Sains Malaysiana 53(11)(2024): 3573-3591

http://doi.org/10.17576/jsm-2024-5311-03

 

Pengenalpastian dan Pencirian Lokus Jenis Pengawanan (mat) yang Mengawal Proses Pengawanan Seksual Kulat Patogen Kelapa Sawit Ganoderma boninense

(Identification and Characterization of the Mating Type (MAT) Loci that Control the Sexual Mating Process of the Oil Palm Pathogenic Fungus Ganoderma boninense)

 

ANIS FARHAN FATIMI AB WAHAB^1,2, IZWAN BHARUDIN¹, SHARMILAH VETARYAN², FARAH DIBA ABU BAKAR¹ & ABDUL MUNIR ABDUL MURAD^1,*

 

¹Department of Biological Sciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangssan Malaysia, 43600 UKM Bangi, Selangor, Malaysia

²FGV R&D Sdn. Bhd., FGV Innovation Centre (Biotechnology), PT. 23417 Lengkuk Teknologi, 71760 Bandar Enstek, Negeri Sembilan, Malaysia

 

Received: 29 April 2024/Accepted: 7 August 2024

 

Abstrak

Ganoderma boninense merupakan kulat patogen utama penyebab penyakit reput pangkal batang (BSR) terhadap tanaman kelapa sawit. Sepanjang kitar hidupnya, kulat ini menghasilkan dua jenis miselium iaitu miselium monokarion dan miselium dwikarion. Walau bagaimanapun, hanya miselium dwikarion (miselium sekunder) sahaja yang berkeupayaan untuk menjangkiti pokok kelapa sawit. Miselium dwikarion terbentuk apabila dua miselium monokarion yang membawa lokus jenis pengawanan berbeza, bertemu, melakur dan seterusnya mengawan untuk membentuk miselium dwikarion. Sehingga kini, masih tiada penelitian dilakukan terhadap gen jenis pengawanan yang terdapat pada lokus jenis pengawanan kulat ini. Oleh itu, objektif kajian ini adalah untuk mengenal pasti gen jenis pengawanan kulat G. boninensemenggunakan kaedah perlombongan data genom G. boninenseG3 yang terdapat pada pangkalan NCBI dan mencirikan gen tersebut secara in-silico. Berdasarkan analisis yang dilakukan, dua lokus jenis pengawanan, iaitu lokus jenis pengawanan A (matA) yang menempatkan gen mengekod faktor transkripsi homeodomain 1 (HD1) dan homeodomain 2 (HD2), dan lokus jenis pengawanan B (matB) yang menempatkan lapan gen ste3 yang mengekod protein reseptor feromon dan lima gen phr yang mengekod protein pelopor feromon pengawanan telah berjaya dikenal pasti masing-masing terletak pada LG-2 dan LG-7. Kebanyakan gen jenis pengawanan ini menunjukkan variasi jujukan yang tinggi dengan gen jenis pengawanan daripada Ganoderma sp. yang lain. Kesimpulannya, kehadiran dua lokus jenis pengawanan dalam genom G. boninenseini telah mengesahkan secara molekul bahawa pengawanan seksual kulat ini dikawal oleh sistem pengawanan jenis tetrakutub.

 

Kata kunci: Ganoderma boninense; lokus jenis pengawanan; penyakit reput pangkal batan

 

Abstract

Ganoderma boninense is the main causal agent for basal stem rot (BSR) disease in oil palm. During its life cycle, this fungus produces two types of mycelia, known as the monokaryotic and dikaryotic mycelia. However, only dikaryotic mycelia are capable of infecting the living oil palm and causing the BSR disease. Dikaryotic mycelia are formed when two compatible monokaryons successfully mate. However, the mating components and process for this fungus are poorly understood at the molecular level. Hence, the objectives of this study were to identify proteins that may be involved in the mating process via genome mining using the G. boninense G3 genome database and to perform in-silico characterization on the identified putative mating-type genes. Based on the analysis, two mating-type loci, known as the mating-type A (matA) locus where the homeodomain 1 (HD1) and homeodomain 2 (HD2) genes reside, and the mating-type B (matB) locus where eight ste3 and five phr genes are located, have been successfully discovered at LG-2 and LG-7, respectively. Even among Ganoderma species, the majority of mating-type genes show significant sequence variation. In conclusion, the presence of two mating-type loci in the G. boninense G3 genome has molecularly confirmed that this fungus harbors the tetrapolar mating system that governs its sexual reproduction process.

