OnlineFirst Articles
Research Papers

Occurrence and characterization of Stemphylium and Alternaria species associated with lettuce leaf spot in Algeria

PDF
  • Nabahat BESSADAT,
  • Nelly BATAILLÉ-SIMONEAU,
  • Justine COLOU,
  • Bruno HAMON,
  • Mabrouk KIHAL,
  • Philippe SIMONEAU
Nabahat BESSADAT
University of Angers, Institut Agro, INRAE, UMR IRHS, SFR QUASAV, 42 rue G. Morel, CS60057, 49071 Beaucouzé, France – Laboratoire de Microbiologie Appliquée, University Oran1 Ahmed Ben Bella, BP1524 El M’naouer, Oran 31000, Algeria
Nelly BATAILLÉ-SIMONEAU
University of Angers, Institut Agro, INRAE, UMR IRHS, SFR QUASAV, 42 rue G. Morel, CS60057, 49071 Beaucouzé, France
Justine COLOU
University of Angers, Institut Agro, INRAE, UMR IRHS, SFR QUASAV, 42 rue G. Morel, CS60057, 49071 Beaucouzé, France
Bruno HAMON
University of Angers, Institut Agro, INRAE, UMR IRHS, SFR QUASAV, 42 rue G. Morel, CS60057, 49071 Beaucouzé, France
Mabrouk KIHAL
Laboratoire de Microbiologie Appliquée, University Oran1 Ahmed Ben Bella, BP1524 El M’naouer, Oran 31000, Algeria
Philippe SIMONEAU
University of Angers, Institut Agro, INRAE, UMR IRHS, SFR QUASAV, 42 rue G. Morel, CS60057, 49071 Beaucouzé, France
DOI: https://doi.org/10.36253/phyto-16548
Categories

Published 2025-11-03

Keywords

  • Lactuca sativa,
  • morphology,
  • Pleosporaceae,
  • phylogeny,
  • Pathogenicity,
  • Foliar disease
    • ...More
    Less

How to Cite

[1]
N. BESSADAT, BATAILLÉ-SIMONEAU N., J. COLOU, B. HAMON, M. KIHAL, and P. SIMONEAU, “Occurrence and characterization of Stemphylium and Alternaria species associated with lettuce leaf spot in Algeria”, Phytopathol. Mediterr., pp. 493–512, Nov. 2025.

Copyright (c) 2025 Nabahat BESSADAT, Nelly BATAILLÉ-SIMONEAU, Justine COLOU, Bruno HAMON, Mabrouk KIHAL, Philippe SIMONEAU

Creative Commons License

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

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

Lettuce leaves (Lactuca sativa) with leaf spot symptoms were collected from an organic farm and from farm markets in Oran Province, Oran, northwest Algeria, during the 2022 and 2023 growing seasons. A total of 119 isolates with morphological characteristics of Stemphylium and Alternaria were obtained from brown necrotic lesions on lettuce leaves. Based on morphological and multi-gene sequencing analyses, these isolates were identified as Stemphylium lycopersici, S. vesicarium, S. eturmiunum, S. amaranthi, and S. gracilariae, and Alternaria in sections Alternaria and Eureka. Pathogenicity tests with 24 representative isolates were conducted on young lettuce plants under greenhouse conditions, and lesions similar to those observed on the field and market collected plants developed on leaves of inoculated plants. Stemphylium gracilariae and S. lycopersici were the most aggressive fungi, causing extensive leaf necroses and defoliation, while other Stemphylium and Alternaria isolates develop small necrotic spots on mature leaves. A series of cross-inoculation experiments compared disease severity when plants were inoculated with one of four Stemphylium species alone or paired with one of five Alternaria isolates (20 combinations total). Differences in pathogenicity of mixed inoculations compared to single inoculation were detected, but synergistic increases in leaf spot severity were not detected for any mixed inoculations. These results demonstrate the potential of emerging fungal pathogens to cause lettuce leaf spot, and that Stemphylium and Alternaria species combinations can damage economically important lettuce crops.

PDF

Downloads

Download data is not yet available.

