Articles
Published 2021-05-13
Keywords
- Carica,
- Erysiphales,
- Erysiphe necator,
- host range expansion,
- phylogenetic analysis
- Pseudoidium ...More
How to Cite
[1]
D. SERESS, G. M. KOVÁCS, O. MOLNÁR, and M. Z. NÉMETH, “Infection of papaya (Carica papaya) by four powdery mildew fungi”, Phytopathol. Mediterr., vol. 60, no. 1, pp. 37–49, May 2021.
Abstract
Papaya (Carica papaya L.) is an important fruit crop in many tropical and subtropical countries. Powdery mildew commonly affects this host, causing premature leaf loss, reduced yields and poor fruit quality. At least fifteen different fungi have been identified as the causal agents of papaya powdery mildew. Powdery mildew symptoms were detected on potted papaya plants growing in two locations in Hungary. This study aimed to identify the causal agents. Morphology of powdery mildew samples was examined, and sequences of two loci were used for molecular taxonomic identifications. Only anamophs were detected in all samples, and four morphological types were distinguished. Most samples had Pseudoidium anamorphs, while some were of the Fibroidium anamorph. Based on morphology and molecular taxonomy, the Fibroidium anamorph was identified as Podosphaera xanthii. The Pseudoidium anamorphs corresponded to three different Erysiphe species: E. cruciferarum, E. necator and an unidentified Erysiphe sp., for which molecular phylogenetic analyses showed it belonged to an unresolved species complex of E. malvae, E. heraclei and E. betae. Infectivity of P. xanthii and E. necator on papaya was verified with cross inoculations. A review of previous records of powdery mildew fungi infecting papaya is also provided. Podosphaera xanthii was known to infect, and E. cruciferarum was suspected to infect Carica papaya, while E. necator was recorded on this host only once previously. No powdery mildew fungus belonging to the E. malvae/E. heraclei/E. betae species complex is known to infect papaya or any other plants in the Caricaceae, so the unidentified Erysiphe sp. is a new record on papaya and the Caricaceae. This study indicates host range expansion of this powdery mildew fungus onto papaya.
Downloads
Download data is not yet available.
Metrics
Metrics Loading ...
References
Alcorn J.L., 1968. Cucurbit powdery mildew on pawpaw. Queensland Journal of Agricultural and Animal Sciences 2: 161–164.
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.
Aziz A., Poinssot B., Daire X., Adrian M., Bézier A., ... Pugin A., 2003. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interactions 16: 1118–1128. https://doi.org/10.1094/MPMI.2003.16.12.1118
Beenken L., 2017. First records of the powdery mildews Erysiphe platani and E. alphitoides on Ailanthus altissima reveal host jumps independent of host phylogeny. Mycological Progress 16: 135–143. https://doi.org/10.1007/s11557-016-1260-2
Boesewinkel H., 1982. The identity of Oidium caricae and the first recording on papaya, mountain papaya and babaco in New Zealand. Fruits 37: 473–504.
Bolay A., 2005. Les Oïdiums de Suisse (Erysiphacées). Cryptogamica Helvetica 20: 1–173.
Braun U., Cook R.T.A., 2012. Taxonomic Manual of the Erysiphales (Powdery Mildews). CBS-KNAW Fungal Biodiversity Centre, Utrecht.
Braun U., Meeboon J., Takamatsu S., Blomquist C., Fernandez Pavia S., ... Macedo D.M. 2017. Powdery mildew species on papaya – a story of confusion and hidden diversity. Mycosphere 8: 1403–1423. https://doi.org/10.5943/mycosphere/8/9/7
Brewer M.T., Milgroom M.G., 2010. Phylogeography and population structure of the grape powdery mildew fungus, Erysiphe necator, from diverse Vitis species. BMC Evolutionary Biology 10: 268. https://doi.org/10.1186/1471-2148-10-268
Carvalho F.A., e–Monograph of Caricaceae. Version 1, November 2013 http://herbaria.plants.ox.ac.uk/bol/Caricaceae, Accessed 19 May 2020
Carvalho F.A., Filer D., Renner S.S., 2015. Taxonomy in the electronic age and an e-monograph of the papaya family (Caricaceae) as an example. Cladistics 31: 321–329. https://doi.org/10.1111/cla.12095
Cook R.T.A., Denton J.O., Denton G., 2015. Pathology of oak–wisteria powdery mildew. Fungal Biology 119: 657–671. https://doi.org/10.1016/j.funbio.2015.02.008
Cunningham B., Nelson S., 2012. Powdery mildew of papaya in Hawai‘i. Colleague of Tropical Agriculture and Human Resources, University of Hawaii at Mānoa, Plant Disease PD 90: 1–4.
