Vol. 62 No. 3 (2023)
Articles

A new disease of kumquat (Fortunella margarita) caused by Colletotrichum karsti: twig and branch dieback

PDF
  • Giuseppa Rosaria LEONARDI,
  • Dalia AIELLO,
  • Gaetano CAMILLERI,
  • Valeria PIATTINO,
  • Giancarlo POLIZZI,
  • Vladimiro GUARNACCIA
Giuseppa Rosaria LEONARDI
Dipartimento di Agricoltura, Alimentazione e Ambiente, sez. Patologia Vegetale, University of Catania, Via S. Sofia 100, 95123 Catania
Bio
Dalia AIELLO
Dipartimento di Agricoltura, Alimentazione e Ambiente, sez. Patologia Vegetale, University of Catania, Via S. Sofia 100, 95123 Catania
Gaetano CAMILLERI
Piante Faro S.S. Agricola di Venerando Faro & C., Via San Giuseppe 3, 95014 Giarre (CT)
Valeria PIATTINO
Centre for Innovation in the Agro-Environmental Sector, AGROINNOVA, University of Torino, Largo Braccini 2, 10095 Grugliasco (TO)
Giancarlo POLIZZI
Dipartimento di Agricoltura, Alimentazione e Ambiente, sez. Patologia Vegetale, University of Catania, Via S. Sofia 100, 95123 Catania
Vladimiro GUARNACCIA
Centre for Innovation in the Agro-Environmental Sector, AGROINNOVA, University of Torino, Largo Braccini 2, 10095 Grugliasco (TO)
DOI: https://doi.org/10.36253/phyto-14544

Published 2023-09-15

Keywords

  • Fungal disease,
  • phylogenetic analysis,
  • pathogenicity,
  • Aggressiveness

How to Cite

[1]
G. R. LEONARDI, D. AIELLO, G. CAMILLERI, V. PIATTINO, G. POLIZZI, and V. GUARNACCIA, “A new disease of kumquat (Fortunella margarita) caused by Colletotrichum karsti: twig and branch dieback”, Phytopathol. Mediterr., vol. 62, no. 3, pp. 333–348, Sep. 2023.

Copyright (c) 2023 Giuseppa Rosaria LEONARDI, Dalia AIELLO, Gaetano CAMILLERI, Valeria PIATTINO, Giancarlo POLIZZI, Vladimiro GUARNACCIA

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

Citrus fruit crops are important in many countries. Anthracnose, post bloom fruit drop, fruit stem-end rot, twig and branch dieback and gummosis, caused by Colletotrichum spp., are diseases that seriously threaten citrus production. Surveys of kumquat (Fortunella margarita) orchards were conducted in Eastern Sicily, Southern Italy, during 2022-23. Fungi isolated from twig and branch dieback of F. margarita were identified as Colletotrichum karsti through multi-locus (gapdh, tub2 and act) phylogeny. Pathogenicity and aggressiveness on detached apple fruit and kumquat plants were confirmed for a selection of representative isolates, although with different levels of disease incidence observed. This is the most comprehensive study on identification of C. karsti as the causal agent of twig and branch dieback of kumquat.