References

  1. Algeria Climate Fact Sheet (2023) IFRC. 12pp. Available at: https://prddsgofilestorage.blob.core.windows.net/api/documents/Algeria_Climate_Fact_Sheet/Algeria_Climate_Fact_Sheet_EN.pdf Accessed January5, 2025.
  2. Al Ghafri A., Maharachchikumbura S., Hyde K., Al-Saady N. Al-Sadi A., 2019. A new section and a new species of Alternaria encountered from Oman. Phytotaxa 405: 279–289. https://doi.org/10.11646/phytotaxa.405.6.1
  3. Ariyawansa H. A., Thambugala K. M., Manamgoda D. S., Jayawardena R., Camporesi E., … Hyde K. D., 2015. Towards a natural classification and backbone tree for Pleosporaceae. Fungal Diversity 71: 85–139. https://doi.org/10.1007/s13225-015-0323-z
  4. Basallote-Ureba M. J., Prados-Ligero A. M., Melero-Vara J. M., 1999. Aetiology of leaf spot of garlic and onion caused by Stemphylium vesicarium in Spain. Plant Pathology 48: 139–145. https://doi.org/10.1046/j.1365-3059.1999.00313.x
  5. Berbee M. L., Pirseyedi M., Hubbard S., 1999. Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia 91: 964–977. https://doi.org/10.1080/00275514.1999.12061106
  6. Bessadat N., Berruyer R., Hamon B., Bataillé-Simoneau N., Benichou S., … Simoneau, P., 2017. Alternaria species associated with early blight epidemics on tomato and other Solanaceae crops in northwestern Algeria. European Journal of Plant Pathology 148: 181–197. https://doi.org/0.1007/s10658-016-1081-9.
  7. Bessadat N., Hamon B., Bataillé-Simoneau N., Colou J., Kihal M., Simoneau P., 2022. Characterization of Stemphylium spp. Associated with tomato foliar diseases in Algeria. Phytopathologia Mediterranea 61(1): 39– 53. https://doi.org/10.36253/phyto-13033
  8. Bessadat N., Hamon B., Bataillé-Simoneau N., Kihal M., Simoneau P., 2019. Alternaria foliar diseases of solanaceous crops in Algeria: a multi-species threat? Acta Horticulturae 1257: 63–72. https://doi.org/10.17660/ActaHortic.2019.1257.10
  9. Blancard D., 2021. Salads: Diseases and Pests. Ephytia - INRAE. Available at: http://ephytia.inra.fr/en/C/5360/Salads-Salads-List-of-diseases-and-pests Accessed August 28, 2025.
  10. Brahamanage R. S., Hyde K. D., Li X. H., Jayawardena R. S., McKenzie E. H. C., Yan J. Y., 2018. Are pathogenic isolates of Stemphylium host specific and cosmopolitan? Plant Pathology Quarantine 8(2): 153–164. https://doi.org/10.5943/ppq/8/2/7
  11. Brahmanage R., Wanasinghe D., Dayarathne M., Jeewon R., Yan J., … Li X., 2019. Morphology and phylogeny reveal Stemphylium dianthi sp. nov. and new host records for the sexual morphs of S. beticola, S. gracilariae, S. simmonsii and S. vesicarium from Italy and Russia. Phytotaxa 411: 243–263. https://doi.org/10.11646/phytotaxa.411.4.1
  12. Câmara M. P., O’Neill N. R., Van Berkum P., 2002. Phylogeny of Stemphylium spp. based on ITS and glyceraldehyde– 3–phosphate dehydrogenase gene sequences. Mycologia 94: 660–672. https://doi.org/10.1080/15572536.2003.11833194
  13. Campbell C. L., Madden L. V., 1990. Introduction to Plant Disease Epidemiology. John Wiley & Sons, New York City. Available at: https://www.rdocumentation.org/packages/agricolae/versions/1.3-7/topics/audpc. Accessed January 30, 2025.
  14. Crous P.W., Cowan D. A., Maggs-Kolling G., Yilmaz N., Larsson E., … Groenewald J. Z., 2020. Fungal Planet description sheets: 1112–1181. Persoonia 45: 251–409. https://doi.org/10.3767/persoonia.2020.45.10
