Sains Malaysiana 48(9)(2019): 1841–1853

http://dx.doi.org/10.17576/jsm-2019-4809-05

 

Molecular Markers and Their Application in Fusarium Wilt Studies in Musa spp.

(Penanda Molekul dan Aplikasinya dalam Kajian Layu Fusarium pada Musa spp.)

 

IVAN KABIITA ARINAITWE1,2,4, CHEE HOW TEO4, FATIMAH KAYAT3, ROBOONI TUMUHIMBISE2, BRIGITTE UWIMANA5, JEROME KUBIRIBA2, JENNIFER ANN HARIKRISHNA1,4 & ROFINA YASMIN OTHMAN1*

 

1Institute of Biological Sciences (Genetics), Faculty of Sciences, University of Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

 

2National Banana Research Program, National Agricultural Research Organization, Kampala, Uganda

 

3Universiti Malaysia Kelantan, Kampus Jeli, 17600 Jeli, Kelantan Darul Naim, Malaysia

 

4Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

 

5International Institute of Tropical Agriculture (IITA), Kampala, Uganda

 

Diserahkan: 21 November 2018/Diterima: 25 Jun 2019

 

ABSTRACT

Bananas and plantains (Musa spp.) are an important socio-economic fruit crop grown worldwide. Their production across the regions where they are grown is largely hampered by pests and diseases. Fusarium wilt is a disastrous diseases of bananas caused by the fungal pathogen Fusarium oxysporum f.sp. cubense (Foc). Managing it with chemicals, biological control agents and cultural methods is ineffective. Host plant resistance is the most effective and durable approach of managing most pest and disease epidemics in most plant species and could equally be effective in managing Fusarium wilt in bananas. Crossbreeding as one of the ways to introgress disease resistance genes and phenotyping for biotic and abiotic stresses currently used in banana breeding is apparently difficult to apply because of banana’s low fertility, gigantic size, and long-life cycle which prolongs its breeding cycle. There is, therefore, a need to apply molecular markers in banana genetic improvement for Fusarium wilt resistance because of their accuracy, speed, robustness and effectiveness of operation. The objective of this article was to review and discuss molecular markers that have been successfully used in studying Fusarium wilt in bananas and some other important crops. Molecular markers discussed in this article include Random Amplified Polymorphic DNA, Sequence Characterized Amplified Region, Simple Sequence Repeat, Inter-Simple Sequence Repeat, and Single Nucleotide Polymorphism. The information discussed in this article informs future decisions to identify suitable marker systems for fine mapping of target regions and accelerated identification of quantitative trait loci for Foc resistance in bananas.

 

Keywords: Banana; Fusarium oxysporum f.sp. cubense; molecular markers; quantitative trait loci; resistance

 

ABSTRAK

Pisang dan plantain (Musa spp.) adalah tanaman buah-buahan sosio-ekonomi penting yang berkembang di seluruh dunia. Pengeluarannya merentasi sempadan dengan sebahagian besar penanamannya dibantutkan oleh penyakit dan perosak. Layu Fusarium adalah sejenis penyakit pisang yang disebabkan oleh kulat patogen Fusarium oxysporum f.sp. cubense (Foc). Kaedah mengawal penyakit ini dengan menggunakan bahan kimia, agen kawalan biologi atau kaedah kultur tidak berkesan. Kerintangan tumbuhan perumah adalah pendekatan yang paling berkesan dan bertahan lama untuk mengawal wabak penyakit dan perosak dalam kebanyakan spesies tumbuhan dan berkesan dalam menguruskan layu Fusarium pada pisang. Pembiakbakaan kacukan merupakan salah satu cara untuk introgres gen rintangan penyakit dan fenotip bagi tegasan biotik dan abiotiknya yang digunakan dalam penanaman pisang namun teknik ini sukar untuk diaplikasikan kerana kesuburan pisang yang rendah, saiz yang besar dan hayat kitaran yang panjang yang turut memanjangkan kitaran pembiakannya. Oleh itu, ada keperluan untuk menggunakan penanda molekul dalam meningkatkan genetik pisang untuk menghalang layu Fusarium kerana ketepatan, kelajuan, keteguhan dan keberkesanan operasinya. Objektif kajian ini adalah untuk meneliti dan membincangkan penanda molekul yang telah berjaya digunakan dalam mengkaji layu Fusarium pisang dan sesetengah tanaman lain yang penting. Penanda molekul yang dibincangkan dalam kertas ini merangkumi DNA Polimorfik Rawak Teramplifikasi, Rantau Jujukan Pencirian Teramplifikasi, Pengulangan Jujukan Mudah, Pengulangan Jujukan Inter-Mudah dan Polimorfisme Nukleotida Tunggal. Maklumat yang dibincangkan dalam kajian ini menunjukkan keputusan pada masa depan dalam mengenal pasti sistem penanda sesuai bagi pemetaan kawasan sasaran lengkap dan pemecutan pengenalpastian lokus khi kuantitatif untuk rintangan Foc dalam pisang.

