Endophytic Fungi of Citrus Plants
Abstract
:1. Introduction
2. Endophytic Occurrence of Citrus Pathogens
3. Other Endophytic Fungi and Their Interactions with Pests and Pathogens of Citrus
4. Biotechnological Implications
5. Conclusions
Funding
Conflicts of Interest
References
- De Bary, A. Morphologie und Physiologie der Pilze, Flechten und Myxomyceten; Engelmann: Leipzig, Germany, 1866. [Google Scholar]
- Hyde, K.D.; Soytong, K. The fungal endophyte dilemma. Fungal Divers. 2008, 33, 163–173. [Google Scholar]
- Turner, T.R.; James, E.K.; Poole, P.S. The plant microbiome. Genome Biol. 2013, 14, 209. [Google Scholar] [CrossRef] [PubMed]
- McOnie, K.C. The latent occurrence in Citrus and other hosts of a Guignardia easily confused with G. citricarpa, the black spot pathogen. Phytopathology 1964, 54, 64–67. [Google Scholar]
- Meyer, L.; Slippers, B.; Korsten, L.; Kotze, J.M.; Wingfield, M.J. Two distinct Guignardia species associated with citrus in South Africa. S. Afr. J. Sci. 2001, 97, 191–194. [Google Scholar]
- Baayen, R.P.; Bonants, P.J.M.; Verkley, G.; Carroll, G.C.; van der Aa, H.A.; de Weerdt, M.; van Brouwershaven, I.R.; Schutte, G.C.; Maccheroni, W., Jr.; Glienke de Blanco, C.; et al. Nonpathogenic isolates of the citrus black spot fungus, Guignardia citricarpa, identified as a cosmopolitan endophyte of woody plants, G. mangiferae (Phyllosticta capitalensis). Phytopathology 2002, 92, 464–477. [Google Scholar] [CrossRef]
- Zavala, M.G.M.; Er, H.L.; Goss, E.M.; Wang, N.Y.; Dewdney, M.; van Bruggen, A.H.C. Genetic variation among Phyllosticta strains isolated from citrus in Florida that are pathogenic or nonpathogenic to citrus. Trop. Plant Pathol. 2014, 39, 119–128. [Google Scholar] [CrossRef]
- Guarnaccia, V.; Gehrmann, T.; Silva-Junior, G.J.; Fourie, P.H.; Haridas, S.; Vu, D.; Spatafora, J.; Martin, F.M.; Robert, V.; Grigoriev, I.V.; et al. Phyllosticta citricarpa and sister species of global importance to Citrus. Mol. Plant Pathol. 2019. [Google Scholar] [CrossRef]
- Wikee, S.; Udayanga, D.; Crous, P.W.; Chukeatirote, E.; McKenzie, E.H.; Bahkali, A.H.; Dai, D.Q.; Hyde, K.D. Phyllosticta—An overview of current status of species recognition. Fungal Divers. 2011, 51, 43–61. [Google Scholar] [CrossRef]
- Wikee, S.; Lombard, L.; Crous, P.W.; Nakashima, C.; Motohashi, K.; Chukeatirote, E.; Alias, S.A.; McKenzie, E.H.C.; Hyde, K.D. Phyllosticta capitalensis, a widespread endophyte of plants. Fungal Divers. 2013, 60, 91–105. [Google Scholar] [CrossRef]
- Okane, I.; Nakagiri, A.; Ito, T.; Lumyong, S. Extensive host range of an endophytic fungus, Guignardia endophyllicola (anamorph: Phyllosticta capitalensis). Mycoscience 2003, 44, 353–363. [Google Scholar] [CrossRef]
- Bonants, P.J.; Carroll, G.C.; De Weerdt, M.; van Brouwershaven, I.R.; Baayen, R.P. Development and validation of a fast PCR-based detection method for pathogenic isolates of the citrus black spot fungus, Guignardia citricarpa. Eur. J. Plant Pathol. 2003, 109, 503–513. [Google Scholar] [CrossRef]
- Meyer, L.; Sanders, G.M.; Jacobs, R.; Korsten, L. A one-day sensitive method to detect and distinguish between the citrus black spot pathogen Guignardia citricarpa and the endophyte Guignardia mangiferae. Plant Dis. 2006, 90, 97–101. [Google Scholar] [CrossRef]
- Meyer, L.; Jacobs, R.; Kotzé, J.M.; Truter, M.; Korsten, L. Detection and molecular identification protocols for Phyllosticta citricarpa from citrus matter. S. Afr. J. Sci. 2012, 108, 53–59. [Google Scholar] [CrossRef]
- Peres, N.A.; Harakava, R.; Carroll, G.C.; Adaskaveg, J.E.; Timmer, L.W. Comparison of molecular procedures for detection and identification of Guignardia citricarpa and G. mangiferae. Plant Dis. 2007, 91, 525–531. [Google Scholar] [CrossRef]
- Van Gent-Pelzer, M.P.E.; Van Brouwershaven, I.R.; Kox, L.F.F.; Bonants, P.J.M. A TaqMan PCR method for routine diagnosis of the quarantine fungus Guignardia citricarpa on citrus fruit. J. Phytopathol. 2007, 155, 357–363. [Google Scholar] [CrossRef]
