The emerging pathogen of chestnut Gnomoniopsis castaneae: the challenge posed by a versatile fungus
- 163 Downloads
Abstract
Gnomoniopsis castaneae is an emerging fungal pathogen currently scored as the major nut rot agent on chestnut, although it is also associated with cankers on both chestnut and hazelnut, as well as with necrosis on chestnut galls and leaves. Described for the first time in 2012, G. castaneae has been reported in several countries across Europe, Asia and Australasia, often in relation to severe outbreaks. The goal of this review is to provide a comprehensive summary of the state of the art about G. castaneae, highlighting the main results achieved by the research and stressing the most relevant knowledge gaps that still need to be filled. This overview includes topics encompassing the taxonomy of the fungal pathogen, its host range and geographic distribution, the symptomatology and the diagnostic methods available for its detection, its impact, biology, ecology and epidemiology. The main interactions between G. castaneae and other organisms are also discussed, as well as the possible control strategies. In these past few years, relevant progresses in the knowledge of G. castaneae have been achieved, yet the complexity of the challenges that this pathogen poses to chestnut growers and to the scientific community advocates for further advances.
Keywords
Canker Castanea spp. Dryocosmus kuriphilus Gnomoniopsis smithogilvyi Nut rot ReviewNotes
Acknowledgements
This work was carried out within the activities of the Eurochestnut - Fungi Thematic Group. The Authors wish to thank Thomas Sieber of ETH Zürich (Switzerland), Anne Chandelier of the Walloon Agricultural Research Centre (Belgium), Patricia van Rijswick of the National Plant Protection Organization (the Netherlands) for proving personal communications and comments useful to this review. The Authors wish to thank the anonymous Reviewers for their useful comments and suggestions which contributed to improve the manuscript.
Funding
The work was co-funded by the F.E.A.S.R. 2014/2020, Project #castagnopiemonte, and by Regione Piemonte through the activity of the Chestnut Growing Centre.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
Informed consent was not applicable to this article since no information regarding individual participants was included in the study.
References
- Addario, E., & Turchetti, T. (2011). Parasitic fungi on Dryocosmus kuriphilus in Castanea sativa necrotic galls. Bulletin of Insectology, 64(2), 269–273.Google Scholar
- Blaiotta, G., Di Capua, M., Romano, A., Coppola, R., & Aponte, M. (2014). Optimization of water curing for the preservation of chestnuts (Castanea sativa Mill.) and evaluation of microbial dynamics during process. Food Microbiology, 42, 47–55.Google Scholar
- Bounous, G., & Torello Marinoni, D. (2005). Chestnut: botany, horticulture, and utilization. Horticultural Reviews, 31, 291–347.Google Scholar
- Brussino, G., Bosio, G., Baudino, M., Giordano, R., Ramello, F., & Melika, G. (2002). Pericoloso insetto esotico per il castagno europeo. L’Informatore Agrario, 37, 59–61.Google Scholar
- Chandelier, A., Massot, M., Fabreguettes, O., Gischer, F., Teng, F., & Robin, C. (2018). Early detection of Cryphonectria parasitica by real-time PCR. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-018-1538-0.
- Conedera, M., Manetti, M. C., Giudici, F., & Amorini, E. (2004). Distribution and economic potential of the sweet chestnut (Castanea sativa Mill.) in Europe. Ecologia Mediterranea, 30(2), 179–193.Google Scholar
- Csóka, G., Stone, G. N., & Melika, G. (2017). Non-native gall-inducing insects on forest trees: a global review. Biological Invasions, 19(11), 3161–3181.Google Scholar
- Dar, M. A., & Rai, M. (2015). Gnomoniopsis smithogilvyi, a canker causing pathogen on Castanea sativa: first report. Mycosphere, 6(3), 327–336.Google Scholar
- Dennert, F., Broggini, G., Gessler, C., & Storari, M. (2015). Gnomoniopsis castanea is the main chestnut nut rot agent in Switzerland. Phytopathologia Mediterrranea, 54(2), 199–211.Google Scholar
- Donis-González, I. R., Guyer, D. E., & Fulbright, D. W. (2016). Quantification and identification of microorganisms found on shell and kernel of fresh edible chestnuts in Michigan. Journal of the Science of Food and Agriculture, 96(13), 4514–4522.Google Scholar
- EPPO - European and Mediterranean Plant Protection Organization (2017). EPPO reporting service no. 02–2017 Num. article: 2017/047. http://archives.eppo.int/EPPOReporting/2017/Rse-1702.pdf Accessed 13 May 2018.
