal diversity associated to the olive moth, Prays oleae Bernard: a survey for potential entomopathogenic fungi. Microb Ecol 63:964–974

    Article  PubMed  Google Scholar 

  22. Seaby RM, Henderson PA (2006) Species diversity and richness version 4. Pisces Conservation, Lymington

    Google Scholar 

  23. Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples, Version 9. http://purl.oclc.org/estimates. Accessed 7 Jan 2016

  24. R Core Team (2014) R: a language and environment for statistical computing. http://www.R-project.org/. Accessed 22 Mar 2016

  25. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effect models and extensions in ecology with R. Springer, Berlin

    Book  Google Scholar 

  26. Magurran AE (2004) Measuring biological diversity2nd edn. Blackwell Science Ltd, Oxford

    Google Scholar 

  27. Bray JR, Curtis JT (1957) An ordination of upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  28. Clarke KR, Gorley RN (2015) PRIMER v7: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  29. Henderson PA, Seaby RMH (2007) Community analysis package 4.0. Pisces Conservation Ltd, Lymington

    Google Scholar 

  30. Dolédec S, Chessel D (1994) Co-inertia analysis: an alternative method for studying species environment relationships. Freshw Biol 31:277–294

    Article  Google Scholar 

  31. Mcardle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  32. Abdelfattah A, Nicosia MGLD, Cacciola SO, Droby S, Schena L (2015) Metabarcoding analysis of fungal diversity in the phyllosphere and carposphere of olive (Olea europaea). PLoS One 10:e0131069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Zambell CB, White JF (2014) In the forest vine Smilax rotundifolia, fungal epiphytes show site-wide spatial correlation, while endophytes show evidence of niche partitioning. Fungal Divers 75:279–297

    Article  Google Scholar 

  34. Gessler NN, Egorova AS, Belozerskaya TA (2014) Melanin pigments of fungi under extreme environmental conditions (review). Appl Biochem Microbiol 50:105–113

    Article  CAS  Google Scholar 

  35. Kembel SW, Mueller RC (2014) Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92:303–311

    Article  Google Scholar 

  36. Kharwar RN, Gond SK, Kumar A, Mishra AA (2010) A comparative study of endophytic and epiphytic fungal association with leaf of Eucalyptus citriodora Hook., and their antimicrobial activity. World J Microbiol Biotechnol 26:1941–1948

    Article  Google Scholar 

  37. Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S et al (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6:e02527–e02514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Singh DK, Sharma VK, Kumar J, Mishra A, Verma SK, Sieber TN, Kharwar RN (2017) Diversity of endophytic mycobiota of tropical tree Tectona grandis Linn. f.: spatiotemporal and tissue type effects. Sci Rep 7:3745

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kim C, Eo J, Eom A (2013) Diversity and seasonal variation of endophytic fungi isolated from three conifers in Mt. Taehwa, Korea. Mycobiology 41:82–85

    Article  PubMed  PubMed Central  Google Scholar 

  40. Peñuelas J, Rico L, Ogaya R, Jump AS, Terradas J (2012) Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biol 14:565–575

    Article  PubMed  Google Scholar 

  41. Vacher C, Hampe A, Porte AJ, Sauer U, Compant S, Morris CE (2016) The phyllosphere: microbial jungle at the plant–climate interface. Annu Rev Ecol Evol Syst 47:1–24

    Article  Google Scholar 

  42. Jumpponen A, Jones KL (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513

    Article  PubMed  CAS  Google Scholar 

  43. Verma SK, Gond SK, Mishra A, Sharma VK, Kumar J, Singh DK, Kumar A, Goutam J, Kharwar RN (2014) Impact of environmental variables on the isolation, diversity and antibacterial activity of endophytic fungal communities from Madhuca indica Gmel. at different locations in India. Ann Microbiol 64:721–734

    Article  CAS  Google Scholar 

  44. Sun X, Ding Q, Hyde KD, Guo LD (2012) Community structure and preference of endophytic fungi of three woody plants in a mixed forest. Fungal Ecol 5:624–632

    Article  Google Scholar 

  45. Laforest-Lapointe I, Messier C, Kembel SW (2016) Tree phyllosphere bacterial communities: exploring the magnitude of intra- and inter-individual variation among host species. Peer J 4:e2367

    Article  PubMed  Google Scholar 

  46. Osono T, Mori A (2003) Colonization of Japanese beech leaves by phyllosphere fungi. Mycoscience 44:437–441

    Article  Google Scholar 

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Acknowledgements

This work is funded by FEDER funds through COMPETE (Programa Operacional Factores de Competitividade) and by national funds by FCT (Fundação para a Ciência e a Tecnologia) within the framework of the project EXCL/AGR-PRO/0591/2012. T. Gomes thanks FCT, POPH-QREN, and FSE for PhD SFRH/BD/98127/2013 grant.

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Authors and Affiliations

  1. School of Agriculture—Polytechnic Institute of Bragança, CIMO, Campus Sta Apolónia, 5300-253, Bragança, Portugal

    Teresa Gomes, José Alberto Pereira, Jacinto Benhadi & Paula Baptista

  2. Biosystems & Integrative Sciences Institute (BioISI), Plant Functional Biology Center (CBFP), University of Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    Teresa Gomes & Teresa Lino-Neto

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  1. Teresa Gomes
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  2. José Alberto Pereira
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  3. Jacinto Benhadi
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  4. Teresa Lino-Neto
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  5. Paula Baptista
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Correspondence to Paula Baptista.

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Gomes, T., Pereira, J.A., Benhadi, J. et al. Endophytic and Epiphytic Phyllosphere Fungal Communities Are Shaped by Different Environmental Factors in a Mediterranean Ecosystem. Microb Ecol 76, 668–679 (2018). https://doi.org/10.1007/s00248-018-1161-9

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  • DOI: https://doi.org/10.1007/s00248-018-1161-9

Keywords

  • Climatic factors
  • Fungal community structure
  • Olea europaea L.
  • Organ specificity
  • Seasonal patterns