Ellingham O., David J., Culham A., 2019. Enhancing identification accuracy for powdery mildews using previously underexploited DNA loci. Mycologia 111: 798–812. https://doi.org/10.1080/00275514.2019.1643644
Fan C., Cui H., Ding Z., Gao P., Luan F., 2019. First report of powdery mildew caused by Podosphaera xanthii on okra in China. Plant Disease 103: 1027–1027. https://doi.org/10.1094/PDIS-09-18-1543-PDN
Fonseca W., Cardoso J., Ootani M., Brasil S., Assunção F., ... Martins M.V.V., 2019. Morphological, molecular phylogenetic and pathogenic analyses of Erysiphe spp. causing powdery mildew on cashew plants in Brazil. Plant Pathology 68: 1157–1164. https://doi.org/10.1111/ppa.13032
Gorter G., 1993. A revised list of South African Erysiphaceae (powdery mildews) and their host plants. South African Journal of Botany 59: 566–566.
Honoré M.N., Belmonte-Ureña L.J., Navarro-Velasco A., Camacho-Ferre F., 2020. Effects of the size of papaya (Carica papaya L.) seedling with early determination of sex on the yield and the quality in a greenhouse cultivation in continental Europe. Scientia Horticulturae 265: 109218. https://doi.org/10.1016/j.scienta.2020.109218
Joa J., Chung B., Han K., Cho S., Shin H.-D., 2013. First report of powdery mildew caused by Podosphaera xanthii on papaya in Korea. Plant Disease 97: 1514–1514. https://doi.org/10.1094/PDIS-06-13-0581-PDN
Katoh K., Standley D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
Kiss L., Cook R.T.A., Saenz G.S., Cunnington J.H., Takamatsu S., ... Rossman A.Y., 2001. Identification of two powdery mildew fungi, Oidium neolycopersici sp. nov. and O. lycopersici, infecting tomato in different parts of the world. Mycological Research 105: 684–697. https://doi.org/10.1017/S0953756201004105
Liberato J.R., Barreto R.W., Louro R.P., 2004. Streptopodium caricae sp. nov., with a discussion of powdery mildews on papaya, and emended descriptions of the genus Streptopodium and Oidium caricae. Mycological Research 108: 1185–1194. https://doi.org/10.1017/s0953756204000991
Limkaisang S., Cunnington J.H., Wui L.K., Salleh B., Sato Y., ... Takamatsu S., 2006. Molecular phylogenetic analyses reveal a close relationship between powdery mildew fungi on some tropical trees and Erysiphe alphitoides, an oak powdery mildew. Mycoscience 47: 327–335. https://doi.org/10.1007/s10267-006-0311-y
Miller P.A., 1938. Cucurbit powdery mildew on Carica papaya. Phytopathology 28: 672.
Mukhtar I., van Peer A., 2018. Occurrence of powdery mildew caused by Pseudoidium neolycopersici on papaya (Carica papaya) in China. Plant Disease 102: 2645–2645. https://doi.org/10.1094/PDIS-10-17-1642-PDN
Munjal R.L., Kapoor J.N., 1973. Carica papaya: a new host of Sphaerotheca fuliginea. Indian Phytopathology 26: 366–367.
Murashige T., Skoog F., 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15: 473–497.