  15. D’Amico M., Frisullo S., Cirulli M., 2008. Endophytic fungi occurring in fennel, lettuce, chicory, and celery — commercial crops in southern Italy. Mycological Research 112(1): 100–107. https://doi.org/10.1016/j.mycres.2007.11.007
  16. Damialis A., Kaimakamis E., Konoglou M. Akritidis I., Traidl‐Hoffmann C., Gioulekas, D., 2017. Estimating the abundance of airborne pollen and fungal spores at variable elevations using an aircraft: how high can they fly? Scientific Reports 7: 44535. https://doi.org/10.1038/srep44535
  17. Das A., Dutta S., Jash S., Barman A. R., Das R., Kumar S., Gupta S., 2019. Current Knowledge on Pathogenicity and Management of Stemphylium botryosum in Lentils (Lens culinaris ssp. culinaris Medik). Pathogens 8: 225. https://doi.org/10.3390/pathogens8040225
  18. De Mers M., 2022. Alternaria alternata as endophyte and pathogen. Microbiology 168: 3. https://doi.org/10.1099/MIC.0.001153
  19. Faraway J. J., 2002. Practical Regression and Anova using R. The R project. Available at: https://cran.r-project.org/doc/contrib/Faraway-PRA.pdf. Accessed December 10, 2024, from
  20. Farr D.F., Rossman, A.Y., 2017. Fungal databases, U.S. National Fungus Collections. U.S. Department of Agriculture, Agricultural Research Service. https://nt.ars-grin.gov/fungaldatabases/
  21. Fearnley-Whittingstall H., 2013. Grilled lettuce with goats’ cheese. BBC. Available at: https://www.bbc.co.uk/food/recipes/grilledlettucewithgo_14300. Accessed October 6, 2023.
  22. Gannibal P. B., Orina A. S., Gasich E. L., 2022. A new section for Alternaria helianthiinficiens found on sunflower and new asteraceous hosts in Russia. Mycological Progress 21: 34. https://doi.org/10.1007/s11557-022-01780-6
  23. González M., Barilli E., Rispail N., Rubiales D., 2024. Optimization of inoculum production of Stemphylium botryosum for large-scale resistance screening of lentils. Plant Methods 20: 51. https://doi.org/10.1186/s13007-024-01177-4
  24. Gossen B. D., Tayviah C. S., McDonald M. R., 2021. The Role of Ascospores and Conidia, in Relation to Weather Variables, in the Epidemiology of Stemphylium Leaf Blight of Onion. Plant Disease 105(7): 1912–1918. https://doi.org/10.1094/PDIS-06-20-1283-RE
  25. Grewling Ł., Bogawski P., Szymańska A., Nowak M., Kostecki Ł., Smith, M., 2020. Particle size distribution of the major Alternaria alternata allergen, Alt a 1, derived from airborne spores and subspore fragments. Fungal Biology 124(3-4): 219–227. https://doi.org/10.1016/j.funbio.2020.02.005
  26. Grum-Grzhimaylo A. A., Georgieva M. L., Bondarenko S. A., Debets A. J. M., Bilanenko, E. N., 2016. On the diversity of fungi from soda soils. Fungal Diversity 76(1): 27–74. https://doi.org/10.1007/s13225-015-0320-2
  27. Gullino M. L., Gilardi G., Garibaldi A., 2019. Ready-to-Eat Salad Crops: A Plant Pathogen’s Heaven. Plant Disease 103(9): 2153–2170. https://doi.org/10.1094/PDIS-03-19-0472-FE
  28. Guo R. T., Shi Y. X., Zhao Q., Li B. J., 2018. Identification of the pathogens causing leaf spot on lettuce. Acta Phytopathologia Sinica 48(3): 418–422. https://doi.org/10.13926/j.cnki.apps.000131
  29. Gutiérez-Rodriguez A., Postigo I., Guisantes A. J., Sunen E., Martinez J., 2011. Identification of allergens homologous to Alt a 1 from Stemphylium botryosum and Ulocladium botrytis. Medical Mycology 49: 892–896. https://doi.org/10.3109/13693786.2011.576350