- Fernandez-Conradi, P. (2017). Diversité des arbres et résistance des forêts aux invasions biologiques: application au châtaignier et son complexe de bioagresseurs exotiques, chancre (Cryphonectria parasitica) et cynips (Dryocosmus kuriphilus). Interactions entre organismes. Université de Bordeaux.Google Scholar
- Fernandez-Conradi, P., Borowiec, N., Capdevielle, X., Castagneyrol, B., Maltoni, A., Robin, et al. (2017). Plant neighbour identity and invasive pathogen infection affect associational resistance to an invasive gall wasp. Biological Invasions, 20, 1459–1473. https://doi.org/10.1007/s10530-017-1637-4.Google Scholar
- Gaffuri, F., Longa, C. M. O., Turchetti, T., Danti, R., & Maresi, G. (2017). ‘Pink rot’: infection of Castanea sativa fruits by Colletotrichum acutatum. Forest Pathology, 47(2), e12307.Google Scholar
- Garbelotto, M., Schmidt, D., Swain, S., Hayden, K., & Lione, G. (2017). The ecology of infection between a transmissive and a dead-end host provides clues for the treatment of a plant disease. Ecosphere, 8(5), e01815.Google Scholar
- Gentile, S., Valentino, D., Visentin, I., & Tamietti, G. (2009). Discula pascoe infections of sweet chestnut fruits in North-West Italy. Australian Nutgrower, 23, 23–25.Google Scholar
- Gold, M. A., Cernusca, M. M., & Godsey, L. D. (2006). Competitive market analysis: chestnut producers. HortTechnology, 16(2), 360–369.Google Scholar
- Hrubik, P., & Juhasova, G. (1970). Pests and diseases of sweet chestnut fruits and their control. Lesnicky Casopis, 16(2), 127–141.Google Scholar
- Ibrahim, M., Sieber, T. N., & Schlegel, M. (2017). Communities of fungal endophytes in leaves of Fraxinus ornus are highly diverse. Fungal Ecology, 29, 10–19.Google Scholar
- Lewis, A., Gorton, C., Rees, H., Webber, J., & Pérez-Sierra, A. (2017). First report of Gnomoniopsis smithogilvyi causing lesions and cankers of sweet chestnut in the United Kingdom. New Disease Reports, 35, 20.Google Scholar
- Linaldeddu, B. T., Deidda, A., Scanu, B., Franceschini, A., Alves, A., Abdollahzadeh, J., & Phillips, A. J. L. (2016). Phylogeny, morphology and pathogenicity of Botryosphaeriaceae, Diatrypaceae and Gnomoniaceae associated with branch diseases of hazelnut in Sardinia (Italy). European Journal of Plant Pathology, 146(2), 259–279.Google Scholar
- Lione, G. (2016). Ecology and epidemiology of the emerging plant pathogen Gnomoniopsis castaneae. Journal of Plant Pathology, 98(4sup), 5.Google Scholar
- Lione, G., & Gonthier, P. (2016). A permutation-randomization approach to test the spatial distribution of plant diseases. Phytopathology, 106(1), 19–28.Google Scholar
- Lione, G., Giordano, L., Sillo, F., & Gonthier, P. (2015). Testing and modelling the effects of climate on the incidence of the emergent nut rot agent of chestnut Gnomoniopsis castanea. Plant Pathology, 64(4), 852–863.Google Scholar
- Lione, G., Giordano, L., Ferracini, C., Alma, A., & Gonthier, P. (2016). Testing ecological interactions between Gnomoniopsis castaneae and Dryocosmus kuriphilus. Acta Oecologica, 77, 10–17.Google Scholar
- Magro, P., Speranza, S., Stacchiotti, M., Martignoni, D., & Paparatti, B. (2010). Gnomoniopsis associated with necrosis of leaves and chestnut galls induced by Dryocosmus kuriphilus. Plant Pathology, 59(6), 1171.Google Scholar
