Articles
Published 2023-01-13
Keywords
- Apiaceae,
- Daucus carota,
- 50°C,
- seed import-export,
- FAO-IPPC emergency action
How to Cite
[1]
L. TIZZANI, A. GENTILI, A. TAGLIENTI, S. BERTIN, and V. ILARDI, “Response of carrot seed germination to heat treatment, the emergency measure to reduce the risk of ‘Candidatus Liberibacter solanacearum’ seed transmission”, Phytopathol. Mediterr., vol. 61, no. 3, pp. 513–522, Jan. 2023.
Funding data
-
Ministero delle Politiche Agricole Alimentari e Forestali
Grant numbers Progetto "Proteggo"
Abstract
In Europe and the Mediterranean region, ‘Candidatus Liberibacter solanacearum’ (Lso) is associated with emerging diseases of Apiaceae crops, mainly carrot. Emergency measures for import of carrot seed were set, requiring seed to be heat-treated at 50°C or tested as Lso-negative by PCR. The germination response to heat treatment was assessed for 24 carrot cultivar and hybrid seed lots. Ten parsley, five fennel, and two celery seed lots were also analysed. Of these 41 seed lots, 21 were Lso-infected. Water heat treatment significantly decreased germinability compared to dry heat treatment, indicating that dry heat treatment is a cheaper and less detrimental procedure. However, the dry heat treatment significantly decreased seed germination compared to untreated controls in four of 24 seed lots of carrot, four of ten parsley seed lots, three of five fennel seed lots, and one of two celery seed lots. For parsley, the heat treatment reduced germinability to a lesser extent in Lso-infected than Lso-free seed lots. These data show that heat treatment can affect the germination of Apiaceae seeds to varying degrees, depending on species or variety, the type of heat treatment, and the sanitary status of the seeds.
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References
Ark P.A. Gardner M.W., 1944. Carrot bacterial blight as it affects the roots. Phytopathology 34: 416-420.
Baker F.S., 1929. Effect of excessively high temperatures on coniferous reproduction. Journal of Forestry 27: 949–975. https://doi.org/10.1093/jof/27.8.949
Bertolini E., Teresani G.R., Loiseau M., Tanaka F.A.O., Barbé S., Martinez C., Gentit P., Lopez M., Cambra, M., 2015. Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology 64: 276-285. https://doi.org/10.1111/ppa.12245
Carosem GmbH, 2022. Commercial production of carrot seed. Available at: https://carosem.eu/seed-production/
Council Directive 2002/55/EC of 13 June 2002 on the marketing of vegetable seed. Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32002L0055&from=EN
European Food Safety Authority (EFSA), Loiseau M., Schrader G., Camilleri M., Diakaki M., Vos S. 2019. Pest survey card on ‘Candidatus Liberibacter solanacearum’. EFSA Supporting Publications 16(6): 1632E. https://doi.org/10.2903/sp.efsa.2019.EN-1632
European Plant Protection Organization (EPPO) PM 7/143 (1) 2020a. ‘Candidatus Liberibacter solanacearum’. EPPO Bulletin 50: 49-68. https://doi.org/10.1111/epp.12611
European Plant Protection Organization (EPPO), 2020b. Available at: https://www.eppo.int/ACTIVITIES/plant_quarantine/A1_list
FAO/IPPC Emergency Action (2016). Proposed revision of List of the plants subject to Specific Phytosanitary Measures to be carried out in Exporting Countries (Annexed Table 2–2 of the Ordinance for Enforcement of the Plant Protection Act). Available at: http://www.maff.go.jp/j/syouan/keneki/kikaku/pdf/04_at2_2_specific_measures.pdf
Fujikawa T., Taguchi M., Kido K., Kusano S., Enya J., … Sato M., 2020a. Evaluation of an RNA-based PCR assay to detect viable ‘Candidatus Liberibacter solanacearum’ (Lso) in Lso-contaminated carrot seeds using different disinfection methods. Journal of Plant Pathology 102: 205–211. doi: https://doi.org/10.1007/s42161-019-00405-4
Fujikawa T., Yamamura K., Osaki K., Onozuka N., Taguchi M., … Sato M., 2020b. Seed transmission of ‘Candidatus Liberibacter solanacearum’ is unlikely in carrot. Journal of General Plant Pathology 86(4): 266-273. https://doi.org/10.1007/s10327-020-00927-1
Godefroid S., Van der Vyver A., Stoffelen P., Vandeborght B., 2017. Effectiveness of dry heat as seed sterilisation technique: Implications for ex situ conservation. Plant Biosystems 151(6): 1054–1061. doi: https://doi.org/10.1080/11263504.2016.1231140
Grondeau C., Ladonne F., Fourmond A., Poutier F., Samson R., 1992. Attempt to eradicate Pseudomonas syringae pv. pisi from pea seeds by heat treatments. Seed Science and Technology 20: 515-525.
