1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 74, Issue 2

Diversity and distribution of species across different types of riparian vegetation in Italy with the description of sp. nov. No Access

Abstract

Riparian formations encompass a diverse suite of transitional zones between terrestrial and aquatic ecosystems. During the last decades, these formations have been impacted by several emerging diseases. The first outbreaks were detected on alder formations, but have progressively also been observed on other plant species such as , , , , and . Declining plants showed a plethora of symptoms (leaf spot, shoot blight, bleeding cankers and root rot) indicative of infections. Since there is little information about the aetiology of these pathosystems, from November 2019 to March 2023, an in-depth study was conducted in 46 riparian ecosystems spanning from the Mediterranean to Alpine regions. Overall, 744 symptomatic samples (stem bleeding cankers and root with rhizosphere) from 27 host species were collected for isolation. Based on morphology and DNA sequence data, 20 known species belonging to seven phylogenetic clades have been identified: (202 isolates), (156), (84), (57), (31), (30), (20), (19), (13), (13), (9), (6), (6), (4), (4), (3), (2) (2), (2) and (2). In addition, 26 isolates of a new putative species obtained from and are described here as sp. nov. The new species proved to be pathogenic on grey alder causing symptoms congruent with field observations. This study represents the most comprehensive investigation on the species associated with declining riparian vegetation in Italy and highlights that the polyphagous pathogen represents a growing threat to Mediterranean, temperate and alpine ecosystems.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biodiversity , emerging disease , oomycetes and pathogenicity
© 2024 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006272
2024-02-26
2024-04-27
Loading full text...

Full text loading...

References

  1. Naiman RJ, Bechtold JS, Drake DC, Latterell JJ, O’Keefe TC et al. Origins, patterns, and importance of heterogeneity in riparian systems. Ecosyst Func Het Landsc 2005; 279–309: [View Article]
     [Google Scholar]
  2. Dufour S, Rodríguez-González PM, Laslier M. Tracing the scientific trajectory of riparian vegetation studies: main topics, approaches and needs in a globally changing world. Sci Total Environ 2019; 653:1168–1185 [View Article] [PubMed]
     [Google Scholar]
  3. Riis T, Kelly-Quinn M, Aguiar FC, Manolaki P, Bruno D et al. Global overview of ecosystem services provided by riparian vegetation. BioScience 2020; 70:501–514 [View Article]
     [Google Scholar]
  4. Kristensen P, Kristensen E, Riis T, Anette A, Larsen S et al. Riparian forest as a management tool for moderating future thermal conditions of lowland temperate streams. IW 2015; 5:27–38 [View Article]
     [Google Scholar]
  5. Trimmel H, Weihs P, Leidinger D, Formayer H, Kalny G et al. Can riparian vegetation shade mitigate the expected rise in stream temperatures due to climate change during heat waves in a human-impacted pre-alpine river?. Hydrol Earth Syst Sci 2018; 22:437–461 [View Article]
     [Google Scholar]
  6. Rosenberg DK, Noon BR, Meslow EC. Biological corridors: form, function, and efficacy. BioScience 1997; 47:677–687 [View Article]
     [Google Scholar]
  7. de la Fuente B, Mateo-Sánchez MC, Rodríguez G, Gastón A, Pérez de Ayala R et al. Natura 2000 sites, public forests and riparian corridors: the connectivity backbone of forest green infrastructure. Land Use Policy 2018; 75:429–441 [View Article]
     [Google Scholar]
  8. Urbanič G, Politti E, Rodríguez-González PM, Payne R, Schook D et al. Riparian zones—from policy neglected to policy integrated. Front Environ Sci 2022; 10:868527 [View Article]