PDF

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

  1. Aiello D., Carrieri R., Guarnaccia V., Vitale A., Lahoz A., Polizzi G., 2015. Characterization and pathogenicity of Colletotrichum gloeosporioides and C. karstii causing preharvest disease on Citrus sinensis in Italy. Journal of Phytopathology 163: 168–177. https://doi.org/10.1111/jph.12299
  2. Al-Saman M.A., Abdella A., Mazrou K.E., Tayel A.A., Irmak S., 2019. Antimicrobial and antioxidant activities of different extracts of the peel of kumquat (Citrus japonica Thunb). Food Measure 13: 3221–3229. https://doi.org/10.1007/s11694-019-00244-y
  3. Baroncelli R., Zapparata A., Sarocco S., Sukno S.A., Lane C.R., … Sreenivasaprasad S., 2015. Molecular diversity of anthracnose pathogen populations associated with UK strawberry production suggests multiple introductions of three different Colletotrichum species. PLoS One 10(6): e0129140. https://doi.org/10.1371/journal.pone.0129140
  4. Bernstein B., Zehr E.I., Dean R.A., Shabi E., 1995. Characteristics of Colletotrichum from peach, apple, pecan and other hosts. Plant Disease 79: 478–482. https://doi.org/ 10.1094/PD-79-0478
  5. Bezerra J.D.P., Crous P.W., Aiello D., Gullino M.L., Polizzi G., Guarnaccia V., 2021. Genetic Diversity and Pathogenicity of Botryosphaeriaceae Species Associated with Symptomatic Citrus Plants in Europe. Plants 10: 492. https://doi.org/10.3390/plants10030492
  6. Brown A.E., Sreenivasaprasad S., Timmer L.W., 1996. Molecular characterization of slow-growing orange and key lime anthracnose strains of Colletotrichum from citrus as C. acutatum. Phytopathology 86: 523–527. https://doi.org/10.1094/Phyto-86-523
  7. Camiletti B.X., Lichtemberg P.S.L, Paredes J.A., Carraro T.A., Velascos J., Michailides T.J., 2022. Characterization of Colletotrichum Isolates Causing Colletotrichum Dieback of Citrus in California. Phytopathology 112: 1454–1466. 10.1016/j.funbio.2022.02.003
  8. Cannon P.F., Buddie A.G., Bridge P.D., 2008. The typification of Colletotrichum gloeosporioides. Mycotaxon 104: 189–204. https://nora.nerc.ac.uk/id/eprint/11421
  9. Cannon P.F., Damm U., Johnston P.R., Weir B.S., 2012. Colletotrichum – current status and future directions. Studies in Mycology 73: 181–213. https://doi.org/10.3114/sim0014
  10. Carbone I., Kohn L.M., 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556. https://doi.org/10.1080/00275514.1999.12061051
  11. Chen M.H., Yang K.M., Huang T.C., Wu M.L., 2017. Traditional Small-Size Citrus from Taiwan: Essential Oils, Bioactive Compounds and Antioxidant Capacity. Medicines 4: 28. https://doi.org/10.3390/medicines4020028
  12. Chen Y., Fu D., Wang W., Gleason M.L., Zhang R., Liang X., Sun G., 2022. Diversity of Colletotrichum species causing apple bitter rot and Glomerella leaf spot in China. Journal of Fungi 2022 8: 740. https://doi.org/10.3390/jof8070740
  13. Crous P.W., Groenewald J.Z., Slippers B., Wingfield M.J., 2016. Global food and fibre security threatened by current inefficiencies in fungal identification. Philosophical Transactions of the Royal Society 371: 1709. https://doi.org/10.1098/rstb.2016.0024
  14. Damm U., Woudenberg J.H.C., Cannon P.F., Crous P.W., 2009. Colletotrichum species with curved conidia from herbaceous hosts. Fungal Diversity 39: 45–87.
  15. Damm U., Cannon P.F., Woudenberg J.H.C., Johnston P.R., Wier B.S., … Crous P.W., 2012a. The Colletotrichum acutatum species complex. Studies in Mycology 73: 37–113. https://doi.org/10.3114/sim0010
