Abstract
Eucalypt, mostly Eucalyptus globulus, is the exotic tree species occupying the largest area of Portuguese planted forest. Eucalypts were introduced in the country more than one hundred years ago, but it was only in the second half of the twentieth century that the area of plantations grew with the onset of their use in the paper and pulp industry. As an exotic species, it was free from pests and diseases but gradually the number of insects and pathogens affecting these plants increased. In recent year, a new disease causing root rot and dieback has been detected with increasing frequency. In this work, two Phytophthora species, P. cinnamomi and P. alticola, were identified associated with these symptoms. Koch’s postulates were fulfilled, proving that these two species are pathogenic to E. globulus. This is the first report of P. alticola outside South Africa. Although presently unknown, the possible factors associated with the increased occurrence of this disease are discussed.
Similar content being viewed by others
Data availability
Sequences are available at GenBank (https://www.ncbi.nlm.nih.gov/genbank) and alignments and trees are deposited in TreeBase (https://treebase.org).
References
Abad, G., Burgess, T., Bienapfl, J. C., Redford, A. J., Coffey, M., & Knight, L. (2019). IDphy: molecular and morphological identification of Phytophthora based on the types. https://idtools.org/id/phytophthora/index.php. Accessed 24 Mar 2022.
Balci, Y., Balci, S., Blair, J. E., Park, S.-Y., Kang, S., & Macdonald, W. L. (2008). Phytophthora quercetorum sp. nov., a novel species isolated from eastern and north-Central USA oak forest soils. Mycological Research, 112(8), 906–916. https://doi.org/10.1016/j.mycres.2008.02.008
Barradas, C., Phillips, A. J. L., Correia, A., Diogo, E., Bragança, H., & Alves, A. (2016). Diversity and potential impact of Botryosphaeriaceae species associated with Eucalyptus globulus plantations in Portugal. European Journal of Plant Pathology, 146(2), 1–13. https://doi.org/10.1007/s10658-016-0910-1
Barradas, C., Pinto, G., Correia, B., Jesus, C., & Alves, A. (2019). Impact of Botryosphaeria, Diplodia and Neofusicoccum species on two Eucalyptus species and a hybrid: From pathogenicity to physiological performance. Forest Pathology, 49, 1–11. https://doi.org/10.1111/efp.12493
Batini, F. (2018). Response to the article “Relative importance of site, weather and Phytophthora cinnamomi in the decline and death of Eucalyptus marginata - jarrah dieback investigations in the 1970s to 1990s E M Davison, (2018) 47,245”. Australasian Plant Pathology, 47(5), 463–464. https://doi.org/10.1007/s13313-018-0581-9
Bayly, M. J. (2016). Phylogenetic studies of eucalypts: Fossils, morphology and genomes. Proceedings. Royal Society of Victoria, 128(1), 12–24. https://doi.org/10.1071/RS16002
Blair, J. E., Coffey, M. D., Park, S.-Y., Geiser, D. M., & Kang, S. (2008). A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology, 45, 266–277. https://doi.org/10.1016/j.fgb.2007.10.010
Borralho, N. M. G., Almeida, M. H., & Potts, B. M. (2007). O Melhoramento do Eucalipto em Portugal. In A. A. M., J. S. Pereira, & J. M. . N. Silva (Eds.), O Eucaliptal em Portugal (pp. 61–112). Isa Press.
Bose, T., Burgess, T. I., Roux, J., & Wingfield, M. J. (2017). Phytophthora alticola; emended description based on new collections and a neotype. Sydowia, 69, 161–170. https://doi.org/10.12905/0380.sydowia69-2017-0161
Bose, T., Roux, J., Burgess, T. I., Shaw, C., & Wingfield, M. J. (2019). Susceptibility of Eucalyptus grandis and Acacia mearnsii seedlings to five Phytophthora species common in south African plantations. Forest Pathology, 49(6), 1–8. https://doi.org/10.1111/efp.12560
Bragança, H., Diogo, E. L. F., Neves, L., Valente, C., Araújo, C., Bonifácio, L., & Phillips, A. J. L. (2016). Quambalaria eucalypti a pathogen of Eucalyptus globulus newly reported in Portugal and in Europe. Forest Pathology, 46(1), 67–75. https://doi.org/10.1111/efp.12221
Brasier, C. M. (1996). Phytophthora cinnamomi and oak decline southern Europe . Environmental constraints including climate change. Annales des Sciences Forestières, 53, 347–358.