Nayak A.K., Babu B.K., 2019. First report of powdery mildew caused by Podosphaera fusca on Euphorbia hirta in Odisha state, India. Journal of Plant Pathology 101: 191–191. https://doi.org/10.1007/s42161-018-0143-6
Nemes K., Salánki K., Pintye A., 2019. Punica granatum (pomegranate) as new host of Erysiphe platani and Podosphaera xanthii. Phytopathologia Mediterranea 58: 707–711. https://doi.org/10.14601/Phyto-10890
Nomura Y., Takamatsu S., Fujioka K., 2003. Teleomorph of Erysiphe necator var. necator on Vitis vinifera and Ampelopsis brevipedunculata var. heterophylla (Vitaceae) newly found in Japan. Mycoscience 44: 157–158. https://doi.org/10.1007/s10267-003-0094-3
Pérez‐García A., Romero D., Fernández‐Ortuño D., López‐ruiz F., De Vicente A., Tores J.A., 2009. The powdery mildew fungus Podosphaera fusca (synonym Podosphaera xanthii), a constant threat to cucurbits. Molecular Plant Pathology 10: 153–160. https://doi.org/10.1111/j.1364-3703.2008.00527.x
Pieroni L.P., Gorayeb E.S., Benso L.A., Kurokawa S.Y.S., Siqueira O.A.P.A., ... Furtado E.L., 2020. First report of Erysiphe necator causing powdery mildew to rubber tree (Hevea brasiliensis) in Brazil. Plant Disease: in press. https://doi.org/10.1094/PDIS-04-20-0848-PDN
Pintye A., Németh M.Z., Molnár O., Horváth Á.N., Spitzmüller Z., ... Kovács G.M., 2020. Improved DNA extraction and quantitative real-time PCR for genotyping Erysiphe necator and detecting the DMI fungicide resistance marker A495T, using single ascocarps. Phytopathologia Mediterranea 59: 97–106. https://doi.org/10.14601/Phyto-11098
Rawal R.D., 2010. Fungal diseases of papaya and their management. Acta Horticulturae 851: 443-446. 10.17660/ActaHortic.2010.851.68
Scholler M., Schmidt A., Siahaan S.A.S., Takamatsu S., Braun U., 2016. A taxonomic and phylogenetic study of the Golovinomyces biocellatus complex (Erysiphales, Ascomycota) using asexual state morphology and rDNA sequence data. Mycological Progress 15: 56. https://doi.org/10.1007/s11557-016-1197-5
Sequeira M., 1992. Notes on Erysiphaceae. Powdery mildew on Carica papaya. Garcia de Orta. Série de Estudos Agronómicos 18: 23–26.
Shin H.-D., La Y.-J., 1993. Morphology of edge lines of chained immature conidia on conidiophores in powdery mildew fungi and their taxonomic significance. Mycotaxon 46: 445–451.
Shin H.-D., Meeboon J., Takamatsu S., Adhikari M.K., Braun U., 2019. Phylogeny and taxonomy of Pseudoidium pedaliacearum. Mycological Progress 18: 237–246. https://doi.org/10.1007/s11557-018-1429-y
Shirouzu T., Takamatsu S., Hashimoto A., Meeboon J., Ohkuma M., 2020. Phylogenetic overview of Erysiphaceae based on nrDNA and MCM7 sequences. Mycoscience: in press. https://doi.org/10.1016/j.myc.2020.03.006
Silvestro D., Michalak I., 2012. raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12: 335–337. https://doi.org/10.1007/s13127-011-0056-0
Staden R., Beal K.F., Bonfield J.K., 2000. The Staden package, 1998. Methods in Molecular Biology 132: 115–130. https://doi.org/10.1385/1-59259-192-2:115
Stamatakis A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stöver B.C., Müller K.F., 2010. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 7. https://doi.org/10.1186/1471-2105-11-7
Sz. Nagy G., Kiss L., 2006. A check-list of powdery mildew fungi of Hungary. Acta Phytopathologica et Entomologica Hungarica 41: 79-91.