 

Kata kunci: Fusarium oxysporum f.sp. cubense; lokus khi kuantitatif; penanda molekul; pisang; rintangan

RUJUKAN

 

Abate, T. 2017. Inter Simple Sequence Repeat (ISSR) markers for genetic diversity studies in trifolium species. Advances in Life Science and Technology 55: 34-37.

Abdurakhmonov, I.Y. 2016. Introduction to Microsatellites: Basics, Trends and Highlights. In Microsatellite Markers. InTech.

Adss, I.A.A., Abdel-Gaye, M.A., Botros, W. & Hafez, E.E. 2016. Multilocus genetic techniques, RAPD-PCR and ISSR-PCR markers and polygalacturonase activity as tools for differentiation among alternaria solani isolates on tomato fruits and relation to their pathogenicity in Egypt. Asian Journal of Plant Pathology 11(1): 18-27.

Amorim, E.P., Silva, P.H., Ferreira, C.F., Amorim, V.B.O., Santos, V.J., Vilarinhos, A.D. & Miller, R.N.G. 2012. New microsatellite markers for bananas (Musa spp). Genetics and Molecular Research 11(2): 1093-1098.

Arif, I.A., Bakir, M.A., Khan, H.A., Al Farhan, A.H., Al Homaidan, A.A., Bahkali, A.H. & Shobrak, M. 2010. A brief review of molecular techniques to assess plant diversity. International Journal of Molecular Sciences 11(5): 2079- 2096.

Athe, R., Naha, B., Neerasa, G., Parthasarathi, P.C.B., Nukala, R. & Devara, D. 2018. Molecular markers-characteristics and applications in animal breeding. International Journal of Livestock Research 8(1): 1-7.

Azam, S., Munir, A., Saad Khan, M., Fazal, S., Mehmood, A., Ali, S. & Hussain, S. 2017. In-silico identification of novel resistant genes for fungal pathogen Fusarium oxysporum f.sp. cubense Race 4: Causative agent of banana vascular wilt disease. Journal of Plant Biochemistry & Physiology 05: 01. doi: 10.4172/2329-9029.1000175.

Bai, T.T., Xie, W.B., Zhou, P.P., Wu, Z.L., Xiao, W.C., Zhou, L., Li, H.P., Sun, J. & Ruan, X.L. 2013. Transcriptome and expression profile analysis of highly resistant and susceptible banana roots challenged with Fusarium oxysporum f.sp. cubense Tropical Race 4. PLoS ONE 8(9): e73945.

Borse, N., Chimote, V.P. & Jadhav, A.S. 2011. Stability of micropropagated Musa acuminata cv. Grand Naine over clonal generations: A molecular assessment. Scientia Horticulturae 129(3): 390-395.

Brown, A., Tumuhimbise, R., Amah, D., Uwimana, B., Nyine, M., Mduma, H. & Swennen, R. 2017. Bananas and plantains (Musa spp.). In Genetic Improvement of Tropical Crops, edited by Campos, H. & Caligari, P.D.S. Basel, Switzerland: Springer. pp. 219-240.

Catanzariti, A.M. & Jones, D.A. 2010. Effector proteins of extracellular fungal plant pathogens that trigger host resistance. Functional Plant Biology 37(10): 901-907.

Cheng, Z., Yu, X., Li, S. & Wu, Q. 2018. Genome-wide transcriptome analysis and identification of benzothiadiazole- induced genes and pathways potentially associated with defense response in banana. BMC Genomics 19(1): 454. https://doi.org/10.1186/s12864-018-4830-7.