- Baldassari, R.B.; Wickert, E.; de Goes, A. Pathogenicity, colony morphology and diversity of isolates of Guignardia citricarpa and G. mangiferae isolated from Citrus spp. Eur. J. Plant Pathol. 2008, 120, 103–110. [Google Scholar] [CrossRef]
- Stringari, D.; Glienke, C.; Christo, D.D.; Maccheroni, W., Jr.; Azevedo, J.L.D. High molecular diversity of the fungus Guignardia citricarpa and Guignardia mangiferae and new primers for the diagnosis of the citrus black spot. Braz. Arch. Biol. Technol. 2009, 52, 1063–1073. [Google Scholar] [CrossRef]
- Hu, J.; Johnson, E.G.; Wang, N.Y.; Davoglio, T.; Dewdney, M.M. qPCR quantification of pathogenic Guignardia citricarpa and nonpathogenic G. mangiferae in citrus. Plant Dis. 2014, 98, 112–120. [Google Scholar] [CrossRef]
- Schirmacher, A.M.; Tomlinson, J.A.; Barnes, A.V.; Barton, V.C. Species-specific real-time PCR for diagnosis of Phyllosticta citricarpa on Citrus species. EPPO Bull. 2019. [Google Scholar] [CrossRef]
- Everett, K.R.; Rees-George, J. Reclassification of an isolate of Guignardia citricarpa from New Zealand as Guignardia mangiferae by sequence analysis. Plant Pathol. 2006, 55, 194–199. [Google Scholar] [CrossRef]
- Romão, A.S.; Spósito, M.B.; Andreote, F.D.; Azevedo, J.L.D.; Araújo, W.L. Enzymatic differences between the endophyte Guignardia mangiferae (Botryosphaeriaceae) and the citrus pathogen G. citricarpa. Genet. Mol. Res. 2011, 10, 243–252. [Google Scholar] [CrossRef] [PubMed]
- Munari Rodrigues, C.; Takita, M.A.; Silva, N.V.; Ribeiro-Alves, M.; Machado, M.A. Comparative genome analysis of Phyllosticta citricarpa and Phyllosticta capitalensis, two fungi species that share the same host. BMC Genom. 2019, 20, 554. [Google Scholar] [CrossRef]
- Wikee, S.; Lombard, L.; Nakashima, C.; Motohashi, K.; Chukeatirote, E.; Cheewangkoon, R.; McKenzie, E.H.C.; Hyde, K.D.; Crous, P.W. A phylogenetic re-evaluation of Phyllosticta (Botryosphaeriales). Stud. Mycol. 2013, 76, 1–29. [Google Scholar] [CrossRef] [PubMed]
- Wulandari, N.F.; Toanun, C.; Hyde, K.D.; Duong, L.M.; de Gruyter, J.; Meffert, J.P.; Groenewald, J.Z.; Crous, P.W. Phyllosticta citriasiana sp. nov., the cause of Citrus tan spot of Citrus maxima in Asia. Fungal Divers. 2009, 34, 23–39. [Google Scholar]
- Wang, X.; Chen, G.; Huang, F.; Zhang, J.; Hyde, K.D.; Li, H. Phyllosticta species associated with citrus diseases in China. Fungal Divers. 2012, 52, 209–224. [Google Scholar] [CrossRef]
- Guarnaccia, V.; Groenewald, J.Z.; Li, H.; Glienke, C.; Carstens, E.; Hattingh, V.; Fourie, P.H.; Crous, P.W. First report of Phyllosticta citricarpa and description of two new species, P. paracapitalensis and P. paracitricarpa, from citrus in Europe. Stud. Mycol. 2017, 87, 161–185. [Google Scholar] [CrossRef]
- Glienke, C.; Pereira, O.L.; Stringari, D.; Fabris, J.; Kava-Cordeiro, V.; Galli-Terasawa, L.; Cunnington, J.; Shivas, R.G.; Groenewald, J.Z.; Crous, P.W. Endophytic and pathogenic Phyllosticta species, with reference to those associated with citrus black spot. Persoonia 2011, 26, 47–56. [Google Scholar] [CrossRef]
- Schubert, T.S.; Dewdney, M.M.; Peres, N.A.; Palm, M.E.; Jeyaprakash, A.; Sutton, B.; Mondal, S.N.; Wang, N.Y.; Rascoe, J.; Picton, D.D. First report of Guignardia citricarpa associated with citrus black spot on sweet orange (Citrus sinensis) in North America. Plant Dis. 2012, 96, 1225. [Google Scholar] [CrossRef]
- Jeger, M.; Bragard, C.; Caffier, D.; Candresse, T.; Chatzivassiliou, E.; Dehnen-Schmutz, K.; Gilioli, G.; Gregoire, J.C.; Jaques Miret, J.A.; MacLeod, A.; et al. Evaluation of a paper by Guarnaccia et al. (2017) on the first report of Phyllosticta citricarpa in Europe. EFSA J. 2018, 16, 5114. [Google Scholar]
- Tran, N.T.; Miles, A.K.; Dietzgen, R.G.; Drenth, A. Phyllosticta capitalensis and P. paracapitalensis are endophytic fungi that show potential to inhibit pathogenic P. citricarpa on citrus. Australas. Plant Pathol. 2019, 48, 281–296. [Google Scholar] [CrossRef]
- Wickert, E.; de Macedo Lemos, E.G.; Kishi, L.T.; de Souza, A.; de Goes, A. Genetic diversity and population differentiation of Guignardia mangiferae from “Tahiti” acid lime. Sci. World J. 2012. [Google Scholar] [CrossRef]