Grondeau C., Samson R., Sands D.D.C., 1994. A Review of Thermotherapy to Free Plant Materials from Pathogens, Especially Seeds from Bacteria. Critical Reviews in Plant Sciences 13(1): 57-75. https://doi.org/10.1080/07352689409701908
Haapalainen M., 2014. Biology and epidemics of ‘Candidatus Liberibacter’ species, psyllid‐transmitted plant‐pathogenic bacteria. Annals of applied biology 165(2): 172-198. https://doi.org/10.1111/aab.12149
Haapalainen M., Kivimäki P., Latvala S., Rastas M., Hannukkala A., Jauhiainen L., Lemmetty A., Pirhonen M., Virtanen A., Nissinen A. I., 2017. Frequency and occurrence of the carrot pathogen ‘Candidatus Liberibacter solanacearum’ haplotype C in Finland. Plant Pathology 66: 559–570. https://doi.org/10.1111/ppa.12613
Haapalainen M., Latvala S., Wickström A., Wang J., Pirhonen M., Nissinen A. I., 2020. A novel haplotype of ‘Candidatus Liberibacter solanacearum’ found in Apiaceae and Polygonaceae family plants. European Journal of Plant Pathology 156(2): 413-423. https://doi.org/10.1007/s10658-019-01890-0
International Seed Testing Association. 2020. The germination test. In International rules for seed testing. Chapter 5: 1-57. doi: https://doi.org/10.15258/istarules.2022.05
Ilardi V., Catara V., 2013. ‘Candidatus Liberibacter’ spp. Emerging Threats for Agriculture in the European and Mediterranean Region. Biosafety 2: E135. https://doi.org/10.4172/2167-0331.1000e135
Ilardi V., Di Nicola E., Tavazza, M., 2016. First report of ‘Candidatus Liberibacter solanacearum’ in commercial carrot seeds in Italy. Journal of Plant Pathology 98(2). DOI: http://dx.doi.org/10.4454/JPP.V98I2.040
Ilardi V., Lumia V., Di Nicola E., Tavazza M., 2019. Identification, intra-and inter-laboratory validation of a diagnostic protocol for ‘Candidatus Liberibacter solanacearum’ in carrot seeds. European Journal of Plant Pathology, 153(3): 879-890. https://doi.org/10.1007/s10658-018-01606-w
Karahan, A., Altundag, S., Saracoglu, M., Duman, K., Ozdemir, I.,… Demir Ozden, E., 2022. First report of ‘Candidatus Liberibacter solanacearum’ on carrot and parsley in Turkey. New Disease Reports, 45, e12095. https://doi.org/10.1002/ndr2.12095
Koppenaal, R.S., Colombo, S.J., 1988. Heat tolerance of actively growing, bud-initiated, and dormant black spruce seedlings. Canadian Journal of Forest Research, 18: 1103–1105. https://doi.org/10.1139/x88-169
Kuan T. L., Minsavage G. V., Gabrielson R. L.,1985. Detection of Xanthomonas campestris pv. carotae in carrot seed. Plant Disease 69(9): 758-760. https://doi.org/10.1094/PD-69-758
