Advertisement

Epidemiological Investigations Shed Light on the Ecological Role of the Endophyte Phomopsis quercina in Mediterranean Oak Forests

  • Salvatore Moricca
  • Gloria Innocenti
  • Alessandro Ragazzi
Chapter
Part of the Forestry Sciences book series (FOSC, volume 86)

Abstract

Findings of a study extending over a number of years on some key aspects of the biology and ecology of Phomopsis quercina in Mediterranean oak forests are reported. The main biometric parameters and physiological requirements of this significant endophytic fungus were determined in the laboratory. The microorganism was also studied in the field to explore its lifestyle in natural oak stands. The isolation frequencies of the fungus in various oak species were also related to the vitality of the trees (healthy or declining) and this showed that the fungus is involved in the widespread phenomenon of oak decline. In planta studies have proved the pathogenic activity of P. quercina in oak, and have found that it remains latent for a long time in the inner wood of oaks, but may turn into an aggressive and harmful coloniser of the tree if this is weakened by some stress factors. An important part of the study concerns an examination of the antagonism that some other endophytes, which colonise the same oak tissues and organs as P. quercina, display against this fungus. The increasing presence and abundance of P. quercina in declining (and especially drought-stressed) oaks suggests that climate change is having a significant role in destabilising the precarious balance between the host tree and the fungus, to the benefit of the latter. Lastly, some practical suggestions are offered on ways to counter the epidemic spread of this latent pathogen.

Abbreviations

IF

Isolation frequency

DI

Disease index

PDA

Potato-dextrose-agar

PDB

Potato-dextrose-broth

ME

Malt-extract

MEA

Malt-extract-agar

AI

Antagonism index

BCA

Biological control agent

Notes

Acknowledgements

Particular thanks to Dr. Celeste Vizzuso and Dr. Elena Turco, who shared with us their valuable experiences and expert knowledge on studies on endophytes of forest trees. The Authors wish also to thank Mrs. Irene Dellavalle, of the Institute for Sustainable Plant Protection of CNR, Florence, Italy, for technical assistance in the field and in the laboratory.

