Alternaria Black Spot of Crucifers: Symptoms, Importance of Disease, and Perspectives of Resistance Breeding

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Alternaria Black Spot of Crucifers: Symptoms, Importance of Disease, and Perspectives of Resistance Breeding

Alternaria black spot of cruciferous vegetables, incited by different species of Alternaria, remains an increasing threat to Brassicaceae crops throughout the world, including Poland. Brassica plants are attacked by conidia of A. brassicae (Berk.) Sacc., A. brassicicola (Schw.) Wiltsh., A. raphani Groves & Skolko, and A. alternata (Fr.) Kreissler. The pathogens have a wide spectrum of hosts, such as head cabbage, Chinese cabbage, cauliflower, broccoli, and other crucifers including cultivated and wild grown plants. Alternaria pathogens usually cause damping-off of seedlings, spotting of leaves of cabbages, blackleg of heads of cabbages, and spotting of cauliflower curds and broccoli florets. In oilseed rape, A. brassicae is the dominant invasive species, while in the cruciferous vegetables, both species, A. brassicae, and A. brassicicola are encountered. Infected seeds with spores on the seed coat or mycelium under the seed coat are the main means of distribution for these pathogens. The fungus can overwinter on susceptible weeds or crop debris and on seed plants, as well as on stecklings.

Methods for disease prevention and control are based on combining agricultural management practices with chemical control. Using disease-free seeds or seeds treated with fungicides can greatly reduce disease incidence. After appearance of the first symptoms of disease, stringent fungicide spray program is an effective way to reduce losses. Many authors seem to agree, that the most economically feasible method of disease control is the development of resistant Brassicaceae crops varieties, as transgenic approach proved unsuccessful. Due to our increasing understanding of pathogen-host plant interactions, identification of resistance sources, and assessment of the resistance trait inheritance mode, breeding programs of Brassica crops for Alternaria resistance can be enhanced. This is of particular importance since recent years experience dynamic development of ecological and integrated plant production with an emphasis on plant biotic stress resistance. Highly resistant genetic resources have not been reported in Brassica cultivated species, although some varieties differ in their resistance/susceptibility level.

Strong cross-incompatibility, polygenic background of the resistance (additive and dominant gene interactions), as well as the differences in ploidy between the Brassica species of interest, render the transfer of Alternaria resistance from the wild species into the cultivated forms difficult. Additionally, it is often connected with employment of in vitro hybridization techniques, including somatic hybridization, embryo and ovary rescue, or protoplast fusion.

Bart P. H., Thomma J. 2003. Alternaria spp.: from general saprophyte to specific parasite. Molecular Plant Pathology 4(4): 225-236. [DOI: 10.1046/j.1364-3703.2003.00173.x]

Bassey E. O., Gabrielson R. L. 1983. The effects of humidity, seed infection level, temperature and nutrient stress on cabbage seedling disease caused by Alternaria brassicicola. Seed Science and Technology 11: 403-410.

Brun H., Plessis J., Renard M. 1987. Resistance of some crucifers to Alternaria brassicae (Berk.) Sacc. Proc. Seventh Int. Rapeseed Congr. Poznan, Poland: 1222-1227.

Buchwaldt L., Green H. 1992. Phytotoxicity of destruxin B and its possible role in the pathogenesis of Alternaria brassicae. Plant Pathology 41: 55-63. [DOI: 10.1111/j.1365-3059.1992.tb02316.x]

Chevre A. M., Eber F., Brun H., Plessis J., Primard C., Renard M. 1991. Cytogenetic studies of Brassica napus - Sinapsis alba hybrids from ovary culture and protoplast fusion. Attempts to introduce Alternaria resistance into rapeseed. Proceedings of International Rapeseed Conference 8: 346-351.

Chirco E. M., Harman G. E. 1979. The effects of Alternaria brassicicola infection on Brassica seed vigor and viability. Journal of Seed Technology 3: 12-22.