Brasier, C. M., Robredo, F., & Ferraz, J. F. P. (1993). Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathology, 42(1), 140–145. https://doi.org/10.1111/j.1365-3059.1993.tb01482.x
Bregant, C., Mulas, A. A., Rossetto, G., Deidda, A., Maddau, L., Piras, G., & Linaldeddu, B. T. (2021). Phytophthora mediterranea sp. nov., a new species closely related to Phytophthora cinnamomi from nursery plants of Myrtus communis in Italy. Forests, 12(6), 682. https://doi.org/10.3390/f12060682
Cooke, D. E. L., Drenth, A., Duncan, J. M., Wagels, G., & Brasier, C. M. (2000). A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology, 30, 17–32. https://doi.org/10.1006/fgbi.2000.1202
Davison, E. M. (2014). Resolving confusions about jarrah dieback - don’t forget the plants. Australasian Plant Pathology, 43(6), 691–701. https://doi.org/10.1007/s13313-014-0302-y
Davison, E. M. (2018). Relative importance of site, weather and Phytophthora cinnamomi in the decline and death of Eucalyptus marginata - jarrah dieback investigations in the 1970s to 1990s. Australasian Plant Pathology, 47, 245–257. https://doi.org/10.1007/s13313-018-0581-9
Davison, E. M., & Shearer, B. L. (1989). Phytophthora spp. in indigenous forests in Australia. New Zealand Journal of Forestry Science, 19(2–3), 277–289.
de Sampaio e Paiva Camilo-Alves, C., da Clara, M. I. E., & de Almeida Ribeiro, N. M. C. (2013). Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. European Journal of Forest Research, 132(3), 411–432. https://doi.org/10.1007/s10342-013-0688-z
Diogo, E., Gonçalves, C. I., Silva, A. C., Valente, C., Bragança, H., & Phillips, A. J. L. (2021). Five new species of Neopestalotiopsis associated with diseased Eucalyptus spp. in Portugal. Mycological Progress, 20, 1441–1456. https://doi.org/10.1007/s11557-021-01741-5
Diogo, E. L. F., Santos, J. M., & Phillips, A. J. L. (2010). Phylogeny, morphology and pathogenicity of Diaporthe and Phomopsis species on almond in Portugal. Fungal Diversity, 44(1), 107–115. https://doi.org/10.1007/s13225-010-0057-x
Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. : American Phytopathological Society.
Hasegawa, M., Kishino, H., & Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22(2), 160–174. https://doi.org/10.1007/BF02101694
Hüberli, D., Calver, M. C., Tommerup, I. C., Colquhoun, I. J., & Hardy, G. E. S. (2002). Temperature and inoculation method influence disease phenotypes and mortality of Eucalyptus marginata clonal lines inoculated with Phytophthora cinnamomi. Australasian Plant Pathology, 31(2), 107. https://doi.org/10.1071/AP01078
Hurley, B. P., Garnas, J., Wingfield, M. J., Branco, M., Richardson, D. M., & Slippers, B. (2016). Increasing numbers and intercontinental spread of invasive insects on eucalypts. Biological Invasions, 18(4), 921–933. https://doi.org/10.1007/s10530-016-1081-x
ICNF. (2019). 6o Inventário Florestal Nacional (IFN6) - 2015 Relatório Final. Lisboa. http://www2.icnf.pt/portal/florestas/ifn/ifn6
Iglesias-Trabado, G., & Wilstermann, D. (2008). Eucalyptus universalis. Global cultivated eucalypt forests map 2008. Version 1.0.1 in GIT forestry Consulting’s EUCALYPTOLOGICS: Information resource on Eucalyptus cultivation worldwide. http://git-forestry-blog.blogspot.com/2008/09/eucalyptus-global-map-2008-cultivated.html
Jeffers, S. N., & Martin, S. B. (1986). Comparison of two media selective for Phytophthora and Pythium species. Plant Disease, 70, 1038–1043.
