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Can the Seed Trade Provide a Potential Pathway for the Global Distribution of Foliar Pathogens? An Investigation into the Use of Heat Treatments to Reduce Risk of Dothistroma septosporum Transmission via Seed Stock

. 2023 Dec 13 ; 9 (12) : . [epub] 20231213

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article

The international plant trade results in the accidental movement of invasive pests and pathogens, and has contributed significantly to recent range expansion of pathogens including Dothistroma septosporum. Seeds are usually thought to present a lower biosecurity risk than plants, but the importation of Pinus contorta seeds from North America to Britain in the mid-1900s, and similarities between British and Canadian D. septosporum populations suggests seeds could be a pathway. Dothistroma septosporum has not been isolated from seeds, but inadequately cleaned seed material could contain infected needle fragments. This case study investigated whether cone kilning, and wet and dry heat treatments could reduce D. septosporum transmission without damaging seed viability. Pinus needles infected with D. septosporum were incubated alongside cones undergoing three commercial seed extraction processes. Additional needles were exposed to temperatures ranging from 10 to 67 °C dry heat for up to 48 h, or incubated in water heated to between 20 and 60 °C for up to one hour. Pinus sylvestris seeds were exposed to 60 and 65 dry heat °C for 48 h, and further seed samples incubated in water heated to between 20 and 60 °C for up to one hour. Dothistroma septosporum survived the three kilning processes and while seeds were not damaged by dry heat exceeding 63.5 °C, at this temperature no D. septosporum survived. Wet heat treatments resulted in less than 10% pathogen survival following incubation at 40 °C, while at this temperature the seeds suffered no significant impacts, even when submerged for one hour. Thus, commercial seed kilning could allow D. septosporum transmission, but elevated wet and dry heat treatments could be applied to seed stock to minimise pathogen risk without significantly damaging seed viability.

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Brasier C.M. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 2008;57:792–808. doi: 10.1111/j.1365-3059.2008.01886.x. DOI

Pergl J., Pyšek P., Bacher S., Essl F., Genovesi P., Harrower C.A., Hulme P.E., Jeschke J.M., Kenis M., Kühn I., et al. Troubling travellers: Are ecologically harmful alien species associated with particular introduction pathways? NeoBiota. 2017;32:1–20. doi: 10.3897/neobiota.32.10199. DOI

Santini A., Ghelardini L., De Pace C., Desprez-Loustau M.L., Capretti P., Chandelier A., Cech T., Chira D., Diamandis S., Gaitniekis T., et al. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol. 2013;197:238–250. doi: 10.1111/j.1469-8137.2012.04364.x. PubMed DOI

Shirley S.M., Kark S. Amassing efforts against alien invasive species in Europe. PLoS Biol. 2006;4:e279. doi: 10.1371/journal.pbio.0040279. PubMed DOI PMC

Wingfield M.J., Brockerhoff E.G., Wingfield B.D., Slippers B. Planted forest health: The need for a global strategy. Science. 2015;349:832–836. doi: 10.1126/science.aac6674. PubMed DOI

European Union . Council Directive 2000/29/EC of 8 May 2000 on Protective Measures against the Introduction into the Community of Organisms Harmful to Plants or Plant Products and against Their Spread within the Community. European Union; Brussels, Belgium: 2000.

Hulme P.E. Unwelcome exchange: International trade as a direct and indirect driver of biological invasions worldwide. One Earth. 2021;4:666–679. doi: 10.1016/j.oneear.2021.04.015. DOI

Klapwijk M.J., Hopkins A.J., Eriksson L., Pettersson M., Schroeder M., Lindelöw Å., Rönnberg J., Keskitalo E.C.H., Kenis M. Reducing the risk of invasive forest pests and pathogens: Combining legislation, targeted management and public awareness. Ambio. 2016;45:223–234. doi: 10.1007/s13280-015-0748-3. PubMed DOI PMC

Roques A., Rabitsch W., Rasplus J.Y., Lopez-Vaamonde C., Nentwig W., Kenis M. Alien terrestrial invertebrates of Europe. In: Hulme P.E., Nentwig W., Pysek P., Vila M., editors. Handbook of Alien Species in Europe. Springer; Dordrecht, The Netherlands: 2009. pp. 63–79.