Conn K. L., Tewari J. P. 1986. Hypersensitive reaction induced by Alternaria brassicae in Eruca sativa, an oil-yielding crucifer. Canadian Journal of Plant Pathology 8: 348.

Conn K. L., Tewari J. P., Dahiya J. S. 1988. Resistance to Alternaria brassicae and phytoalexins-elicitation in rapeseed and other crucifers. Plant Science 56: 21-25. [DOI: 10.1016/0168-9452(88)90180-X]

Degenhardt K. J., Petrie G. A., Morrall R. A. A. 1982. Effects of temperature on spore germination and infection of rapeseed by Alternaria brassicae, A. brassicicola, and A. raphani. Canadian Journal of Plant Pathology 4: 115-118. [DOI: 10.1080/07060668209501311]

Doullah M. A. U., Meah M. B., Okazaki K. 2006. Development of an effective screening method for partial resistance to Alternaria brassicicola (dark leaf spot) in Brassica rapa. European Journal of Plant Pathology 116: 33-43. [DOI: 10.1007/s10658-006-9035-2]

Fahleson J., Rahlen L., Glimelius K. 1988. Analysis of plants regenerated from protoplast fusions between Brassica napus and Eruca sativa. Theoretical and Applied Genetics 76(4): 507-512. [DOI: 10.1007/BF00260900]

Hansen L. H. 1998. Intertribal somatic hybridization between rapid cycling Brassica oleracea (L.) and Camelina sativa (L) Cranz. Euphytica 104: 173-179. [DOI: 10.1023/A:1018604919488]

Hansen L. H., Earle E. D. 1995. Transfer of resistance to Xanthomonas campestris pv. campestris (L.) by protoplast fusion. Theoretical and Applied Genetics 91: 1293-1300. [DOI: 10.1007/BF00220944]

Hansen L. H., Earle E. D. 1997. Somatic hybrids between Brassica oleracea (L.) and Sinapis alba (L.) with resistance to Alternaria brassicae (Berk.) Sacc. Theoretical and Applied Genetics 94: 1078-1085. [DOI: 10.1007/s001220050518]

Ho W. C., Wu T. Y., Su H. J., Ko W. H. 2007. Effect of oriental medicinal plant extracts on spore germination of Alternaria brassicicola and nature of inhibitory substances from speedweed. Plant Disease 91: 1621-1624. [DOI: 10.1094/PDIS-91-12-1621]

Humpherson-Jones F. M. 1989. Survival of Alternaria brassicae and Alternaria brassicicola on crop debris of oilseed rape and cabbage. Annals of Applied Biology 115: 45-50. [DOI: 10.1111/j.1744-7348.1989.tb06810.x]

Humpherson-Jones F. M., Maude R. B. 1982. Studies on the epidemiology of Alternaria brassicicola in Brassica oleracea seed production crops. Annals of Applied Biology 100: 61-71. [DOI: 10.1111/j.1744-7348.1982. tb07192.x]

Humpherson-Jones F. M., Phelps K. 1989. Climatic factors influencing spore production in Alternaria brassicae and Alternaria brassicicola. Annals of Applied Biology 114: 449-458. [DOI: 10.1111/j.1744-7348.1989. tb03360.x]

Jiang J. J., Zhao X. X., Tian W., Li T. B., Wang Y. P. 2009. Intertribal somatic hybrids between Brassica napus and Camelina sativa with high linolenic acid contents. Plant Cell, Tissue and Organ Culture 99: 91-95. [DOI: 10.1007/s11240-009-9579-x]

Kagan I. A., Hammerschmidt R. 2002. Arabidopsis ecotype variability in camalexin production and reaction to infection by Alternaria brassicicola. Journal of Chemical Ecology 28: 2121-2140.

Kirk P. M., Cannon P. F., Minter D. W., Stalpers J. A. 2008. Dictionary of the Fungi. 10th ed. Wallingford: CABI. p. 22. ISBN 0-85199-826-7.

Kolte S. J. 1985. Diseases of annual edible oilseed crops. Vol. II, Rapeseed-mustard and sesame diseases. CRC Press Inc. Boca Raton, Florida, pp. 135.

