Evaluation of Durum Wheat Genotypes for Resistance against Root Rot Disease Caused by Moroccan Fusarium culmorum Isolates |
Bouarda, Jamila
(Laboratory of Botanic, Biotechnology and Plant Protection, Department of Biology, Faculty of Science University Ibn Tofail)
Bassi, Filippo M. (International Center for Agricultural Research in the Dry Areas (ICARDA), Biodiversity and Integrated Gene Management) Wallwork, Hugh (South Australian Research and Development Institute) Benchacho, Mohammed (Laboratory of Botanic, Biotechnology and Plant Protection, Department of Biology, Faculty of Science University Ibn Tofail) Labhilili, Mustapha (Research Unit of Plant Breeding and Conservation of Plant Genetic Resources, National Institute for Agricultural Research) Maafa, Ilyass (International Center for Agricultural Research in the Dry Areas (ICARDA), Biodiversity and Integrated Gene Management) El Aissami, Aicha (Research Center in Plant and Microbial Biotechnologies, Biodiversity and Environment, Faculty of Sciences, Mohammed V University of Rabat) Bentata, Fatiha (Research Unit of Plant Breeding and Conservation of Plant Genetic Resources, National Institute for Agricultural Research) |
1 | Burgess, L. W., Backhouse, D., Summerell, B. A. and Swan, L. J. 2001. Crown rot of wheat. In: Fusarium- Paul E. Nelson Memorial Symposium, eds. by B. A. Summerell, J. F. Leslie, D. Backhouse, W. L. Bryden and L. W. Burgess, pp. 271-294. The American Phytopathological Society Press, St. Paul, MN, USA. |
2 | Chakraborty, S., Liu, C. J., Mitter, V., Scott, J. B., Akinsanmi, O. A., Ali, S., Dill-Macky, R., Nicol, J., Backhouse, D. and Simpfendorfer, S. 2006. Pathogen population structure and epidemiology are keys to wheat crown rot and Fusarium head blight management. Australas. Plant Pathol. 35:643-655. DOI |
3 | Jones, D. G. and Clifford, B. C. 1978. Cereal diseases: their pathology and control. BASF, Ipswich, UK. 279 pp. |
4 | Kang, Z. and Buchenauer, H. 1999. Immunocytochemical localization of fusarium toxins in infected wheat spikes by Fusarium culmorum. Physiol. Mol. Plant Pathol. 55:275-288. DOI |
5 | Kazan, K. and Gardiner, D. M. 2018. Fusarium crown rot caused by Fusarium pseudograminearum in cereal crops: recent progress and future prospects. Mol. Plant Pathol. 19:1547-1562. DOI |
6 | Kazan, K., Gardiner, D. M. and Manners, J. M. 2012. On the trail of a cereal killer: recent advances in Fusarium graminearum pathogenomics and host resistance. Mol. Plant Pathol. 13:399-413. DOI |
7 | Kosiak, B., Torp, M., Skjerve, E. and Thrane, U. 2003. The prevalence and distribution of Fusarium species in Norwegian cereals: a survey. Acta Agric. Scand. 53:168-176. |
8 | Okubara, P. A. and Paulitz, T. C. 2005. Root defense responses to fungal pathogens: a molecular perspective. Plant Soil 274:215-226. DOI |
9 | Parry, D. W., Jenkinson, P. and McLeod, L. 1995. Fusarium ear blight (scab) in small grain cereals: a review. Plant Pathol. 44:207-238. DOI |
10 | Pacheco, A., Vargas, M., Alvarado, G., Rodriguez, F., Crossa, J. and Burgueno, J. 2015. GEA-R (Genotype x Environment analysis with R for windows) version 4.1. CIMMYT Research Data & Software Repository Network, Texcoco, Mexico. |
11 | Paulitz, T. C. 2006. Low input no-till cereal production in the Pacific Northwest of the U.S.: the challenges of root diseases. Eur. J. Plant Pathol. 115:271-281. DOI |
12 | Phalip, V., Delalande, F., Carapito, C., Goubet, F., Hatsch, D., Leize-Wagner, E., Dupree, P., Dorsselaer, A. V. and Jeltsch, J. M. 2005. Diversity of the exoproteome of Fusarium graminearum grown on plant cell wall. Curr. Genet. 48:366-379. DOI |