Cunha, C.M.S., Hinz, R.H., Pereira, A., Tcacenco, F.A., Paulino, E.C. & Stadnik, M.J. 2015. A SCAR marker for identifying susceptibility to Fusarium oxysporum f.sp. cubense in banana. Scientia Horticulturae 191: 108-112.

Dale, J., James, A., Paul, J.Y., Khanna, H., Smith, M., Peraza- Echeverria, S., Garcia-Bastidas, F., Koma, G., Waterhouse, P., Mengersen, K. & Harding, R. 2017. Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4. Nature Communications 8(1): 1496. doi: 10.1038/s41467- 017-01670-6.

Dequan, S., Yulin, H., Lubin, Z., Yiwei, M. & Jianghui, X. 2009. Cloning and analysis of Fusarium wilt resistance gene analogs in 'Goldfinger' banana. Molecular Plant Breeding 7(6): 1215-1222.

D'hont, A., Denoeud, F., Aury, J.M., Baurens, F.C., Carreel, F., Garsmeur, O. & Wincker, P. 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488(7410): 213-217.

Dotto, J., Matemu, A.O. & Ndakidemi, P.A. 2018. Potential of cooking bananas in addressing food security in East Africa. International Journal of Biosciences 13(4): 278-294.

FAOSTAT. 2016. Crops and products domain. http://www.fao. org/faostat/en/#data/QC. Accessed on September 18, 2018.

FAOSTAT. 2010. Crops and products domain. http://www.fao. org/faostat/en/#data/QC. Accessed on April 12, 2018.

Francia, E., Tacconi, G., Crosatti, C., Barabaschi, D., Bulgarelli, D., Dall'Aglio, E. & Valè, G. 2005. Marker assisted selection in crop plants. Plant Cell, Tissue and Organ Culture 82(3): 317-342.

Ghag, S.B., Shekhawat, U.K.S. & Ganapathi, T.R. 2012. Petunia floral defensins with unique prodomains as novel candidates for development of Fusarium wilt resistance in transgenic banana plants. PLoS ONE 7(6): e39557.

Gramaje, D., León, M., Santana, M., Crous, P.W. & Armengol, J. 2014. Multilocus ISSR markers reveal two major genetic groups in Spanish and South African populations of the grapevine fungal pathogen cadophora luteo-olivacea. PLoS ONE 9(10): e110417.

Gonzalez-Cendales, Y., Catanzariti, A.M., Baker, B., Mcgrath, D.J. & Jones, D. 2016. Identification of I-7 expands the repertoire of genes for resistance to Fusarium wilt in tomato to three resistance gene classes. Molecular Plant Pathology 17(3): 448-463.

Haji-Allahverdipoor, K., Bahramnejad, B. & Amini, J. 2011. Selection of molecular markers associated with resistance to ‘Fusarium’ wilt disease in chickpea (Cicer arietinum L.) using multivariate statistical techniques. Australian Journal of Crop Science 5(13): 1801-1809.

Hawkins, L.K., Dane, F., Kubisiak, T.L., Rhodes, B.B. & Jarret, R.L. 2001. Linkage mapping in a watermelon population segregating for Fusarium wilt resistance. J. Amer. Soc. Hor. Sci. 126(3): 344-350.

Irish, B.M., Cuevas, H.E., Simpson, S.A., Scheffler, B.E., Sardos, J., Ploetz, R. & Goenaga, R. 2014. Musa spp. germplasm management: Microsatellite fingerprinting of USDA-ARS national plant germplasm system collection. Crop Science 54(5): 2140-2151.

Jarocki, P., Podleśny, M., Komoń-Janczara, E., Kucharska, J., Glibowska, A. & Targoński, Z. 2016. Comparison of various molecular methods for rapid differentiation of intestinal bifidobacteria at the species, subspecies and strain level. BMC Microbiology 16(1): 159. doi: 10.1186/s12866-016-0779-3.

Javed, M., Chai, M. & Othman, R.Y. 2004. Study of Resistance of Musa acuminata to Fusarium oxysporum using RAPD markers. Biologia Plantarum 48(1): 93-99.

Jehan, T. & Lakhanpaul, S. 2006. Single nucleotide polymorphism (SNP) - methods and applications in plant genetics: A review. Indian Journal of Biotechnology 5(4): 435-459.