Desprez-Loustau M.L. Alien fungi of Europe. In: Hulme P.E., Nentwig W., Pysek P., Vila M., editors. Handbook of Alien Species of Europe. Springer; Dordrecht, The Netherlands: 2009. pp. 15–28.

Liebhold A.M., Brockerhoff E.G., Garrett L.J., Parke J.L., Britton K.O. Live plant imports: The major pathway for forest insect and pathogen invasions of the US. Front. Ecol. Environ. 2012;10:135–143. doi: 10.1890/110198. DOI

Roques A. Alien forest insects in a warmer world and a globalised economy: Impacts of changes in trade, tourism and climate on forest biosecurity. N. Z. J. For. Sci. 2010;40:77–94.

Evira-Recuenco M., Iturritxa E., Raposo R. Impact of Seed Transmission on the Infection and Development of Pitch Canker Disease in Pinus radiata. Forests. 2015;6:3353–3368. doi: 10.3390/f6093353. DOI

Mittal R.K., Anderson R.L., Mathur S.B. Microorganisms Associated with Tree Seeds: World Checklist 1990. Forestry Canada, Petawawa National Forestry Institute; Chalk River, ON, Canada: 1990. 57p Information Report PI-X-96.

Cleary M., Oskay F., Doğmuş H.T., Lehtijärvi A., Woodward S., Vettraino A.M. Cryptic risks to forest biosecurity associated with the global movement of commercial seed. Forests. 2019;10:459. doi: 10.3390/f10050459. DOI

Franić I., Prospero S., Hartmann M., Allan E., Auger-Rozenberg M.A., Grünwald N.J., Kenis M., Roques A., Schneider S., Sniezko R., et al. Are traded forest tree seeds a potential source of nonnative pests? Ecol. Appl. 2019;29:e01971. doi: 10.1002/eap.1971. PubMed DOI

James R.L. Effects of Water Rinse Treatments on Occurrence of Fungi on Spruce Seed from the Towner Nursery, North Dakota. United States Department of Agriculture Forest Service Northern Region; Missoula, MT, USA: 1987. 4p

Willis R., Littke A., Browning J.E. Assaying for seed-borne fungi of Douglas-fir and true fir species; Proceedings of the IUFRO Working Party S2.07-09 (Diseases and Insects in Forest Nurseries); Victoria, BC, Canada. 22–30 August 1990; pp. 251–258.

Wingfield M.J., Slippers B., Roux J., Wingfield B.D. Worldwide movement of exotic forest fungi, especially in the tropics and the southern hemisphere: This article examines the impact of fungal pathogens introduced in plantation forestry. Bioscience. 2001;51:134–140. doi: 10.1641/0006-3568(2001)051[0134:WMOEFF]2.0.CO;2. DOI

Forestry Commission . Forestry Commission; Edinburgh, UK: 2018. Guidance for Seed Testing at Forestry Commission Approved Forest Tree Seed Testing Facilities.55p. Internal Document. Unpublished Work.