13 | Proctor, R. H., Hohn, T. M. and McCormick, S. P. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant-Microbe Interact. 8:593-601. DOI |
14 | Purss, G. S. 1971. Pathogenic specialization in Fusarium graminearum. Aust. J. Agric. Res. 22:553-561. DOI |
15 | Rossi, V., Cervi, C., Chiusa, G. and Languasco, L. 1995. Fungi associated with foot rots on winter wheat in Northwest Italy. J. Phytopathol. 143:115-119. DOI |
16 | Akinsanmi, O. A., Mitter, V., Simpfendorfer, S., Backhouse, D. and Chakraborty, S. 2004. Identity and pathogenicity of Fusarium spp. isolated from wheat fields in Queensland and northern New South Wales. Aust. J. Agric. Res. 55:97-107. DOI |
17 | Alahmad, S., Dinglasan, E., Leung, K. M., Riaz, A., Derbal, N., Voss-Fels, K. P., Able, J. A., Bassi, F. M., Christopher, J. and Hickey, L. T. 2018. Speed breeding for multiple quantitative traits in durum wheat. Plant Methods 14:36. DOI |
18 | Chekali, S., Gargouri, S., Berraies, S., Gharbi, M. S., Nicol, M. J. and Nasraoui, B. 2013. Impact of Fusarium foot and root rot on yield of cereals in Tunisia. Tunis. J. Plant Prot. 8:75-86. |
19 | Wang, Q., Vera Buxa, S., Furch, A., Friedt, W. and Gottwald, S. 2015. Insights into Triticum aestivum seedling root rot caused by Fusarium graminearum. Mol. Plant-Microbe Interact. 28:1288-1303. DOI |
20 | Beccari, G., Covarelli, L. and Nicholson, P. 2011. Infection processes and soft wheat response to root rot and crown rot caused by Fusarium culmorum. Plant Pathol. 60:671-684. DOI |
21 | Collard, B. C. Y., Grams, R. A., Bovill, W. D., Percy, C. D., Jolley, R., Lehmensiek, A., Wildermuth, G. and Sutherland, M. W. 2005. Development of molecular markers for crown rot resistance in wheat: mapping of QTL for seedling resistance in a '2-49' x 'Janz' population. Plant Breed. 124:532-537. DOI |
22 | Clement, J. A. and Parry, D. W. 1998. Stem-base disease and fungal colonisation of winter wheat grown in compost inoculate with Fusarium culmorum, F. graminearum and Microdochium nivale. Eur. J. Plant Pathol. 104:323-330. DOI |
23 | Gelisse, S., Pelzer, E., Dore, T. and Lannou, C. 2006. Contamination des epis et des grains par la fusariose du ble : test de la voie systemique et risque lie aux contaminations tardives [Contamination of ears and grains by Fusarium wilt of wheat: test of the systemic route and risk associated with late contamination]. Phytoma la Defense des Vegetaux 596:28-32 (in French). |
24 | Scherm, B., Balmas, V., Spanu, F., Pani, G., Delogu, G., Pasquali, M. and Migheli, Q. 2013. Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Mol. Plant Pathol. 14:323-341. DOI |
25 | Smiley, R. W., Gourlie, J. A., Easley, S. A., Patterson, L. M. and Whittaker, R. G. 2005. Crop damage estimates for crown rot of wheat and barley in the Pacific Northwest. Plant Dis. 89:595-604. DOI |
26 | Zheng, Z., Kilian, A., Yan, G. and Liu, C. 2014. QTL conferring fusarium crown rot resistance in the elite bread wheat variety EGA Wylie. PLoS ONE 9:e96011. DOI |
27 | Winter, M., Koopmann, B., Doll, K., Karlovsky, P., Kropf, U., Schluter, K. and von Tiedemann, A. 2013. Mechanisms regulating grain contamination with trichothecenes translocated from the stem base of wheat (Triticum aestivum) infected with Fusarium culmorum. Phytopathology 103:682-689. DOI |
28 | Xu, F., Yang, G., Wang, J., Song, Y., Liu, L., Zhao, K., Li, Y. and Han, Z. 2018. Spatial distribution of root and crown rot fungi associated with winter wheat in the North China plain and its relationship with climate variables. Front. Microbiol. 9:1054. DOI |
29 | Zadoks, J. C., Chang, T. T. and Konzak, C. F. 1974. A decimal code for the growth stages of cereals. Weed Res. 14:415-421. DOI |
