Rapid diagnostics for Gnomoniopsis smithogilvyi (syn. Gnomoniopsis castaneae) in chestnut nuts: new challenges by using LAMP and real-time PCR methods

Abdullah AS, Turo C, Moffat CS, Lopez-Ruiz FJ, Gibberd MR, Hamblin J, Zerihun A (2018) Real-time PCR for diagnosing and quantifying co-infection by two globally distributed fungal pathogens of wheat. Front Plant Sci 9:1086. https://doi.org/10.3389/fpls.2018.01086 Abdulmawjood A, Grabowski N, Fohler S, Kittler S, Nagengast H, Klein G (2014) Development of loop-mediated isothermal amplification (LAMP) assay for rapid and sensitive identification of ostrich meat. PLoS ONE 9:e100717. https://doi.org/10.1371/journal.pone.0100717 Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 Anonymous (2004) Update on PPQ diagnostics for SOD: diagnostic procedures approved by APHIS and diagnostic analyses performed by APHIS PPQ for Phytophthora ramorum. United States Department of Agriculture, Animal and Plant Health Inspection Service, USA Anonymous (2006) EPPO protocol for regulated pests. Phytophthora ramorum EPPO Bulletin 36:145–155 Barreira JCM, Casal S, Ferreira ICFR, Oliveira MBPP, Pereira JA (2009) Nutritional, fatty acid and triacylglycerol profiles of Castanea sativa Mill. cultivars: a compositional and chemometric approach. J Agr Food Chem 57:2836–2842. https://doi.org/10.1021/jf803754u Broeders S, Huber I, Grohmann L, Berben G, Taverniers I, Mazzara M, Roosens N, Morisset D (2014) Guidelines for validation of qualitative real-time PCR methods. Trends Food Sci Technol 37:115–126. https://doi.org/10.1016/j.tifs.2014.03.008 Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. https://doi.org/10.1373/clinchem.2008.112797 Catal M, Adams GC, Chastagner GA (2001) Detection, identification and quantification of latent needlecast pathogens and endophytes in symptomless conifer foliage by PCR and dot-blot assays. In Proceedings of the IUFRO Working Party 7.02,02 Shoot and foliage Diseases, Meeting at Hyytiala, Finland, 17–22 June 2001, Finnish Forest Research Institute Res. Papers. Vol. 829 ed. Uotila, A. and Ahola, V. Vantaa: Finnish Forest Research Institute pp. 164–168. Conedera M, Krebs P, Tinner W, Pradella M, Torriani D (2004) The cultivation of C. sativa in Europe, from its origin to its diffusion on a continental scale. Veg His Archaeobot 13:161–179. https://doi.org/10.1007/s00334-004-0038-7 De Vasconcelos MC, Bennett RN, Rosa EA, Ferreira-Cardoso JV (2010) Composition of European chestnut (Castanea sativa Mill.) and association with health effects: fresh and processed products. J Sci Food Agric 90:1578–1589. https://doi.org/10.1002/jsfa.4016 Dennert F, Broggini G, Gessler C, Storari M (2015) Gnomoniopsis castanea is the main chestnut nut rot agent in Switzerland. Phytopathol Med 54:199–211. https://doi.org/10.14601/Phytopathol_Mediterr-14712 Enicks DA, Bomberger RA, Amiri A (2020) Development of a portable LAMP assay for detection of Neofabraea perennans in commercial apple fruit. Plant Dis 104:2346–2353. https://doi.org/10.1094/PDIS-09-19-2036-RE EPPO (2017) European and Mediterranean Plant Protection Organization. PM 7/76 (4) Use of EPPO diagnostic protocols. Bull OEPP 47:7–9 EPPO (2019) European and Mediterranean Plant Protection Organization. PM 7/98 (4) Specific requirements for laboratories preparing accreditation for a plant pest diagnostic activity. Bull OEPP 49:530–563 FAOSTAT (2021) Food and Agiculture Organization of the United Nations. http://www.fao.org/faostat. Gaffuri F, Longa CMO, Turchetti T, Danti R, Maresi G (2017) 'Pink rot’: infection of Castanea sativa fruits by Colletotrichum acutatum. For Pathol 47:e12307. https://doi.org/10.1111/efp.12307 Hariharan G, Prasannath K (2021) Recent advances in molecular diagnostics of fungal plant pathogens: a mini review. Front Cell Infect Microbiol 10:600234. https://doi.org/10.3389/fcimb.2020.600234 Hughes KJD, Tomlinson JA, Giltrap PM, Barton V, Hobden