     [Google Scholar]
  9. Corbacho C, Sánchez JM, Costillo E. Patterns of structural complexity and human disturbance of riparian vegetation in agricultural landscapes of a Mediterranean area. Agriculture, Ecosystems & Environment 2003; 95:495–507 [View Article]
     [Google Scholar]
  10. Fierro P, Bertrán C, Tapia J, Hauenstein E, Peña-Cortés F et al. Effects of local land-use on riparian vegetation, water quality, and the functional organization of macroinvertebrate assemblages. Sci Total Environ 2017; 609:724–734 [View Article] [PubMed]
     [Google Scholar]
  11. Politti E, Bertoldi W, Gurnell A, Henshaw A. Feedbacks between the riparian Salicaceae and hydrogeomorphic processes: a quantitative review. Earth-Science Reviews 2018; 176:147–165 [View Article]
     [Google Scholar]
  12. Ren BQ, Xiang XG, Chen ZD. Species identification of Alnus (Betulaceae) using nrDNA and cpDNA genetic markers. Mol Ecol Resour 2010; 10:594–605 [View Article] [PubMed]
     [Google Scholar]
  13. Lytle DA, Poff NL. Adaptation to natural flow regimes. Trends Ecol Evol 2004; 19:94–100 [View Article] [PubMed]
     [Google Scholar]
  14. Nagel JH, Slippers B, Wingfield MJ, Gryzenhout M. Multiple Phytophthora species associated with a single riparian ecosystem in South Africa. Mycologia 2015; 107:915–925 [View Article] [PubMed]
     [Google Scholar]
  15. Dunstan WA, Howard K, StJ Hardy GE, Burgess TI. An overview of Australia’s Phytophthora species assemblage in natural ecosystems recovered from a survey in Victoria. IMA Fungus 2016; 7:47–58 [View Article] [PubMed]
     [Google Scholar]
  16. Stamler RA, Sanogo S, Goldberg NP, Randall JJ. Phytophthora species in rivers and streams of the Southwestern United States. Appl Environ Microbiol 2016; 82:4696–4704 [View Article] [PubMed]
     [Google Scholar]
  17. Bregant C, Rossetto G, Meli L, Sasso N, Montecchio L et al. Diversity of Phytophthora species involved in new diseases of mountain vegetation in Europe with the description of Phytophthora pseudogregata sp. nov. Forests 2023; 14:1515 [View Article]
     [Google Scholar]
  18. Sims LL, Sutton W, Reeser P, Hansen EM. The Phytophthora species assemblage and diversity in riparian alder ecosystems of western Oregon, USA. Mycologia 2015; 107:889–902 [View Article] [PubMed]
     [Google Scholar]
  19. Bregant C, Sanna GP, Bottos A, Maddau L, Montecchio L et al. Diversity and pathogenicity of Phytophthora species associated with declining alder trees in Italy and description of Phytophthora alpina sp. nov. Forests 2020; 11:848 [View Article]
     [Google Scholar]
  20. Trzewik A, Orlikowski LB, Oszako T, Nowakowska JA, Orlikowska T. The characterization of Phytophthora isolates obtained from diseased Alnus glutinosa in Poland. Balt For 2015; 21:44–50
     [Google Scholar]
  21. Aday Kaya AG, Lehtijärvi A, Şaşmaz Y, Nowakowska JA, Oszako T et al. Phytophthora species detected in the rhizosphere of Alnus glutinosa stands in the floodplain forests of Western Turkey. Forest Pathology 2018; 48: [View Article]
     [Google Scholar]
  22. Bregant C, Batista E, Hilário S, Linaldeddu BT, Alves A. Phytophthora species involved in Alnus glutinosa decline in Portugal. Pathogens 2023; 12:276 [View Article]
     [Google Scholar]
  23. Navarro S, Sims L, Hansen E. Pathogenicity to alder of Phytophthora species from riparian ecosystems in western Oregon. Forest Pathology 2015; 45:358–366 [View Article]
     [Google Scholar]
  24. Seddaiu S, Linaldeddu BT. First report of Phytophthora acerina, P. plurivora, and P. pseudocryptogea associated with declining common Alder trees in Italy. Plant Dis 2020; 104:1874 [View Article]
     [Google Scholar]
