Identification and pathogenicity of Ceratocystis manginecans causing wilt disease on Acacia mangium in Sabah, Malaysia

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NADZIRAH MOHD YUNUS
MANDY MAID
https://orcid.org/0000-0002-8025-7249
WILSON THAU LYM YONG
FIONA EVELYN ANTHONY
MAHMUD SUDIN
PAUL W. J. TAYLOR

Abstract

Abstract. Yunus NM, Maid M, Yong WTL, Anthony FE, Sudin M, Taylor PWJ. 2024. Identification and pathogenicity of Ceratocystis manginecans causing wilt disease on Acacia mangium in Sabah, Malaysia. Biodiversitas 25: 2170-2182. An alarming incidence of wilt disease has been reported in an Acacia mangium plantation in Ulu Kukut, Kota Belud District, Sabah, Malaysia. Infected trees exhibited symptoms such as severe wilting, sapwood discoloration or black lesion, and a fruity-sweet odor emanating from the fermentation exudate at the wound lesion. This is the first investigation of the causal wilt pathogen in a commercial A. mangium plantation in Ulu Kukut, located in the western region of Sabah. This study aimed to identify the causal fungal pathogen from infected A. mangium trees using morphological characterization and DNA sequence comparisons for the regions of Internal Transcribed Spacer (ITS), beta-tubulin 1 (bt1), transcription elongation factor-1 alpha (tef1), guanine nucleotide-binding protein subunit beta-like protein (ms204), and second largest subunits of RNA polymerase II (rpb2). The fungal isolates shared morphological characteristics with the wilt pathogen Ceratocystis sp., including a globose base with a long neck-ended tip with ostiolar hyphae. Sequence-based phylogenetic analysis confirmed the identity of Ceratocystis manginecans, distinguishing them from all other Ceratocystis species. Bioassays inoculating phyllodes and twigs of 1-year-old A. mangium trees confirmed that C. manginecans was the cause of wilt disease. Confirming the identity of the causal agent of the increasingly destructive and severe wilt disease aids in developing effective disease management strategies for Acacia-based plantations.

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References
Al Adawi AO, Barnes I, Khan IA, Al Subhi AM, Al Jahwari AA, Deadman ML, Wingfield B D, Wingfield MJ. 2013. Ceratocystis manginecans associated with a serious wilt disease of two native legume trees in Oman and Pakistan. Australasian Plant Pathology 42(2): 179–193. DOI: 10.1007/s13313-012-0196-5.
Al Adawi AO, Barnes I, Khan IA, Deadman ML, Wingfield BD, Wingfield, MJ. 2014. Clonal structure of Ceratocystis manginecans populations from mango wilt disease in Oman and Pakistan. Australasian Plant Pathology, 43, 393-402.
Ambrose A, Liam J, Terhem R. 2022. New and emerging disease threats to forest plantations in Sarawak Borneo, Malaysia. In C. Bellé (ed.), Current and Emerging Challenges in the Diseases of Trees IntechOpen. DOI: 10.5772/intechopen.107027.
Barnes I, Rauf MA, Fourie A, Japarudin Y, Wingfield M. 2023. Ceratocystis manginecans and not C. fimbriata a threat to propagated Acacia spp. in Sabah, Malaysia. Journal of Tropical Forest Science 35:16–26. https://www.jstor.org/stable/48730997.
Bini D, dos Santos CA, Bouillet JP, Gonçalves JLM, Cardoso EJBN. 2013. Eucalyptus grandis and Acacia mangium in monoculture and intercropped plantations: evolution of soil and litter microbial and chemical attributes during early stages of plant development. Applied Soil Ecology 63:57–66. DOI: 10.1016/j.apsoil.2012.09.012.
Brawner J, Japarudin Y, Lapammu M, Rauf R, Boden D, Wingfield MJ. 2015. Evaluating the inheritance of Ceratocystis acaciivora symptom expression in a diverse Acacia mangium breeding population. Southern Forests 77(1): 83–90. DOI: 10.2989/20702620.2015.1007412
Chi NM, Thu PQ, Hinh TX, Dell B. 2019. Management of Ceratocystis manginecans in plantations of Acacia through optimal pruning and site selection. Australasian Plant Pathology 48(4): 343–350. DOI: 10.1007/s13313-019-00635-1.
Chi NM. 2022. Pathogenicity of Ceratocystis manginecans in inoculated Acacia roots. Indian Phytopathology 75(1): 231–237. DOI: 10.1007/s42360-021-00418-z.
