Effects of nutritional and environmental factors on Phyllosticta citricarpa, the causal agent of citrus black spot

Sabrine Mannai, Najwa Benfradj, Naima Boughalleb-M’Hamdi

Abstract


Citrus black spot, caused by Phyllosticta citricarpa, has been reported in Tunisia since 2020 and has negatively impacted yield and marketability. The environmental conditions required for the growth of P. citricarpa remain poorly understood, limiting further biological and epidemiological studies. In the present study, the effects of different pH levels, culture media, temperatures, and citrus juices on the development of P. citricarpa were evaluated both in vitro and in vivo. The results showed significant differences in mycelial growth based on pH values, culture media, and their interaction. Mycelial growth ranged from 0 cm on OA medium at pH 5 to 7.26 cm on the same medium at pH 9, one month after incubation. Furthermore, P. citricarpa was able to grow within a temperature range of 15°C to 35°C, with optimal colony growth observed at 25°C. Among the citrus juices tested, juice from mature fruits of Citrus aurantium exhibited the strongest inhibitory effect on the mycelial growth of P. citricarpa in vitro and reduced symptom development in vivo assay. These findings enhance our understanding of the optimal conditions for P. citricarpa growth and highlight the potential of C. aurantium juice as a natural inhibitor for managing citrus black spot.


Keywords


Phyllosticta citricarpa, Citrus black spot, Mycelial growth, Environmental factors, Nutritional media

Full Text:

PDF

References


Aguilera-Cogley, V., Vicent, A. 2019. Etiology and distribution of foliar fungal diseases of citrus in Panama. Tropical Plant Pathology 44(6), 519-532.

Andrade, A. G. D., Pimenta, A. A., Goes, A. D. 2009. Influência do alinhamento de plantio na severidade da mancha-preta-dos-citros, produção e qualidade do suco. Revista Brasileira de Fruticultura 31, 1033-1041.

Benfradj, N., Mannai, S., Jeandel, C., Boughalleb‐M'Hamdi, N., 2024. Geographic distribution, prevalence, and incidence of citrus black spot caused by Phyllosticta citricarpa in Tunisia. Journal of Phytopathology 172(2), e13292.

Blank, C.A., Murray, T.D., 1998. Influence of pH and matric potential on germination of Cephalosporium gramineum conidia. Plant Disease 82, 975-978.

Boughalleb-M'Hamdi, N., Fathallah, A., Benfradj, N., Ben Mahmoud, S., Ali, B. H., Medhioub, A., Jaouadi, I., Huber, J., Jeandel, C., Ioos, R. 2020. First report of citrus black spot disease caused by Phyllosticta citricarpa on Citrus limon and C. sinensis in Tunisia. New Disease Reports, 41(1), 8.

Brodrick, H.T., Rabie, C.J., 1970. Light and temperature effects on symptom development and sporulation of Guignardia citricarpa Kiely on Citrus sinensis (Linn) Osbeck. Phytophylactica 2, 157-164.

Buijs, V. A., Zuijdgeest, X. C., Groenewald, J. Z., Crous, P. W., De Vries, R. P. 2021. Carbon utilization and growth-inhibition of citrus-colonizing Phyllosticta species. Fungal Biology 125(10), 815-825.

Campbell, R. G., Wagner, M. M., Teegarden, G. J., Boudreau, C. A., Durbin, E. G. 2001. Growth and development rates of the copepod Calanus finmarchicus reared in the laboratory. Marine Ecology Progress Series 221, 161-183.

Cánovas, M., García-Cases, L., Iborra, J.L., 1997. Shifts in metabolism and morphology of Rhodococcus fascians when debittering synthetic citrus juices in the absence of aeration. Biotechnology Letters 19, 1181-1184.

Carstens, E., Linde, C.C., Slabbert, R., Miles, A.K., Donovan, N.J., Li, H., Zhang, K., Dewdney, M.M., Rollins, J.A., Glienke, C., Schutte, G.C., Fourie, P.H., McLeod, A., 2017. A global perspective on the population structure and reproductive system of Phyllosticta citricarpa. Phytopathology 107, 758-768.

EFSA., 2014. PLH Panel (EFSA Panel on Plant Health), Scientific Opinion on the risk of Phyllosticta citricarpa (Guignardia citricarpa) for the EU territory with identification and evaluation of risk reduction options. EFSA Journal 12, 243.

Emmett, R.W., Parbery, D.G., 1975. Appressoria. Annual Review of Phytopathology 13, 147-165.

Er, H.L., Hendricks, K., Goss, E.M., Smith, M., Schubert, T.S., Roberts, P.D., van Bruggen, A.H.C., 2014. Isolation and biological characterization of Guignardia species from citrus in Florida. Journal of Plant Pathology 96, 1-13.

Fateh, F.S., Mukhtar, T., Kazmi, M.R., Abbassi, N.A., Arif, A.M., 2017. Prevalence of citrus decline in district Sargodha. Pakistan Journal of Agricultural Sciences 54, 9-13.

Ferreira, J. R., Sierra-Garcia, I. N., Guieu, S., Silva, A., da Silva, R. N., Cunha, Â. 2021. Photodynamic control of citrus crop diseases. World Journal of Microbiology and Biotechnology 37(12), 1-11.

Frare, G.F., Silva-Junior, G.J., Bassanezi, R.B., Ramires, T.G., Amorim, L., 2019. Sweet orange fruit age and inoculum concentration affect expression of citrus black spot symptoms. Plant Disease 103, 913-921.

