Abstract
The etiology and distribution of foliar fungal diseases of citrus in Panama were studied in this work. In total, 85 orchards spanning six provinces were surveyed from 2011 to 2013. Symptoms observed ranged from yellow-brown spots on the abaxial surface of the leaves, brown lesions on petals, twig dieback as well as raised pustules on leaves and fruit. Representative fungal isolates obtained from symptomatic plant tissues were identified based on morphological characteristics, sequences of the ITS, EF1-α and TUB2 loci, and pathogenicity tests. Citrus greasy spot, caused by Zasmidium citri-griseum (=Mycosphaerella citri), was identified as the most prevalent fungal disease of citrus in Panama, confirmed in 68.2% of the orchards. Postbloom fruit drop (PFD) and Key lime anthracnose, caused by Colletotrichum acutatum sensulato, and melanose, caused by Diaporthe citri, were identified for the first time in Panama. Citrus scab, caused by Elsinoë fawcettii, was also detected. Greasy spot was found mainly in areas with a tropical monsoon climate (Am) and to a lesser extent in tropical savanna (Aw) and tropical rainforest (Af) climates. Melanose, PFD and citrus scab were detected only in areas with Am and Af climates. Information about the etiology and geographic distribution of fungal diseases in Panama will help to design effective strategies for disease management.
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References
Agostini JP, Timmer LW, Mitchell DJ (1992) Morphological and pathological characteristics of strains of Colletotrichum gloeosporioides from citrus. Phytopathology 82:1377–1382
Agostini JP, Bushong PM, Bhatia A, Timmer LW (2003) Influence of environmental factors on severity of citrus scab and melanose. Plant Dis 87:1102–1106
Aguilera-Cogley VA, Berbegal M, Català S, Brentu FC, Armengol J, Vicent A (2017) Characterization of Mycosphaerellaceae species associated with citrus greasy spot in Panama and Spain. PLoS One 12:e0189585
Agustí M, Zaragoza S, Bleiholder H, Buhr L, Hack H, Klose R, Stauss R (1997) Adaptation de l’échelle BBCH à la description des stades phénologiques des agrumes du genre Citrus. Fruits 52:287–295
Alves A, Crous PW, Correia A, Phillips AJ (2008) Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Divers 28:1–13
Bitancourt AA, Jenkins AE (1936) Elsinoë fawcetti, the perfect stage of the citrus scab fungus. Phytopathology 26:393–396
Brown AE, Sreenivasaprasad S, Timmer LW (1996) Molecular characterization of slow–growing orange and key lime anthracnose strains of Colletotrichum from citrus as C. acutatum. Phytopathology 86:523–527
CCKP, Climate Change Knowledge Portal (2018) Global Climate Data. Available at: http://sdwebx.worldbank.org/climateportal/index.cfm?page=country_historical_climate&ThisRegion=North%20America&ThisCCode=PAN. Accessed 20 July 2018
Choi YW, Hyde KD, Ho W (1999) Single spore isolation of fungi. Fungal Divers 3:28–39
Crous PW, Verkley GJM, Groenewald JZ, Samson RA (2009) Fungal biodiversity. CBS Laboratory manual series 1. Centraalbureau voor Schimmelcultures, Utrecht, 269 pp.