 

Keywords: Basal stem rot disease; Ganoderma boninense; mating-type loci

 

REFERENCES

Ab Wahab, A.F.F., Ahmad Zairun, M., Mohd Daud, K.H., Abu Bakar, F.D., Bharudin, I. & Murad, A.M.A. 2022. Evaluation and improvement of protocols for Ganoderma boninense protoplast isolation and regeneration. Malaysian Applied Biology 51: 43-57.

Acuña-Amador, L., Primot, A., Cadieu, E., Roulet, A. & Barloy-Hubler, F. 2018. Genomic repeats, misassembly and reannotation: A case study with long-read resequencing of Porphyromonas gingivalis reference strains. BMC Genomics 19: 54.

Alexander, A., Sipaut, C.S., Dayou, J. & Chong, K-P. 2017. Oil palm roots colonisation by Ganoderma boninense: An insight study using scanning electron microscopy. Journal of Oil Palm Research 29: 262-266.

Aravind, L., Anantharaman, V., Balaji, S., Babu, M.M. & Iyer, L.M. 2005. The many faces of the helix-turn-helix domain: Transcription regulation and beyond. FEMS Microbiology Reviews 29: 231-262.

Auxier, B., Scholtmeijer, K., van Peer, A.F., Baars, J.J., Debets, A.J. & Aanen, D.K. 2021. Cytoplasmic mixing, not nuclear coexistence, can explain somatic incompatibility in basidiomycetes. Microorganisms 9(6): 1248.

Bahari, M.N.A., Sakeh, N.M., Abdullah, S.N.A., Ramli, R.R. & Kadkhodaei, S. 2018 Transciptome profiling at early infection of Elaeis guineensis by Ganoderma boninense provides novel insights on fungal transition from biotrophic to necrotrophic phase. BMC Plant Biology 18: 377.

Bartas, M., Červeň, J., Guziurová, S., Slychko, K. & Pečinka, P. 2021. Amino acid composition in various types of nucleic acid-binding proteins. International Journal of Molecular Sciences 22(2): 922.

Bharudin, I., Ab Wahab, A.F.F., Abd Samad, M.A., Xin Yie, N., Zairun, M.A., Abu Bakar, F.D. & Murad, A.M.A. 2022. Review update on the life cycle, plant–microbe interaction, genomics, detection and control strategies of the oil palm pathogen Ganoderma boninense. Biology 11: 251.

Bucci, G., Bentivoglio, D. & Finco, A. 2018. Precision agriculture as a driver for sustainable farming systems: State of art in literature and research. Calitatea 19: 114-121.

Casselton, L.A. & Olesnicky, N.S. 1998. Molecular genetics of mating recognition in basidiomycete fungi. Microbiology and Molecular Biology Reviews 62: 55-70.

Chan, J.J., Latiffah, Z., Liew, K.W. & Idris, A.S. 2011. Pathogenicity of monokaryotic and dikaryotic mycelia of Ganoderma boninense on oil palm seedlings and germinated seeds in Malaysia. Australasian Plant Pathology 40: 222-227.

Chong, K.P., Dayou, J. & Alexander, A. 2017. Pathogenic nature of Ganoderma boninense and basal stem rot disease. In Detection and Control of Ganoderma boninense in Oil Palm Crop, edited by Chong, K.P., Dayou, J. & Alexander, A. Cham: Springer International Publishing. pp. 5-12.

Clark-Cotton, M.R., Jacobs, K.C. & Lew, D.J. 2022. Chemotropism and cell-cell fusion in fungi. Microbiology and Molecular Biology Reviews 86: e00165-00121.

Coelho, M.A., Bakkeren, G., Sun, S., Hood, M.E. & Giraud, T. 2017. Fungal sex: The Basidiomycota. Microbiology Spectrum 5(3). https://doi.org/10.1128/microbiolspec.funk-0046-2016

Defitri, Y. 2017. Identifikasi patogen penyebab penyakit tanaman sawit (Elaeis guineensis Jacq.) di Desa Bertam Kecamatan Jambi Luar Kota. Jurnal Ilmiah Universitas Batanghari Jambi 15: 129-133.