  16. Damm U., Cannon P., Woudenberg J., Johnston P., Weir B., Tan Y., Shivas R., Crous P.W., 2012b. The Colletotrichum boninense species complex. Studies in Mycology 73: 1–36. https://doi.org/10.3114/sim0002
  17. Dean R., Van Kan J.A.L., Pretorius Z.A., Hammond-Kosack K.E., Di Pietro A., … Foster G.D., 2012. The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13: 414–430. https://doi.org/10.1111/j.1364-3703. 2011.00783.x
  18. De Silva D.D., Ades P.K., Taylor P.W.J., 2021. Pathogenicity of Colletotrichum species causing anthracnose of Capsicum in Asia. Plant Pathology 70: 875–884. https://doi.org/10.1111/PPA.13351
  19. Diéguez-Uribeondo J., Förster H., Adaskaveg, J.E., 2011. Effect of wetness duration and temperature on the development of anthracnose on selected almond tissues and comparison of cultivar susceptibility. Phytopathology 101: 1013–1020. https://doi.org/10.1094/phyto-07-10-0193
  20. FAOSTAT Online Database (available at http://faostat.fao.org/, accessed on March 2023)
  21. Freeman S., Shabi E., 1996. Cross-infection of subtropical and temperate fruits by Colletotrichum species from various hosts. Physiological and Molecular Plant Pathology 49(6): 395–404. https://doi.org/10.1006/pmpp.1996.0062
  22. Freeman S., Katan T., Shabi E., 1998. Characterization of Colletotrichum Species Responsible for Anthracnose Diseases of Various Fruits. Plant Disease 82(6): 596–605. https://doi.org/10.1094/PDIS.1998.82.6.596
  23. Giblin F.R., Coates L.M., Irwin J.A.G., 2010. Pathogenic diversity of avocado and mango isolates of Colletotrichum gloeosporioides causing anthracnose and pepper spot in Australia. Australasian Plant Pathology 39: 50–62. https://doi.org/10.1071/AP09055
  24. Glass N.L., Donaldson G.C., 1995. Development of primer sets designed for use with the PCR to amplify con served genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
  25. Guarnaccia V., Crous P.W., 2017. Emerging citrus diseases in Europe caused by species of Diaporthe. International Mycological Association Fungus 8: 317–334. https://doi.org/10.5598/imafungus.2017.08.02.07
  26. Guarnaccia V., Groenewald J.Z., Polizzi G., Crous P.W., 2017. High species diversity in Colletotrichum associated with citrus diseases in Europe. Persoonia: Molecular Phylogeny and Evolution of Fungi 39: 32–50. https://doi.org/10.3767/persoonia.2017.39.02
  27. Guarnaccia V., Gilardi G., Martino I., Garibaldi A., Gullino M.L., 2019. Species Diversity in Colletotrichum Causing Anthracnose of Aromatic and Ornamental Lamiaceae in Italy. Agronomy 9: 613. https://doi.org/10.3390/agronomy9100613
  28. Guarnaccia V., Martino I., Gilardi G. Garibaldi A., Gullino M., 2021. Colletotrichum spp. causing anthracnose on ornamental plants in northern Italy. Journal of Plant Pathology 103: 127–137. https://doi.org/10.1007/s42161-020-00684-2
  29. Guerber J.C., Liu B., Correll J.C., Johnston P.R., 2003. Characterization of diversity in Colletotrichum acutatum sensu lato by sequence analysis of two gene introns, mtDNA and intron RFLPs, and mating compatibility. Mycologia 95: 872–895. https://doi.org/10.2307/3762016
  30. Gui Q., Zhao J., Yu Z., Sun W., Mo J., … Hsiang T., 2020. First Report of Trunk Canker and Gummosis of Kumquat Caused by Lasiodiplodia theobromae in China. Plant Disease 104: 971–971. https://doi.org/10.1094/PDIS-02-19-0424-PDN
  31. Huang F., Chen G.Q., Hou X., Fu Y.S. Cai L., Hyde K.D., Li H.Y., 2013. Colletotrichum species associated with cultivated citrus in China. Fungal Diversity 61: 61–74. https://doi.org/10.1007/s13225-013-0232-y