  30. Hay F., Stricker S., Gossen B. D., McDonald M. R., Heck D., … Pethybridge S., 2021. Stemphylium Leaf Blight: A Re-Emerging Threat to Onion Production in Eastern North America. Plant Disease 105(12): 3780–3794. https://doi.org/10.1094/PDIS-05-21-0903-FE
  31. Inderbitzin P., Mehta Y. R., Berbee M. L. 2009. Pleospora species with Stemphylium anamorphs: a four locus phylogeny resolves new lineages yet does not distinguish among species in the Pleospora herbarum clade. Mycologia 101: 329–339. https://doi.org/10.3852/08-071
  32. Institut Technique des Cultures Maraîchères et Industrielles. 2010. Fiches techniques valorisées des cultures maraichères et industrielles, La culture de Laitue. Available at: https://itcmi-dz.org/wp-content/uploads/2022/06/LAITUE.pdf. Accessed January 5, 2025.
  33. Kalyaanamoorthy S., Minh B., Wong T., von Haeseler A., Jermiin, L. S., 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14(6): 587–589. https://doi.org/10.1038/nmeth.4285
  34. Katz S. H., Weaver W.W., 2003. Encyclopedia of food and culture. Scribner. 376 pp.
  35. Kim M. J., Moon Y., Tou J. C., Mou B., Waterland, N. L., 2016. Nutritional value, bioactive compounds and health benefits of lettuce (Lactuca sativa L.). Journal of Food Composition and Analysis 49: 19–34. https://doi.org/10.1016/j.jfca.2016.03.004
  36. Kim B.S., Yu S.H., Cho H.J., Hwang H.S., 2004. Gray leaf spot in peppers caused by Stemphylium solani and S. lycopersici. The Plant Pathology Journal 20, 85–91. https://doi.org/10.5423/PPJ.2004.20.2.085
  37. Koike S. T., Smith R. F., Cahn M. D., Pryor B. M., 2017. Association of the carrot pathogen Alternaria dauci with new diseases, Alternaria leaf speck, of lettuce and celery in California. Plant Health Progress 18(2): 136–143. https://doi.org/10.1094/PHP-12-16-0074-RS
  38. Kornerup A., Wanscher J. H., 1978. Methuen Handbook of Colour, 3rd ed. Methuen, London, UK. 252pp.
  39. Kumar S., Stecher G., Tamura K., 2016. MEGA 7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054
  40. Lahlali R., Taoussi M., Laasli S. E., Gachara G., Ezzouggari R., … Ait Barka, E., 2024. Effects of climate change on plant pathogens and host-pathogen interactions. Crop Environment 3(3): 159–170. https://doi.org/10.1016/j.crope.2024.05.003
  41. Lallouche B., Hadj Kouider B., Belloudah A., Ben Madani R., Boutekrabt A., 2020. Phenotypic characterization of some lettuce cultivars (Lactuca sativa L.) cultivated in Algeria. Revue Agrobiologia 10(1): 1787–96.
  42. Lamichhane J. R., Venturi V., 2015. Synergisms between microbial pathogens in plant disease complexes: a growing trend. Front Plant Sci. 27(6): 385. https://doi.org/10.3389/fpls.2015.00385. PMID: 26074945; PMCID: PMC4445244.
  43. Lawrence D. P., Gannibal P. B., Peever T. L., Pryor B. M., 2013. The sections of Alternaria: Formalizing species-groups concepts. Mycologia 105: 530–546. https://doi.org/10.3852/12-249
  44. Letunic I., Bork P., 2024. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Research 52: 78–82. https://doi.org/10.1093/nar/gkae268
  45. Li J., Jiang H., Jeewon R., Hongsanan S., Bhat D. J., … Phookamsak R., 2023. Alternaria: update on species limits, evolution, multi-locus phylogeny, and classification. Studies in Fungi 8: 1. https://doi.org/10.48130/SIF-2023-0001