Foulongne-Oriol, M., Taskent, O., Kües, U., Sonnenberg, A.S., van Peer, A.F. & Giraud, T. 2021. Mating-type locus organization and mating-type chromosome differentiation in the bipolar edible button mushroom Agaricus bisporus. Genes 12: 1079.

Fraser, J.A. & Heitman, J. 2003. Fungal mating-type loci. Current Biology 13: R792-R795.

Fraser, J.A., Hsueh, Y.P., Findley, K.M. & Heitman, J. 2007. Evolution of the mating‐type locus: The basidiomycetes. In Sex in Fungi: Molecular Determination and Evolutionary Implications, edited by Heitman, J., Kronstad, J.W., Taylor, J.W. & Casselton, l.A. Washington: ASM Press. hlm. 19-34.

Gao, W., Qu, J., Zhang, J., Sonnenberg, A., Chen, Q., Zhang, Y. & Huang, C. 2018. A genetic linkage map of Pleurotus tuoliensis integrated with physical mapping of the de novo sequenced genome and the mating type loci. BMC Genomics 19(1): 18.

Govender, N. & Wong, M.Y. 2017. Detection of oil palm root penetration by Agrobacterium-mediated transformed Ganoderma boninense, expressing green fluorescent protein. Phytopathology 107: 483-490.

Guan, D., McCarthy, S.A., Wood, J.M., Sims, Y., Chow, W., Ning, Z., Howe, K., Wang, G., Wang, Y. & Durbin, R. 2022. Genome sequence assembly evaluation using long-range sequencing data. bioRxiv https://doi.org/10.1101/2022.05.10.491304

Heimel, K., Scherer, M., Schuler, D. & Kämper, J. 2010. The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. The Plant Cell 22: 2908-2922.

Hushiarian, R., Yusof, N.A. & Dutse, S.W. 2013. Detection and control of Ganoderma boninense: Strategies and perspectives. SpringerPlus 2: 555.

James, T.Y., Srivilai, P., Kües, U. & Vilgalys, R. 2006. Evolution of the bipolar mating system of the mushroom Coprinellus disseminatus from its tetrapolar ancestors involves loss of mating-type-specific pheromone receptor function. Genetics 172: 1877-1891.

James, T.Y., Sun, S., Li, W., Heitman, J., Kuo, H-C., Lee, Y-H., Asiegbu, F.O. & Olson, Å. 2013. Polyporales genomes reveal the genetic architecture underlying tetrapolar and bipolar mating systems. Mycologia 105: 1374-1390.

Jones Jr., S.K. & Bennett, R.J. 2011. Fungal mating pheromones: Choreographing the dating game. Fungal Genetics and Biology 48: 668-676.

Käll, L., Krogh, A. & Sonnhammer, E.L. 2007. Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Research 35: W429-W432.

Kothe, E. 2001. Mating-type genes for basidiomycete strain improvement in mushroom farming. Applied Microbiology and Biotechnology 56: 602-612.

Krogh, A., Larsson, B., Von Heijne, G. & Sonnhammer, E.L. 2001. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. Journal Of Molecular Biology 305: 567-580.

Kües, U. & Casselton, L.A. 1992. Homeodomains and regulation of sexual development in basidiomycetes. Trends Genet 8: 154-155.

Kües, U., James, T.Y. & Heitman, J. 2011. 6 mating type in basidiomycetes: Unipolar, bipolar, and tetrapolar patterns of sexuality. In Evolution of Fungi and Fungal-Like Organisms, edited by Pöggeler, S. & Wöstemeyer, J. Heidelberg: Springer. hlm. 97-160.

Kües, U., Nelson, D.R., Liu, C., Yu, G-J., Zhang, J., Li, J., Wang, X-C. & Sun, H. 2015. Genome analysis of medicinal Ganoderma spp. with plant-pathogenic and saprotrophic life-styles. Phytochemistry 114: 18-37.

Kües, U., Granado, J., Hermann, R., Boulianne, R., Kertesz-Chaloupková, K. & Aebi, M. 1998. The A mating type and blue light regulate all known differentiation processes in the basidiomycete Coprinus cinereus. Molecular and General Genetics 260: 81-91.