Drenkhan R., Tomešova-Haataja V., Fraser S., Bradshaw R.E., Vahalik P., Mullett M.S., Martin-Garcia J., Bulman L.S., Wingfield M.J., Kirisits T., et al. Global geographic distribution and host range of Dothistroma species: A comprehensive review. For. Pathol. 2016;46:408–442. doi: 10.1111/efp.12290. DOI

Mullett M.S., Tubby K.V., Webber J.F., Brown A.V. A reconsideration of natural dispersal of the pine pathogen Dothistroma septosporum. Plant Pathol. 2016;65:1462–1472. doi: 10.1111/ppa.12522. DOI

Tomšovský M., Tomešová V., Palovčíková D., Kostovčík M., Rohrer M., Hanáček P., Jankovský L. The gene flow and mode of reproduction of Dothistroma septosporum in the Czech Republic. Plant Pathol. 2013;62:59–68. doi: 10.1111/j.1365-3059.2012.02625.x. DOI

Jankovský L., Bednářová M., Palovčíková D. Dothistroma needle blight Mycosphaerella pini E. Rostrup, a new quarantine pathogen of pines in the CR. J. For. Sci. 2014;50:319–326. doi: 10.17221/4629-JFS. DOI

Barnes I., Wingfield M.J., Carbone I., Kirisits T., Wingfield B.D. Population structure and diversity of an invasive pine needle pathogen reflects anthropogenic activity. Ecol. Evol. 2014;4:3642–3661. doi: 10.1002/ece3.1200. PubMed DOI PMC

EFSA Panel on Plant Health (PLH) European Food Safety Authority Scientific opinion on the risk to plant health posed by Dothistroma septosporum (Dorog.) M. Morelet (Mycosphaerella pini E. Rostrup, syn. Scirrhia pini) and Dothistroma pini Hulbary to the EU territory with the identification and evaluation of risk reduction options. EFSA Panel on Plant Health (PLH), Parma, Italy. EFSA J. 2013;11:3026.

Mullett M.S., Brown A.V., Fraser S., Baden R., Tubby K.V. Insights into the pathways of spread and potential origins of Dothistroma septosporum in Britain. Fungal Ecol. 2017;26:85–98. doi: 10.1016/j.funeco.2017.01.002. DOI

Lines R. Experiments on Lodgepole Pine Seed Origins in Britain. Forestry Commission; Edinburgh, Scotland: 1996. 148p Technical Paper 10.

Forest Research . Forest Research, Alice Holt Lodge; Surrey, UK: Archived Seed Testing Certificates 1930s to Current Day. Unpublished Data 1930–2023.

Mullett M., Peace A., Brown A. Persistence of Dothistroma septosporum on abscised pine needles and its implications for disease management. Plant Dis. 2016;100:1271–1277. doi: 10.1094/PDIS-11-15-1306-RE. PubMed DOI

Ivory M.H. Spore germination and growth in culture of Dothistroma pini var. Keniensis. Trans. Br. Mycol. Soc. 1967;50:563–572. doi: 10.1016/S0007-1536(67)80088-3. DOI

Escamilla D., Rosso M.L., Zhang B. Identification of fungi associated with soybeans and effective seed disinfection treatments. Food Sci. Nutr. 2019;7:3194–3205. doi: 10.1002/fsn3.1166. PubMed DOI PMC

Jaquette C.B., Beuchat L.R., Mahon B.E. Efficacy of chlorine and heat treatment in killing Salmonella stanley inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl. Environ. Microbiol. 1996;62:2212–2215. doi: 10.1128/aem.62.7.2212-2215.1996. PubMed DOI PMC

Mancini V., Romanazzi G. Seed treatments to control seedborne fungal pathogens of vegetable crops. Pest Manag. Sci. 2014;70:860–868. doi: 10.1002/ps.3693. PubMed DOI

Mangwende E., Chirwa P.W., Aveling T.A.S. Evaluation of seed treatments against Colletotrichum kahawae subsp. cigarro on Eucalyptus spp. Crop Prot. 2020;132:105113. doi: 10.1016/j.cropro.2020.105113. DOI

Campbell A. Conventional Spices Treated with Hazardous Chemicals, Natural Health. Volume 365. CDC, Centers for Disease Control and Prevention; Atlanta, GA, USA: 2015. [(accessed on 10 March 2019)]. Available online: https://www.naturalhealth365.com/spices-irradiation-ethylene-oxide-1585.html.