  46. Liu H., Wang H., Zhong J., Lu X., Pan X., T. … Zhou Q., 2019. First Report of Stemphylium lycopersici and Stemphylium vesicarium causing Leaf Spot on Lettuce (Lactuca sativa) in China. Plant Disease 103(11): 2957. https://doi.org/10.1094/PDIS-05-19-1052-PDN
  47. Manaaki Whenua - Landcare Research., 2023. New Zealand Fungi Names Databases - Stemphylium lycopersici (Enjoji) W. Yamam. 1960. Available at: https://BiotaNZ.landcareresearch.co.nz/scientific-names/1cb1a5ca-36b9-11d5-9548-00d0592d548c. Accessed October 4, 2023.
  48. Marin-Felix Y., Hernandez-Restrepo M., Iturrieta- Gonzalez I., Garcia D., Gene J., … Crous P. W., 2019. Genera of phytopathogenic fungi: GOPHY 3. Studies in Mycology 94: 1–124. https://doi.org/10.1016/j.simyco.2019.05.001
  49. Matić S., Tabone G., Garibaldi A., Gullino M. L., 2020. Alternaria Leaf Spot Caused by Alternaria Species: An Emerging Problem on Ornamental Plants in Italy. Plant Disease 104(8): 2275–2287. https://doi.org/10.1094/PDIS-02-20-0399-RE
  50. Miranda-Apodaca J., Artetxe U., Aguado I., Martin-Souto L., Ramirez-Garcia A., … Pérez-López U., 2023. Stress Response to Climate Change and Postharvest Handling in Two Differently Pigmented Lettuce Genotypes: Impact on Alternaria alternata Invasion and Mycotoxin Production. Plants 12: 1304. https:// doi.org/10.3390/plants12061304
  51. Mishra S., Srivastava A., Singh A., Pandey G. C., Srivastava G., 2024. An overview of symbiotic and pathogenic interactions at the fungi-plant interface under environmental constraints. Frontiers in Fungal Biology 5: 1363460. https://doi.org/10.3389/ffunb.2024.1363460
  52. Moses E., Akrofi S., Beseh P., 2016. Alternaria leaf spot on lettuce-Ghana. Plantwise https://doi.org/10.1079/pwkb.20177800648
  53. Naglaa A. S. M., Safa E. E., 2020. Salts as controlling agents of lettuce leaf spot diseases. Plant Protection and Pathology Research. Zagazig Journal of Agricultural Research 47 (1): 119–133. https://doi.org/10.21608/zjar.2020.70230
  54. Nasehi A., Kadir J. B., Esfahani M. N., Mahmodi F., Ghadirian H., … Soleimani N., 2013. Leaf Spot on Lettuce (Lactuca sativa) Caused by Stemphylium solani, a New Disease in Malaysia. Plant Disease 97(5): 689. https://doi.org/10.1094/PDIS-10-12-0902-PDN
  55. Nasehi A., Kadir J. B., Nasr-Esfahani M., Abed-Ashtiani F., Wong M. Y., … Golkhandan E., 2014. Analysis of genetic and virulence variability of Stemphylium lycopersici associated with leaf spot of vegetable crops. European Journal of Plant Pathology 140: 261–273. https://doi.org/10.1007/s10658-014-0460-3
  56. Nguyen L. T., Schmidt H. A., von Haeseler A., Minh B. Q., 2015. Minh, B.Q. IQ-Tree: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 532(1): 268–6274. https://doi.org/10.1093/molbev/msu300
  57. Nischwitz C., 2016. Purple blotch and Stemphylium leaf blight. In: Cannon C ed. Utah vegetable production and pest management guide. Utah State University IPM Program, Logan, UT 84322. pp. 103–104.
  58. O’Neill T., 2019. Diseases of lettuce crops. AHDB Horticulture, Stoneleigh Park, Kenilworth, Warwickshire, CV8 2TL. 28 pp. Available at: https://projectblue.blob.core.windows.net/media/Default/Imported%20Publication%20Docs/AHDB%20Horticulture%20/LettuceDiseases1846_190109_WEB.pdf. Accessed October 4, 2023.
  59. Olsen K. J. K., Rossman A., Andersen B., 2018. Metabolite production by species of Stemphylium. Fungal Biology 122(2-3): 172–181. https://doi.org/10.1016/j.funbio.2017.12.012