- Huang, F.; Chen, G.Q.; Hou, X.; Fu, Y.S.; Cai, L.; Hyde, K.D.; Li, H.Y. Colletotrichum species associated with cultivated citrus in China. Fungal Divers. 2013, 61, 61–74. [Google Scholar] [CrossRef]
- Waculicz-Andrade, C.E.; Savi, D.C.; Bini, A.P.; Adamoski, D.; Goulin, E.H.; Silva, G.J., Jr.; Massola, N.S., Jr.; Terasawa, L.G.; Kava, V.; Glienke, C. Colletotrichum gloeosporioides sensu stricto: An endophytic species or citrus pathogen in Brazil? Australas. Plant Pathol. 2017, 46, 191–203. [Google Scholar] [CrossRef]
- Durán, E.L.; Ploper, L.D.; Ramallo, J.C.; Piccolo Grandi, R.A.; Hupper Giancoli, Á.C.; Azevedo, J.L. The foliar fungal endophytes of Citrus limon in Argentina. Can. J. Bot. 2005, 83, 350–355. [Google Scholar] [CrossRef]
- Douanla-Meli, C.; Langer, E.; Mouafo, F.T. Fungal endophyte diversity and community patterns in healthy and yellowing leaves of Citrus limon. Fungal Ecol. 2013, 6, 212–222. [Google Scholar] [CrossRef]
- Mohali, S.; Burgess, T.I.; Wingfield, M.J. Diversity and host association of the tropical tree endophyte Lasiodiplodia theobromae revealed using simple sequence repeat markers. For. Pathol. 2005, 35, 385–396. [Google Scholar] [CrossRef]
- Slippers, B.; Wingfield, M.J. Botryosphaeriaceae as endophytes and latent pathogens of woody plants: Diversity, ecology and impact. Fungal Biol. Rev. 2007, 21, 90–106. [Google Scholar] [CrossRef]
- Zhao, W.; Bai, J.; McCollum, G.; Baldwin, E. High incidence of preharvest colonization of huanglongbing-symptomatic Citrus sinensis fruit by Lasiodiplodia theobromae (Diplodia natalensis) and exacerbation of postharvest fruit decay by that fungus. Appl. Environ. Microbiol. 2015, 81, 364–372. [Google Scholar] [CrossRef] [Green Version]
- Udayanga, D.; Liu, X.; McKenzie, E.H.C.; Chukeatirote, E.; Bahkali, A.H.A.; Hyde, K.D. The genus Phomopsis: Biology, applications, species concepts and names of common phytopathogens. Fungal Divers. 2011, 50, 189–225. [Google Scholar] [CrossRef]
- Gomes, R.R.; Glienke, C.; Videira, S.I.R.; Lombard, L.; Groenewald, J.Z.; Crous, P.W. Diaporthe: A genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 2013, 31, 1–41. [Google Scholar] [CrossRef] [Green Version]
- Savi, D.C.; Aluizio, R.; Glienke, C. Brazilian plants: An unexplored source of endophytes as producers of active metabolites. Planta Med. 2019, 85, 619–636. [Google Scholar]
- Huang, F.; Hou, X.; Dewdney, M.M.; Fu, Y.; Chen, G.; Hyde, K.D.; Li, H. Diaporthe species occurring on citrus in China. Fungal Divers. 2013, 61, 237–250. [Google Scholar] [CrossRef]
- Guarnaccia, V.; Crous, P.W. Emerging citrus diseases in Europe caused by species of Diaporthe. IMA Fungus 2017, 8, 317–334. [Google Scholar] [CrossRef] [Green Version]
- Huang, F.; Udayanga, D.; Wang, X.; Hou, X.; Mei, X.; Fu, Y.; Hyde, K.D.; Li, H. Endophytic Diaporthe associated with Citrus: A phylogenetic reassessment with seven new species from China. Fungal Biol. 2015, 119, 331–347. [Google Scholar] [CrossRef]
- Peever, T.L.; Canihos, Y.; Olsen, L.; Ibáñez, A.; Liu, Y.C.; Timmer, L.W. Population genetic structure and host specificity of Alternaria spp. causing brown spot of Minneola tangelo and rough lemon in Florida. Phytopathology 1999, 89, 851–860. [Google Scholar] [CrossRef] [Green Version]
- Akimitsu, K.; Peever, T.L.; Timmer, L.W. Molecular, ecological and evolutionary approaches to understanding Alternaria diseases of citrus. Mol. Plant Pathol. 2003, 4, 435–446. [Google Scholar] [CrossRef]
- Sadeghi, F.; Samsampour, D.; Seyahooei, M.A.; Bagheri, A.; Soltani, J. Diversity and spatiotemporal distribution of fungal endophytes associated with Citrus reticulata cv. Siyahoo. Curr. Microbiol. 2019, 76, 279–289. [Google Scholar] [CrossRef]
- Juybari, H.Z.; Tajick Ghanbary, M.A.; Rahimian, H.; Karimi, K.; Arzanlou, M. Seasonal, tissue and age influences on frequency and biodiversity of endophytic fungi of Citrus sinensis in Iran. For. Pathol. 2019, e12559. [Google Scholar] [CrossRef]