Takamatsu S., Ito H., Shiroya Y., Kiss L., Heluta V., 2015. First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage. Mycologia 107: 475–489. https://doi.org/10.3852/15-007
Takamatsu S., Kano Y., 2001. PCR primers useful for nucleotide sequencing of rDNA of the powdery mildew fungi. Mycoscience 42: 135–139. https://doi.org/10.1007/BF02463987
Takamatsu S., Siahaan S.A., Moreno-Rico O., Cabrera de Álvarez M.G., Braun U., 2016. Early evolution of endoparasitic group in powdery mildews: molecular phylogeny suggests missing link between Phyllactinia and Leveillula. Mycologia 108: 837–850. https://doi.org/10.3852/16-010
Thines M., 2019. An evolutionary framework for host shifts – jumping ships for survival. New Phytologist 224: 605–617. https://doi.org/10.1111/nph.16092
Tsay J.-G., Chen R.-S., Wang H.-L., Wang W.-L., Weng B.-C., 2011. First report of powdery mildew caused by Erysiphe diffusa, Oidium neolycopersici, and Podosphaera xanthii on papaya in Taiwan. Plant Disease 95: 1188–1188. https://doi.org/10.1094/PDIS-05-11-0362
Vági P., Kovács G.M., Kiss L., 2006. Host range expansion in a powdery mildew fungus (Golovinomyces sp.) infecting Arabidopsis thaliana: Torenia fournieri as a new host. European Journal of Plant Pathology 117: 89–93. https://doi.org/10.1007/s10658-006-9072-x
Ventura J.A., Costa H., da Silva Tatagiba J., 2004. Papaya diseases and integrated control. In Diseases of Fruits and Vegetables: Volume II Springer, 201-268.
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.
Aziz A., Poinssot B., Daire X., Adrian M., Bézier A., ... Pugin A., 2003. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interactions 16: 1118–1128. https://doi.org/10.1094/MPMI.2003.16.12.1118
Beenken L., 2017. First records of the powdery mildews Erysiphe platani and E. alphitoides on Ailanthus altissima reveal host jumps independent of host phylogeny. Mycological Progress 16: 135–143. https://doi.org/10.1007/s11557-016-1260-2
Boesewinkel H., 1982. The identity of Oidium caricae and the first recording on papaya, mountain papaya and babaco in New Zealand. Fruits 37: 473–504.
Bolay A., 2005. Les Oïdiums de Suisse (Erysiphacées). Cryptogamica Helvetica 20: 1–173.
Braun U., Cook R.T.A., 2012. Taxonomic Manual of the Erysiphales (Powdery Mildews). CBS-KNAW Fungal Biodiversity Centre, Utrecht.
Braun U., Meeboon J., Takamatsu S., Blomquist C., Fernandez Pavia S., ... Macedo D.M. 2017. Powdery mildew species on papaya – a story of confusion and hidden diversity. Mycosphere 8: 1403–1423. https://doi.org/10.5943/mycosphere/8/9/7
Brewer M.T., Milgroom M.G., 2010. Phylogeography and population structure of the grape powdery mildew fungus, Erysiphe necator, from diverse Vitis species. BMC Evolutionary Biology 10: 268. https://doi.org/10.1186/1471-2148-10-268
Carvalho F.A., e–Monograph of Caricaceae. Version 1, November 2013 http://herbaria.plants.ox.ac.uk/bol/Caricaceae, Accessed 19 May 2020
Carvalho F.A., Filer D., Renner S.S., 2015. Taxonomy in the electronic age and an e-monograph of the papaya family (Caricaceae) as an example. Cladistics 31: 321–329. https://doi.org/10.1111/cla.12095
Cook R.T.A., Denton J.O., Denton G., 2015. Pathology of oak–wisteria powdery mildew. Fungal Biology 119: 657–671. https://doi.org/10.1016/j.funbio.2015.02.008
Cunningham B., Nelson S., 2012. Powdery mildew of papaya in Hawai‘i. Colleague of Tropical Agriculture and Human Resources, University of Hawaii at Mānoa, Plant Disease PD 90: 1–4.
Ellingham O., David J., Culham A., 2019. Enhancing identification accuracy for powdery mildews using previously underexploited DNA loci. Mycologia 111: 798–812. https://doi.org/10.1080/00275514.2019.1643644
Fan C., Cui H., Ding Z., Gao P., Luan F., 2019. First report of powdery mildew caused by Podosphaera xanthii on okra in China. Plant Disease 103: 1027–1027. https://doi.org/10.1094/PDIS-09-18-1543-PDN
Fonseca W., Cardoso J., Ootani M., Brasil S., Assunção F., ... Martins M.V.V., 2019. Morphological, molecular phylogenetic and pathogenic analyses of Erysiphe spp. causing powdery mildew on cashew plants in Brazil. Plant Pathology 68: 1157–1164. https://doi.org/10.1111/ppa.13032
Gorter G., 1993. A revised list of South African Erysiphaceae (powdery mildews) and their host plants. South African Journal of Botany 59: 566–566.