30 | Oufensou, S., Balmas, V., Scherm, B., Rau, D., Camiolo, S., Prota, V. A., Ben-Attia, M., Gargouri, S., Pasquali, M., El- Bok, S. and Migheli, Q. 2019. Genetic variability, chemotype distribution, and aggressiveness of Fusarium culmorum on durum wheat in Tunisia. Phytopathol. Mediterr. 58:103-113. |
31 | Lyamani, A. 1988. Wheat root rot in west central Morocco and effects of Fusarium culmorum and Helminthosporium sativum seed and soil-born inoculum on root rot development, plant emergence and crop yield. Ph.D. thesis. Iowa State University, Ames, IA, USA. |
32 | Bovill, W. D., Horne, M., Herde, D., Davis, M., Wildermuth, G. B. and Sutherland, M. W. 2010. Pyramiding QTL increases seedling resistance to crown rot (Fusarium pseudograminearum) of wheat (Triticum aestivum). Theor. Appl. Genet. 121:127-136. DOI |
33 | Bovill, W. D., Ma, W., Ritter, K., Collard, B. C. Y., Davis, M., Wildermuth, G. B. and Sutherland, M. W. 2006. Identification of novel QTL for resistance to crown rot in the doubled haploid wheat population 'W21MMT70' × 'Mendos'. Plant Breed. 125:538-543. DOI |
34 | Alvarado, G., Lopez, M., Vargas, M., Pacheco, A., Rodriguez, F., Burgueno, J. and Crossa, J. 2015. META-R (Multi environment trial analysis with R for windows) Version 6.04. CIMMYT Research Data & Software Repository Network, Texcoco, Mexico. |
35 | Mitter, V., Zhang, M. C., Liu, C. J., Ghosh, R., Ghosh, M. and Chakraborty, S. 2006. A high-throughput glasshouse bioassay to detect crown rot resistance in wheat germplasm. Plant Pathol. 55:433-441. DOI |
36 | Van Wyk, P. S., Los, O., Rheeder, J. P. and Marasas, W. F. O. 1987. Fusarium species associated with crown rot of wheat in the Humansdorp District, Cape Province. Phytophylactica 19:343-344. |
37 | Ma, L. J., van der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M. J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P. M., Kang, S., Shim, W. B., Woloshuk, C., Xie, X., Xu, J. R., Antoniw, J., Baker, S. E., Bluhm, B. H., Breakspear, A., Brown, D. W., Butchko, R. A., Chapman, S., Coulson, R., Coutinho, P. M., Danchin, E. G., Diener, A., Gale, L. R., Gardiner, D. M., Goff, S., Hammond-Kosack, K. E., Hilburn, K., Hua-Van, A., Jonkers, W., Kazan, K., Kodira, C. D., Koehrsen, M., Kumar, L., Lee, Y. H., Li, L., Manners, J. M., Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S. Y., Proctor, R. H., Regev, A., Ruiz-Roldan, M. C., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D. C., Turgeon, B. G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C. A., Kistler, H. C. and Rep, M. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367-373. DOI |
38 | Snijders, C. H. A. 1990. Systemic fungal growth of Fusarium culmorum in stems of winter wheat. J. Phytopathol. 129:133-140. DOI |
39 | Strausbaugh, C. A., Overturf, K. and Koehn, A. C. 2005. Pathogenicity and real-time PCR detection of Fusarium spp. in wheat and barley roots. Can. J. Plant Pathol. 27:430-438. DOI |
40 | Tunali, B., Nicol, J. M., Hodson, D., Uckun, Z., Buyuk, O., Erdurmus, D., Hekimhan, H., Aktas, H., Akbudak, M. A. and Bagci, S. A. 2008. Root and crown rot fungi associated with spring, facultative, and winter wheat in Turkey. Plant Dis. 92:1299-1306. DOI |
41 | Voigt, C. A., Schafer, W. and Salomon, S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42:364-375. DOI |
42 | Wagacha, J. M. and Muthomi, J. W. 2007. Fusarium culmorum: infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Prot. 26:877-885. DOI |
43 | Demeke, T., Clear, R. M., Patrick, S. K. and Gaba, D. 2005. Species-specific PCR-based assays for the detection of Fusarium species and a comparison with the whole seed agar plate method and trichothecene analysis. Int. J. Food Microbiol. 103:271-284. DOI |