- Maresi, G., Longa, O., & Turchetti, T. (2013). Brown rot on nuts of Castanea sativa Mill: an emerging disease and its causal agent. iForest, 6(5), 294–301.Google Scholar
- McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40(1), 349–379.Google Scholar
- Mellano, M. G., Beccaro, G. L., Donno, D., Torello-Marinoni, D., Boccacci, P., Canterino, S., et al. (2012). Castanea spp. biodiversity conservation: collection and characterization of the genetic diversity of an endangered species. Genetic Resources and Crop Evolution, 59(8), 1727–1741.Google Scholar
- Meyer, J. B., Gallien, L., & Prospero, S. (2015). Interaction between two invasive organisms on the European chestnut: does the chestnut blight fungus benefit from the presence of the gall wasp? FEMS Microbiology Ecology, 91(11), fiv122.Google Scholar
- Meyer, J. B., Trapiello, E., Senn-Irlet, B., Sieber, T. N., Cornejo, C., Aghayeva, D., González, A. J., & Prospero, S. (2017). Phylogenetic and phenotypic characterisation of Sirococcus castaneae comb. nov. (synonym Diplodina castaneae), a fungal endophyte of European chestnut. Fungal Biology, 121(8), 625–637.Google Scholar
- Migliorini, M., Funghini, L., Marinelli, C., Turchetti, T., Canuti, S., & Zanoni, B. (2010). Study of water curing for the preservation of marrons (Castanea sativa Mill., Marrone fiorentino cv). Postharvest Biology and Technology, 56(1), 95–100.Google Scholar
- Notomi, T., Okayama, H., Masubuchi, H., Yonekawa, T., Watanabe, K., Amino, N., et al. (2000). Loop-mediated isothermal amplification of DNA. Nucleic Acids Research, 28(12), e63.Google Scholar
- Overy, D. P., Seifert, K. A., Savard, M. E., & Frisvad, J. C. (2003). Spoilage fungi and their mycotoxins in commercially marketed chestnuts. International Journal of Food Microbiology, 88(1), 69–77.Google Scholar
- Panagou, E. Z., Vekiari, S. A., Sourris, P., & Mallidis, C. (2005). Efficacy of hot water, hypochlorite, organic acids and natamycin in the control of post-harvest fungal infection of chestnuts. The Journal of Horticultural Science and Biotechnology, 80(1), 61–64.Google Scholar
- Pasche, S., Calmin, G., Auderset, G., Crovadore, J., Pelleteret, P., Mauch-Mani, B., Barja, F., Paul, B., Jermini, M., & Lefort, F. (2016a). Gnomoniopsis smithogilvyi causes chestnut canker symptoms in Castanea sativa shoots in Switzerland. Fungal Genetics and Biology, 87, 9–21.Google Scholar
- Pasche, S., Crovadore, J., Pelleteret, P., Jermini, M., Mauch-Mani, B., Oszako, T., & Lefort, F. (2016b). Biological control of the latent pathogen Gnomoniopsis smithogylvyi in European chestnut grafting scions using Bacillus amyloliquefaciens and Trichoderma atroviride. Dendrobiology, 75, 113–122.Google Scholar
- Prencipe, S., Siciliano, I., Contessa, C., Botta, R., Garibaldi, A., Gullino, M. L., & Spadaro, D. (2018). Characterization of Aspergillus section Flavi isolated from fresh chestnuts and along the chestnut flour process. Food Microbiology, 69, 159–169.Google Scholar
- Quacchia, A., Moriya, S., Bosio, G., Scapin, I., & Alma, A. (2008). Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. BioControl, 53(6), 829–839.Google Scholar