Coetzee MPA, Wingfield BD, Golani GD, Tjahjono B, Gafur A, Wingfield MJ. 2011. A single dominant Ganoderma species is responsible for root rot of Acacia mangium and Eucalyptus in Sumatra. Southern Forests 73(3–4): 175–180. DOI: 10.2989/20702620.2011.639488.
EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Chatzivassiliou E, Dehnen-Schmutz K, Gilioli G, Miret JAJ, MacLeod A, Navarro MN, Niere B, Parnell S, Potting R, Rafoss T, Urek G, Bruggen AV, Van der Werf W, West J, Winter S, Santini A, Tsopelas P, Vloutoglou I, Pautasso M, Rossi V. 2016. Risk assessment and reduction options for Ceratocystis platani in the EU. EFSA Journal 14(12): e04640. DOI: 10.2903/j.efsa.2016.4640.
Epron D, Nouvellon Y, Mareschal L, Moreira RM, Koutika LS, Geneste B, Delgado-Rojas JS, Laclau JP, Sola G, Gonçalves JLM, Bouillet JP. 2013. Partitioning of net primary production in Eucalyptus and Acacia stands and in mixed-species plantations: two case-studies in contrasting tropical environments. Forest Ecology and Management 301:102–111. DOI: 10.1016/j.foreco.2012.10.034.
Farid AM, Terhem R, Aswad RM, Agustini L, Ho WM, Indrayadi H, Hidayati N. 2023. Diseases of Acacia and control measures in the tropics. In Forest Microbiology (pp. 375-400). Academic Press. DOI: 10.1016/B978-0-443-18694-3.00012-2.
Fourie A, Wingfield MJ, Wingfield BD, Barnes I. 2015. Molecular markers delimit cryptic species in Ceratocystis sensu stricto. Mycological Progress 14(1): 1020. DOI: 10.1007/s11557-014-1020-0.
Fourie A, Wingfield MJ, Wingfield BD, Thu PQ, Barnes I. 2016. A possible centre of diversity in South East Asia for the tree pathogen, Ceratocystis manginecans. Infection, Genetics and Evolution 41:73–83. DOI: 10.1016/j.meegid.2016.03.011.
Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61(4):1323–1330. DOI: 10.1128/aem.61.4.1323-1330.1995.
Glen M, Bougher NL, Francis AA, Nigg SQ, Lee SS, Irianto R, Barry KM, Beadle CL, Mohammed CL. 2009. Ganoderma and Amauroderma species associated with root-rot disease of Acacia mangium plantation trees in Indonesia and Malaysia. Australasian Plant Pathology 38(4):345–356. DOI: 10.1071/AP09008.
Hegde M, Palanisamy K, Yi JS. 2013. Acacia mangium Willd. a fast-growing tree for tropical plantation. Journal of Forest and Environmental Science 29(1): 1–14. DOI: 10.7747/jfs.2013.29.1.1.
IBM Corp. 2021. IBM SPSS Statistics for Windows, Version 28.0. Armonk, NY: IBM Corp.
Jacobs K, Bergdahl DR, Wingfield MJ, Halik S, Seifert KA, Bright DE, Wingfield, BD. 2004. Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycological Research 108(4): 411–418. DOI: 10.1017/S0953756204009748.
Jha SK. 2020. Identification and management of heart-rot fungi. Banko Janakari, 30(2), 71-77. DOI: 10.3126/banko.v30i2.33482.
Koutika LS, Richardson DM. 2019. Acacia mangium Willd: benefits and threats associated with its increasing use around the world. Forest Ecosystems, 6, 1-13. DOI: 10.1186/s40663-019-0159-1.
Lapammu M, Warburton P, Japarudin Y, Boden D, Wingfield M, Brawner J. 2023. Verification of tolerance to infection by Ceratocystis manginecans in clones of Acacia mangium. Journal of Tropical Forest Science 35:42–50. https://www.jstor.org/stable/48730999.
Lee KL, Ong KH, King PJH, Chubo JK, Su DSA. 2015. Stand productivity, carbon content, and soil nutrients in different stand ages of Acacia mangium in Sarawak, Malaysia. Turkish Journal of Agriculture and Forestry 39(1): 18. DOI: 10.3906/tar-1404-20.
Lee SS. 2018. Observations on the successes and failures of Acacia plantations in Sabah and Sarawak and the way forward. Journal of Tropical Forest Science 30(5):468–475. DOI: 10.26525/jtfs2018.30.5.468475.