- Sandoval-Denis, M.; Guarnaccia, V.; Polizzi, G.; Crous, P.W. Symptomatic Citrus trees reveal a new pathogenic lineage in Fusarium and two new Neocosmospora species. Persoonia 2018, 40, 1–25. [Google Scholar] [CrossRef] [Green Version]
- Childs, J.F.L.; Kopp, L.E.; Johnson, R.E. A species of Physoderma present in Citrus and related species. Phytopathology 1965, 55, 681–687. [Google Scholar]
- Ho, M.Y.; Chung, W.C.; Huang, H.C.; Chung, W.H.; Chung, W.H. Identification of endophytic fungi of medicinal herbs of Lauraceae and Rutaceae with antimicrobial property. Taiwania 2012, 57, 229–241. [Google Scholar]
- Santos Gai, C.; Teixeira Lacava, P.; Maccheroni, W., Jr.; Glienke, C.; Araújo, W.L.; Miller, T.A.; Azevedo, J.L. Diversity of endophytic yeasts from sweet orange and their localization by scanning electron microscopy. J. Basic Microbiol. 2009, 49, 441–451. [Google Scholar]
- Rodríguez, P.; Reyes, B.; Barton, M.; Coronel, C.; Menéndez, P.; Gonzalez, D.; Rodríguez, S. Stereoselective biotransformation of α-alkyl-β-keto esters by endophytic bacteria and yeast. J. Mol. Catal. B Enzym. 2011, 71, 90–94. [Google Scholar] [CrossRef]
- Bamisile, B.S.; Dash, C.K.; Akutse, K.S.; Qasim, M.; Ramos Aguila, L.C.; Wang, F.; Keppanan, R.; Wang, L. Endophytic Beauveria bassiana in foliar-treated Citrus limon plants acting as a growth suppressor to three successive generations of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Insects 2019, 10, 176. [Google Scholar] [CrossRef] [Green Version]
- Araújo, W.L.; Maccheroni, W., Jr.; Aguilar-Vildoso, C.I.; Barroso, P.A.; Saridakis, H.O.; Azevedo, J.L. Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can. J. Microbiol. 2001, 47, 229–236. [Google Scholar] [CrossRef]
- Glienke-Blanco, C.; Aguilar-Vildoso, C.I.; Vieira, M.L.C.; Barroso, P.A.V.; Azevedo, J.L. Genetic variability in the endophytic fungus Guignardia citricarpa isolated from citrus plants. Genet. Mol. Biol. 2002, 25, 251–255. [Google Scholar] [CrossRef]
- Manoharan, G.; Sairam, T.; Thangamani, R.; Ramakrishnan, D.; Tiwari, M.K.; Lee, J.K.; Marimuthu, J. Identification and characterization of type III polyketide synthase genes from culturable endophytes of ethnomedicinal plants. Enzyme Microb. Technol. 2019, 131, 109396. [Google Scholar] [CrossRef]
- Ling, L.; Li, Z.; Jiao, Z.; Zhang, X.; Ma, W.; Feng, J.; Zhang, J.; Lu, L. Identification of novel endophytic yeast strains from tangerine peel. Curr. Microbiol. 2019, 76, 1066–1072. [Google Scholar] [CrossRef]
- Paz, Z.; Burdman, S.; Gerson, U.; Sztejnberg, A. Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora. J. Appl. Microbiol. 2007, 103, 2570–2579. [Google Scholar] [CrossRef]
- Pena, L.C.; Jung, L.F.; Savi, D.C.; Servienski, A.; Aluizio, R.; Goulin, E.H.; Galli-Terasawa, L.V.; Lameiro de Noronha Sales Maia, B.H.; Annies, V.; Cavichiolo Franco, C.R.; et al. A Muscodor strain isolated from Citrus sinensis and its production of volatile organic compounds inhibiting Phyllosticta citricarpa growth. J. Plant Dis. Prot. 2017, 124, 349–360. [Google Scholar] [CrossRef]
- Rodrigues, K.F.; Sieber, T.N.; Grünig, C.R.; Holdenrieder, O. Characterization of Guignardia mangiferae isolated from tropical plants based on morphology, ISSR-PCR amplifications and ITS1-5.8 S-ITS2 sequences. Mycol. Res. 2004, 108, 45–52. [Google Scholar] [CrossRef]
- Miles, A.K.; Tan, Y.P.; Tan, M.K.; Donovan, N.J.; Ghalayini, A.; Drenth, A. Phyllosticta spp. on cultivated citrus in Australia. Australas. Plant Pathol. 2013, 42, 461–467. [Google Scholar] [CrossRef]
- Schüepp, H. Untersuchungen über Guignardia citricarpa Kiely, den Erreger der Schwarzfleckenkrankheit auf Citrus. J. Phytopathol. 1960, 40, 258–271. [Google Scholar] [CrossRef]
- Azevedo, J.L.; Maccheroni, W., Jr.; Pereira, J.O.; de Araújo, W.L. Endophytic microorganisms: A review on insect control and recent advances on tropical plants. Electron. J. Biotechnol. 2000, 3, 15–16. [Google Scholar] [CrossRef]
- Hawksworth, D.L.; Crous, P.W.; Redhead, S.A.; Reynolds, D.R.; Samson, R.A.; Seifert, K.A.; Taylor, J.W.; Wingfield, M.J.; Abaci, O.; Aime, C.; et al. The Amsterdam declaration on fungal nomenclature. IMA Fungus 2011, 2, 105–112. [Google Scholar] [CrossRef] [Green Version]