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547-1549.

Kurihara, J., Koo, V-C., Guey, C.W., Lee, Y.P. & Abidin, H. 2022. Early detection of basal stem rot disease in oil palm tree using unmanned aerial vehicle-based hyperspectral imaging. Remote Sensing 14: 799.

Latifah Zakaria & Ho, Y.W. 2005. Morphological characteristics and somatic incompatibility of ganoderma from infected oil palm from three inland estates. Malaysian Journal of Microbiology 1(2): 46-52.

Lee, S.C., Ni, M., Li, W., Shertz, C. & Heitman, J. 2010. The evolution of sex: A perspective from the fungal kingdom. Microbiology and Molecular Biology Reviews 74: 298-340.

Liebscher, I., Cevheroğlu, O., Hsiao, C.C., Maia, A.F., Schihada, H., Scholz, N., Soave, M., Spiess, K., Trajković, K., Kosloff, M. & Promel, S. 2021. A guide to adhesion GPCR research. The FEBS Journal 289(24): 7610-7630.

Maluin, F.N., Hussein, M.Z. & Idris, A.S. 2020. An overview of the oil palm industry: Challenges and some emerging opportunities for nanotechnology development. Agronomy 10: 356.

Martinez, D., Challacombe, J., Morgenstern, I., Hibbett, D., Schmoll, M., Kubicek, C.P., Ferreira, P., Ruiz-Duenas, F.J., Martinez, A.T. & Kersten, P. 2009. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proceedings of the National Academy of Sciences 106: 1954-1959.

Midekso, F.D. & Yi, G. 2022. RFfiller: A robust and fast statistical algorithm for gap filling in draft genomes. PeerJ 10: e14186.

Miller, R.N.G., Holderness, M., Bridge, P.D., Chung, G.F. & Zakaria, M.H. 1999. Genetic diversity of Ganoderma in oil palm plantings. Plant Pathology 48: 595-603.

Murphy, D.J., Goggin, K. & Paterson, R.R.M. 2021. Oil palm in the 2020s and beyond: Challenges and solutions. CABI Agriculture and Bioscience  2: 39.

Nasehi, A., Sathyapriya, H. & Wong, M. 2020. First report of leaf spot on oil palm caused by Phyllosticta capitalensis in Malaysia. Plant Disease 104(1). https://doi.org/10.1094/PDIS-06-19-1232-PDN

Omasits, U., Ahrens, C.H., Müller, S. & Wollscheid, B. 2014. Protter: Interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30: 884-886.

Parveez, G.K.A., Tarmizi, A.H.A., Sundram, S., Loh, S.K., Ong-Abdullah, M., Palam, K.D.P., Salleh, K.M., Ishak, S.M. & Idris, Z. 2021. Oil palm economic performance in Malaysia and R&D progress in 2020. Journal of Oil Palm Research 33(2): 181-214.

Paterson, R.R.M. 2020. Oil palm survival under climate change in Kalimantan and alternative SE Asian palm oil countries with future basal stem rot assessments. Forest Pathology 50: e12604.

Paterson, R.R.M. 2019. Ganoderma boninense disease of oil palm to significantly reduce production after 2050 in Sumatra if projected climate change occurs. Microorganisms 7(1): 24.

Pilotti, C.A. Sanderson, F.R. & Aitken, E.A.B. 2002. Sexuality and interactions of monokaryotic and dikaryotic mycelia of Ganoderma boninense. Mycological Research 106(11): 1315-1322.

Piskacek, M., Havelka, M., Rezacova, M. & Knight, A. 2016. The 9aaTAD transactivation domains: From Gal4 to p53. PLoS ONE 11: e0162842.

Pornsuriya, C., Sunpapao, A., Srihanant, N., Worapattamasri, K., Kittimorakul, J., Phithakkit, S. & Petcharat, V. 2013. A survey of diseases and disorders in oil palms of southern Thailand. Plant Pathology Journal 12: 169-175.

Ramli, N.R., Mohamed, M.S., Seman, I.A., Zairun, M.A. & Mohamad, N. 2016. The potential of endophytic bacteria as a biological control agent for Ganoderma disease in oil palm. Sains Malaysiana 45(3): 401-409.