- Rigling, D., & Prospero, S. (2018). Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Molecular Plant Pathology, 19(1), 7–20.Google Scholar
- Rodrigues, P., Venâncio, A., & Lima, N. (2012). Mycobiota and mycotoxins of almonds and chestnuts with special reference to aflatoxins. Food Research International, 48(1), 76–90.Google Scholar
- Ruocco, M., Lanzuise, S., Lombardi, N., Varlese, R., Aliberti, A., Carpenito, et al. (2016). New tools to improve the shelf life of chestnut fruit during storage. Acta Horticulturae, 1144, 309–316.Google Scholar
- Russell, E. W. (1987). Pre-blight distribution of Castanea dentata (Marsh.) Borkh. Bulletin of the Torrey Botanical Club, 114(2), 183–190.Google Scholar
- Sartor, C., Dini, F., Torello-Marinoni, D., Mellano, M. G., Beccaro, G. L., Alma, A., et al. (2015). Impact of the Asian wasp Dryocosmus kuriphilus (Yasumatsu) on cultivated chestnut: yield loss and cultivar susceptibility. Scientia Horticulturae, 197, 454–460.Google Scholar
- Seddaiu, S., Cerboneschi, A., Sechi, C., & Mello, A. (2017). Gnomoniopsis castaneae associated with Dryocosmus kuriphilus galls in chestnut stands in Sardinia (Italy). iForest, 10(2), 440–445.Google Scholar
- Senanayake, I. C., Crous, P. W., Groenewald, J. Z., Maharachchikumbura, S. S., Jeewon, R., Phillips, A. J., et al. (2017). Families of Diaporthales based on morphological and phylogenetic evidence. Studies in Mycology, 86, 217–296.Google Scholar
- Shuttleworth, L. A., & Guest, D. I. (2017). The infection process of chestnut rot, an important disease caused by Gnomoniopsis smithogilvyi (Gnomoniaceae, Diaporthales) in Oceania and Europe. Australasian Plant Pathology, 46(5), 397–405.Google Scholar
- Shuttleworth, L. A., Guest, D. I., & Liew, E. C. Y. (2012). Fungal planet description sheet 108: Gnomoniopsis smithogilvyi L.A. Shuttleworth, E.C.Y. Liew & D.I. Guest, sp. nov. Persoonia, 28, 142–143.Google Scholar
- Shuttleworth, L. A., Liew, E. C. Y., & Guest, D. I. (2013). Survey of the incidence of chestnut rot in South-Eastern Australia. Australasian Plant Pathology, 42(1), 63–72.Google Scholar
- Shuttleworth, L. A., Walker, D. M., & Guest, D. I. (2015). The chestnut pathogen Gnomoniopsis smithogilvyi (Gnomoniaceae, Diaporthales) and its synonyms. Mycotaxon, 130(4), 929–940.Google Scholar
- Sieber, T. N., Jermini, M., & Conedera, M. (2007). Effects of the harvest method on the infestation of chestnuts (Castanea sativa) by insects and moulds. Journal of Phytopathology, 155(7–8), 497–504.Google Scholar
- Sillo, F., Zampieri, E., Giordano, L., Lione, G., Colpaert, J. V., Balestrini, R., & Gonthier, P. (2015). Identification of genes differentially expressed during the interaction between the plant symbiont Suillus luteus and two plant pathogenic allopatric Heterobasidion species. Mycological Progress, 14(11), 106.Google Scholar
- Sillo, F., Giordano, L., Zampieri, E., Lione, G., De Cesare, S., & Gonthier, P. (2017). HRM analysis provides insights on the reproduction mode and the population structure of Gnomoniopsis castaneae in Europe. Plant Pathology, 66(2), 293–303.Google Scholar
- Sillo, F., Giordano, L., & Gonthier, P. (2018). Fast and specific detection of the invasive forest pathogen Heterobasidion irregulare through a loop-mediated isothermal AMPlification (LAMP) assay. Forest Pathology, 48(2), e12396.Google Scholar