Li W., Abad J.A., French-Monar R.D., Rascoe J., Wen A., … Levy L., 2009. Multiplex real-time PCR for detection, identification and quantification of ‘Candidatus Liberibacter solanacearum’ in potato plants with zebra chip. Journal of Microbiological Methods 78: 59-65. https://doi.org/10.1016/j.mimet.2009.04.009
Loiseau M., Renaudin I., Cousseau-Suhard P., Poliakoff F., Gentit P., 2017a. Transmission tests of ‘Candidatus Liberibacter solanacearum’ by carrot seeds. Acta Horticolturae 41-46. https://doi.org/10.17660/ActaHortic.2017.1153.7
Loiseau M., Renaudin I., Cousseau-Suhard P., Lucas P.-M., Forveille A., Gentit P., 2017b. Lack of evidence of vertical transmission of ‘Candidatus Liberibacter solanacearum’ by carrot seeds suggests that seed is not a major transmission pathway. Plant Disease 101: 2104–2109. https://doi.org/10.1094/PDIS-04-17-0531-RE
Mawassi M., Dror O., Bar-Joseph M., Piasezky A., Sjolund J.M., … Bahar O., 2018. ‘Candidatus Liberibacter solanacearum’ is Tightly Associated with Carrot Yellows Symptoms in Israel and Transmitted by the Prevalent Psyllid Vector Bactericera trigonica. Phytopathology 108(9): 1056-1066. https://doi.org/10.1094/PHYTO-10-17-0348-R
Merfield C., Hampton J., Hill M., Wratten S., 2005. The effect of seed moisture content and the duration and temperature of hot water treatment on carrot seed viability and the control of Alternaria radicina. Proceedings of the First Scientific Conference of the International Society of Organic Agriculture Research (ISOFAR), Adelaide, Australia.
Monger W.A., Jeffries C.J, 2016. First report of ‘Candidatus Liberibacter solanacearum’ in parsley (Petroselinum crispum) seed. New Disease Reports 34: 31. doi: http://dx.doi.org/10.5197/j.2044-0588.2016.034.031
Monger W.A., Jeffries C.J., 2018. A survey of ‘Candidatus Liberibacter solanacearum’ in historical seed from collections of carrot and related Apiaceae species. European Journal of Plant Pathology 150: 803–815. https://doi.org/10.1007/s10658-017-1322-6
Munyaneza J.E., Crosslin J.M., Upton, J.E., 2007. Association of Bactericera cockerelli (Homoptera: Psyllidae) with zebra chip, a new potato disease in southwestern United States and Mexico. Journal of Economic Entomology 100(3): 656–663. https://doi.org/10.1603/0022-0493(2007)100[656:aobchp]2.0.co;2
Nakamura, H., 1982. Effects of Dry Heat Treatment for Seed Disinfection on Germination in Vegetables. Japan Agricultural Research Quarterly 15(4): 243-247.
