The use of effector gene based-markers to facilitate identification of Fusarium sp. infected shallot in Java, Indonesia
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Abstract. Herlina L, Istiaji B. 2020. The use of effector gene based-markers to facilitate identification of Fusarium sp. infected shallot in Java, Indonesia. Biodiversitas 21: 4677-4685. One of the most important diseases and become challenge in breeding resistant variety of shallots in Indonesia is Fusarium disease, caused by Fusarium oxysporum f.sp. cepae (FOC). To discriminate the F. oxysporum into forma speciales is uneasy, often managed through laborious and time-intensive disease assays., therefore molecular approaches become the most relevant choice. FOCs from Indonesia were examined by molecular criteria based on putative and effector genes-based markers, i.e.: SIX-genes, C5-gene, and CRX1-2-genes. The alignment analysis discovered some regions which sequences highly contained conserved bases, while amplification result bands vary in size, between 400 - 500 bp. The combined of 7 SIX-genes primers and 3 effector primers (C5 and CRX1-2) used in the clustering analysis of 15 FOC isolates in this study showed that they succeeded in separating 15 FOC isolates into 4 groups through NTSys. Clustering analysis showed that those markers succeeded in grouping 15 FOC isolates into different clades (by coefficient of similarity: 0.69). Phylogenetic analysis based on CRX genes sequence as putative effector genes confirmed that CRX1 and CRX2 genes were able to classify the FOC into their forma speciales. Those effectors genes are potential to serve as marker-templates to facilitate identification of FOC which infested shallots in Indonesia.
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References
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Kageyama, K., Komatsu, T. and Suga, H. 2003. Refined PCRprotocol for detection of plant pathogens in soil. J Gen Plant Pathol. 69:153–160.
Vincelli, P. and Tisserat, N. 2008. Nucleic acid-basedpathogen detection in applied plant pathology. Plant Dis. 92:660–669.
Kuruppu PU. 1999. First report of Fusarium oxysporum causing leaf twisting disease on Allium cepa var. ascalonicum in Sri Lanka. Plant Disease. 83:695.
Lievens B, Houterman PM and Rep M. 2009. Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiol. Lett. 300:201-215.
Lievens B, Thomma BPHJ. 2005. Recent developments in pathogen detection arrays: implications for fungal plant pathogens and use in practice. Phytopathology 95:1374–1380. https://doi.org/10.1094/PHYTO -95-1374.
Mbofung GCY, Fessehaie A, Bhattacharyya MK, Leandro LFS. 2011. A new TaqMan real-time polymerase chain reaction assay for quanti?cation of Fusarium virguliforme in soil. Plant Dis 95:1420–1426. https://doi.org/10 .1094/PDIS-02-11-0120.
Maldonado BLD, Villarruel O JL, Calderón O MA, Sánchez E AC. 2018. Secreted in Xylem (Six) Genes in Fusarium oxysporum f. sp. cubense and Their Potential Acquisition by Horizontal Transfer. Adv Biotech & Micro. 10(1): 555779. doi: 10.19080/AIBM.2018.10.5557780012
Rabiei-Motlagh E, Falahati-Rastegar M, Rouhani H, Jafarpour B, Jahanbakhsh V. 2010. Root disease of onion caused by root colonizing fungi in northeast of Iran. American-Eurasian J. Agric & Environ. Sci. 7(4): 484-491.
Recorbet G, Steinberg C, Olivain C, Edel V, Trouvelot S, Dumas-Gaudot E, Gianinazzi S, Alabouvette C. 2003. Wanted: pathogenesis-related marker molecules for Fusarium oxysporum. New Phytol 159:73–92. https://doi .org/10.1046/j.1469-8137.2003.00795.x.
Singha IM, Kakoty Y, Unni BG, Das J, Kalita MC. 2016. Identification and characterization of Fusarium sp. using ITS and RAPD causing fusarium wilt of tomato isolated from Assam, North East India. Journal of Genetic Engineering and Biotechnology. 14: 99-105
Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599.
Taylor A, Vagany V, Jackson AC, Harrison RJ, Rainoni A, Clarkson JP. 2016. Identification of pathogenicity-related genes in Fusarium oxysporum f. sp. cepae. Molecular Plant Pathology. 17(7):1032–1047. DOI: 10.1111/mpp.12346.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-speci?c gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680.
Tondok ET. 2001. Twisting disease caused by Fusarium oxysporum on shallot (Allium cepa L. var. agregatum G. Don.) in Indonesia. [Disertasi]. Jerman (DE): Institute of Plant Protection, Faculty of Agriculture, Georg-August-University Geottingen, Germany.
Urban, M.; Irvine, A.G.; Cuzick, A.; Hammond-Kosack, K.E. Using the Pathogen-Host Interactions Database (PHI-Base) to Investigate Plant Pathogen Genomes and Genes Implicated in Virulence. Front. Plant Sci. 6:605.