Jordão, M. (2019). Indústrias de Base Florestal em Portugal. Direção-Geral das Atividades Económicas. https://www.dgae.gov.pt. Accessed 17 Mar 2022
Jung, T., Blaschke, H., & Neumann, P. (1996). Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. European Journal of Forest Pathology, 26, 253–272.
Jung, T., Chang, T. T., Bakonyi, J., Seress, D., Pérez-Sierra, A., Yang, X., Hong, C., Scanu, B., Fu, C. H., Hsueh, K. L., Maia, C., Abad-Campos, P., Léon, M., & Horta Jung, M. (2017). Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathology, 66(2), 194–211. https://doi.org/10.1111/ppa.12564
Jung, T., Jung, M. H., Cacciola, S. O., Cech, T., Bakonyi, J., Seress, D., Mosca, S., Schena, L., Seddaiu, S., Pane, A., di San Lio, G. M., Maia, C., Cravador, A., Franceschini, A., & Scanu, B. (2017). Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus, 8(2), 219–244. https://doi.org/10.5598/imafungus.2017.08.02.02
Jung, T., Orlikowski, L., Henricot, B., Abad-Campos, P., Aday, A. G., Aguín Casal, O., Bakonyi, J., Cacciola, S. O., Cech, T., Chavarriaga, D., Corcobado, T., Cravador, A., Decourcelle, T., Denton, G., Diamandis, S., Doğmuş-Lehtijärvi, H. T., Franceschini, A., Ginetti, B., Green, S., et al. (2016). Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46, 134–163. https://doi.org/10.1111/efp.12239
Jurskis, V. (2005). Eucalypt decline in Australia, and a general concept of tree decline and dieback. Forest Ecology and Management, 215(1–3), 1–20. https://doi.org/10.1016/j.foreco.2005.04.026
Katoh, K., Rozewicki, J., & Yamada, K. D. (2019). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20(4), 1160–1166. https://doi.org/10.1093/bib/bbx108
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
Linde, C., Kemp, G. H. J., & Wingfield, M. J. (1994). Diseases of pines and eucalypts in South Africa associated with Pythium and Phytophthora species. Southern African Forestry Journal, 169(1), 25–32. https://doi.org/10.1080/00382167.1994.9629663
Marks, G. C., Smith, I. W., & Kassaby, F. Y. (1981). Trunk infection of Eucalyptus species by Phytophthora cinnamomi. Australian Forest Research, 11, 257–267.
Maseko, B., Burgess, T. I., Coutinho, T. A., & Wingfield, M. J. (2007). Two new Phytophthora species from south African Eucalyptus plantations. Mycological Research, 111(11), 1321–1338. https://doi.org/10.1016/j.mycres.2007.08.011
Morales-Rodríguez, C., Wang, Y., Martignoni, D., & Vannini, A. (2020). Phytophthora cathayensis sp. nov., a new species pathogenic to Chinese Hickory (Carya cathayensis) in Southeast China. Fungal Systematics and Evolution, 7(June), 99–111. https://doi.org/10.3114/fuse.2021.07.05
Nagel, J. H., Gryzenhout, M., Slippers, B., & Wingfield, M. J. (2013). The occurrence and impact of Phytophthora on the African continent. In K. Lamour (Ed.), Phytophthora: A global perspective (pp. 204–2014). CABI International.
Naves, P., Bragança, H., Nóbrega, F., & Valente, C. (2019). Ambrosiodmus rubricollis (Eichhoff) (Coleoptera; Curculionidae; Scolytinae) associated with young Tasmanian blue gum trees. Journal of Applied Entomology, 143(10), 1200–1204. https://doi.org/10.1111/jen.12700
Newhook, F. J., & Podger, F. D. (1972). The role of Phytophthora Cinnamomi in Australian and New Zealand forests. Annual Review of Phytopathology, 10(1), 299–326. https://doi.org/10.1146/annurev.py.10.090172.001503
O’Gara, E., Howard, K., Wilson, B., & Hardy, G. E. S. (2005). Management of Phytophthora cinnamomi for biodiversity conservation in Australia: Part 2 - National Best Pratice Guidelines. Murdoch University, Western Australia. http://www.environment.gov.au/biodiversity/invasive-species/publications/management-phytophthora-cinnamomi-biodiversity-conservation
Paine, T. D., Steinbauer, M. J., & Lawson, S. A. (2011). Native and exotic pests of eucalyptus: A worldwide perspective. Annual Review of Entomology, 56(1), 181–201. https://doi.org/10.1146/annurev-ento-120709-144817
Podger, F. D. (1972a). Phytophthora cinnamomi, a cause of lethal disease in indigenous plant communities in Western Australia. Phytopathology, 62(9), 972–981. https://doi.org/10.1094/phyto-62-972
Podger, F. D. (1972b). Suscetptibility to Phytophthora cinnamomi root-rot of thirty six species of Eucalytpus. Australian Forest Research, 5(3), 9–20.