Nissinen A.I., Haapalainen M., Ojanen H., Pirhonen M., Jauhiainen, L., 2021. Spreading of Trioza apicalis and development of ‘Candidatus Liberibacter solanacearum’ infection on carrot in the field conditions. Annals of Applied Biology 178(1): 39-50. https://doi.org/10.1111/aab.12644
Oishi M., Hoshino S., Fujiwara Y., Ushiku S., Kobayashi Y., Namba I., 2017. A Comparison of Protocols to Detect Candidatus Liberibacter solanacearum from Carrot Seeds. Research on the Effectiveness of Propidium Monoazide Treatment and Evaluation of Seed Transmission in Carrot. Research bulletin of the plant protection service, 53: 111-117. doi: http://www.maff.go.jp/pps/j/guidance/r_bulletin/pdf/rb053_016.pdf
Que F., Hou X. L., Wang G. L., Xu Z. S., Tan,G. F., Xiong A. S., 2019. Advances in research on the carrot, an important root vegetable in the Apiaceae family. Horticulture Research 6. https://doi.org/10.1038/s41438-019-0150-6
Strandberg J.O., White J.M., 1989. Response of carrot seeds to heat treatments. Journal of the American Society for Horticultural Science 114(5): 766-769. https://doi.org/10.21273/JASHS.114.5.766
Wright, H.A., 1970. A method to determine heat-caused mortality in bunchgrasses. Ecology 51: 582–587. https://doi.org/10.2307/1934038
Zhang X., Wang R., Ning H., Li W., Bai Y., Li, Y., 2020. Evaluation and management of fungal-infected carrot seeds. Scientific Reports 10(1): 1-8. https://doi.org/10.1038/s41598-020-67907-
Baker F.S., 1929. Effect of excessively high temperatures on coniferous reproduction. Journal of Forestry 27: 949–975. https://doi.org/10.1093/jof/27.8.949
Bertolini E., Teresani G.R., Loiseau M., Tanaka F.A.O., Barbé S., Martinez C., Gentit P., Lopez M., Cambra, M., 2015. Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology 64: 276-285. https://doi.org/10.1111/ppa.12245
Carosem GmbH, 2022. Commercial production of carrot seed. Available at: https://carosem.eu/seed-production/
Council Directive 2002/55/EC of 13 June 2002 on the marketing of vegetable seed. Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32002L0055&from=EN
European Food Safety Authority (EFSA), Loiseau M., Schrader G., Camilleri M., Diakaki M., Vos S. 2019. Pest survey card on ‘Candidatus Liberibacter solanacearum’. EFSA Supporting Publications 16(6): 1632E. https://doi.org/10.2903/sp.efsa.2019.EN-1632
European Plant Protection Organization (EPPO) PM 7/143 (1) 2020a. ‘Candidatus Liberibacter solanacearum’. EPPO Bulletin 50: 49-68. https://doi.org/10.1111/epp.12611
European Plant Protection Organization (EPPO), 2020b. Available at: https://www.eppo.int/ACTIVITIES/plant_quarantine/A1_list
FAO/IPPC Emergency Action (2016). Proposed revision of List of the plants subject to Specific Phytosanitary Measures to be carried out in Exporting Countries (Annexed Table 2–2 of the Ordinance for Enforcement of the Plant Protection Act). Available at: http://www.maff.go.jp/j/syouan/keneki/kikaku/pdf/04_at2_2_specific_measures.pdf
Fujikawa T., Taguchi M., Kido K., Kusano S., Enya J., … Sato M., 2020a. Evaluation of an RNA-based PCR assay to detect viable ‘Candidatus Liberibacter solanacearum’ (Lso) in Lso-contaminated carrot seeds using different disinfection methods. Journal of Plant Pathology 102: 205–211. doi: https://doi.org/10.1007/s42161-019-00405-4
Fujikawa T., Yamamura K., Osaki K., Onozuka N., Taguchi M., … Sato M., 2020b. Seed transmission of ‘Candidatus Liberibacter solanacearum’ is unlikely in carrot. Journal of General Plant Pathology 86(4): 266-273. https://doi.org/10.1007/s10327-020-00927-1
Godefroid S., Van der Vyver A., Stoffelen P., Vandeborght B., 2017. Effectiveness of dry heat as seed sterilisation technique: Implications for ex situ conservation. Plant Biosystems 151(6): 1054–1061. doi: https://doi.org/10.1080/11263504.2016.1231140
Grondeau C., Ladonne F., Fourmond A., Poutier F., Samson R., 1992. Attempt to eradicate Pseudomonas syringae pv. pisi from pea seeds by heat treatments. Seed Science and Technology 20: 515-525.