Krishnia S. K., Saharan G. S., Singh D. 2000. Genetic variation for multiple disease resistance in the families of interspecific cross of Brassica juncea x B. carinata. Cruciferae Newsletter 22: 51-53.

Maude R. B., Humpherson-Jones F. M. 1980. Studies on the seed-borne phases of dark leaf spot (Alternaria brassicicola) and gray leaf spot (Alternaria brassicae) of brassicas. Annals of Applied Biology 95: 311-319. [DOI: 10.1111/j.1744-7348.1980.tb04752.x]

Maude R. B., Humpherson-Jones F. M., Shuring C. G. 1984. Treatments to control Phoma and Alternaria infections of brassica seeds. Plant Pathology 33: 525-535. [DOI: 10.1111/j.1365-3059.1984.tb02877.x]

Meena P. D., Awasthi R. P., Chattopadhyay C., Kolte S. J., Kumar A. 2010. Alternaria blight: a chronic disease in rapeseed-mustard. Journal of Oilseed Brassica 1(1): 1-11.

Narasimhulu S. B., Kirti P. B., Bhat S. R., Prakash S., Chopra V. L. 1994. Intergeneric protoplast fusion between Brassica carinata and Camelina sativa. Plant Cell Reports 13: 657-660. [DOI: 10.1007/BF00232940]

Nishimura S., Kohmoto K. 1983. Host-specific toxins and chemical structures from Alternaria species. Annual Review of Phytopathology 21: 87-116. [DOI: 10.1146/ 21.090183.000511]

Nowakowska M., Niezgoda A., Kozik E. U. 2011. [Alternaria disease of cabbage plants. Part I: Pathogen characteristic, symptoms and importance.] Nowości Warzywnicze/Veget. Crops News 52: 33-40 [in Polish with English summary].

Otani H., Kohnobe A., Kodama M., Kohmoto K. 1998. Production of a host-specific toxin by germinating spores of Alternaria brassicicola. Physiological and Molecular Plant Pathology 52: 285-295. [DOI: 10.1006/pmpp.1998.0147]

Otani H., Kohnobe A., Narita M., Shiomi H., Kodama M., Kohmoto K. 2001. A new type of host-selective toxin, a protein from Alternaria brassicicola. In: N. T. Keen, S. Mayama, J. E. Leach and S. Tsuyumu (Eds.). Delivery and perception of pathogen signals in plants. APS Press, St. Paul, MN, pp. 68-76.

Pace M. A., Campbell R. 1974. The effect of saprophytes on infection of leaves of Brassica spp. by Alternaria brassicicola. Transaction of the British Mycological Society 63: 193-196. [DOI: 10.1006/pmpp.1998.0147]

Parada R. Y., Sakuna E., Mori N., Oka K., Egusa M., Kodoma M., Otani H. 2008. Alternaria brassicae produces a host-specific protein toxin from germinating spores on host leaves. Phytopathology 98: 458-463. [DOI: 10.1094/PHYTO-98-4-0458]

Primard C., Vedel F., Mathieu C., Pelletier G., Chevre A. M. 1988. Interspecific somatic hybridization between Brassica napus and Brassica hirta (Sinapis alba L.) Theoretical and Applied Genetics 75: 546-552. [DOI: 10.1007/BF00289119]

Ripley V., Thorpe M., Iler S., Mizier K., Beversdorf W. D. 1992. Isozyme analysis as a tool for introgression of Sinapis alba germ plasm into Brassica napus. Theoretical and Applied Genetics 84: 403-410. [DOI: 10.1007/BF00229500]

Ryschka U., Schumann G., Klocke E., Scholze P., Neumann M. 1996. Somatic hybridization in Brassicaceae. Acta Hortic 407: 201-208.

Sharma T. R., Singh B. M. 1992. Transfer of resistance to Alternaria brassicae in Brassica juncea through interspecific hybridization among Brassica. Journal of Genetics and Breeding 46: 373-378.