  25. Senanayake IC, Rossi W, Leonardi M, Weir A, McHugh M et al. Fungal diversity notes 1611–1716: taxonomic and phylogenetic contributions on fungal genera and species emphasis in south China. Fungal Diversity 2023; 122:161–403 [View Article]
     [Google Scholar]
  26. Hüberli D, Hardy GEStJ, White D, Williams N, Burgess TI. Fishing for Phytophthora from Western Australia’s waterways: a distribution and diversity survey. Australasian Plant Pathol 2013; 42:251–260 [View Article]
     [Google Scholar]
  27. Linderman RG, Zeitoun F. Phytophthora cinnamomi causing root rot and wilt of nursery-grown native Western azalea and Salal. Plant Disease Reporter 1977; 61:1045–1048
     [Google Scholar]
  28. Brasier CM. Observations on the sexual mechanism in Phytophthora palmivora and related species. Trans Brit Mycol Soc 1972; 58:237–251 [View Article]
     [Google Scholar]
  29. Mehrlich FP. Non-sterile soil Leachate stimulating to Zoosporangia production by Phytophthora SP. Phytopathology 1935; 25:432–443
     [Google Scholar]
  30. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis MA, Gelfand DH, Sninsky JJ, White J. eds PCR Protocols, a Guide to Methods and Applications San Diego, CA, USA: Academic Press; 1990 pp 315–322
     [Google Scholar]
  31. Yang X, Tyler BM, Hong C. An expanded phylogeny for the genus Phytophthora. IMA Fungus 2017; 8:355–384 [View Article]
     [Google Scholar]
  32. Martin FN, Tooley PW. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 2003; 95:269–284 [PubMed]
     [Google Scholar]
  33. Kroon L, Bakker FT, van den Bosch GBM, Bonants PJM, Flier WG. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet Biol 2004; 41:766–782 [View Article] [PubMed]
     [Google Scholar]
  34. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25:4876–4882 [View Article] [PubMed]
     [Google Scholar]
  35. Hall TA. Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
     [Google Scholar]
  36. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
     [Google Scholar]
  37. Orlikowski LB, Oszako T, Szkuta G. First record of Alder Phytophthora in Poland. J Plant Protect Res 2003; 43:33–39
     [Google Scholar]
  38. Lamari L. Assess: image analysis software for plant disease quantification APS press; 2002
     [Google Scholar]
  39. Jung T, Stukely MJC, Hardy GESJ, White D, Paap T et al. Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Persoonia 2011; 26:13–39 [View Article] [PubMed]
     [Google Scholar]
  40. Bjelke U, Boberg J, Oliva J, Tattersdill K, McKie BG. Dieback of riparian alder caused by the Phytophthora alni complex: projected consequences for stream ecosystems. Freshwater Biology 2016; 61:565–579 [View Article]
     [Google Scholar]
  41. Brasier CM, Kirk SA, Delcan J, Cooke DEL, Jung T et al. Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol Res 2004; 108:1172–1184 [View Article] [PubMed]
     [Google Scholar]
  42. Corcobado T, Cech TL, Daxer A, Ďatková H, Janoušek J et al. Phytophthora, Nothophytophthora and Halophytophthora diversity in rivers, streams and riparian alder ecosystems of Central Europe. Mycol Progress 2023; 22:50 [View Article]
     [Google Scholar]
  43. Brasier CM, Cooke DEL, Duncan JM, Hansen EM. Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides-P. megasperma ITS Clade 6, which tend to be high-temperature tolerant and either inbreeding or sterile. Mycol Res 2003; 107:277–290 [View Article] [PubMed]
     [Google Scholar]
  44. Coomber A, Saville A, Carbone I, Ristaino JB. An open-access T-BAS phylogeny for emerging Phytophthora species. PLoS One 2023; 18:e0283540 [View Article] [PubMed]
     [Google Scholar]
  45. Aghighi S, Hardy GEStJ, Scott JK, Burgess TI. Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia. Eur J Plant Pathol 2012; 133:841–855 [View Article]
     [Google Scholar]