- Davis, E.C.; Franklin, J.B.; Shaw, A.J.; Vilgalys, R. Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: Phylogenetics, distribution, and symbiosis. Am. J. Bot. 2003, 90, 1661–1667. [Google Scholar] [CrossRef]
- U’Ren, J.M.; Miadlikowska, J.; Zimmerman, N.B.; Lutzoni, F.; Stajich, J.E.; Arnold, A.E. Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota). Mol. Phylogenet. Evol. 2016, 98, 210–232. [Google Scholar] [CrossRef] [Green Version]
- Nicoletti, R.; Fiorentino, A. Plant bioactive metabolites and drugs produced by endophytic fungi of Spermatophyta. Agriculture 2015, 5, 918–970. [Google Scholar] [CrossRef] [Green Version]
- Camargo Dos Santos, P.J.; Savi, D.C.; Rodrigues Gomes, R.; Goulin, E.H.; Da Costa Senkiv, C.; Ossamu Tanaka, F.A.; Rodrigues Almeida, A.M.; Galli-Terasawa, L.; Kava, V.; Glienke, C. Diaporthe endophytica and D. terebinthifolii from medicinal plants for biological control of Phyllosticta citricarpa. Microbiol. Res. 2016, 186, 153–160. [Google Scholar] [CrossRef]
- Hartley, S.E.; Gange, A.C. Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Ann. Rev. Entomol. 2009, 54, 323–342. [Google Scholar] [CrossRef]
- Eberl, F.; Uhe, C.; Unsicker, S.B. Friend or foe? The role of leaf-inhabiting fungal pathogens and endophytes in tree-insect interactions. Fungal Ecol. 2019, 38, 104–112. [Google Scholar] [CrossRef]
- Martinuz, A.; Schouten, A.; Menjivar, R.D.; Sikora, R.A. Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biol. Control 2012, 62, 206–212. [Google Scholar] [CrossRef]
- Bogner, C.W.; Kamdem, R.S.; Sichtermann, G.; Matthäus, C.; Hölscher, D.; Popp, J.; Proksch, P.; Grundler, F.M.; Schouten, A. Bioactive secondary metabolites with multiple activities from a fungal endophyte. Microb. Biotechnol. 2017, 10, 175–188. [Google Scholar] [CrossRef] [PubMed]
- Brakhage, A.A.; Schroeckh, V. Fungal secondary metabolites–strategies to activate silent gene clusters. Fungal Genet. Biol. 2011, 48, 15–22. [Google Scholar] [CrossRef] [PubMed]
- Deepika, V.B.; Murali, T.S.; Satyamoorthy, K. Modulation of genetic clusters for synthesis of bioactive molecules in fungal endophytes: A review. Microbiol. Res. 2016, 182, 125–140. [Google Scholar] [CrossRef] [PubMed]
- Kumaran, R.S.; Muthumary, J.; Hur, B.K. Taxol from Phyllosticta citricarpa, a leaf spot fungus of the angiosperm Citrus medica. J. Biosci. Bioeng. 2008, 106, 103–106. [Google Scholar] [CrossRef] [PubMed]
- Nicoletti, R.; Fiorentino, A. Antitumor metabolites of fungi. Curr. Bioact. Comp. 2014, 10, 207–244. [Google Scholar] [CrossRef]
- Savi, D.C.; Shaaban, K.A.; Mitra, P.; Ponomareva, L.V.; Thorson, J.S.; Glienke, C.; Rohr, J. Secondary metabolites produced by the citrus phytopathogen Phyllosticta citricarpa. J. Antibiot. 2019, 72, 306–310. [Google Scholar] [CrossRef]
- Buckel, I.; Andernach, L.; Schüffler, A.; Piepenbring, M.; Opatz, T.; Thines, E. Phytotoxic dioxolanones are potential virulence factors in the infection process of Guignardia bidwellii. Sci. Rep. 2017, 7, 8926. [Google Scholar] [CrossRef] [Green Version]
- Yuan, W.H.; Liu, M.; Jiang, N.; Guo, Z.K.; Ma, J.; Zhang, J.; Song, Y.C.; Tan, R.X. Guignardones A–C: Three meroterpenes from Guignardia mangiferae. Eur. J. Org. Chem. 2010, 33, 6348–6353. [Google Scholar] [CrossRef]
- Guimarães, D.O.; Lopes, N.P.; Pupo, M.T. Meroterpenes isolated from the endophytic fungus Guignardia mangiferae. Phytochem. Lett. 2012, 5, 519–523. [Google Scholar] [CrossRef]
- Han, W.B.; Dou, H.; Yuan, W.H.; Gong, W.; Hou, Y.Y.; Ng, S.W.; Tan, R.X. Meroterpenes with toll-like receptor 3 regulating activity from the endophytic fungus Guignardia mangiferae. Planta Med. 2015, 81, 145–151. [Google Scholar] [CrossRef] [Green Version]
- Sun, Z.H.; Liang, F.L.; Wu, W.; Chen, Y.C.; Pan, Q.L.; Li, H.H.; Ye, W.; Liu, H.X.; Li, S.N.; Tan, G.H.; et al. Guignardones P–S, new meroterpenoids from the endophytic fungus Guignardia mangiferae A348 derived from the medicinal plant smilax glabra. Molecules 2015, 20, 22900–22907. [Google Scholar] [CrossRef] [Green Version]