Kabir, M.H., Mamun, A.N., Fatema, H. & Amin, R. 2015. paper publications assessment of genetic diversity in 13 local banana (Musa spp.) cultivars using simple sequence repeat (SSR) Markers. International Journal of Recent Research in Life Sciences 2(1): 65-69.

Kayat, F., Javed, M.A., Wah, H.Y., Othman, R.Y., Berhad, U.P., Intan, T. & Michel, G. 2004. Identification of molecular markers for disease resistance genes to Fusarium oxysporum f.sp. cubense in Musa acuminata spp. malaccensis for marker assisted selection (MAS). The 4th Annual Seminar of National Science Fellowship 2004. pp. 40-44.

Kennedy, G., Raneri, J., Stoian, D., Attwood, S., Burgos, G., Ceballos, H., Ekesa, B., Johnson, V., Low, J.W. & Talsma, E.F. 2018. Roots, tubers and bananas: Contributions to food security. In Encyclopedia of Food Security and Sustainability, edited by Ferranti, P., Anderson, J.R. & Berry, E.M. Elsevier. Volume 3. pp. 231-256.

Khan, S. 2015. QTL mapping: A tool for improvement in crop plants. Research Journal of Recent Sciences 4: 7-12.

Khatri, A., Bibi, S., Umar Dahot, M., Ahmed Khan, I. & Shah Nizamani, G. 2011. In vitro mutagenesis in banana and variant screening through ISSR. Pak. J. Bot. 43(5): 2427-2431.

Kumar, P., Rao, T.M., Sane, A., Kumar, R. & Dhananjaya, M.V. 2016. Characterization of Fusarium wilt in resistant and susceptible gladiolus (Gladiolus spp.) genotypes using DNA markers. The Indian Journal of Agricultural Sciences 86(7): 849-853.

Kumar, B., Shankar, U., Nayaka, C. & Kini, S.R. 2010. Biochemical characterization of Fusarium oxysporum f.sp. cubense isolates from India. African Journal of Biotechnology 9(4): 523-530.

Kwon, O.C., Lee, C.S. & Park, Y.J. 2019. SNP and SCAR markers for specific discrimination of antler-shaped Ganoderma lucidum. Microorganisms 7(1): 12. doi:10.3390/ microorganisms7010012.

Labuschagne, C., Nupen, L., Kotzé, A., Grobler, P.J. & Dalton, D.L. 2015. Assessment of microsatellite and SNP markers for parentage assignment in ex situ African Penguin (Spheniscus demersus) populations. Ecology and Evolution 5(19): 4389- 4399.

Lamare, A. & Rao, S.R. 2015. Efficacy of RAPD, ISSR and DAMD markers in assessment of genetic variability and population structure of wild Musa acuminata colla. Physiology and Molecular Biology of Plants 21(3): 349-358.

Lambel, S., Lanini, B., Vivoda, E., Fauve, J., Patrick Wechter, W., Harris-Shultz, K.R. & Levi, A. 2014. A major QTL associated with Fusarium oxysporum race 1 resistance identified in genetic populations derived from closely related watermelon lines using selective genotyping and genotyping-by-sequencing for SNP discovery. Theoretical and Applied Genetics 127(10): 2105-2115.

Lema, M. 2018. Marker assisted selection in comparison to conventional plant breeding: Review article. Aricultural Research and Technology 14(2): 555914.

Li, E., Wang, G., Xiao, J., Ling, J., Yang, Y. & Xie, B. 2016. A SIX1 Homolog in Fusarium oxysporum f.sp. conglutinans is required for full virulence on cabbage. PLoS ONE 11(3): e0152273.

Li, X., Peng, T., Xu, F., Xie, J. & Chen, Y.T.H. 2012. Genetic diversity analysis for different wilt disease resistant bananas by ISSR. Guangdong Agricultural Sciences 39(9): 6-8.

Looney, N.E. 2016. Fruits, vegetables and tubers: Bountiful resources for achieving and sustaining food and nutrition security. In Routledge Handbook of Food and Nutrition Security, edited by Pritchard, B., Ortiz, R. & Shekar, M. London: Routledge. pp. 56-76.

Lv, H., Fang, Z., Yang, L., Zhang, Y., Wang, Q., Liu, Y. & Wang, X. 2014. Mapping and analysis of a novel candidate Fusarium wilt resistance gene Foc 1 in Brassica oleracea. BMC Genomics 15(1): 1094.