Van Der Does HC, Lievens B, Claes L, Houterman PM, Cornelissen BJC, Rep M. 2008. The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environ Microbiol 10:1475–1485. https://doi.org/10.1111/j.1462-2920.2007.01561.x.
Van Dam P, Fokkens L, Schmidt SM, Linmans JHJ, Kistler HC, Ma L-J, Rep M. 2016. Effector pro?les distinguish formae speciales of Fusarium oxysporum. Environ Microbiol 18:4087–4102. https://doi.org/10.1111/1462 -2920.13445.
Zhang Z, Zhang J, Wang Y, Zheng X. 2005. Molecular detection of Fusarium oxysporum f. sp. niveum and Mycosphaerella melonis in infected plant tissues and soil. FEMS Microbiol Lett 249:39–47. https://doi .org/10.1016/j.femsle.2005.05.057.
An B, Hou X, Guo Y, Zhao S, Luo H, He C, Wan Q. 2019. The effector SIX8 is required for virulence of Fusarium oxysporum f.sp. cubense tropical race 4 to Cavendish banana. Fungal Biology. 123 (5): 423-430.Aguayo J, Mostert D, Fourrier-Jeandel C, Cerf-Wendling I, Hostachy B, Viljoen A, Ioos R. 2017. Development of a hydrolysis probe-based realtime assay for the detection of tropical strains of Fusarium oxysporum f. sp. cubense race 4. PLoS One. 12:e0171767. https://doi.org/10.1371/ journal.pone.0171767.
Baayen RP, O’Donnell K, Bonants PJM, Cigelnik E, Kroon LPNM, et al. 2000. Gene genealogies andAFLP analyses in the Fusarium oxysporum complex identify monophyletic and nonmonophyletic formae speciales causing wilt and rot disease. Phytopathology. 90:891–900.
Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle LD. 2007. RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol. Plant Microbe Interact. 20:627–36.
Burgess, L.W., B.A. Summerell, S. Bullock, K.P. Gott & D. Backhouse, 1994. Laboratory Manual for Fusarium Research, 3rd Ed.Univ of Syndey, Sydney, Australia, 133 pp.
Cenis JL, Tello J, Cifuentes D. 2003. Genetic relationships among seven specialized forms of Fusarium oxysporum determined by DNA sequencing of the ITS region and AFLPs. Spanish J Agric Res 1:55–63. https:// doi.org/10.5424/sjar/2003013-35.
Chang W, Li H, Chen H, Qiao F, Zeng H. Identification of mimp-associated effector genes in Fusarium oxysporum f. sp. cubense race 1 and race 4 and virulence confirmation of a candidate effector gene. Microbiol Res. 232:126375. doi:10.1016/j.micres.2019.126375.
Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, et al. 2009. Thegenome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618.
Covey PA, Kuwitzky B, Hanson M, Webb KM. 2014. Multilocus analysis using putative fungal effectors to describe a population of Fusarium oxysporum from sugar beet. Phytopathology 104:886–896. https://doi .org/10.1094/PHYTO-09-13-0248-R.
Cramer C. 2000. Breeding and genetics of Fusarium basal rot resistance in onion. Euphytica. 115:159-166.
De Wit, P.J.G.M.; Mehrabi, R.; Van Den Burg, H.A.; Stergiopoulos, I. Fungal Effector Proteins: Past, Present and Future. 2009. Mol. Plant. Pathol. 10:735–747.
Entwistle AR. 1990. Root diseases. In: Rabinowitch HD, Brewster JL (eds) Onions and allied crops, vol II. CRC Press, Boca Raton, FL, pp 103–154.
Fraser?Smith S, Czislowski E, Meldrum R, Zander M, O’Neill W, Balali G. 2014. Sequence variation in the putative effector gene SIX8 facilitates molecular differentiation of Fusarium oxysporum f. sp. cubense. Plant Pathol. 63(5): 1044–52
Galván GA, Koning-Boucoiran CFS, Koopman WJM, Burger-Meijer K, González PH, Waalwijk C, Kik C dan Scholten OE 2008. Genetic variation among Fusarium isolates from onion, and resistance to Fusarium basal rot in related Allium species. Eur J Plant Pathol. 121:499–512.
Geiser DM, Klich MA, Frisvad JC, Peterson SW, Varga J, and Samson RA. 2007. The current status of species recognition and identification in Aspergillus. Studies in Mycology. 5: 1–10.
Haegi A, CatalanoV, LuongoL, VitaleS, ScottonM, FiccadentiN, Belisario A. 2013. A newly developed real-time PCR assay for detection and quanti?cation of Fusarium oxysporum and its use in compatible and incompatible interactions with grafted melon genotypes. Phytopathology. 103:802–810. https://doi.org/10.1094/PHYTO-11-12-0293-R.