  46. Nechwatal J, Bakonyi J, Cacciola SO, Cooke DEL, Jung T et al. The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp. nov. Plant Pathology 2013; 62:355–369 [View Article]
     [Google Scholar]
  47. Hansen EM, Reeser PW, Sutton W. Ecology and pathology of Phytophthora ITS clade 3 species in forests in western Oregon, USA. Mycologia 2017; 109:100–114 [View Article]
     [Google Scholar]
  48. Crous PW, Cowan DA, Maggs-Kölling G, Yilmaz N, Thangavel R et al. Fungal planet description sheets: 1182-1283. Persoonia 2021; 46:313–528 [View Article] [PubMed]
     [Google Scholar]
  49. Drechsler C. Repetitional diplanetism in the genus Phytophthora. J Agric Res 1930; 40:6
     [Google Scholar]
  50. Waterhouse GM. The genus Phytophthora de Bary. diagnoses (or descriptions) and figures from the original papers Ed. 2. Mycol Pap 1970; 122:
     [Google Scholar]
  51. Erwin DC, Ribeiro OK. Phytophthora Diseases Worldwide American Phytopathological Society (APS Press); 1996
     [Google Scholar]
  52. Brown AV, Brasier CM. Colonization of tree xylem by Phytophthora ramorum, P. Kernoviae and other Phytophthora species. Plant Pathol 2007; 56:227–241 [View Article]
     [Google Scholar]
  53. Durán A, Gryzenhout M, Slippers B, Ahumada R, Rotella A et al. Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathol 2008; 57:715–727 [View Article]
     [Google Scholar]
  54. Jung T, Nechwatal J. Phytophthora gallica sp. nov., a new species from rhizosphere soil of declining oak and reed stands in France and Germany. Mycol Res 2008; 112:1195–1205 [View Article] [PubMed]
     [Google Scholar]
  55. Linaldeddu BT, Scanu B, Maddau L, Franceschini A. Diplodia corticola and Phytophthora cinnamomi: the main pathogens involved in Holm oak decline on Caprera Island (Italy). For Pathol 2014; 44:191–200 [View Article]
     [Google Scholar]
  56. Reeser PW, Sutton W, Hansen EM, Remigi P, Adams GC. Phytophthora species in forest streams in Oregon and Alaska. Mycologia 2011; 103:22–35 [View Article] [PubMed]
     [Google Scholar]
  57. Fajardo SN, Valenzuela S, Dos Santos AF, González MP, Sanfuentes EA. Phytophthora pseudosyringae associated with the mortality of Nothofagus obliqua in a pure stand in central‐southern Chile. Forest Pathology 2017; 47: [View Article]
     [Google Scholar]
  58. Grünwald NJ, Flier WG. The biology of Phytophthora infestans at its center of origin. Annu Rev Phytopathol 2005; 43:171–190 [View Article] [PubMed]
     [Google Scholar]
  59. Panabieres F, Ali GS, Allagui MB, Dalio R, Gudmestad NC et al. Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathol Mediterr 201620–40
     [Google Scholar]
  60. Chen XR, Wen K, Zhou X, Zhu MY, Liu Y et al. The devastating oomycete phytopathogen Phytophthora cactorum: insights into its biology and molecular features. Mol Plant Pathol 2023; 24:1017–1032 [View Article] [PubMed]
     [Google Scholar]
  61. Linaldeddu BT, Rossetto G, Maddau L, Vatrano T, Bregant C. Diversity and pathogenicity of botryosphaeriaceae and Phytophthora species associated with emerging olive diseases in Italy. Agriculture 2023; 13:1575 [View Article]
     [Google Scholar]
  62. Schoebel CN, Stewart J, Grünwald NJ, Rigling D, Prospero S. Population history and pathways of spread of the plant pathogen Phytophthora plurivora. PLoS One 2014; 9:e85368 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006272
Loading
Diversity and distribution of Phytophthora species across different types of riparian vegetation in Italy with the description of Phytophthora heteromorpha sp. nov.
Int J Syst Evol Microbiol 74, 006272 (2024); https://doi.org/10.1099/ijsem.0.006272
/content/journal/ijsem/10.1099/ijsem.0.006272
/content/journal/ijsem/10.1099/ijsem.0.006272
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error