References

  1. Amusa NA (2006) Microbially produced phytotoxins and plant disease management. Afr J Biotechnol 5:405–414Google Scholar
  2. Anselmi N, Cellerino GP, Franceschini A et al (2004) Geographic distribution of fungal endophytes of Quercus sp. in Italy. In: Ragazzi A, Moricca S, Dellavalle I (eds) Endophytism in forest trees. Accademia Italiana di Scienze Forestali, Firenze, pp 73–89Google Scholar
  3. Badalyan SM, Innocenti G, Garibyan NG (2002) Antagonistic activity of xylotrophic mushrooms against pathogenic fungi in dual culture. Phytopathol Mediterr 41:200–225Google Scholar
  4. Brayford D (1990) Variation in Phomopsis isolates from Ulmus species in the British Isles and Italy. Mycol Res 94:691–697CrossRefGoogle Scholar
  5. Bhuiyan SA, Ryley MJ, Galea VJ et al (2003) Evaluation of potential biocontrol agents against Claviceps africana in vitro and in vivo. Plant Pathol 52:60–67CrossRefGoogle Scholar
  6. Carmichael JW, Kendrick WB, Conners IL et al (1980) Genera of hyphomycetes. The University of Alberta Press, Alberta 386 ppGoogle Scholar
  7. Chepkirui C, Stadler M (2017) The genus Diaporthe: a rich source of diverse and bioactive metabolites. Mycol Prog 16:477–494CrossRefGoogle Scholar
  8. Cohen SD (2004) Endophytic-host selectivity of Discula umbrinella on Quercus alba and Quercus rubra characterized by infection, pathogenicity and mycelial compatibility. Eur J Plant Pathol 110:713–721CrossRefGoogle Scholar
  9. Ferretti M (1994) Mediterranean forest trees. A guide for crown assessment. CEC UN/ECE, Brussels, p 15Google Scholar
  10. Fiss M, Kucheryava N, Schonherr J et al (2000) Isolation and characterization of epiphytic fungi from the phyllosphere of apple as potential biocontrol agents against apple scab (Venturia inequalis). J Pl Dis Protect 107:1–11Google Scholar
  11. Führer E (1998) Oak decline in Central Europe: a synopsis of hypotheses. In ML McManus and AM Liebhold (eds) Proceedings: population dynamics, impacts and integrated management of forest defoliating insects. USDA Forest Service General Technical Report NE-247, pp 7–24Google Scholar
  12. Gams W (1971) Cephalosporium-artige Schimmelpilze (hyphomycetes). Gustav Fischer-Verlag, Stuttgart, p 262Google Scholar
  13. Girish K, Shankara BS, Raveesha KA (2009) Crude toxin extract from culture filtrate of Phomopsis azadirachtae infecting neem and its phytotoxicity. Int J Integr Biol 6:79–84Google Scholar
  14. Gonthier P, Gennaro M, Nicolotti G (2006) Effects of water stress on the endophytic mycota of Quercus robur. Fungal Diver 21:69–80Google Scholar
  15. Horn WS, Simmonds MSJ, Scwarthz RE et al (1996) Variation in production of Phomodiol and Phomopsolide B by Phomopsis spp. Mycologia 88:588–595CrossRefGoogle Scholar
  16. Keča N, Koufakis I, Dietershagen J et al (2016) European Oak decline phenomenon in relation to climatic changes. Folia For Pol Ser A For 58:170–177Google Scholar
  17. Kirk PM, Cannon PF, David JC et al (eds) (2001) Ainsworth and Bisby’s dictionary of the Fungi, 9th edn. CAB International, KewGoogle Scholar
  18. Kulik MM (1984) Symptomless infection, persistence and production of pycnidia in host and non-host plants by Phomopsis batatae, Phomopsis phaseoli and Phomopsis sojae and the taxonomic implications. Mycologia 76:274–291CrossRefGoogle Scholar
  19. Luciano P (2009) Tecniche di monitoraggio fitosanitario e utilizzo di dati georeferenziati. Atti Accad Naz It Entomol, LVII, pp 83–97Google Scholar
  20. Madrigal C, Melgarejo P (1995) Morphological effects of Epicoccum nigrum and its antibiotic flavipin on Monilinia laxa. Can J Bot 18:425–431CrossRefGoogle Scholar
  21. Moricca S, Bracalini M, Croci F et al (2018) Biotic factors affecting ecosystem services in urban and peri-urban forests in Italy: the role of introduced and impending pathogens and pests. Forests 9(2):65.  https://doi.org/10.3390/f9020065CrossRefGoogle Scholar
  22. Moricca S, Ginetti B, Ragazzi A (2012) Species and organ specificity in endophytes colonizing healthy and declining Mediterranean oaks. Phytopathol Mediterr 51:587–598Google Scholar