  32. Ismail A.M., Cirvilleri G., Yaseen T., Epifani F., Perrone G., Polizzi G., 2015. Characterisation of Colletotrichum species causing anthracnose disease of mango in Italy. Journal of Plant Pathology 97(1): 167–171. http://sipav.org/…/3252
  33. 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
  34. Ko W.H., Wang I.T., Ann P.J., 2004. Lasiodiplodia theobromae as a Causal Agent of Kumquat Dieback in Taiwan. Plant Disease 88(12): 1383–1383. https://doi.org/10.1094/PDIS.2004.88.12.1383A
  35. Kumar S., Stecher G., Tamura K., 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. https://doi.org/10.1093/molbev/msw054
  36. Lakshmi B.K.M., Reddy P., Prasad R.J., 2011. Cross-infection Potential of Colletotrichum gloeosporioides Penz. Isolates Causing Anthracnose in Subtropical Fruit Crops. Tropical Agricultural Research 22: 183–193. https://doi.org/10.4038/TAR.V22I2.2827
  37. Leandro L.F.S., Gleason M.L., Nutter F.W., Wegulo S.N., Dixon P.M., 2003. Influence of temperature and wetness duration on conidia and appressoria of Colletotrichum acutatum on symptomless strawberry leaves. Phytopathology 93: 513–520. https://doi.org/10.1094/PHYTO.2003.93.4.513
  38. Lima N.B., Marques M.W., Michereff S.J., Morais M.A., Barbosa M.A.G., Câmara M.P.S., 2013. First Report of Mango Anthracnose Caused by Colletotrichum karstii in Brazil. Plant Disease 97(9): 1248–1248. https://doi.org/10.1094/PDIS-01-13-0002-PDN
  39. Lima W.G., Sposito M.B., Amorim L., Goncalves F.P., de Filho P.A.M., 2011. Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. European Journal of Plant Pathology 131: 157–165. https://doi.org/10.1007/s10658-011-9795-1
  40. Liu Y., Heying E., Tanumihardjo S.A., 2012. History, Global Distribution, and Nutritional Importance of Citrus Fruits. Food Science and Food Safety 11: 530–545. https://doi.org/10.1111/j.1541-4337.2012.00201.x
  41. Marcelino J., Giordano R., Gouli S, Gouli V., Parker B.L., … Cesnik R., 2008. Colletotrichum acutatum var. fioriniae (teleomorph: Glomerella acutata var. fioriniae var. nov.) infection of a scale insect. Mycologia 100: 353–374. https://doi.org/10.3852/07-174R
  42. Mayorquin J., Nouri M.T., Peacock B.B., Trouillas F.P., Douhan G.W., Kallsen C., Eskalen A., 2019. Identification, Pathogenicity, and Spore Trapping of Colletotrichum karstii Associated with Twig and Shoot Dieback in California. Plant Disease 103(7): 1464–1473. https://doi.org/10.1094/PDIS-08-18-1425-RE
  43. McGovern R.J., Seijo T.E., Hendricks K., Roberts P.D., 2012. New report of Colletotrichum gloeosporioides causing postbloom fruit drop on citrus in Bermuda. Canadian Journal of Plant Pathology 34: 187–194. https://doi.org/10.1080/07060661.2012.670137
  44. Moral J., Agustí-Brisach C., Agalliu G., de Oliveira R., Pérez-Rodríguez M., … Trapero A., 2018. Preliminary selection and evaluation of fungicides and natural compounds to control olive anthracnose caused by Colletotrichum species. Crop Protection 114: 167–176. https://doi.org/10.1016/J.CROPRO.2018.08.033
  45. Moriwaki J., Sato T., Tsukiboshi T., 2003. Morphological and molecular characterization of Colletotrichum boninense sp. nov. from Japan. Mycoscience 44: 47–53. https://doi.org/10.1007/S10267-002-0079-7
  46. Morton J., 1987. Kumquat. In: Fruits of Warm Climates (J.F. Morton ed.), Miami, Florida, United States of America, 182–185.