- Chen, K.; Zhang, X.; Sun, W.; Liu, J.; Yang, J.; Chen, C.; Liu, X.; Gao, L.; Wang, J.; Li, H.; et al. Manginoids A–G: Seven monoterpene–shikimate-conjugated meroterpenoids with a spiro ring system from Guignardia mangiferae. Org. Lett. 2017, 19, 5956–5959. [Google Scholar] [CrossRef]
- Li, T.X.; Yang, M.H.; Wang, X.B.; Wang, Y.; Kong, L.Y. Synergistic antifungal meroterpenes and dioxolanone derivatives from the endophytic fungus Guignardia sp. J. Nat. Prod. 2015, 78, 2511–2520. [Google Scholar] [CrossRef]
- Eze, P.M.; Ojimba, N.K.; Abonyi, D.O.; Chukwunwejim, C.R.; Abba, C.C.; Okoye, F.B.C.; Esimone, C.O. Antimicrobial activity of metabolites of an endophytic fungus isolated from the leaves of Citrus jambhiri (Rutaceae). Trop. J. Nat. Prod. Res. 2018, 2, 145–149. [Google Scholar] [CrossRef]
- Doty, S.L. Growth-promoting endophytic fungi of forest trees. In Endophytes of Forest Trees; Pirttilä, A., Frank, A., Eds.; Springer: Berlin, Germany, 2011; pp. 151–156. [Google Scholar]
- Waqas, M.; Khan, A.L.; Kamran, M.; Hamayun, M.; Kang, S.M.; Kim, Y.H.; Lee, I.J. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 2012, 17, 10754–10773. [Google Scholar] [CrossRef]
- Suwannarach, N.; Kumla, J.; Bussaban, B.; Nuangmek, W.; Matsui, K.; Lumyong, S. Biofumigation with the endophytic fungus Nodulisporium spp. CMU-UPE34 to control postharvest decay of citrus fruit. Crop Prot. 2013, 45, 63–70. [Google Scholar] [CrossRef]
- Gomes, A.A.M.; Queiroz, M.V.; Pereira, O.L. Mycofumigation for the biological control of post-harvest diseases in fruits and vegetables: A review. Austin J. Biotechnol. Bioeng. 2015, 2, 1051. [Google Scholar]
- Kaddes, A.; Fauconnier, M.L.; Sassi, K.; Nasraoui, B.; Jijakli, M.H. Endophytic fungal volatile compounds as solution for sustainable agriculture. Molecules 2019, 24, 1065. [Google Scholar] [CrossRef] [Green Version]
- Huang, Z.; Yang, J.; Cai, X.; She, Z.; Lin, Y. A new furanocoumarin from the mangrove endophytic fungus Penicillium sp. (ZH16). Nat. Prod. Res. 2012, 26, 1291–1295. [Google Scholar] [CrossRef]
- Zaher, A.M.; Moharram, A.M.; Davis, R.; Panizzi, P.; Makboul, M.A.; Calderón, A.I. Characterisation of the metabolites of an antibacterial endophyte Botryodiplodia theobromae Pat. of Dracaena draco L. by LC–MS/MS. Nat. Prod. Res. 2015, 29, 2275–2281. [Google Scholar] [CrossRef]
- Balakumaran, M.D.; Ramachandran, R.; Kalaichelvan, P.T. Exploitation of endophytic fungus, Guignardia mangiferae for extracellular synthesis of silver nanoparticles and their in vitro biological activities. Microbiol. Res. 2015, 178, 9–17. [Google Scholar] [CrossRef]
- Busby, P.E.; Ridout, M.; Newcombe, G. Fungal endophytes: Modifiers of plant disease. Plant Mol. Biol. 2016, 90, 645–655. [Google Scholar] [CrossRef]
- Schlaeppi, K.; Bulgarelli, D. The plant microbiome at work. Mol. Plant Microbe Interact. 2015, 28, 212–217. [Google Scholar] [CrossRef]
- Ahlholm, J.U.; Helander, M.; Henriksson, J.; Metzler, M.; Saikkonen, K. Environmental conditions and host genotype direct genetic diversity of Venturia ditricha, a fungal endophyte of birch trees. Evolution 2002, 56, 1566–1573. [Google Scholar] [CrossRef]
- Balint, M.; Tiffin, P.; Hallstrom, B.; O’Hara, R.B.; Olson, M.S.; Fankhauser, J.D.; Piepenbring, M.; Schmitt, I. Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS ONE 2013, 8, e53987. [Google Scholar] [CrossRef] [Green Version]
Endophyte 1 | Plant Species | Country | Reference |
---|---|---|---|
Alternaria alternata | C. limon, C. tangelo | Florida | [46] |
Citrus spp. | Japan | [47] | |
C. limon | Argentina | [35] | |
C. reticulata | Iran | [48] | |
Alternaria brassicicola | C. reticulata | Iran | [48] |
Alternaria carthami | C. reticulata | Iran | [48] |
Alternaria citri | C. sinensis | Iran | [49] |
Alternaria infectoria | C. sinensis | Iran | [49] |
Alternaria rosae | C. sinensis | Iran | [49] |
Alternaria sp. | C. kotokan | Taiwan | [52] |
C. sinensis | Iran | [49] | |
Annulohypoxylon stygium | C. sinensis | Iran | [49] |
Arthrinium sp. | C. japonica | Taiwan | [52] |