  60. Padhi S., Panda M. K., Das D., Tayung K., 2015. ITS2 RNA secondary structure analysis reveals close affinity between endophytic and pathogenic fungi: a case study in Fusarium species. Annals of Microbiology 66: 625–633. https://doi.org/10.1007/s13213-015-1142-x
  61. Pathak M., Barik S., Dash S., Moharana D., 2023. Impact of Climate Change on Leafy and Salad Vegetables Production. In: Solankey S.S., Kumari M. (eds) Advances in Research on Vegetable Production Under a Changing Climate Vol. 2. Advances in Olericulture. Springer, Cham. https://doi.org/10.1007/978-3-031-20840-9_5
  62. Pegg K., Duff J., Manners A. 2014. Alternaria diseases in production nurseries. Agri-science Queensland, Department of Agriculture, Fisheries and Forestry (DAFF). Available at: https://www.vegkit.com.au/globalassets/hort-innovation/resource-assets/ny11001-alternaria-diseases.pdf. Accessed September 29, 2023.
  63. Pei Y. F., Geng Y., Wang Y., Zhang X. G., 2009. Two new species of Stemphylium from Sinkiang, China. Mycotaxon 109: 493–497. https://doi.org/10.5248/109.493
  64. Poursafar A., Ghosta Y., Javan-Nikkhah M., 2018. An emended description of Stemphylium amaranthi with its first record for Iran mycobiota. Phytotaxa 371: 93. https://doi.org/10.11646/phytotaxa.371.2.3
  65. Pryor M. B., Gilbertson R. L., 2000. Molecular phylogenetic relationships amongst Alternaria species and related fungi based upon analysis of nuclear ITS and mt SSU rDNA sequences. Mycological Research 104 (11): 1312–1321. https://doi.org/10.1017/S0953756200003002
  66. Roberts A. J., Punja, Z. K., 2021. Pathogenicity of seedborne Alternaria and Stemphylium species and stem-infecting Neofusicoccum and Lasiodiplodia species to cannabis (Cannabis sativa L., marijuana) plants. Canadian Journal of Plant Pathology 44(2):250–269. https://doi.org/10.1080/07060661.2021.1988712
  67. Saleemi M. K., Khan M. Z., Khan A., Javed I., Ul Hasan Z., … Mehmood M. A., 2012. Occurrence of toxigenic fungi in maize and maize-gluten meal from Pakistan. Phytopathologia Mediterranea 51(1): 219–224. https://doi.org/10.14601/Phytopathol_Mediterr-9858
  68. Samson R. A., Houbraken J., Thrane U., Frisvad J. C., Andersen B., 2010. CBS laboratory manual series 2 - Food and indoor fungi. CBS Fungal Biodiversity Centre, Utrecht, The Netherlands.
  69. Sánchez P., Vélez-del-Burgo A., Suñén E., Martínez J., Postigo I., 2022. Fungal Allergen and Mold Allergy Diagnosis: Role and Relevance of Alternaria alternata Alt a 1 Protein Family. Journal of Fungi 8(3): 277. https://doi.org/10.3390/jof8030277
  70. Schlub R. L., Hudson J., Hahn E., 2022. Foliar Pathogens in Guam: Alternaria and Stemphylium: Diseases: Early Blight, Bull’s Eye, Leaf Blight, Gray Leaf Spot. University of GUAM, Cooperative Extension & Outreach, Technical Report pp. 2–22.
  71. Shatilov N. V., Razin A. F., Ivanova M. I., 2019. Analysis of the world lettuce market. IOP Conference Series: Earth and Environmental Science 395: 012053. https://doi.org/10.1088/1755-1315/395/1/012053
  72. Simmons E.G., 1967. Typification of Alternaria, Stemphylium, and Ulocladium. Mycologia 59(1):67-92.
  73. Simmons E.G., 1969. Perfect states of Stemphylium. Mycologia 61: 1–26.
  74. Simmons E.G., 2001. Perfect states of Stemphylium—IV. Harvard Papers in Botany 199–208.