  47. Nodet P., Da Lio D., Dubreuil N., Leboulanger A., Le Floch G., 2023. First report of grapefruit rot caused by Colletotrichum gloeosporioides and C. karsti in France. Plant Disease. https://doi.org/10.1094/PDIS-04-23-0659-PDN.
  48. Nylander J.A.A., 2004. MrModeltest v. 2. Program distributed by the author. Uppsala Evolutionary Biology Centre Uppsala University.
  49. Peres N., MacKenzie S., Peever T., Timmer L.W., 2008. Postbloom fruit drop of citrus and key lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum. Phytopathology 98: 345–352. https://doi.org/10.1094/PHYTO-98-3-0345
  50. Phoulivong S., Lei C., Parinn N., Hang C., Abd-Elsalam K.A., Chukeatirot, E., Hyde K.D., 2011. A new species of Colletotrichum from Cordyline fruticosa and Eugenia javanica causing anthracnose disease. Mycotaxon 114: 247–257. https://doi.org/10.5248/114.247
  51. Piccirillo G., Carrieri R., Polizzi G., Azzaro A., Lahoz E., Fernández-Ortuño D., Vitale A., 2018. In vitro and in vivo activity of QoI fungicides against Colletotrichum gloeosporioides causing fruit anthracnose in Citrus sinensis. Scientia Horticulturae 236: 90–95. https://doi.org/10.1016/j.scienta.2018.03.044
  52. Polizzi G., Aiello D., Guarnaccia V., Vitale A., Perrone G., Stea G., 2011. First Report of Damping-Off on Strawberry Tree Caused by Colletotrichum acutatum and C. simmondsii in Italy. Plant Disease 95:1588. https://doi.org/10.1094/PDIS-07-11-0567
  53. Ramos A.P., Talhinhas P., Sreenivasaprasad S., Oliveira E., 2016. Characterization of Colletotrichum gloeosporioides, as the main causal agent of citrus anthracnose, and C. karstii as species preferentially associated with lemon twig dieback in Portugal. Phytoparasitica 44: 549–561. https://doi.org/10.1007/s12600-016-0537-y
  54. Rhaiem A, Taylor P.W., 2016. Colletotrichum gloeosporioides associated with anthracnose symptoms on citrus, a new report for Tunisia. European Journal of Plant Pathology 146: 219–224. https://doi.org/10.1007/s10658-016-0907-9
  55. Riolo M., Aloi F., Pane A., Cara M., Cacciola S.O., 2021. Twig and Shoot Dieback of Citrus, a New Disease Caused by Colletotrichum Species. Cells 10: 449. https://doi.org/10.3390/cells10020449
  56. Rios J.A., Pinho D.B., Moreira W.R., Pereira O.L., Rodrigues F.A., 2015. First report of Colletotrichum karstii causing anthracnose on blueberry leaves in Brazil. Plant Disease 99: 157–158. https://doi.org/10.1094/PDIS-07-14-0717-PDN
  57. Ronquist F., Teslenko M., Van der Mark P., Ayres D.L., Darling A., … Huelsenbeck J.P., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029.
  58. Schena L., Mosca S., Cacciola S.O., Faedda R., Sanzani S.M., … Magnano di San Lio G., 2014. Species of the Colletotrichum gloeosporioides and C. boninense complexes associated with olive anthracnose. Plant Pathology 63: 437–446. https://doi.org/10.1111/PPA.12110
  59. Shivas R.G., Tan Y.P., 2009. A taxonomic reassessment of Colletotrichum acutatum, introducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Diversity 39: 111–122.
  60. Sottile F., Del Signore M.B., Barone E., 2019. Ornacitrus: Citrus plants (Citrus spp.) as ornamentals. Folia Horticulturae 31(2): 239–251. https://doi.org/10.2478/fhort-2019-0018
  61. Swingle W.T., 1943. The botany of Citrus and its wild relatives of the orange family, in The Citrus Industry, I, Berkeley-Los Angeles, United States of America (USA).
  62. Taheri H., Javan-Nikkhah M., Elahinia S.A., Khodaparast S.A., Golmohammadi M., 2016. Species of Colletotrichum associated with citrus trees in Iran. Mycologia Iranica 3(1): 1–14. https://doi.org/10.22043/MI.2017.42395.1073