Rane B., Bridges D.F., Wu V.C. Gaseous antimicrobial treatments to control foodborne pathogens on almond kernels and whole black peppercorns. Food Microbiol. 2020;92:103576. doi: 10.1016/j.fm.2020.103576. PubMed DOI

Baker K.F. Thermotherapy of planting material. Phytopathology. 1962;52:1244–1255.

Baker K.F. Seed pathology—Concepts and methods of control. J. Seed Technol. 1979;4:57–67.

Cram M.M., Fraedrich S.W. Seed diseases and seedborne pathogens of North America. Tree Plant. Notes. 2009;53:35–44.

Dumroese R.K., James R.L., Wenny D.L., Gilligan C.J. Douglas fir seed treatments: Effect on seed germination and seed—Borne organisms; Proceedings of the Combined Meeting of the Western Forest Nursery Associations; Vernon, BC, Canada. 8–11 August 1988; pp. 155–160.

Agustí-Brisach C., Pérez-Sierra A., Armengol J., García-Jimenez J., Berbegal M. Efficacy of hot water treatment to reduce the incidence of Fusarium circinatum on Pinus radiata seeds. Forestry. 2012;85:629–635. doi: 10.1093/forestry/cps074. DOI

Berbegal M., Landeras E., Sánchez D., Abad-Campos P., Pérez-Sierra A., Armengol J. Evaluation of Pinus radiata seed treatments to control Fusarium circinatum: Effects on seed emergence and disease incidence. For. Pathol. 2015;45:525–533. doi: 10.1111/efp.12204. DOI

Clear R.M., Patrick S.K., Wallis R., Turkington T.K. Effect of dry heat treatment on seed-borne Fusarium graminearum and other cereal pathogens. Can. J. Plant Pathol. 2002;24:489–498. doi: 10.1080/07060660209507038. DOI

Gilbert J., Woods S.M., Turkington T.K., Tekauz A. Effect of heat treatment to control Fusarium graminearum in wheat seed. Can. J. Plant Pathol. 2005;27:448–452. doi: 10.1080/07060660509507244. DOI

Koch E., Schmitt A., Stephan D., Kromphardt C., Jahn M., Krauthausen H.J., Forsberg G., Werner S., Amein T., Wright S.A., et al. Evaluation of non-chemical seed treatment methods for the control of Alternaria dauci and A. radicina on carrot seeds. Eur. J. Plant Pathol. 2010;127:99–112. doi: 10.1007/s10658-009-9575-3. DOI

Bari M.L., Inatsu Y., Isobe S., Kawamoto S. Hot water treatments to inactivate Escherichia coli O157: H7 and Salmonella in mung bean seeds. J. Food Prot. 2008;71:830–834. doi: 10.4315/0362-028X-71.4.830. PubMed DOI

Crosse J.E. Bacterial canker of stone-fruits. IV. Investigation of a method for measuring the inoculum potential of cherry trees. Ann. Appl. Biol. 1959;47:306–317. doi: 10.1111/j.1744-7348.1959.tb02546.x. DOI

Ioos R., Fabre B., Saurat C., Fourrier C., Frey P., Marçais B. Development, comparison, and validation of real-time and conventional PCR tools for the detection of the fungal pathogens causing brown spot and red band needle blights of pine. Phytopathology. 2010;100:105–114. doi: 10.1094/PHYTO-100-1-0105. PubMed DOI

Bradshaw R.E., Ganley R.J., Jones W.T., Dyer P.S. High levels of dothistromin toxin produced by the forest pathogen Dothistroma pini. Mycol. Res. 2000;104:325–332. doi: 10.1017/S0953756299001367. DOI

Gosling P.G. The effect of moist chilling on the subsequent germination of some temperate conifer seeds over a range of temperatures. J. Seed Technol. 1988;12:90–98.

International Seed Testing Association (ISTA) Determination of Moisture Content. International Seed Testing Association; Basserdorf, Switzerland: 2009. International rules for seed testing; pp. 9.1–9.20. Chapter 9.