E, Boonham N, Lane CR (2011) Development of a real-time PCR assay for detection of Phytophthora kernoviae and comparison of this method with a conventional culturing technique. Eur J Plant Pathol 131:695–703. https://doi.org/10.1007/s10658-011-9843-x Ioos R, Aloi F, Piškur B, Guinet C, Mullett M, Berbegal M, Bragança H, Cacciola SO, Oskay F, Cornejo C, Adamson K, Douanla-Meli C, Kačergius A, Martínez-Álvarez P, Nowakowska JA, Luchi N, Vettraino AM, Ahumada R, Pasquali M, Fourie G, Kanetis L, Alves A, Ghelardini L, Dvořák M, Sanz-Ros A, Diez JJ, Baskarathevan J, Aguayo J (2019) Are PCR-based diagnostic protocols easily transferable? An international collaborative case study assessing protocols targeting the quarantine pine pathogen Fusarium circinatum. Sci Rep 9:8195. https://doi.org/10.1038/s41598-019-44672-8 Jiang N, Liang LY, Tian CM (2020) Gnomoniopsis chinensis (Gnomoniaceae, Diaporthales), a new fungus causing canker of Chinese chestnut in Hebei Province, China. MycoKeys 67:19–32. https://doi.org/10.3897/mycokeys.67.51133 Jiang N, Tian C (2019) An emerging pathogen from rotted chestnut in China: Gnomoniopsis daii sp. nov. Forests 10:1016. https://doi.org/10.3390/f10111016 Keng H (1974) Economic plants of ancient North China as mentioned in Shih Ching (Book of Poetry). Econ Bot 28:391–410. https://doi.org/10.1007/BF02862856 Kim HK, An DS, Lee SJ, Lee DS (2012) Dependence of individual primary package atmosphere on retail display temperature and micro-perforations in a master packaging system for chestnuts. J Food Agric Environ 10:168–172. https://doi.org/10.1234/4.2012.3335 Kralik P, Ricchi M (2017) A basic guide to real time PCR in microbial diagnostics: Definitions, parameters, and everything. Front Microbiol 8:108. https://doi.org/10.3389/fmicb.2017.00108 Kutyavin IV, Afonina IA, Mills A, Gorn VV, Lukhtanov EA, Belousov ES, Singer MJ, Walburger DK, Lokhov SG, Gall AA, Dempcy R, Reed MW, Meyer RB, Hedgpeth J (2000) 3’-minor groove binder-DNA probes increase sequence specificity at PCR extension temperatures. Nucleic Acids Res 28:655–661. https://doi.org/10.1093/nar/28.2.655 Lee UK, Joo S, Klopfenstein NB, Kim MS (2016) Efficacy of washing treatments in the reduction of postharvest decay of chestnuts (Castanea crenata ‘Tsukuba’) during storage. Can J Plant Sci 96:1–5. https://doi.org/10.1139/cjps2015-0089 Li L, Tsao R, Yang R, Kramer JKG, Hernandez M (2007) Fatty acid profiles, tocopherol contents, and antioxidant activities of heartnut (Juglans ailanthifolia var. cordiformis) and Persian walnut (Juglans regia L.). J Agric Food Chem 55:1164–1169. https://doi.org/10.1021/jf062322d Lione G, Danti R, Fernandez-Conradi P, Ferreira-Cardoso JV, Lefort F, Marques G, Meyer JB, Prospero S, Radócz L, Robin C, Turchetti T, Vettraino AM, Gonthier P (2019) The emerging pathogen of chestnut Gnomoniopsis castaneae: the challenge posed by a versatile fungus. Eur J Plant Pathol 153:671–685. https://doi.org/10.1007/s10658-018-1597-2 Luchi N, Capretti P, Vettraino AM, Vannini A, Pinzani P, Pazzagli M (2006) Early detection of Biscogniauxia nummularia in symptomless European beech (Fagus sylvatica L.) by TaqManTM quantitative real-time PCR. Lett App Microbiol 43:33–38. https://doi.org/10.1111/j.1472-765X.2006.01920.x Luchi N, Ioos R, Santini A (2020) Fast and reliable molecular methods to detect fungal pathogens in woody plants. Appl Microbiol Biotechnol 104:2453–2468. https://doi.org/10.1007/s00253-020-10395-4 Maresi G, Oliveira Longa CM, Turchetti T (2013) Brown rot on nuts of Castanea sativa Mill: an emerging disease and its causal agent. iForest 6:294–301. https://doi.org/10.3832/ifor0952-006 Meyer FG (1980) Carbonized food plants of Pompeii, Herculaneum, and the Villa at Torre Annunziata. Econom Bot 34:401–437. https://doi.org/10.1007/BF02858317 Migliorini D, Ghelardini L, Tondini E, Luchi N, Santini A (2015) The potential of symptomless potted plants for carrying