- Smith, H. C., & Agri, M. (2008). The life cycle, pathology and taxonomy of two different nut rot fungi in chestnut. Australian Nutgrower, 22, 11–15.Google Scholar
- Smith, H. C., & Ogilvy, D. (2008). Nut rot in chestnuts. The Australian Nutgrower, 2, 10–15.Google Scholar
- Tamietti, G. (2016). On the fungal species Gnomoniopsis castaneae (“castanea”) and its synonym G. smithogilvyi. Journal of Plant Pathology, 98(2), 189–190.Google Scholar
- Tomlinson, J. A., Dickinson, M. J., & Boonham, N. (2010). Rapid detection of Phytophthora ramorum and P. kernoviae by two-minute DNA extraction followed by isothermal amplification and amplicon detection by generic lateral flow device. Phytopathology, 100(2), 143–149.Google Scholar
- Trapiello, E., Feito, I., & González, A. J. (2017). First report of Gnomoniopsis castaneae causing canker on hybrid plants of Castanea sativa x C. crenata in Spain. Plant Disease. https://doi.org/10.1094/PDIS-12-17-1874-PDN.
- Vannini, A., Vettraino, A., Martignoni, D., Morales-Rodriguez, C., Contarini, M., Caccia, R., Paparatti, B., & Speranza, S. (2017). Does Gnomoniopsis castanea contribute to the natural biological control of chestnut gall wasp? Fungal Biology, 121(1), 44–52.Google Scholar
- Vannini, A., Morales-Rodriguez, C., Aleandri, M., Bruni, N., Dalla Valle, M., Mazzetto, T., et al. (2018). Emerging new crown symptoms on Castanea sativa (Mill.): attempting to model interactions among pests and fungal pathogens. Fungal Biology. https://doi.org/10.1016/j.funbio.2018.05.006.
- Vettraino, A. M., Morel, O., Perlerou, C., Robin, C., Diamandis, S., & Vannini, A. (2005a). Occurrence and distribution of Phytophthora species in European chestnut stands, and their association with Ink Disease and crown decline. European Journal of Plant Pathology, 111(2), 169–180.Google Scholar
- Vettraino, A. M., Paolacci, A., & Vannini, A. (2005b). Endophytism of Sclerotinia pseudotuberosa: PCR assay for specific detection in chestnut tissues. Mycological Research, 109(1), 96–102.Google Scholar
- Vinale, F., Ruocco, M., Manganiello, G., Guerrieri, E., Bernardo, U., Mazzei, P., Piccolo, A., Sannino, F., Caira, S., Woo, S. L., & Lorito, M. (2014). Metabolites produced by Gnomoniopsis castanea associated with necrosis of chestnut galls. Chemical and Biological Technologies in Agriculture, 1(1), 8.Google Scholar
- Visentin, I., Gentile, S., Valentino, D., Gonthier, P., Tamietti, G., & Cardinale, F. (2012). Gnomoniopsis castanea sp. nov (Gnomoniaceae, Diaporthales) as the causal agent of nut rot in sweet chestnut. Journal of Plant Pathology, 94(2), 411–419.Google Scholar
- Washington, W. S., Allen, A. D., & Dooley, L. B. (1997). Preliminary studies on Phomopsis castanea and other organisms associated with healthy and rotted chestnut fruit in storage. Australasian Plant Pathology, 26(1), 37–43.Google Scholar
- Zampieri, E., Giordano, L., Lione, G., Vizzini, A., Sillo, F., Balestrini, R., & Gonthier, P. (2017). A nonnative and a native fungal plant pathogen similarly stimulate ectomycorrhizal development but are perceived differently by a fungal symbiont. New Phytologist, 213(4), 1836–1849.Google Scholar