R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2022. [(accessed on 1 December 2023)]. Available online: https://www.R-project.org/

Hartig F. R Package ‘DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. [(accessed on 1 December 2023)]. Available online: https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html.

Fox J., Weisberg S. An {R} Companion to Applied Regression. 2nd ed. Sage; Thousand Oaks, CA, USA: 2011. [(accessed on 1 December 2023)]. Available online: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.

Archibald S. Ph.D. Thesis. Imperial College London; London, UK: 2009. Red Band Needle Blight of Conifers in Britain.

Kais A.G. Environmental factors affecting brown spot infection on longleaf pine. Phytopathology. 1975;65:1389–1392. doi: 10.1094/Phyto-65-1389. DOI

Gordon A.G. Seed Manual for Forest Trees. Forestry Commission; Edinburgh, UK: 1992. The processing of cones and seeds; pp. 86–97. Bulletin 83.

Bewley J.D., Bradford K.J., Hilhorst H.W.M., Nonogaki H. Seeds: Physiology of Development, Germination and Dormancy. 3rd ed. Springer; New York, NY, USA: 2013. DOI

Walters C., Hill L.M., Wheeler L.J. Dying while dry: Kinetics and mechanisms of deterioration in desiccated organisms. Integr. Comp. Biol. 2005;45:751–758. doi: 10.1093/icb/45.5.751. PubMed DOI

Leinonen I. Dependence of dormancy release on temperature in different origins of Pinus sylvestris and Betula pendula seedlings. Scand. J. For. Res. 1996;11:122–128. doi: 10.1080/02827589609382919. DOI

Barnett J.P. Sterilizing southern pine seeds with peroxide. Tree Plant. Notes. 1976;27:17–19.

McCartan S.A., Forster J., Jinks R.L., Rampart M.P., Cahalan C.M. The effect of temperature during cone and seed development on primary dormancy of Scots pine (Pinus sylvestris L.) seeds. New For. 2022;53:935–946. doi: 10.1007/s11056-021-09884-9. DOI

Enomoto K., Takizawa T., Ishikawa N., Suzuki T. Hot-water treatments for disinfecting alfalfa seeds inoculated with Escherichia coli Atcc 25922. Food Sci. Technol. Res. 2002;8:247–251. doi: 10.3136/fstr.8.247. DOI

Núñez M.R., Calvo L. Effect of high temperatures on seed germination of Pinus sylvestris and Pinus halepensis. For. Ecol. Manag. 2000;131:183–190. doi: 10.1016/S0378-1127(99)00211-X. DOI

Hellum A.K., Pelchat M. Temperature and time affect the release and quality of seed from cones of lodgepole pine from Alberta. Can. J. For. Res. 1979;9:154–159. doi: 10.1139/x79-029. DOI

Bulman L.S., Bradshaw R.E., Fraser S., Martín-García J., Barnes I., Musolin D.L., La Porta N., Woods A.J., Diez J.J., Koltay A., et al. A worldwide perspective on the management and control of Dothistroma needle blight. For. Pathol. 2016;46:472–488. doi: 10.1111/efp.12305. DOI

Tubby K., Adamcikova K., Adamson K., Akiba M., Barnes I., Boroń P., Bragança H., Bulgakov T., Burgdorf N., Capretti P., et al. The increasing threat to European forests from the invasive foliar pine pathogen, Lecanosticta acicola. For. Ecol. Manag. 2023;536:120847. doi: 10.1016/j.foreco.2023.120847. PubMed DOI PMC

Ogris N., Drenkhan R., Vahalík P., Cech T., Mullett M., Tubby K. The potential global distribution of an emerging forest pathogen, Lecanosticta acicola, under a changing climate. Front. For. Glob. Chang. 2023;6:1221339. doi: 10.3389/ffgc.2023.1221339. DOI

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