Sharma G., Kumar V. D., Haque A., Bhat S. R., Prakash S., Chopra V. L. 2002. Brassica coenospecies: a rich reservoir for genetic resistance to leaf spot caused by Alternaria brassicae. Euphytica, 125, 411-417. [DOI: 10.1023/A:1016050631673]

Sigareva M. A., Earle E. D. 1997. Direct transfer of a cold-tolerant Ogura male sterile cytoplasm into cabbage (Brassica oleracea ssp. capitata) via protoplast fusion. Theoretical and Applied Genetics 94: 213-220. [DOI: 10.1007/s001220050402]

Sikdar S. R., Chatterjee G., Das S., Sen S. K. 1990. "Erussuca" the inergeneric fertile somatic hybrid developed through protoplast fusion between Eruca sativa Lam. and Brassica jencea (L.) Czern. Theoretical and Applied Genetics 79: 561-567. [DOI: 10.1007/BF00226168]

Singh B. P., Singh S. P., Mohammad A., Sinha P. P. 1992. Effect of nitrogen, phosphorus and potash on the development of Alternatria leaf spot of cabbage. Indian Phytopathology 45(2): 245.

Sodelade M., Pedras C., Khallaf I. 2012. Molecular interactions of the phytotoxins destruxin B and sirodesmin PL with crucifers and cereals. Metabolism and elicitation of plant defenses. Phytochemistry 77: 129-139. [DOI: 10.1016/j.phytochem.2012.02.010]

Survilienė E., Valiuškaitė A., Duchovskienė L., Kavaliauskaitė D. 2010. Influence of fungicide treatment on grey mould of cabbage. Vegetable Crops Research Bulletin 73: 133-142. [DOI: 10.2478/v10032-010-0025-8]

Tewari J. P. 1991a. Structural and biochemical bases of the black spot diseases of crucifers. Adv. Struc. Biol. 1: 25-34.

Tewari J. P. 1991b. Resistance to Alternaria brassicae in crucifers. Bulletin SROP 14 (6): 154-161.

Tewari J. P., Conn K. L. 1993. Reactions of some wild crucifers to Alternaria brassicae. Bulletin-OILS-SROP 16: 53-58.

Tierens K. F. M. J., Thomma B. P. H. J., Bari R. P., Garmier M., Eggermont K., Brouwer M., et al. 2002. Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defense responses by reactive oxygen generating compounds. Plant Journal 29: 131-140. [DOI: 10.1046/j.1365-313x.2002.01199.x]

Tylkowska K., Grabarkiewicz-Szczęsna J., Iwanowska H. 2003. Production of toxins by Alternaria alternata and A. radicina and their effects on germination of carrot seeds. Seed Science and Technology 31 (2): 309-316.

Tylkowska K., Korbas M., Kurzawińska H., Rataj-Guranowska M. 2004. Objawy chorób powodowanych przez grzyby rodzaju Alternaria. s. 3-11. W: "Kompendium symptomów chorób roślin oraz morfologii ich sprawców" (M. Rataj-Guranowska, red.). Bogucki Wydawnictwo Naukowe, Poznań [in Polish].

Warwick S. I. 2011. Brassicaceae in agriculture. In: Schmidt R., Bancroft I. (Eds.), Genetics and genomics of the Brassicaceae. Plant genetics and genomics: Crop models 9. Springer Science+Business Media, LLC. pp: 33-65. [DOI: 10.1007/978-1-4419-7118-0_2]

Wight W.D, Kim K.-H., Lawrence C. B., Walton J. D. 2009. Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. MPMI 22(10): 1258-1267. [DOI: 10.1094/MPMI-22-10-1258]

Zhang F. L., Xu J. B., Yan H., Li M. Y. 1997. A study on inheritance of resistance to black leaf spot in seedlings of Chinese cabbage. Acta Agriculture Borealis Sinica 12: 115-119.

Zhou N., Tootle T. L., Glazebrook J. 1999. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11: 2419-2428. [DOI: 10.2307/3870965] (print) [DOI: 10.1105/tpc.11.12.2419] (online)

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