Honoré M.N., Belmonte-Ureña L.J., Navarro-Velasco A., Camacho-Ferre F., 2020. Effects of the size of papaya (Carica papaya L.) seedling with early determination of sex on the yield and the quality in a greenhouse cultivation in continental Europe. Scientia Horticulturae 265: 109218. https://doi.org/10.1016/j.scienta.2020.109218
Joa J., Chung B., Han K., Cho S., Shin H.-D., 2013. First report of powdery mildew caused by Podosphaera xanthii on papaya in Korea. Plant Disease 97: 1514–1514. https://doi.org/10.1094/PDIS-06-13-0581-PDN
Katoh K., Standley D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
Kiss L., Cook R.T.A., Saenz G.S., Cunnington J.H., Takamatsu S., ... Rossman A.Y., 2001. Identification of two powdery mildew fungi, Oidium neolycopersici sp. nov. and O. lycopersici, infecting tomato in different parts of the world. Mycological Research 105: 684–697. https://doi.org/10.1017/S0953756201004105
Liberato J.R., Barreto R.W., Louro R.P., 2004. Streptopodium caricae sp. nov., with a discussion of powdery mildews on papaya, and emended descriptions of the genus Streptopodium and Oidium caricae. Mycological Research 108: 1185–1194. https://doi.org/10.1017/s0953756204000991
Limkaisang S., Cunnington J.H., Wui L.K., Salleh B., Sato Y., ... Takamatsu S., 2006. Molecular phylogenetic analyses reveal a close relationship between powdery mildew fungi on some tropical trees and Erysiphe alphitoides, an oak powdery mildew. Mycoscience 47: 327–335. https://doi.org/10.1007/s10267-006-0311-y
Miller P.A., 1938. Cucurbit powdery mildew on Carica papaya. Phytopathology 28: 672.
Mukhtar I., van Peer A., 2018. Occurrence of powdery mildew caused by Pseudoidium neolycopersici on papaya (Carica papaya) in China. Plant Disease 102: 2645–2645. https://doi.org/10.1094/PDIS-10-17-1642-PDN
Munjal R.L., Kapoor J.N., 1973. Carica papaya: a new host of Sphaerotheca fuliginea. Indian Phytopathology 26: 366–367.
Murashige T., Skoog F., 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15: 473–497.
Nayak A.K., Babu B.K., 2019. First report of powdery mildew caused by Podosphaera fusca on Euphorbia hirta in Odisha state, India. Journal of Plant Pathology 101: 191–191. https://doi.org/10.1007/s42161-018-0143-6
Nemes K., Salánki K., Pintye A., 2019. Punica granatum (pomegranate) as new host of Erysiphe platani and Podosphaera xanthii. Phytopathologia Mediterranea 58: 707–711. https://doi.org/10.14601/Phyto-10890
Nomura Y., Takamatsu S., Fujioka K., 2003. Teleomorph of Erysiphe necator var. necator on Vitis vinifera and Ampelopsis brevipedunculata var. heterophylla (Vitaceae) newly found in Japan. Mycoscience 44: 157–158. https://doi.org/10.1007/s10267-003-0094-3
Pérez‐García A., Romero D., Fernández‐Ortuño D., López‐ruiz F., De Vicente A., Tores J.A., 2009. The powdery mildew fungus Podosphaera fusca (synonym Podosphaera xanthii), a constant threat to cucurbits. Molecular Plant Pathology 10: 153–160. https://doi.org/10.1111/j.1364-3703.2008.00527.x
Pieroni L.P., Gorayeb E.S., Benso L.A., Kurokawa S.Y.S., Siqueira O.A.P.A., ... Furtado E.L., 2020. First report of Erysiphe necator causing powdery mildew to rubber tree (Hevea brasiliensis) in Brazil. Plant Disease: in press. https://doi.org/10.1094/PDIS-04-20-0848-PDN
Pintye A., Németh M.Z., Molnár O., Horváth Á.N., Spitzmüller Z., ... Kovács G.M., 2020. Improved DNA extraction and quantitative real-time PCR for genotyping Erysiphe necator and detecting the DMI fungicide resistance marker A495T, using single ascocarps. Phytopathologia Mediterranea 59: 97–106. https://doi.org/10.14601/Phyto-11098
Rawal R.D., 2010. Fungal diseases of papaya and their management. Acta Horticulturae 851: 443-446. 10.17660/ActaHortic.2010.851.68
Scholler M., Schmidt A., Siahaan S.A.S., Takamatsu S., Braun U., 2016. A taxonomic and phylogenetic study of the Golovinomyces biocellatus complex (Erysiphales, Ascomycota) using asexual state morphology and rDNA sequence data. Mycological Progress 15: 56. https://doi.org/10.1007/s11557-016-1197-5
Sequeira M., 1992. Notes on Erysiphaceae. Powdery mildew on Carica papaya. Garcia de Orta. Série de Estudos Agronómicos 18: 23–26.