Magambo, B., Harjeet, K., Arinaitwe, G., Arinaitwe, S.T.I.K., Kubiriba, J., Tushemereirwe, W. & Dale, J. 2016. Inhibition of cell death as an approach for development of transgenic resistance against Fusarium wilt disease. African Journal of Biotechnology 15(19): 786-797.

Mahdavi, F., Sariah, M. & Maziah, M. 2012. Expression of rice thaumatin-like protein gene in transgenic banana plants enhances resistance to Fusarium wilt. Applied Biochemistry and Biotechnology 166(4): 1008-1019.

Mahendhiran, M., Ramirez-Prado, J.H., Escobedo-Gracia Medrano, R.M., Canto-Canché, B., Tzec-Simá, M., Grijalva- Arango, R. & James-Kay, A. 2014. Single nucleotide polymorphisms in partial sequences of the gene encoding the large sub-units of ADP-glucose pyrophosphorylase within a representative collection of 10 Musa genotypes. Electronic Journal of Biotechnology 17(3): 137-147.

Mammadov, J., Aggarwal, R., Buyyarapu, R. & Kumpatla, S. 2012. SNP markers and their impact on plant breeding. International Journal of Plant Genomics 2012: 728398.

Migicovsky, Z. & Myles, S. 2017. Exploiting wild relatives for genomics-assisted breeding of perennial crops. Frontiers in Plant Science 8: 460. https://doi.org/10.3389/fpls.2017.00460.

Miller, R.N., Passos, M.A., Menezes, N.N., Souza, M.T., Do Carmo Costa, M.M., Azevedo, V.C. & Ciampi, A.Y. 2010. Characterization of novel microsatellite markers in Musa acuminata subsp. burmannicoides, var. Calcutta 4. BMC Research Notes 3(1): 148. doi: 10.1186/1756-0500-3-148.

Miri, S.M., Mousavi, A., Naghavi, M.R. & Khiabani, B.N. 2014. Molecular analysis of Musa mutants resistant to salinity by microsatellite markers. Trakia Journal of Sciences 12(2): 114-120.

Mkada-Driss, I., Lahmadi, R., Chakroun, A.S., Talbi, C., Guerbouj, S., Driss, M., Elamine, E.M., Cupolillo, E., Mukhtar, M.M. & Guizani, I. 2014. Screening and characterization of RAPD markers in viscerotropic Leishmania parasites. PLoS ONE 9(10): e109773.

Mmeka, E., Adesoye, A., Vroh, B. & Ubaoji, K. 2013. Single nucleotide polymorphism (SNP) markers discovery within Musa spp. (plantain landraces, AAB genome) for use in beta carotene (Provitamin A) trait mapping. American Journal of Biology and Life Sciences 1(1): 11-19.

Mohandas, S., Sowmya, H.D., Saxena, A.K., Meenakshi, S., Rani, R.T. & Mahmood, R. 2013. Transgenic banana cv. Rasthali (AAB, Silk gp) harboring Ace-AMP1 gene imparts enhanced resistance to Fusarium oxysporum f.sp. cubense race 1. Scientia Horticulturae 164: 392-399.

Mohapatra, D., Mishra, S. & Sutar, N. 2010. Banana and its by-product utilisation: An overview. Journal of Scientific and Industrial Research 69(5): 323-329.

Mostert, D., Molina, A.B., Daniells, J., Fourie, G., Hermanto, C., Chao, C.P. & Viljoen, A. 2017. The distribution and host range of the banana Fusarium wilt fungus, Fusarium oxysporum f.sp. cubense, in Asia. PLoS ONE 12(7): e0181630.

Nadeem, M.A., Nawaz, M.A., Shahid, M.Q., Doğan, Y., Comertpay, G., Yıldız, M., Ahmad, F., Alsaleh, A., Labhane, N., Özkan, H., Chung, G. & Baloch, F.S. 2018. DNA molecular markers in plant breeding: Current status and recent advancements in genomic selection and genome editing. Biotechnology & Biotechnological Equipment 32(2): 261-285.

Natsuaki, K.T. 2011. Achievement Sub-Project on Disease Resistance in Banana, 70. http://www.fnca.mext.go.jp/ english/mb/drb/pdf/whole_drb.pdf.