  23. Moricca S, Ragazzi A (2008a) Biological and integrated means to control rust diseases. In: Ciancio A, Mukerji KG (eds) Integrated management of disease caused by fungi, Phytoplasma and bacteria. Springer, Heidelberg 303–332 ppGoogle Scholar
  24. Moricca S, Ragazzi A (2008b) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology 98:380–386CrossRefPubMedGoogle Scholar
  25. Moricca S, Ragazzi A (2011) The Holomorph Apiognomonia quercina/Discula quercina as a Pathogen/Endophyte in oak. In: Pirttilä AM, Frank C (eds) Endophytes of forest trees: biology, and application. Forestry sciences, vol 80. Springer Science+Business Media, Berlin 47–66 ppCrossRefGoogle Scholar
  26. Moricca S, Linaldeddu BT, Ginetti B et al (2016) Endemic and emerging pathogens threatening cork oak trees: management options for conserving a unique forest ecosystem. Plant Dis 100:2184–2193CrossRefGoogle Scholar
  27. Mostert L, Crous PW, Kang JC et al (2001) Species of Phomopsis and a Libertella sp. occurring on grapevines with specific reference to South Africa: morphological, cultural, molecular and pathological characterization. Mycologia 93:146–167CrossRefGoogle Scholar
  28. Mueller D, Bradley C, Chilvers M et al (2015) Pod and stem blight and Phomopsis seed decay. Soybean Dis Manag CPN-1007Google Scholar
  29. Murali TS, Suryanarayanan TS, Geeta R (2006) Endophytic Phomopsis species: host range and implications for diversity estimates. Can J Microbiol 52:673–680CrossRefPubMedGoogle Scholar
  30. Oszako T, Delatour C (2000) Recent advances on oak health in Europe. Forest Research Institute, Warsaw, p 281Google Scholar
  31. Otero JT, Ackerman JD, Bayman P (2002) Diversity and host specificity of endophytic Rhizoctonia-like fungi from tropical orchids. Am J Bot 89:1852–1858CrossRefGoogle Scholar
  32. Panzavolta T, Panichi A, Bracalini M et al (2017) Dispersal and propagule pressure of Botryosphaeriaceae species in a declining oak stand is affected by insect vectors. Forests 8(7):228.  https://doi.org/10.3390/f8070228CrossRefGoogle Scholar
  33. Philipps DH, Burdekin DA (1992) Diseases of forest and ornamental trees. The MacMillan Press LTD, London, p 537CrossRefGoogle Scholar
  34. Ragazzi A (1989) Popolazioni fungine associate a piante deperenti di Quercus cerris. Micol Ital 18:127–132Google Scholar
  35. Ragazzi A (2004) Endophytism: knowns and unknowns of an age-old phenomenon. In: Ragazzi A, Moricca S, Dellavalle I (eds) Endophytism in forest trees. Accademia Italiana di Scienze Forestali, Firenze, pp 17–32Google Scholar
  36. Ragazzi A, Dellavalle-Fedi I, D’Onofrio G (1986) Osservazioni preliminari su un deperimento di Quercus robur L. e Q. frainetto Ten. In Italia. Atti delle Giornate Fitopatologiche, Riva del Garda 2:241–252Google Scholar
  37. Ragazzi A, Dellavalle Fedi I, Moricca S (1990) Modello di colonizzazione di Quercus cerris da parte di Diplodia mutila e Phomopsis quercina. Phytopathol Mediterr 29:209–212Google Scholar
  38. Ragazzi A, Dellavalle I, Moricca S, Capretti P, Raddi P (2000) Decline of oak species in Italy, problems and perspectives. Accademia Italiana di Scienze Forestali, Firenze, p 257Google Scholar
  39. Ragazzi A, Vagniluca S, Moricca S (1995) European expansion of oak decline, involved micorganisms, and methodological approaches. Phytopathol Mediterr 34:207–226Google Scholar
  40. Ragazzi A, Moricca S, Dellavalle I (1997) Vegetative compatibility and pathogenicity of Diplodia mutila isolates on oak. Eur J For Pathol 27:391–396CrossRefGoogle Scholar
  41. Ragazzi A, Moricca S, Dellavalle I (1999) Epidemiological aspects of Discula quercina on oak: inoculum density and conidia production. J Pl Dis Protect 106:501–506Google Scholar
  42. Ragazzi A, Moricca S, Dellavalle I (2004) Endophytism in forest trees. Accademia Italiana di Scienze Forestali, Firenze, p 239Google Scholar
  43. Ragazzi A, Capretti P, Turco E et al (2002) Endofiti di Quercus cerris: studio comparativo in piante sane e deperenti. Micol Ital 31:66–70Google Scholar