Rannala, B., & Yang, Z. (1996). Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. Journal of Molecular Evolution, 43(3), 304–311. https://doi.org/10.1007/BF02338839
Rea, A. J., Burgess, T. I., Hardy, G. E. S. J., Stukely, M. J. C., & Jung, T. (2011). Two novel and potentially endemic species of Phytophthora associated with episodic dieback of Kwongan vegetation in the south-west of Western Australia. Plant Pathology, 60(6), 1055–1068. https://doi.org/10.1111/j.1365-3059.2011.02463.x
Redondo, M. Á., Pérez-Sierra, A., Abad-Campos, P., Torres, L., Solla, A., Reig-Armiñana, J., & García-Breijo, F. (2015). Histology of Quercus ilex roots during infection by Phytophthora cinnamomi. Trees, 29, 1943–1957. https://doi.org/10.1007/s00468-015-1275-3
Robideau, G. P., De Cock, A. W. A. M., Coffey, M. D., Voglmayr, H., Brouwer, H., Bala, K., et al. (2011). DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources, 11(6), 1002–1011. https://doi.org/10.1111/j.1755-0998.2011.03041.x
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542. https://doi.org/10.1093/sysbio/sys029
Scanu, B., Hunter, G. C., Linaldeddu, B. T., Franceschini, A., Maddau, L., Jung, T., & Denman, S. (2014). A taxonomic re-evaluation reveals that Phytophthora cinnamomi and P. cinnamomi var. parvispora are separate species. Forest Pathology, 44(1), 1–20. https://doi.org/10.1111/efp.12064
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676–682. https://doi.org/10.1038/nmeth.2019
Scott, P. M., Burgess, T. I., Barber, P. A., Shearer, B. L., Stukely, M. J. C., Hardy, G. E. S. J., & Jung, T. (2009). Phytophthora multivora sp. nov., a new species recovered from declining Eucalyptus, Banksia, Agonis and other plant species in Western Australia. Persoonia, 22, 1–13. https://doi.org/10.3767/003158509X415450
Sena, K., Crocker, E., Vincelli, P., & Barton, C. (2018). Phytophthora cinnamomi as a driver of forest change: Implications for conservation and management. Forest Ecology and Management, 409(September 2017), 799–807. https://doi.org/10.1016/j.foreco.2017.12.022
Shearer, B., & Smith, I. (2000). Disease of eucalypts caused by soilborne species of Phytophthora and Pythium. In P. J. Keane, F. D. Podger, & B. N. Brown (Eds.), Diseases and pathogens of eucalypts (pp. 259–291). CSIRO Publishing.
Silva, A. C., Diogo, E., Henriques, J., Ramos, A. P., Sandoval-Denis, M., Crous, P. W., & Bragança, H. (2020). Pestalotiopsis pini sp. nov., an emerging pathogen on stone pine (Pinus pinea L.). Forests, 11(8), 1–17. https://doi.org/10.3390/f11080805
Silva, M. C., Machado, H. N., Neves, L., Araujo, C., & Phillips, A. J. L. (2012). Mycosphaerella and Teratosphaeria species associated with Mycosphaerella leaf disease on Eucalyptus globulus in Portugal. Forest Systems, 21(2), 300–305.