Grondeau C., Samson R., Sands D.D.C., 1994. A Review of Thermotherapy to Free Plant Materials from Pathogens, Especially Seeds from Bacteria. Critical Reviews in Plant Sciences 13(1): 57-75. https://doi.org/10.1080/07352689409701908
Haapalainen M., 2014. Biology and epidemics of ‘Candidatus Liberibacter’ species, psyllid‐transmitted plant‐pathogenic bacteria. Annals of applied biology 165(2): 172-198. https://doi.org/10.1111/aab.12149
Haapalainen M., Kivimäki P., Latvala S., Rastas M., Hannukkala A., Jauhiainen L., Lemmetty A., Pirhonen M., Virtanen A., Nissinen A. I., 2017. Frequency and occurrence of the carrot pathogen ‘Candidatus Liberibacter solanacearum’ haplotype C in Finland. Plant Pathology 66: 559–570. https://doi.org/10.1111/ppa.12613
Haapalainen M., Latvala S., Wickström A., Wang J., Pirhonen M., Nissinen A. I., 2020. A novel haplotype of ‘Candidatus Liberibacter solanacearum’ found in Apiaceae and Polygonaceae family plants. European Journal of Plant Pathology 156(2): 413-423. https://doi.org/10.1007/s10658-019-01890-0
International Seed Testing Association. 2020. The germination test. In International rules for seed testing. Chapter 5: 1-57. doi: https://doi.org/10.15258/istarules.2022.05
Ilardi V., Catara V., 2013. ‘Candidatus Liberibacter’ spp. Emerging Threats for Agriculture in the European and Mediterranean Region. Biosafety 2: E135. https://doi.org/10.4172/2167-0331.1000e135
Ilardi V., Di Nicola E., Tavazza, M., 2016. First report of ‘Candidatus Liberibacter solanacearum’ in commercial carrot seeds in Italy. Journal of Plant Pathology 98(2). DOI: http://dx.doi.org/10.4454/JPP.V98I2.040
Ilardi V., Lumia V., Di Nicola E., Tavazza M., 2019. Identification, intra-and inter-laboratory validation of a diagnostic protocol for ‘Candidatus Liberibacter solanacearum’ in carrot seeds. European Journal of Plant Pathology, 153(3): 879-890. https://doi.org/10.1007/s10658-018-01606-w
Karahan, A., Altundag, S., Saracoglu, M., Duman, K., Ozdemir, I.,… Demir Ozden, E., 2022. First report of ‘Candidatus Liberibacter solanacearum’ on carrot and parsley in Turkey. New Disease Reports, 45, e12095. https://doi.org/10.1002/ndr2.12095
Koppenaal, R.S., Colombo, S.J., 1988. Heat tolerance of actively growing, bud-initiated, and dormant black spruce seedlings. Canadian Journal of Forest Research, 18: 1103–1105. https://doi.org/10.1139/x88-169
Kuan T. L., Minsavage G. V., Gabrielson R. L.,1985. Detection of Xanthomonas campestris pv. carotae in carrot seed. Plant Disease 69(9): 758-760. https://doi.org/10.1094/PD-69-758
Li W., Abad J.A., French-Monar R.D., Rascoe J., Wen A., … Levy L., 2009. Multiplex real-time PCR for detection, identification and quantification of ‘Candidatus Liberibacter solanacearum’ in potato plants with zebra chip. Journal of Microbiological Methods 78: 59-65. https://doi.org/10.1016/j.mimet.2009.04.009
Loiseau M., Renaudin I., Cousseau-Suhard P., Poliakoff F., Gentit P., 2017a. Transmission tests of ‘Candidatus Liberibacter solanacearum’ by carrot seeds. Acta Horticolturae 41-46. https://doi.org/10.17660/ActaHortic.2017.1153.7
Loiseau M., Renaudin I., Cousseau-Suhard P., Lucas P.-M., Forveille A., Gentit P., 2017b. Lack of evidence of vertical transmission of ‘Candidatus Liberibacter solanacearum’ by carrot seeds suggests that seed is not a major transmission pathway. Plant Disease 101: 2104–2109. https://doi.org/10.1094/PDIS-04-17-0531-RE
Mawassi M., Dror O., Bar-Joseph M., Piasezky A., Sjolund J.M., … Bahar O., 2018. ‘Candidatus Liberibacter solanacearum’ is Tightly Associated with Carrot Yellows Symptoms in Israel and Transmitted by the Prevalent Psyllid Vector Bactericera trigonica. Phytopathology 108(9): 1056-1066. https://doi.org/10.1094/PHYTO-10-17-0348-R
Merfield C., Hampton J., Hill M., Wratten S., 2005. The effect of seed moisture content and the duration and temperature of hot water treatment on carrot seed viability and the control of Alternaria radicina. Proceedings of the First Scientific Conference of the International Society of Organic Agriculture Research (ISOFAR), Adelaide, Australia.