invasive soil-borne plant pathogens. Divers Distrib 21:1218–1229 Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28:e63. https://doi.org/10.1093/nar/28.12.e63 Notredame C, Higgins DG, Heringa J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217. https://doi.org/10.1006/jmbi.2000.4042 Rodrigues P, Ferreira T, Nascimento-Gonçalves E, Seixas F, Gil da Costa RM, Martins T, Neuparth MJ, Pires MJ, Lanzarin G, Félix L, Venâncio C, Ferreira ICFR, Bastos MMSM, Medeiros R, Gaivão I, Rosa E, Oliveira PA (2020) Dietary supplementation with Chestnut (Castanea sativa) reduces abdominal adiposity in FVB/n mice: a preliminary study. Biomedicines 8:75. https://doi.org/10.3390/biomedicines8040075 Russell EWB (1987) Pre-blight distribution of Castanea dentata (Marsh.) Borkh. J Torrey Bot Soc 114:183–190. https://doi.org/10.2307/2996129 Seddaiu S, Cerboneschi A, Sechi C, Mello A (2017) Gnomoniopsis castaneae associated with Dryocosmus kuriphilus galls in chestnut stands in Sardinia (Italy). iForest 10:440–445. https://doi.org/10.3832/ifor2064-009 Shuttleworth LA, Guest DI, Walker DM (2018) The fungus, the Code and the mysterious publication date: Why Gnomoniopsis smithogilvyi is still the correct name for the chestnut rot fungus. IMA Fungus 9:A78–A79. https://doi.org/10.1007/BF03449443 Shuttleworth LA, Walker DM, Guest DI (2015) The chestnut pathogen Gnomoniopsis smithogilvyi (Gnomoniaceae, Diaporthales) and its synonyms. Mycotaxon 130:929–940. https://doi.org/10.5248/130.929 Simopoulos AP (1991) Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr 54:438–463. https://doi.org/10.1093/ajcn/54.3.438 Tomlinson JA, Barker I, Boonham N (2007) Faster, simpler, more-specific methods for improved molecular detection of Phytophthora ramorum in the field. Appl Environm Microbiol 73:4040–4047. https://doi.org/10.1128/AEM.01389-07 Vannini A, Vettraino AM, Martignoni D, Morales Rodriguez C, Contarini M, Caccia R, Paparatti B, Speranza S (2017) Does Gnomoniopsis castaneae contribute to the natural biological control of chestnut gall wasp? Fungal Biol 121:44–52. https://doi.org/10.1016/j.funbio.2016.08.013 Vettraino AM, Bianchini L, Caradonna V, Forniti R, Goffi V, Zambelli M, Testa A, Vinciguerra V, Botondi R (2019) Ozone gas as a storage treatment to control Gnomoniopsis castaneae, preserving chestnut quality. J Sci Food Agric 99:6060–6065. https://doi.org/10.1002/jsfa.9883 Vettraino AM, Paolacci A, Vannini A (2005) Endophytism of Sclerotinia pseudotuberosa: PCR assay for specific detection in chestnut tissues. Mycol Res 109:96–102. https://doi.org/10.1017/S0953756204001583 Vettraino AM, Sukno S, Vannini A, Garbelotto M (2010) Diagnostic sensitivity and specificity of different methods used by two laboratories for the detection of Phytophthora ramorum on multiple natural hosts. Plant Pathol 59:289–300. https://doi.org/10.1111/j.1365-3059.2009.02209.x Vettraino AM, Vinciguerra V, Pacini G, Forniti R, Goffi V, Botondi R (2020) Gaseous ozone as a suitable solution for postharvest chestnut storage: evaluation of quality parameter trends. Food Bioproc Tech 13:187–193. https://doi.org/10.1007/s11947-019-02378-9 Visentin I, Gentile S, Valentino D, Gonthier P, Tamietti G, Cardinale F (2012) Gnomoniopsis castaneae sp. nov. (Gnomoniaceae, Diaporthales) as the causal agent of nut rot in sweet chestnut. J Plant Pathol 94:411–419. https://doi.org/10.4454/JPP.FA.2012.045 Washington W, Allen A, Dooley L (1997) Preliminary studies on Phomopsis castanea and other organisms associated with healthy and rotted chestnut fruit in storage. Australas Plant Pathol 26:37–43. https://doi.org/10.1071/AP97006 Zhang SY, Dai DJ, Wang HD, Zhang CQ (2019) One-step loop-mediated isothermal amplification (LAMP) for the rapid and sensitive detection of Fusarium fujikuroi in bakanae disease through NRPS31, an important gene in the gibberellic acid bio-synthesis. Sci Rep 9:3726. https://doi.org/10.1038/s41598-019-39874-z