Gareth Jones, E. B. 1994. Fungal adhesion. Mycological Research, 98961-981.

Guarnaccia, V., Groenewald, J. Z., Li, H., Glienke, C., Carstens, E., Hattingh, V., Fourie, P.H., Crous, P. 2017. First report of Phyllosticta citricarpa and description of two new species, P. paracapitalensis and P. paracitricarpa, from citrus in Europe. Studies in mycology, 87(1), 161-185.

Guarnaccia, V., Gehrmann, T., Silva-Junior, G. J., Fourie, P. H., Haridas, S., Vu, D., Spatafora, J., Martin, M., Robert, V., Grigoriev, I. V., Groenewald, J. Z., Crous, P. W. 2019. Phyllosticta citricarpa and sister species of global importance to Citrus. Molecular Plant Pathology, 20(12), 1619-1635.

Irshad, U., Mukhtar, T., Ashfaq, M., Kayani, M.Z., Kayani, S.B., Hanif, M., Aslam, S., 2012. Pathogenicity of citrus nematode (Tylenchulus semipenetrans) on Citrus jambhiri. Journal of Animal and Plant Sciences 22, 1014-1018.

Issaly, N., Chauveau, H., Aglevor, F., Fargues, J., Durand, A. 2005. Influence of nutrient, pH and dissolved oxygen on the production of Metarhizium flavoviride Mf189 blastospores in submerged batch culture. Process Biochemistry 40(3-4), 1425-1431.

Jaouad, M., Moinina, A., Ezrari, S., Lahlali, R. 2020. Key pests and diseases of citrus trees with emphasis on root rot diseases: An overview. Moroccan Journal of Agricultural Sciences 1(3).

Kiely, T.B., 1948. Preliminary studies on Guignardia citricarpa (n. sp.), the ascigerous stage of Phoma citricarpa McAlp., and its relation to black spot of citrus. Proceedings of the Linnean Society of New South Wales 73, 249-292.

Korf, H.J.G., 1998. Survival of Phyllosticta citricarpa, anamorph of the citrus black spot pathogen. University of Pretoria, Pretoria, South Africa, p. 72.

Kotzé, J.M., 1981. Epidemiology and control of citrus black spot in South Africa. Plant Disease 65, 945-950.

Kotzé, J. M. 2000. Black spot. In L. W. Timmer, S. M. Garnsey, & J. H. Graham (Eds.), Compendium of citrus diseases (2nd ed., pp. 23–25). The American Phytopathological Society.

Kuo, K., Hoch, H.C., 1996. Germination of Phyllosticta ampelicida pycnidiospores: prerequisite of adhesion to the substratum and the relationship of substratum wettability. Fungal Genetics and Biology 20, 18-29.

Lanfranchi, M., 2012. Economic analysis on the enhancement of citrus waste for energy production. Journal of Essential Oil Research 24, 583-591.

Liu, Q., Xiao, C.L., 2005. Influence of nutrient and environmental factors on conidial germination of Potebniamyces pyri. Phytopathology 95, 572-580.

Loos, R., Mannai, S., Jeandel, C., Benfradj, N., Vicent, A., Boughalleb-M’hamdi, N., Aguayo, J., 2024. Mating type and microsatellite genotyping indicate that the Tunisian population of Phyllosticta citricarpa is clonal and thrives only asexually. Fungal Biology 128, 1806-1813.

Martínez-Minaya, J., Conesa, D., López-Quílez, A., Vicent, A., 2015. Climatic distribution of citrus black spot caused by Phyllosticta citricarpa: a historical analysis of disease spread in South Africa. European Journal of Plant Pathology 143, 69-83.

Peres, N. A., Harakava, R., Carroll, G. C., Adaskaveg, J. E., Timmer, L. W. 2007. Comparison of molecular procedures for detection and identification of Guignardia citricarpa and G. mangiferae. Plant Disease 91(5), 525-531.

Saeed, M., Mukhtar, T., Rehman, M.A., 2019. Temporal fluctuations in the population of citrus nematode (Tylenchulus semipenetrans) in the Pothowar region of Pakistan. Pakistan Journal of Zoology 51, 2257-2263.

Stringari, D., Glienke, C., Christo, D. D., Maccheroni Jr, W., Azevedo, J. L. D. 2009. High molecular diversity of the fungus Guignardia citricarpa and Guignardia mangiferae and new primers for the diagnosis of the citrus black spot. Brazilian archives of biology and technology 52, 1063-1073.

Vogelgsang, S., Shamoun, S.F., 2002. Growth, sporulation, and conidia discharge of Valdensinia heterodoxa, a foliar pathogen of salal, as influenced by temperature and photoperiod in vitro. Mycological Research 106, 480-490.

Wang, N.Y., Dewdney, M.M., 2015. The effect of relative humidity on colonization of citrus twigs by Phyllosticta citricarpa, the citrus black spot pathogen. Phytopathology 105, 145-146.

Wang, N.Y., Dewdney, M.M., 2019. The effects of nutrition and environmental factors on conidial germination and appressorium formation of Phyllosticta citricarpa, the causal agent of citrus black spot. Phytopathology 109, 650-658.

Zimmermannová-Pastirčáková, K., 2002. Occurrence of Horsechestnut leaf blotch and cultural characteristics of its causal agent-fungus Phyllosticta sphaeropsoidea, an anamorph of Guignardia aesculi. Folia Oecologica 30, 245-250.




DOI: https://doi.org/10.33804/pp.009.02.5559

Refbacks

  • There are currently no refbacks.