Raudaskoski, M. & Kothe, E. 2010. Basidiomycete mating type genes and pheromone signaling. Eukaryotic Cell 9: 847-859.

Riffiani, R., Chen, F-C., Zhang, W., Wada, T., Shimomura, N., Yamaguchi, T. & Aimi, T. 2021. Identification, characterization and expression of A-mating type genes in monokaryons and dikaryons of the edible mushroom Mycoleptodonoides aitchisonii (Bunaharitake). Mycoscience 62(2): 106-114.

Riquelme, M., Challen, M.P., Casselton, L.A. & Brown, A.J. 2005. The origin of multiple B mating specificities in Coprinus cinereus. Genetics 170: 1105-1119.

Shirouzu, T., Osono, T. & Hirose, D. 2014. Resource utilization of wood decomposers: Mycelium nuclear phases and host tree species affect wood decomposition by Dacrymycetes. Fungal Ecology 9: 11-16.

Sigrist, C.J., De Castro, E., Cerutti, L., Cuche, B.A., Hulo, N., Bridge, A., Bougueleret, L. & Xenarios, I. 2012. New and continuing developments at PROSITE. Nucleic Acids Research 41: D344-D347.

Srivilai, P. & Loutchanwoot, P. 2009. Coprinopsis cinerea as a model fungus to evaluate genes underlying sexual development in basidiomycetes. Pakistan Journal of Biological Sciences 12: 821-835.

Susanto, A., Sudharto, P. & Purba, R. 2005. Enhancing biological control of basal stem rot disease (Ganoderma boninense) in oil palm plantations. Mycopathologia 159: 153-157.

Taylor, J.W., Branco, S., Gao, C., Hann-Soden, C., Montoya, L., Sylvain, I. & Gladieux, P. 2017. Sources of fungal genetic variation and associating it with phenotypic diversity. The Fungal Kingdom 5(5). https://doi.org/10.1128/microbiolspec.funk-0057-2016

Tsirigos, K.D., Peters, C., Shu, N., Käll, L. & Elofsson, A. 2015. The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Research 43: W401-W407.

Tusnady, G.E. & Simon, I. 2001. The HMMTOP transmembrane topology prediction server. Bioinformatics 17: 849-850.

Vaillancourt, L.J., Raudaskoski, M., Specht, C.A. & Raper, C.A. 1997. Multiple genes encoding pheromones and a pheromonereceptor define the Bb1 mating-type specificity in Schizophyllum commune. Genetics 146: 541-551.

Van Peer, A.F., Park, S-Y., Shin, P-G., Jang, K-Y., Yoo, Y-B., Park, Y-J., Lee, B-M., Sung, G-H., James, T.Y. & Kong, W-S. 2011. Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions. PLoS ONE 6: e22249.

Vreeburg, S., Nygren, K. & Aanen, D.K. 2016. Unholy marriages and eternal triangles: How competition in the mushroom life cycle can lead to genomic conflict. Phil. Trans. R. Soc. B 371: 20150533.

Wendland, J., Vaillancourt, L., Hegner, J., Lengeler, K., Laddison, K., Specht, C.A., Raper, C.A. & Kothe, E. 1995. The mating-type locus Bα1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J. 14(21): 5271-5278.

Wirth, S., Freihorst, D., Krause, K. & Kothe, E. 2021. What role might non-mating receptors play in Schizophyllum commune? Journal of Fungi 7: 399.

Wong, W., Tung, H., Fadhilah, M.N., Midot, F., Lau, S., Melling, L., Astari, S., Hadziabdic, Đ., Trigiano, R. & Goh, K. 2021. Genetic diversity and gene flow amongst admixed populations of Ganoderma boninense, causal agent of basal stem rot in African oil palm (Elaeis guineensis Jacq.) in Sarawak (Malaysia), Peninsular Malaysia, and Sumatra (Indonesia). Mycologia 113: 902-917.

Yusoff, A., M. Ashaari, F.H., Abd Samad, M.A., Ab Wahab, A.F.F. & Bharudin, I. 2021. Identification of soil bacteria with antifungus activity towards palm oil pathogen, Ganoderma boninense. Sains Malaysiana 50(12): 3557-3567.

 

*Corresponding author; email: munir@ukm.edu.my