44 | Burgess, L. W., Wearing, A. H. and Toussoun, T. A. 1975. Surveys of Fusaria associated with crown rot of wheat in eastern Australia. Aust. J. Agric. Res. 26:791-799. DOI |
45 | Chakraborty, S., Obanor, F., Westecott, R. and Abeywickrama, K. 2010. Wheat crown rot pathogens Fusarium graminearum and F. pseudograminearum lack specialization. Phytopathology 100:1057-1065. DOI |
46 | Chung, W.-H., Ishii, H., Nishimura, K., Ohshima, M., Iwama, T. and Yoshimatsu, H. 2008. Genetic analysis and PCR-based identification of major Fusarium species causing head blight on wheat in Japan. J. Gen. Plant Pathol. 74:364-374. DOI |
47 | Mergoum, M. 1991. Effects of infection by Fusarium acuminatum, Fusarium culmorum or Cochliobolus sativus on wheat. Ph.D. thesis. Colorado State University, Fort Collins, CO, USA. |
48 | Leslie, J. F. and Summerell, B. A. 2006. The Fusarium laboratory manual. Blackwell Publishing, Ames, IA, USA. 400 pp. |
49 | Li, H. B., Xie, G. Q., Ma, J., Liu, G. R., Wen, S. M., Ban, T., Chakraborty, S. and Liu, C. J. 2010a. Genetic relationships between resistances to Fusarium head blight and crown rot in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 121:941-950. DOI |
50 | Li, X., Zhang, J. B., Song, B., Li, H. P., Xu, H. Q., Qu, B., Dang, F. J. and Liao, Y. C. 2010b. Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. Phytopathology 100:183-191. DOI |
51 | Muthomi, J. W., Schutze, A., Dehne, H. W., Mutitu, E. W. and Oerke, E.-C. 2000. Characterization of Fusarium culmorum isolates by mycotoxin production and aggressiveness to winter wheat. J. Plant Dis. Prot. 107:113-123. |
52 | Nelson, P. E., Toussoun, T. A. and Marasas, W. F. O. 1983. Fusarium species: an illustrated manual for identification. The Pennsylvania State University Press, University Park, PA, USA. 206 pp. |
53 | Mudge, A. M., Dill-Macky, R., Dong, Y., Gardiner, D. M., White, R. G. and Manners, J. M. 2006. A role for the mycotoxin deoxynivalenol in stem colonisation during crown rot disease of wheat caused by Fusarium graminearum and Fusarium pseudograminearum. Physiol. Mol. Plant Pathol. 69:73-85. DOI |
54 | Backhouse, D., Abubakar, A. A., Burgess, L. W., Dennis, J. I., Hollaway, G. J., Wildermuth, G. B., Wallwork, H. and Henry, F. J. 2004. Survey of Fusarium species associated with crown rot of wheat and barley in eastern Australia. Australas. Plant Pathol. 33:255-261. DOI |
55 | Gamba, F. M., Bassi, F. M. and Finckh, M. R. 2017. Race structure of Pyrenophora tritici-repentis in Morocco. Phytopathol. Mediterr. 56:119-126. |
56 | Ishtiaq, M., Hussain, T., Bhatti, K. H., Adesemoye, T., Maqbool, M., Azam, S. and Ghani, A. 2019. Management of root rot diseases of eight wheat varieties using resistance and biological control agents techniques. Pak. J. Bot. 51:327-339. |
57 | Kang, Z. and Buchenauer, H. 2000. Ultrastructural and immunocytochemical investigation of pathogen development and host responses in resistant and susceptible wheat spikes infected by Fusarium culmorum. Physiol. Mol. Plant Pathol. 57:255-268. DOI |
58 | Khabouze, M. 1988. Contribution a l'etude des pourritures racinaires du ble [Contribution to the study of root rots in wheat]. Memoire du 3eme cycle. Institut Agronomique et Veterinaire Hassan II, Rabat, Morocco. 113 pp. (in French). |
59 | El Yacoubi, H., Hassikou, R., Badoc, A., Rochdi, A. and Douira, A. 2012. Complexe fongique de la pourriture racinaire du ble tendre au nord-ouest du maroc [Root rot fungal complex of soft wheat in northwestern Morocco]. Bull. Soc. Pharm. Bordeaux 151:35-48 (in French). |