  63. Tan Q., Schnabel G., Chaisiri C., Yin L.F., Yin W.X., Luo C.X., 2022. Colletotrichum Species Associated with Peaches in China. Journal of Fungi 8: 313. https://doi.org/10.3390/jof8030313
  64. Timmer L.W., Garnsey S.M., Graham J.H., 2000. Compendium of Citrus diseases (second edition). The American Phytopathological Society. https://doi.org/10.1094/9780890545850
  65. Uysal A., Kurt Ş., 2019. First report of Colletotrichum karstii causing anthracnose on citrus in the Mediterranean region of Turkey. Journal of Plant Pathology 101: 753. https://doi.org/10.1007/s42161-018-00215-0
  66. Uysal A., Kurt Ş., Guarnaccia V., 2022. Distribution and characterization of Colletotrichum species associated with Citrus anthracnose in eastern Mediterranean region of Turkey. European Journal of Plant Pathology 163: 125–141. https://doi.org/10.1007/s10658-022-02462-5
  67. Velho A.C., Stadnik M.J., Wallhead M., 2019. Unraveling Colletotrichum species associated with Glomerella leaf spot of apple. Tropical Plant Pathology 44: 197–204. https://doi.org/10.1007/s40858-018-0261-x
  68. Veloso J.S., Lima W.G., Reis A., Doyle V.P., Michereff S.J., Câmara M.P.S., 2021. Factors influencing biological traits and aggressiveness of Colletotrichum species associated with cashew anthracnose in Brazil. Plant Pathology 70: 167– 180. https://doi.org/10.1111/ppa.13276
  69. Vitale A., Alfenas A.C., Siqueira D.L.D., Magistà D., Perrone G., Polizzi G., 2020. Cultivar resistance against Colletotrichum asianum in the world collection of mango germplasm in southeastern Brazil. Plants 9: 182. https://doi.org/10.3390/plants9020182
  70. Vitale A., Aiello D., Azzaro A., Guarnaccia V., Polizzi G., 2021. An Eleven-Year Survey on Field Disease Susceptibility of Citrus Accessions to Colletotrichum and Alternaria Species. Agriculture 11: 536. https://doi.org/10.3390/agriculture11060536
  71. Wang W., de Silva D.D., Moslemi A., Edwards J., Ades P.K., Crous P.W., Taylor P.W.J., 2021. Colletotrichum Species Causing Anthracnose of Citrus in Australia. Journal of Fungi 7: 47. https://doi.org/10.3390/jof7010047
  72. Weir B.S., Johnston P.R., Damm U., 2012. The Colletotrichum gloeosporioides species complex. Studies in Mycology 73: 115–180. https://doi.org/10.3114/sim0011
  73. Yang Y.L., Liu Z.Y., Cai L., Hyde K.D., Yu Z.N., Mckenzie E.H.C., 2009. Colletotrichum anthracnose of Amaryllidaceae. Fungal Diversity 39: 123–146.
  74. Yang Y., Cal L., Yu Z., Liu Z., Hyde K.D., 2011. Colletotrichum species on Orchidaceae in Southwest China. Cryptogamie Mycologie 32: 229–253. https://doi.org/10.7872/crym.v32.iss3.2011.229
  75. Yang H., Qiao K., Teng J., Chen J., Zhong Y., … Li H., 2023. Protease inhibitor ASP enhances freezing tolerance by inhibiting protein degradation in kumquat. Horticulture Research 10: uhad023. https://doi.org/10.1093/hr/uhad023
  76. Zhu L., Chen G.Q., Zhao X.L., Deng C.L., Hyde K.D., Li H.Y., 2013. Fusarium spp. are Responsible for Shoot Canker of Kumquat in China. Journal of Phytopathology 161: 59–62. https://doi.org/10.1111/jph.12019
  77. Zhu C., Chen P., Ye J., Li H., Huang L., … Deng X., 2022. New insights into the phylogeny and speciation of kumquat (Fortunella spp.) based on chloroplast SNP, nuclear SSR and whole-genome sequencing. Frontiers of Agricultural Science and Engineering 9(4): 627‒641. https://doi.org/10.15302/j-fase-2021436

Most read articles by the same author(s)

1 2 > >>