Ascochyta medicaginicola | C. reticulata | Iran | [48] |
Aspergillus nidulans | C. sinensis | Iran | [49] |
Aspergillus niger | C. reticulata | Iran | [48] |
Aspergillus pallidofulvus | C. reticulata | Iran | [48] |
Aspergillus terreus | C. sinensis | Iran | [49] |
Aureobasidium iranianum | C. reticulata | Iran | [48] |
Aureobasidium melanogenum | C. reticulata | Iran | [48] |
Aureobasidium pullulans | C. sinensis | Brazil | [53] |
C. japonica | Uruguay | [54] | |
C. reticulata | Iran | [48] | |
Beauveria bassiana | C. limon | China | [55] |
Biscogniauxia mediterranea | C. sinensis | Iran | [49] |
Biscogniauxia nummularia | C. sinensis | Iran | [49] |
Bjerkandera adusta | C. sinensis | Iran | [49] |
Botryosphaeria sp. | C. aurantium | Taiwan | [52] |
Camarosporium sp. | C. aurantium, C. medica var. sarcodactylis | Taiwan | [52] |
Candida parapsilosis | C. sinensis | Brazil | [53] |
Cercospora sp. | C. limon | Cameroon | [36] |
C. sinensis | Iran | [49] | |
Chaetomium globosum | C. sinensis | Iran | [49] |
Chaetomium sp. | C. sinensis | Taiwan | [52] |
Cladosporium cladosporioides | C. reticulata | Iran | [48] |
Cladosporium sp. | C. limon, C. reshni, C. sinensis, C. sunki, C. trifoliata, C. volkameriana | Brazil | [56] |
Cladosporium xanthochromaticum | C. reticulata | Iran | [48] |
Colletotrichum boninense | C. limon | Cameroon | [36] |
C. sinensis | Iran | [49] | |
Colletotrichum fructicola | C. japonica, C. reticulata | China | [43] |
Colletotrichum gloeosporioides | C. limon, C. reshni, C. sinensis, C. sunki, C. trifoliata, C. volkameriana | Brazil | [56] |
C. limon | Argentina | [35] | |
Cameroon | [36] | ||
C. grandis, C. reticulata, C. sinensis, C. unshiu | China | [43] | |
C. sinensis | Iran | [49] | |
Colletotrichum karstii | C. grandis, C. limon | China | [43] |
Colletotrichum sp. | C. aurantium, C. medica var. sarcodactylis, C. sinensis | Taiwan | [52] |
C. deliciosa, C. reticulata | Brazil | [57] | |
C, aurantifolia | India | [58] | |
Coprinellus radians | C. sinensis | Iran | [49] |
Coprinopsis sp. | C. medica | Taiwan | [52] |
Cryptococcus flavescens | C. sinensis | Brazil | [53] |
Cryptococcus laurentii | C. sinensis | Brazil | [53] |
Cyanodermella sp. | C. medica var. sarcodactylis, Citrus sp. | Taiwan | [52] |
Diaporthe arecae s.c. 2 | C. grandis, C. limon, C. reticulata, C. sinensis, Citrus sp., C. unshiu | China | [45] |
Diaporthe biconispora2,* | C. grandis, C. japonica, C. sinensis | China | [45] |
Diaporthe biguttulata2,* | C. limon | China | [45] |
Diaporthe citri2 | C. reticulata, C. unshiu | China | [43,45] |
Diaporthe citriasiana2 | C. unshiu | China | [43] |
Diaporthe citrichinensis2 | C. grandis, C. japonica | China | [45] |
Diaporthe discoidispora2,* | C. sinensis, C. unshiu | China | [45] |
Diaporthe endophytica2 | C. limon | China | [45] |
Diaporthe eres2 | C. japonica, Citrus sp., C. unshiu | China | [45] |
Diaporthe eucalyptorum2 | C. limon | Cameroon | [36] |
Diaporthe foeniculina2 | C. sinensis | Iran | [49] |
Diaporthe hongkongensis2 | C. grandis, C. reticulata, C. sinensis, C. unshiu | China | [45] |
Diaporthe multiguttulata2,* | C. grandis | China | [45] |
Diaporthe ovalispora2,* | C. limon | China | [45] |
Diaporthe phaseolorum2 | C. limon | Cameroon | [36] |
Diaporthe sojae2 | C. limon, C. reticulata, C. unshiu | China | [45] |
Diaporthe sp. 2 | C. limon | Cameroon | [36] |
C. aurantium, C. medica, C. sinensis | Taiwan | [52] | |
C. japonica | China | [45] | |
C. reticulata | Iran | [48] | |
Diaporthe unshiuensis2,* | C. japonica | China | [45] |
Didymella microchlamydospora | C. reticulata | Iran | [48] |
Discostroma sp. | C. medica | Taiwan | [52] |
Epicoccum nigrum | C. sinensis | Iran | [49] |
Eutypella sp. | C. medica var. sarcodactylis | Taiwan | [52] |
Fusarium culmorum | C. sinensis | Iran | [49] |
Fusarium incarnatum | C. sinensis | Iran | [49] |
Fusarium oxysporum | C. reticulata | Iran | [48] |
Fusarium proliferatum | C. sinensis | Iran | [49] |
Fusarium sarcochroum | C. limon, C. reticulata | Italy, Spain | [50] |
Fusarium sp. | C. sinensis | Taiwan | [52] |