Damm U, Cannon PF, Woudenberg JH, Crous PW (2012) The Colletotrichum acutatum species complex. Stud Mycol 73:37–113
De Goes A, Garrido R, Reis R, Baldassari RB, Soares M (2008) Evaluation of fungicide applications to sweet orange at different flowering stages for control of postbloom fruit drop caused by Colletotrichum acutatum. Crop Prot 27:71–76
Dhingra OD, Sinclair JB (1995) Basic plant pathology methods. CRC Press Inc., Florida
Dyko BJ, Mordue JEM (1979) Colletotrichum acutatum. No. 630 in: CMI Descriptions of pathogenic fungi and bacteria. Commonwealth Mycological Institute, Kew
EPPO, European and Mediterranean Plant Protection Organization (2019) EPPO Global Database, Phyllosticta citricarpa. Available at: http://gd.eppo.int/taxon/GUIGCI. Accessed 22 May 2019
Fagan H (1979) Postbloom fruit drop, a new disease of citrus associated with a form of Colletotrichum gloeosporioides. Ann Appl Biol 91:13–20
Fan XL, Barreto RW, Groenewald JZ, Bezerra JD, Pereira OL, Cheewangkoon R, Crous PW (2017) Phylogeny and taxonomy of the scab and spot anthracnose fungus Elsinoë (Myriangiales, Dothideomycetes). Stud Mycol 87:1–41
FAO, Food and Agriculture Organization of the United Nations (2016) Crop production database FAOSTAT. Available at: http://www.fao.org. Accessed 17 July 2018
Fawcett HS (1912) The cause of stem end rot of citrus fruits (Phomopsis citri n. sp.). Phytopathology 2:109–113
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330
Hidalgo H, Sutton TB, Arauz F (1997) Epidemiology and control of citrus greasy spot on Valencia orange in the humid tropics of Costa Rica. Plant Dis 81:1015–1022
Hijmans RJ (2014) Raster: geographic data analysis and modeling. R package version 2.2–31. Available at: http://CRAN.R-project.org/package=raster
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Huang F, Chen GQ, Hou X, Fu YS, Cai L, Hyde KD, Li HY (2013a) A Colletotrichum species associated with cultivated citrus in China. Fungal Divers 61:61–74
Huang F, Hou X, Dewdney MM, Fu YS, Chen GQ, Hyde KD, Li HY (2013b) Diaporthe species occurring on citrus in China. Fungal Divers 61:237–250
Hyun JW, Paudyal DP (2015) Improved method to increase conidia production from isolates of different pathotypes of citrus scab pathogen Elsinoë spp. Res Plant Dis 21:231–234
Lima W, Sposito M, Amorim L, Gonçalves F, De Filho P (2011) Colletotrichum gloeosporioides, a new causal agent of citrus postbloom fruit drop. Eur J Plant Pathol 131:157–165
McGovern R, Seijo T, Hendricks K, Roberts P (2012) New report of Colletotrichum gloeosporioides causing postbloom fruit drop on citrus in Bermuda. Can J Plant Pathol 34:187–194
MIDA, Ministerio de Desarrollo Agropecuario de Panamá (2016) Dirección Nacional de Agricultura – Programa Nacional de Frutales
Mondal SN, Timmer LW (2006) Greasy spot, a serious endemic problem for citrus production in the Caribbean Basin. Plant Dis 90:532–538
Mondal SN, Agostini JP, Zhang L, Timmer LW (2004) Factors affecting pycnidium production of Diaporthe citri on detached citrus twigs. Plant Dis 88:379–382
Mondal SN, Bhatia A, Shilts T, Timmer LW (2005) Baseline sensitivities of fungal pathogens of fruit and foliage of citrus to azoxystrobin, pyraclostrobin, and fenbuconazole. Plant Dis 89:1186–1194
Orozco-Santos (1995) Enfermedades presentes y potenciales de los cítricos en México. Universidad Autónoma de Chapingo, México. 150 p
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644
Peres NA, Souza NL, Peever TL, Timmer LW (2004) Benomyl sensitivity of isolates of Colletotrichum acutatum and C. gloeosporioides from citrus. Plant Dis 88:125–130
Peres NA, Timmer LW, Adaskaveg JE, Correll JC (2005) Lifestyles of Colletotrichum acutatum. Plant Dis 89:784–796
Peres NA, Mackenzie SJ, Peever TL, Timmer LW (2008) Postbloom fruit drop of citrus and key lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum. Phytopathology 98:345–352