  44. Ragazzi A, Moricca S, Capretti P et al (2003) Differences in composition of endophytic mycobiota in twigs and leaves of healthy and declining Quercus species in Italy. Forest Pathol 33:31–38CrossRefGoogle Scholar
  45. Ragazzi A, Moricca S, Capretti P et al (2001) Endophytic fungi in Quercus cerris: isolation frequency in relation to phenological phase, tree health and the organ affected. Phytopathol Mediterr 40:165–171Google Scholar
  46. Rai M, Agarkar G (2016) Plant–fungal interactions: what triggers the fungi to switch among lifestyles? Crit Rev Microbiol 42:428–438CrossRefPubMedGoogle Scholar
  47. Rossman AY, Farr DF, Castlebury LA (2007) A review of the phylogeny and biology of the Diaporthales. Mycoscience 48:135–144CrossRefGoogle Scholar
  48. Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87–100Google Scholar
  49. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74CrossRefGoogle Scholar
  50. Santos L, Alves A, Alves R (2017) Evaluating multi-locus phylogenies for species boundaries determination in the genus Diaporthe. Peer J 5:e3120.  https://doi.org/10.7717/peerj.31205CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shankar M, Cowling WA, Sweetingham MW et al (1999) Screening for resistance to Diaporthe toxica in lupins by estimation of phomopsins and glucoseamine in individual plants. Plant Pathol 48:320–324CrossRefGoogle Scholar
  52. Schulze B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686CrossRefGoogle Scholar
  53. Schulz B, Guske S, Dammann U et al (1998) Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227Google Scholar
  54. Sutton BC (1980) The Coelomycetes. Fungi Imperfecti with Pycnidia, Acervuli and Stromata. CMI, Kew 696 ppGoogle Scholar
  55. Svabova L, Lebeda A (2005) In vitro selection for improved plant resistance to toxin-producing pathogens. J Phytopathol 153:52–64CrossRefGoogle Scholar
  56. Toti L, Chapela IH, Petrini O (1992) Morphometric evidence for host-specific strain formation in Discula umbrinella (teleomorph: Apiognomonia errabunda). Mycol Res 96:420–424CrossRefGoogle Scholar
  57. Udayanga D, Liu X, Crous PW et al (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers 56:157–171CrossRefGoogle Scholar
  58. Udayanga D, Liu X, Mc Kenzie EHC et al (2011) Genus Phomopsis: biology, applications, specie concepts and names of common phytopathogens. Fungal Divers 50:189–225CrossRefGoogle Scholar
  59. van Kan JAL (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253CrossRefPubMedGoogle Scholar
  60. Vicart N, Ortholand JY, Emeric GY et al (1994) Syntesis and absolute configuration of phomozin. Tehrahedon Lett 35:3917–3918CrossRefGoogle Scholar
  61. Viret O, Toti L, Chapela IH et al (1994) The role of the extracellular sheath in recognition and attachment of conidia of Discula umbrinella (Berk. And Br.) Morelet to the host surface. New Phytol 127:123–131CrossRefGoogle Scholar
  62. Vizzuso C, Turco E, Dellavalle I et al (2007) Interazioni antagonistiche in vitro fra Phomopsis quercina e funghi endofitici di specie quercine. Micol Ital 2:30–38Google Scholar
  63. Von Arx JA (1987) Plant pathogenic fungi. J. Cramer Verlag, Berlin, p 288Google Scholar
  64. Woo SY (2009) Forest decline of the world: a linkage with air pollution and global warming. Afr J Biotechnol 8:7409–7414Google Scholar
  65. Zhang N, Blackwell M (2001) Molecular phylogeny of dogwood anthracnose fungus (Discula destructiva) and the Diaporthales. Mycologia 93:355–365CrossRefGoogle Scholar
  66. Zhang N, Castlebury LA, Miller AN et al (2006) An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny. Mycologia 98:11077–11088CrossRefGoogle Scholar
  67. Zhou DQ, Hyde KD (2001) Host-specificity, host-exclusivity and host-recurrence in saprobic fungi. Mycol Res 105:1449–1457CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Salvatore Moricca
    • 1
  • Gloria Innocenti
    • 2
  • Alessandro Ragazzi
    • 1
  1. 1.Plant Pathology and Entomology Division, Department of Agrifood Production and Environmental SciencesUniversity of FlorenceFlorenceItaly
  2. 2.Department of Agricultural SciencesUniversity of BolognaBolognaItaly

Personalised recommendations