C. reticulata | Iran | [48] | |
Hanseniaspora opuntiae | C. reticulata | China | [59] |
Hypholoma fasciculare | C. sinensis | Iran | [49] |
Hypoxylon investiens | C. sinensis | Iran | [49] |
Lasiodiplodia theobromae | C. sinensis | China | [39] |
Lasmenia sp. | C. medica var. sarcodactylis | Taiwan | [52] |
Meira geulakonigae | C. paradisi | Israel | [60] |
Meyerozyma caribbica | C. reticulata | Iran | [48] |
Meyerozyma guilliermondii | C. sinensis | Brazil | [53] |
C. reticulata | China | [58] | |
Muscodor sp. | C. sinensis | Brazil | [61] |
Mycoleptodiscus sp. | C. aurantium | Taiwan | [52] |
Mycosphaerella sp. | C. limon | Cameroon | [36] |
Myrothecium sp. | C. reticulata | Iran | [48] |
Neocosmospora solani | C. reticulata | Iran | [48] |
Neosetophoma sp. | C. reticulata | Iran | [48] |
Nigrospora oryzae | C. sinensis | Iran | [49] |
Nigrospora sphaerica | C. limon | Argentina | [35] |
Nodulisporium sp. | C. limon | Argentina | [35] |
Passalora loranthi | C. limon | Cameroon | [36] |
Penicillium citrinum | C. reticulata | Iran | [48] |
Pestalotiopsis mangiferae | C. limon | Cameroon | [36] |
Pestalotiopsis microspora | C. limon | Cameroon | [36] |
Pestalotiopsis sp. | C. limon | Cameroon | [36] |
Phaeoacremonium parasiticum | C. reticulata | Iran | [48] |
Phialophora sp. | C. sinensis | Brazil | [53] |
Phoma sp. | C. limon | Cameroon | [36] |
Phyllosticta capitalensis2 | Citrus spp. | South Africa | [4] |
C. deliciosa, C. reticulata | Brazil | [57] | |
C. aurantium, C. natsudaidai, C. trifoliata | Japan | [11] | |
C. aurantium | Brazil | [62] | |
C. latifolia | Brazil | [17] | |
C. limonia, C. sinensis, Citrus sp. | Brazil | [28] | |
C. aurantium, C. australasica | Australia | [63] | |
C. limon | Cameroon | [36] | |
Italy, Malta, Spain Greece, Portugal | [27] | ||
C. aurantifolia | Italy | ||
C. sinensis | Iran | [49] | |
Phyllosticta citribraziliensis2,* | Citrus sp. | Brazil | [28] |
Phyllosticta citricarpa2 | Citrus sp. | South Africa | [64] |
C. reshni, C. sinensis, C. sunki, C. trifoliata, C. volkameriana | Brazil | [56] | |
C. deliciosa, C. reticulata | Brazil | [65] | |
C. limon | Argentina | [35] | |
C. latifolia | Brazil | [17] | |
C. sinensis | Florida | [29] | |
Phyllosticta paracapitalensis2,* | C. aurantifolia C. floridana C. limon | New Zealand Italy Spain | [27] |
C. aurantium, C. australasica, C. hystrix, C. japonica, C. maxima, C. reticulata, C. wintersii | Australia | [31] | |
Phyllosticta sp. 2 | C. medica var. sarcodactylis | Taiwan | [52] |
Physoderma citri | Citrus spp. | Florida | [51] |
Pichia kluyveri | C. reticulata | China | [59] |
Pseudocercospora sp. | C. japonica | Taiwan | [52] |
Pseudopestalotiopsis theae | C. limon | Cameroon | [36] |
Pseudozyma flocculosa | C. reticulata | Iran | [48] |
Rhodotorula dairenensis | C. sinensis | Brazil | [53] |
Rhodotorula mucilaginosa | C. sinensis | Brazil | [53] |
Rosellinia sp. | C. sinensis | Iran | [49] |
Sarocladium subulatum | C. sinensis | Iran | [49] |
Scedosporium apiospermum | C. reticulata | Iran | [48] |
Sordaria fimicola | C. sinensis | Iran | [49] |
Sporobolomyces sp. | C. sinensis | Brazil | [53] |
Sporormiella minima | C. limon | Argentina | [35] |
C. sinensis | Iran | [49] | |
Stemphylium sp. | C. aurantium, C. japonica | Taiwan | [52] |
Stenella sp. | C. limon | Cameroon | [36] |
Talaromyces purpurogenus | C. reticulata | Iran | [48] |
Talaromyces trachyspermus | C. reticulata | Iran | [48] |
Xylaria cubensis | C. sinensis | Iran | [49] |
Xylaria sp. | C. limon | Cameroon | [36] |
C. japonica | Taiwan | [52] | |
Zasmidium sp. | C. limon | Cameroon | [36] |
© 2019 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Nicoletti, R. Endophytic Fungi of Citrus Plants. Agriculture 2019, 9, 247. https://doi.org/10.3390/agriculture9120247
Nicoletti R. Endophytic Fungi of Citrus Plants. Agriculture. 2019; 9(12):247. https://doi.org/10.3390/agriculture9120247
Chicago/Turabian StyleNicoletti, Rosario. 2019. "Endophytic Fungi of Citrus Plants" Agriculture 9, no. 12: 247. https://doi.org/10.3390/agriculture9120247