Simamora, A. V., Stukely, M. J. C., Hardy, G. E. S., & Burgess, T. I. (2015). Phytophthora boodjera sp. nov. a damping-off pathogen in production nurseries and from urban and natural landscapes with an update on the status of P. alticola. IMA Fungus, 6(2), 319–335. https://doi.org/10.5598/imafungus.2015.06.02.04
Swofford, D. L. (2002). Paup. Phylogenetic analysis using parsimony (and other methods) version 4. Sinauer associates: Sunderland, Massachusetts. https://paup.phylosolutions.com/
Thornhill, A. H., Crisp, M. D., Külheim, C., Lam, K. E., Nelson, L. A., Yeates, D. K., & Miller, J. T. (2019). A dated molecular perspective of eucalypt taxonomy, evolution and diversification. Australian Systematic Botany. https://doi.org/10.1071/SB18015
Tippett, J., Hill, T., & Shearer, B. (1985). Resistance of Eucalyptus spp. to invasion by Phytophthora cinnmomi. Australian Journal of Botany, 33(2), 409–418 0067–1924/85/04040.
Umami, M., Parker, L. M., & Arndt, S. K. (2021). The impacts of drought stress and Phytophthora cinnamomi infection on short-term water relations in two year-old Eucalyptus obliqua. Forests, 12, 1–14. https://doi.org/10.3390/f12020109
Valente, C., Gonçalves, C., Vasques, J., Manta, A. C., Bragança, H., & Branco, M. (2021). Pragas e Doenças Associadas aos Eucaliptos. In M. Pestana (Ed.), As plantações de eucalipto e os recursos naturais em Portugal (1st ed., pp. 159–175). INIAV, I.P.
Werres, S., Hahn, R., & Themann, K. (1997). Application of different techniques to detect Phytophthora spp. in roots of commercially produced Chamaecyparis lawsoniana. Journal of Plant Diseases and Protection, 105(5), 474–482.
Werres, S., Marwitz, R., Man, W. A., Veld, I. N. T., Cock, A. W. A. M. D. E., Peter, J. M., et al. (2001). Phytophthora ramorum sp . nov ., a new pathogen on Rhododendron and Viburnum. Mycological Research, 105(10), 1155–1165.
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols (pp. 315–322). Academic Press. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wingfield, M. J., & Knox-Davies, P. S. (1980). Observations on diseases in pine and Eucalyptus plantations in South Africa. Phytophylactica, 12, 57–63.
Wingfield, M. J., Slippers, B., Hurley, B. P., Coutinho, T. A., Wingfield, B. D., & Roux, J. (2008). Eucalypt pests and diseases: growing threats to plantation productivity. Southern Forests: a Journal of Forest Science, 70(2), 139–144. https://doi.org/10.2989/SOUTH.FOR.2008.70.2.9.537
Acknowledgements
This work was partly supported by a collaborative protocol, “Diseases in Eucalyptus, survey and strategies to control new diseases,” established between INIAV - Instituto Nacional de Investigação Agrária e Veterinária I. P., RAIZ - Instituto de Investigação da Floresta e Papel and Altri Florestal. The authors would like to acknowledge Catarina Gonçalves (From RAIZ Institute) for managing the shipment of samples and Joana Henriques, Ana Paula Maduro, Isabel Lourenço, Francisco Martins and Adérito Matos (INIAV) for technical assistance. Helena Bragança acknowledges the support from UIDB/04551/2020 and UIDP/04551/2020 Centre grants to (GREEN-IT) and Alan JL Phillips acknowledges the support from UIDB/04046/2020 and UIDP/04046/2020 Centre grants from FCT, Portugal (to BioISI).
Funding
This work was funded by a collaborative protocol, “Estudo das Doenças do eucalipto – prospecção e controlo” established between INIAV, RAIZ and Altri Florestal S. A.
Author information
Authors and Affiliations
Contributions
E.D., H.B., and H. M. designed the experiments; C. V. and A. R. performed the survey and collect the samples; E.D. and H. M. performed the experiments and data analysis; E.D. wrote the first draft of the manuscript; HB and A.J.L.P. supervised the study. All authors have read, edited, and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Diogo, E., Machado, H., Reis, A. et al. Phytophthora alticola and Phytophthora cinnamomi on Eucalyptus globulus in Portugal. Eur J Plant Pathol 165, 255–269 (2023). https://doi.org/10.1007/s10658-022-02604-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-022-02604-9