Monger W.A., Jeffries C.J, 2016. First report of ‘Candidatus Liberibacter solanacearum’ in parsley (Petroselinum crispum) seed. New Disease Reports 34: 31. doi: http://dx.doi.org/10.5197/j.2044-0588.2016.034.031
Monger W.A., Jeffries C.J., 2018. A survey of ‘Candidatus Liberibacter solanacearum’ in historical seed from collections of carrot and related Apiaceae species. European Journal of Plant Pathology 150: 803–815. https://doi.org/10.1007/s10658-017-1322-6
Munyaneza J.E., Crosslin J.M., Upton, J.E., 2007. Association of Bactericera cockerelli (Homoptera: Psyllidae) with zebra chip, a new potato disease in southwestern United States and Mexico. Journal of Economic Entomology 100(3): 656–663. https://doi.org/10.1603/0022-0493(2007)100[656:aobchp]2.0.co;2
Nakamura, H., 1982. Effects of Dry Heat Treatment for Seed Disinfection on Germination in Vegetables. Japan Agricultural Research Quarterly 15(4): 243-247.
Nissinen A.I., Haapalainen M., Ojanen H., Pirhonen M., Jauhiainen, L., 2021. Spreading of Trioza apicalis and development of ‘Candidatus Liberibacter solanacearum’ infection on carrot in the field conditions. Annals of Applied Biology 178(1): 39-50. https://doi.org/10.1111/aab.12644
Oishi M., Hoshino S., Fujiwara Y., Ushiku S., Kobayashi Y., Namba I., 2017. A Comparison of Protocols to Detect Candidatus Liberibacter solanacearum from Carrot Seeds. Research on the Effectiveness of Propidium Monoazide Treatment and Evaluation of Seed Transmission in Carrot. Research bulletin of the plant protection service, 53: 111-117. doi: http://www.maff.go.jp/pps/j/guidance/r_bulletin/pdf/rb053_016.pdf
Que F., Hou X. L., Wang G. L., Xu Z. S., Tan,G. F., Xiong A. S., 2019. Advances in research on the carrot, an important root vegetable in the Apiaceae family. Horticulture Research 6. https://doi.org/10.1038/s41438-019-0150-6
Strandberg J.O., White J.M., 1989. Response of carrot seeds to heat treatments. Journal of the American Society for Horticultural Science 114(5): 766-769. https://doi.org/10.21273/JASHS.114.5.766
Wright, H.A., 1970. A method to determine heat-caused mortality in bunchgrasses. Ecology 51: 582–587. https://doi.org/10.2307/1934038
Zhang X., Wang R., Ning H., Li W., Bai Y., Li, Y., 2020. Evaluation and management of fungal-infected carrot seeds. Scientific Reports 10(1): 1-8. https://doi.org/10.1038/s41598-020-67907-