Ng, W.L. & Tan, S.G. 2015. Inter-Simple Sequence Repeat (ISSR) markers: Are we doing it right? ASM Science Journal 9(1): 30-39.

Nkongolo, K.K., Gervais, S., Michael, P. & Zhou, Y. 2014. Comparative analysis of inter simple sequence repeats and simple sequence repeats markers: Genetic analysis of Deschampsia cespitosa populations growing in metal contaminated regions in Canada. American Journal of Biochemistry and Biotechnology 10(1): 69-80.

Nyine, M., Uwimana, B., Blavet, N., Hřibová, E., Vanrespaille, H., Batte, M. & Doležel, J. 2018. Genomic prediction in a multiploid crop: Genotype by environment interaction and allele dosage effects on predictive ability in banana. The Plant Genome 11: 2. doi: 10.3835/plantgenome2017.10.0090.

Okubara, P., Keller, K., McClendon, M., Inglis, D., McPhee, K. & Coyne, C. 2005. Y15_999Fw, a dominant SCAR marker linked to the Fusarium wilt race 1 (Fw) resistance gene in pea. Pisum Genetics 37: 30-33.

Padaliya, R.V., Suthar, K.P., Singh, D., Mahatma, M.K. & Patil, V.R. 2013. Marker assisted characterization of chickpea genotypes for wilt resistance. African Journal of Biotechnology 12(50): 6907-6912.

Pathak, R. 2015. Clusterbean: Physiology, Genetics and Cultivation. Singapore: Springer.

Patil, B.S., Ravikumar, R.L., Bhat, J.S. & Soregaon, C.D. 2014. Molecular mapping of QTLs for resistance to early and late Fusarium wilt in chickpea. Czech J. Genet. Plant Breed 50(2): 171-176.

Ploetz, R. 2015. Fusarium wilt of banana. Phytopathology 105(12): 1512-1521.

Ploetz, R.C., Kema, G.H.J. & Ma, L.J. 2015. Impact of diseases on export and smallholder production of banana. Annual Review of Phytopathology 53(1): 269-288.

Prasad, Y.P., Manjunatha, N., Prabhuling, G., Kishor, H. & Abhijith, Y.C. 2018. Early screening of fusarium wilt and molecular analysis of banana variants. International Journal of Current Microbiology and Applied Sciences 7(03): 2313- 2321.

Prasanthi, L., Reddy, B.V., Rani, K., Prasad, Y., Rajeswari, T. & Reddy, K. 2009. Development of Sequence Characterized Amplified Region (SCAR) marker for Fusarium wilt resistance gene in pigeon pea (Cajanus cajan L. Mill sp.). International Journal of Plant Breeding 3(2): 134-138.

Pushpakumari, H.W.L., Samarasinghe, W.L.G. & Senanayake, S. 2009. DNA Typing of dessert banana cultivar, 'Kolikuttu ('Silk') accessions by microsatellite markers. Tropical Agricultural Research and Extension 12(2): 12-15.

Rebouças, T.A., Haddad, F., Ferreira, C.F., de Oliveira, S.A.S., da Silva Ledo, C.A. & Amorim, E.P. 2018. Identification of banana genotypes resistant to Fusarium wilt race 1 under field and greenhouse conditions. Scientia Horticulturae 239: 308-313.

Ren, Y., Jiao, D., Gong, G., Zhang, H., Guo, S., Zhang, J. & Xu, Y. 2015. Genetic analysis and chromosome mapping of resistance to Fusarium oxysporum f.sp. niveum (FON) race 1 and race 2 in watermelon (Citrullus lanatus L.). Molecular Breeding 35(9): 183.

Robinson, J., Daneel, M. & Schoeman, P. 1998. Cultural practises in relation to integrated pest management in bananas. In Mobilizing IPM for Sustainable Banana Production in Africa, edited by Frison, E., Gold, C., Karamura, E. & Sikora, R. Nelspruit, South Africa: INIBAP. pp. 23-28.

Sardos, J., Rouard, M., Hueber, Y., Cenci, A., Hyma, K.E., van den Houwe, I. & Roux, N. 2016. A genome-wide association study on the seedless phenotype in banana (Musa spp.) reveals the potential of a selected panel to detect candidate genes in a vegetatively propagated crop. PloS ONE 11(5): e0154448.