  75. Simmons E.G., 2007. Alternaria. An identification Manual. CSS Siodiversity Series Io. 6. CSS Fungal Biodiversity Centre, Utrecht, the Netherlands. 775 pp.
  76. Singh V., Shrivastava A., Jadon S., Wahi N., Singh A., Sharma N., 2015. Alternaria diseases of vegetable crops and its management control to reduce the low production. International Journal of Agriculture and Biology 7(13):834-840.
  77. Spawton K. A., du Toit L. J., 2024. Characterization of Stemphylium Species Associated with Stemphylium Leaf Spot of Spinach (Spinacia oleracea). Plant Disease 108 (12): 3578–3594. https://doi.org/10.1094/PDIS-10-23-2223-RE
  78. Subbarao K. V., Davis R. M., Gilbertson R. L., Raid R. N., 2017. Diseases of Lettuce (Lactuca sativa L.). The American Phytopathological Society (APS). Available at: https://www.apsnet.org/edcenter/resources/commonnames/Pages/Lettuce.aspx. Accessed July 26, 2023.
  79. Tao J., Cao P., Xiao Y., Wang Z., Huang Z., Jin J., Liu Y., Yin H., Liu T., Zhou Z., 2021. Distribution of the potential pathogenic Alternaria on plant leaves determines foliar fungal communities around the disease spot, Environmental Research https://doi.org/10.1016/j.envres.2021.111715
  80. Tayviah C. S., 2017. Epidemiology and management of Stemphylium leaf blight on onion (Allium cepa L.) in the Holland Marsh, Ontario. Master of Science thesis, University of Guelp. Available at: https://atrium.lib.uoguelph.ca/xmlui/bitstream/handle/10214/10430/Tayviah_CyrilSelasi_201704_MSc.pdf?sequence=1. Accessed October 4, 2023.
  81. Thomma B.P. H. J., 2003. Alternaria spp.: from general saprophyte to specific parasite. Molecular Plant Pathology 4: 225–236. https://doi.org/10.1046/j.1364-3703.2003.00173.x
  82. Velásquez A. C., Castroverde C. D. M., He S. Y., 2018. Plant-Pathogen Warfare under Changing Climate Conditions. Current Biology 21-28(10): 619–63. https://doi.org/10.1016/j.cub.2018.03.054
  83. Waheed A., Haxim Y., Islam W., Ahmad M., Muhammad M., … Zhang D., 2023. Climate change reshaping plant-fungal interaction. Environmental Research 238(2):117–282. https://doi.org/10.1016/j.envres.2023.117282
  84. Wang H., Guo Y., Luo Z., Gao L., Li R., … Chen S., 2022. Recent Advances in Alternaria Phytotoxins: A Review of Their Occurrence, Structure, Bioactivity, and Biosynthesis. Journal of Fungi 8(2):168. https://doi.org/10.3390/jof8020168
  85. White T. J., Bruns T., Lee S., Taylor J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. Academic Press, New York, 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  86. Woudenberg, J. H. C., Groenewald, J. Z., Binder, M., Crous, P. W., 2013. Alternaria redefined. Studies in Mycology 75: 171–212. https://doi.org/10.3114/sim0015
  87. Woudenberg J. H. C., Hanse B., van Leeuwen G. C. M., Groenewald J. Z., Crous P. W., 2017. Stemphylium revisited. Studies in Mycology 87: 77–103. https://doi.org/10.1016/j.simyco.2017.06.001
  88. Yang X., Gil M. I., Yang Q., Tomás-Barberán F. A., 2022. Bioactive compounds in lettuce: Highlighting the benefits to human health and impacts of preharvest and postharvest practices. Comprehensive Reviews in Food Science and Food Safety 21: 4– 45. https://doi.org/10.1111/1541-4337.12877
  89. Zhang X.G., Zhang T.Y., 2002. Taxonomic studies of Stemphylium from China I. Mycosystema 21: 324–326.

Most read articles by the same author(s)