60 | Nsarellah, N., Lhaloui, S. and Nachit, M. 2000. Breeding durum wheat for biotic stresses in the Mediterranean region. In: Durum wheat improvement in the Mediterranean region: new challenges, eds. by C. Royo, M. Nachit, N. Di Fonzo and J. L. Araus, pp. 341-347. CIHEAM, Zaragoza, Spain. |
61 | Li, G. and Yin, Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Sci. 48:1888-1896. DOI |
62 | Poole, G. J., Smiley, R. W., Paulitz, T. C., Walker, C. A., Carter, A. H., See, D. R. and Garland-Campbell, K. 2012. Identification of quantitative trait loci (QTL) for resistance to Fusarium crown rot (Fusarium pseudograminearum) in multiple assay environments in the Pacific Northwestern US. Theor. Appl. Genet. 125:91-107. DOI |
63 | Diaz Arias, M. M. 2012. Fusarium species infecting soybean roots: frequency, aggressiveness, yield impact and interaction with the soybean cyst nematode. Ph.D. thesis. Iowa State University, Ames, IA, USA. |
64 | Cook, R. J. 2010. Fusarium root, crown, and foot rots and associated seedling diseases. In: Compendium of wheat diseases and pests, 3rd ed., eds. by W. W. Bockus, R. L. Bowden, R. M. Hunger, W. L. Morrill, T. D. Murray and R. W. Smiley, pp. 37-39. The American Phytopathological Society, St. Paul, MN, USA. |
65 | Covarelli, L., Beccari, G., Steed, A. and Nicholson, P. 2012. Colonization of soft wheat following infection of the stem base by Fusarium culmorum and translocation of deoxynivalenol to the head. Plant Pathol. 61:1121-1129. DOI |
66 | Doohan, F. M., Brennan, J. and Cooke, B. M. 2003. Influence of climatic factors on Fusarium species pathogenic to cereals. Eur. J. Plant Pathol. 109:755-768. DOI |
67 | El Yousfi, B. 1984. Contribution a l'etude de l'etiologie, de l'epidemiologie et des pertes de rendements dues aux pourritures racinaires du ble et de l'orge [Contribution to the study of the etiology, epidemiology and yield losses due to root rots in wheat and barley]. Memoire du 3eme cycle Agronomique, Institut Agronomique et Veterinaire Hassan II, Rabat, Morocco. 175 pp. (in French). |
68 | El Yousfi, B. 2015. Guide du diagnostic des principales maladies des cereales d'automne au Maroc [Guide to the diagnosis of the main diseases of autumn cereals in Morocco]. INRA CRRA de Settat, Settat, Morocco. 13 pp. (in French). |
69 | Cook, R. J. 1981. Fusarium diseases of wheat and other small grains in North America. In: Fusarium: diseases, biology and taxonomy, eds. by P. E. Nelson, T. A. Toussoun and R. J. Cook, pp. 39-52. Pennsylvania State University Press, University Park, PA, USA. |
70 | Vergne, P., Maene, M., Gabant, G., Chauvet, A., Debener, T. and Bendahmane, M. 2010. Somatic embryogenesis and transformation of the diploid Rosa chinensis cv Old Blush. Plant Cell Tissue Organ Cult. 100:73-81. DOI |
71 | Gebremariam, E. S., Sharma-Poudyal, D., Paulitz, T. C., Erginbas- Orakci, G., Karakaya, A. and Dababat, A. A. 2018. Identity and pathogenicity of Fusarium species associated with crown rot on wheat (Triticum spp.) in Turkey. Eur. J. Plant Pathol. 150:387-399. DOI |
72 | Wallwork, H., Butt, M., Cheong, J. P. E. and Williams, K. J. 2004. Resistance to crown rot in wheat identified through an improved method for screening adult plants. Australas. Plant Pathol. 33:1-7. DOI |
73 | Wang, H., Hwang, S. F., Eudes, F., Chang, K. F., Howard, R. J. and Turnbull, G. D. 2006. Trichothecenes and aggressiveness of Fusarium graminearum causing seedling blight and root rot in cereals. Plant Pathol. 55:224-230. DOI |
74 | Wildermuth, G. B., McNamara, R. B. and Quick, J. S. 2001. Crown depth and susceptibility to crown rot in wheat. Euphytica 122:397-405. DOI |
![]() |