Singh, V.K., Khan, A.W., Saxena, R.K., Kumar, V., Kale, S.M., Sinha, P. & Varshney, R.K. 2016. Next-generation sequencing for identification of candidate genes for Fusarium wilt and sterility mosaic disease in pigeonpea (Cajanus cajan). Plant Biotechnology Journal 14(5): 1183-1194.

Soregaon, C.D. & Ravikumar, R.L. 2010. Marker assisted characterization of wilt resistance in productive Chickpea genotypes. Electronic Journal of Plant Breeding 1(4): 1159-1163.

Spooner, D., Treuren, R. & Van De Vicente, M.C. 2005. Molecular markers for GenBank management. IPGRI Technical Bulletin No. 10. Rome, Italy: International Plant Genetic Resources Institute.

Tourky, M.N., Tarabih, M.E. & El-Eryan, E.E. 2014. Physiological studies on the marketability of williams banana fruits. American Journal of Plant Physiology 9(1): 1-15.

Tullu, A., Muehlbauer, F., Simon, C., Mayer, M., Kumar, J., Kaiser, W. & Kraft, J. 1998. Inheritance and linkage of a gene for resistance to race 4 of Fusarium wilt and RAPD markers in chickpea. Euphytica 102(2): 227-232.

Tumuhimbise, R., Barekye, A., Kubiriba, J., Tushemereirwe, W.K., Akankwasa, K., Arinaitwe, I. & Karamura, D. 2018. New high-yielding cooking banana cultivars with multiple resistances to pests and diseases ('NAROBan1', 'NAROBan2', 'NAROBan3' and 'NAROBan4') released in Uganda. HortScience 53(9): 1387-1389.

Van Dam, P., Fokkens, L., Schmidt, S., Linmans, J., Kistler, H., Ma, L.J. & Rep, M. 2016. Effector profiles distinguish formae speciales of Fusarium oxysporum. Environmental Microbiology 18(11): 4087-4102.

Van Den Berg, N., Viljoen, A., Birch, P.R.J., Wingfield, M.J., Hein, I. & Berger, D.K. 2007. Tolerance in banana to Fusarium wilt is associated with early up-regulation of cell wall-strengthening genes in the roots. Molecular Plant Pathology 8(3): 333-341.

Viljoen, A., Kunert, K., Kiggundu, A. & Escalant, J.V. 2004. Biotechnology for sustainable banana and plantain production in Africa: The South African contribution. South African Journal of Botany 70(1): 67-74.

Wang, F., Xia, L., Lv, S., Xu, C., Niu, Y., Liu, W. & Hu, B. 2018. Development of a mitochondrial SCAR marker related to susceptibility of banana (Musa AAA Cavendish) to Fusarium oxysporum f.sp. cubense Race 4. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 46(2): 509-516.

Wang, W., Sun, D. & Staehelin, C. 2012. Identification and evaluation of two diagnostic markers linked to Fusarium wilt resistance (race 4) in banana (Musa spp.). Mol. Biol. Rep. 39(1): 2-11.

Wechter, W., Whitehead, M., Thomas, C.E. & Dean, R.A. 1995. Identification of a randomly amplified polymorphic DNA marker linked to the fom2 Fusarium wilt resistance gene in muskmelon MR-1. Phytopathology 85: 1245-1249.

Widinugraheni, S., Niño-Sánchez, J., van der Does, H.C., van Dam, P., García-Bastidas, F.A., Subandiyah, S., Meijer, H.J.G., Kistler, H.C., Kema, G.H.J. & Rep, M. 2018. A SIX1 homolog in Fusarium oxysporum f.sp. cubense tropical race 4 contributes to virulence towards Cavendish banana. PLoS ONE 13(10): e0205896.

Zambrano, A.Y., Demey, J.R., Martínez, G., Gutiérrez, Z., Díaz, L., Ruíz, L. & Manzanilla, E. 2007. RAPD marker associated with resistance to Fusarium oxysporum in Musa. Interciencia 32(11): 775-779.

Zheng, X.Y. & Wolff, D.W. 2000. Randomly amplified polymorphic DNA markers linked to Fusarium wilt resistance in diverse melons. Hortscience 35(4): 716-721.

 

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