Hogg AC, Johnston RH, Dyer AT. 2007. Applying real-time quantitative PCR to fusarium crown rot of wheat. Plant Dis. 91:1021–1028. https://doi .org/10.1094/PDIS-91-8-1021.
Jepson SB. 2008. Fusarium rot of garlic bulb. OSU Plant Clinic. [Internet]. [diunduh 2014 Mar 12] Tersedia pada: http://www.science.oregonstate.edu/bpp/Plant_Clinic/Garlic/ Fusarium.pdf
Kageyama, K., Komatsu, T. and Suga, H. 2003. Refined PCRprotocol for detection of plant pathogens in soil. J Gen Plant Pathol. 69:153–160.
Vincelli, P. and Tisserat, N. 2008. Nucleic acid-basedpathogen detection in applied plant pathology. Plant Dis. 92:660–669.
Kuruppu PU. 1999. First report of Fusarium oxysporum causing leaf twisting disease on Allium cepa var. ascalonicum in Sri Lanka. Plant Disease. 83:695.
Lievens B, Houterman PM and Rep M. 2009. Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiol. Lett. 300:201-215.
Lievens B, Thomma BPHJ. 2005. Recent developments in pathogen detection arrays: implications for fungal plant pathogens and use in practice. Phytopathology 95:1374–1380. https://doi.org/10.1094/PHYTO -95-1374.
Mbofung GCY, Fessehaie A, Bhattacharyya MK, Leandro LFS. 2011. A new TaqMan real-time polymerase chain reaction assay for quanti?cation of Fusarium virguliforme in soil. Plant Dis 95:1420–1426. https://doi.org/10 .1094/PDIS-02-11-0120.
Maldonado BLD, Villarruel O JL, Calderón O MA, Sánchez E AC. 2018. Secreted in Xylem (Six) Genes in Fusarium oxysporum f. sp. cubense and Their Potential Acquisition by Horizontal Transfer. Adv Biotech & Micro. 10(1): 555779. doi: 10.19080/AIBM.2018.10.5557780012
Rabiei-Motlagh E, Falahati-Rastegar M, Rouhani H, Jafarpour B, Jahanbakhsh V. 2010. Root disease of onion caused by root colonizing fungi in northeast of Iran. American-Eurasian J. Agric & Environ. Sci. 7(4): 484-491.
Recorbet G, Steinberg C, Olivain C, Edel V, Trouvelot S, Dumas-Gaudot E, Gianinazzi S, Alabouvette C. 2003. Wanted: pathogenesis-related marker molecules for Fusarium oxysporum. New Phytol 159:73–92. https://doi .org/10.1046/j.1469-8137.2003.00795.x.
Singha IM, Kakoty Y, Unni BG, Das J, Kalita MC. 2016. Identification and characterization of Fusarium sp. using ITS and RAPD causing fusarium wilt of tomato isolated from Assam, North East India. Journal of Genetic Engineering and Biotechnology. 14: 99-105
Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599.
Taylor A, Vagany V, Jackson AC, Harrison RJ, Rainoni A, Clarkson JP. 2016. Identification of pathogenicity-related genes in Fusarium oxysporum f. sp. cepae. Molecular Plant Pathology. 17(7):1032–1047. DOI: 10.1111/mpp.12346.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-speci?c gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680.
Tondok ET. 2001. Twisting disease caused by Fusarium oxysporum on shallot (Allium cepa L. var. agregatum G. Don.) in Indonesia. [Disertasi]. Jerman (DE): Institute of Plant Protection, Faculty of Agriculture, Georg-August-University Geottingen, Germany.
Urban, M.; Irvine, A.G.; Cuzick, A.; Hammond-Kosack, K.E. Using the Pathogen-Host Interactions Database (PHI-Base) to Investigate Plant Pathogen Genomes and Genes Implicated in Virulence. Front. Plant Sci. 6:605.
Van Der Does HC, Lievens B, Claes L, Houterman PM, Cornelissen BJC, Rep M. 2008. The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environ Microbiol 10:1475–1485. https://doi.org/10.1111/j.1462-2920.2007.01561.x.
Van Dam P, Fokkens L, Schmidt SM, Linmans JHJ, Kistler HC, Ma L-J, Rep M. 2016. Effector pro?les distinguish formae speciales of Fusarium oxysporum. Environ Microbiol 18:4087–4102. https://doi.org/10.1111/1462 -2920.13445.
Zhang Z, Zhang J, Wang Y, Zheng X. 2005. Molecular detection of Fusarium oxysporum f. sp. niveum and Mycosphaerella melonis in infected plant tissues and soil. FEMS Microbiol Lett 249:39–47. https://doi .org/10.1016/j.femsle.2005.05.057.
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