Pinho DB, Lopes UP, Pereira OL, Silveira AL, de Goes A (2015) Colletotrichum abscissum Pinho & O.L. Pereira, sp. nov. Persoonia 34:236–237
Quaedvlieg W, Binder M, Groenewald J, Summerell BA, Carnegie AJ, Burgess TI, Crous PW (2014) Introducing the consolidated species concept to resolve species in the Teratosphaeriaceae. Persoonia 33:1–40
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. Available at: http://www.R-project.org/
Rossman A, Udayanga D, Castlebury LA, Hyde KD (2013) Proposal to conserve the name Phomopsis citri HS Fawc. (Diaporthe citri), with a conserved type, against Phomopsis citri (Sacc.) Traverso & Spessa (Ascomycota: Diaporthales: Diaporthaceae). Taxon 62:627
Schubert T, Dewdney M, Peres N, Palm M, Jeyaprakash A, Sutton B, Mondal S, Wang N, Rascoe J, Picton D (2014) First report of Guignardia citricarpa associated with citrus black spot on sweet orange (Citrus sinensis) in North America. Plant Dis 98:780–789
Silva AO, Savi DC, Gomes FB, Gos FM, Silva GJ, Glienke C (2017) Identification of Colletotrichum species associated with postbloom fruit drop in Brazil through GAPDH sequencing analysis and multiplex PCR. Eur J Plant Pathol 147:731–748
Timmer LW (1999) Diseases of fruit and foliage. In: Timmer LW, Duncan LW (eds) Citrus health management. APS Press, St. Paul, pp 107–115
Timmer LW (2000a) Postbloom fruit drop. In: Timmer LW, Garnsey SM, Graham JH (eds) Compendium of citrus diseases. APS Press, St. Paul, pp 22–23
Timmer LW (2000b) Scab diseases. In: Timmer LW, Garnsey SM, Graham JH (eds) Compendium of citrus diseases. APS Press, St. Paul, pp 31–33
Timmer LW, Gottwald TR (2000) Greasy spot and similar diseases. In: Timmer LW, Garnsey SM, Graham JH (eds) Compendium of citrus diseases. APS Press, St. Paul, pp 25–28
Timmer LW, Zitko SE (1992) Timing of fungicide applications for control of postbloom fruit drop of citrus in Florida. Plant Dis 76:820–823
Timmer LW, Agostini JP, Zitko SE, Zulfiqar M (1994) Postbloom fruit drop, an increasingly prevalent disease of citrus in the America. Plant Dis 78:329–334
Timmer LW, Peever TL, Solel Z, Akimitsu K (2003) Alternaria diseases of citrus–novel pathosystems. Phytopathol Mediterr 42:99–112
Timmer LW, Mondal SN, Peres NA, Bhatia A (2004) Fungal diseases of fruit and foliage of citrus trees. In: Naqvi SMH (Eds.) Diseases of fruits and vegetables volume I (pp. 191-227). Springer Dordrecht
Traverso GB, Spessa C (1910) La flora micologica del Portugallo, Saggio. Boletim da Sociedade Broteriana 25:26–187
Udayanga D, Castlebury L, Rossman A, Hyde K (2014) Species limits in Diaporthe: molecular re-assessment of D. citri, D. cytosporella, D. foeniculina and D. rudis. Persoonia 32:83–101
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetic. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic Press, San Diego, pp 315–322
Whiteside JO (1970) Etiology and epidemiology of citrus greasy spot. Phytopathology 60:1409–1414
Whiteside JO (1974) Environmental factors affecting infection of citrus leaves by Mycosphaerella citri. Phytopathology 64:115–120
Whiteside JO (1986) Semiselective media for the isolation of Elsinöe fawcettii from citrus scab pustules. Plant Dis 70:204–206
Whiteside JO (2000) Melanosis. In: Timmer LW, Garnsey SM, Graham JH (eds) Compendium of citrus diseases. APS Press, St. Paul, pp 28–30
Acknowledgements
Research partially funded by ‘Programa de Formación de los INIA Iberoamerica’, INIA RTA2010-00105-00-00-FEDER and IDIAP 501.B.1.06. We thank J. Martínez-Minaya (UV) for assistance in the digital maps of Panama with R.
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Aguilera-Cogley, V., Vicent, A. Etiology and distribution of foliar fungal diseases of citrus in Panama. Trop. plant pathol. 44, 519–532 (2019). https://doi.org/10.1007/s40858-019-00309-9
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DOI: https://doi.org/10.1007/s40858-019-00309-9