Shin H.-D., La Y.-J., 1993. Morphology of edge lines of chained immature conidia on conidiophores in powdery mildew fungi and their taxonomic significance. Mycotaxon 46: 445–451.
Shin H.-D., Meeboon J., Takamatsu S., Adhikari M.K., Braun U., 2019. Phylogeny and taxonomy of Pseudoidium pedaliacearum. Mycological Progress 18: 237–246. https://doi.org/10.1007/s11557-018-1429-y
Shirouzu T., Takamatsu S., Hashimoto A., Meeboon J., Ohkuma M., 2020. Phylogenetic overview of Erysiphaceae based on nrDNA and MCM7 sequences. Mycoscience: in press. https://doi.org/10.1016/j.myc.2020.03.006
Silvestro D., Michalak I., 2012. raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12: 335–337. https://doi.org/10.1007/s13127-011-0056-0
Staden R., Beal K.F., Bonfield J.K., 2000. The Staden package, 1998. Methods in Molecular Biology 132: 115–130. https://doi.org/10.1385/1-59259-192-2:115
Stamatakis A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stöver B.C., Müller K.F., 2010. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 7. https://doi.org/10.1186/1471-2105-11-7
Sz. Nagy G., Kiss L., 2006. A check-list of powdery mildew fungi of Hungary. Acta Phytopathologica et Entomologica Hungarica 41: 79-91.
Takamatsu S., Ito H., Shiroya Y., Kiss L., Heluta V., 2015. First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage. Mycologia 107: 475–489. https://doi.org/10.3852/15-007
Takamatsu S., Kano Y., 2001. PCR primers useful for nucleotide sequencing of rDNA of the powdery mildew fungi. Mycoscience 42: 135–139. https://doi.org/10.1007/BF02463987
Takamatsu S., Siahaan S.A., Moreno-Rico O., Cabrera de Álvarez M.G., Braun U., 2016. Early evolution of endoparasitic group in powdery mildews: molecular phylogeny suggests missing link between Phyllactinia and Leveillula. Mycologia 108: 837–850. https://doi.org/10.3852/16-010
Thines M., 2019. An evolutionary framework for host shifts – jumping ships for survival. New Phytologist 224: 605–617. https://doi.org/10.1111/nph.16092
Tsay J.-G., Chen R.-S., Wang H.-L., Wang W.-L., Weng B.-C., 2011. First report of powdery mildew caused by Erysiphe diffusa, Oidium neolycopersici, and Podosphaera xanthii on papaya in Taiwan. Plant Disease 95: 1188–1188. https://doi.org/10.1094/PDIS-05-11-0362
Vági P., Kovács G.M., Kiss L., 2006. Host range expansion in a powdery mildew fungus (Golovinomyces sp.) infecting Arabidopsis thaliana: Torenia fournieri as a new host. European Journal of Plant Pathology 117: 89–93. https://doi.org/10.1007/s10658-006-9072-x
Ventura J.A., Costa H., da Silva Tatagiba J., 2004. Papaya diseases and integrated control. In Diseases of Fruits and Vegetables: Volume II Springer, 201-268.