Lehtijärvi A, Oskay F, Do?mu? Lehtijärvi HT, Aday Kaya AG, Pecori F, Santini A, Woodward S. 2018 Ceratocystis platani is killing plane trees in Istanbul (Turkey). Forest Pathology, 48(1): e12375. DOI: 10.1111/efp.12375.
Lelana NE, Dendang B, Anggraeni I. 2020. Molecular identification of rust disease on Acacia mangium collected from West Java, Indonesia. IOP Conference Series: Earth and Environmental Science, 468(1), 012044. DOI: 10.1088/1755-1315/468/1/012044.
Li Y, Steenwyk JL, Chang Y, Wang Y, James TY, Stajich JE, Spatafora JW, Groenewald M, Dunn CW, Hittinger CT, Shen XX, Rokas A. 2021. A genome-scale phylogeny of the kingdom Fungi. Current Biology 31(8):653–1665. DOI: 10.1016/j.cub.2021.01.074.
Lopes UP, Zambolim L, Pinho DB, Barros AV, Costa H, Pereira OL. 2014. Postharvest rot and mummification of strawberry fruits caused by Neofusicoccum parvum and N. kwambonambiense in Brazil. Tropical Plant Pathology 39(2):178–183. DOI: 10.1590/S1982-56762014000200009.
Maid M, Latif AA, Gan E, Salfinas N, Kitingan C, Maycock CR, Ratnam W. 2018. First report of stem canker disease on Acacia mangium induced by Lasiodiplodia theobromae and Lasiodiplodia pseudotheobromae species in Sabah, Malaysia. Malaysian Applied Biology, 47(3), 147–151. DOI:
Maid M, Ratnam W. 2014. Incidences and severity of vascular wilt in Acacia mangium plantations in Sabah, Malaysia. AIP Conference Proceedings 1614:784–789. DOI: 10.1063/1.4895302.
Midgley SJ, Turnbull JW. 2003. Domestication and use of Australian acacias: case studies of five important species. Australian Systematic Botany 16(1):89–102. DOI: 10.1071/SB01038.
Mohammed CL, Barry KM, Irianto RSB. 2006. Heart rot and root rot in Acacia mangium: identification and assessment. In K. Potter, A. Rimbawanto, C. Beadle (eds.), Heart Rot and Root Rot in Tropical Acacia Plantations. ACIAR Proceedings No. 124 (pp. 26–33). Canberra: Australian Centre for International Agricultural Research (ACIAR).
Moller WJ, DeVay JE. 1968. Carrot as a species-selective isolation medium for Ceratocystis fimbriata. Phytopathology 58(1):123–124.
Nair PR, Kumar BM, Nair VD, Nair PR, Kumar BM, Nair VD. 2021. Multipurpose Trees (MPTs) and Other Agroforestry Species. An Introduction to Agroforestry: Four Decades of Scientific Developments, 281-351. DOI: 10.1007/978-3-030-75358-0_13.
Naranjo-Ortiz MA, Gabaldón T. 2019. Fungal evolution: diversity, taxonomy and phylogeny of the Fungi. Biological Reviews 94(6):2101–2137. DOI: 10.1111/brv.12550.
Newman L, Duffus ALJ, Lee C. 2016. Using the free program MEGA to build phylogenetic trees from molecular data. The American Biology Teacher 78(7):608–612. DOI: 10.1525/abt.2016.78.7.608.
Oliveira LSS, Guimarães LMS, Ferreira MA, Nunes AS, Pimenta LVA, Alfenas AC. 2015. Aggressiveness, cultural characteristics and genetic variation of Ceratocystis fimbriata on Eucalyptus spp. Forest Pathology 45(6):505–514. DOI: 10.1111/efp.12200.
Pornsuriya C, Sunpapao A. 2015. A new sudden decline disease of bullet wood in Thailand is associated with Ceratocystis manginecans. Australasian Plant Disease Notes 10(1):26. DOI: 10.1007/s13314-015-0176-z.
Sang PM, Lamb D, Bonner M, Schmidt S. 2013. Carbon sequestration and soil fertility of tropical tree plantations and secondary forest established on degraded land. Plant and Soil 362(1–2):187–200. DOI: 10.1007/s11104-012-1281-9.
Sitters J, Edwards PJ, Venterink HO. 2013. Increases of soil C, N, and P pools along an Acacia tree density gradient and their effects on trees and grasses. Ecosystems 16(2):347–357. DOI: 10.1007/s10021-012-9621-4.
Sudin M, Lee SS, Hj. Harun A. 1993. A survey of heart rot in some plantations of Acacia mangium in Sabah. Journal of Tropical Forest Science, 6(1), 37–47. http://www.jstor.org/stable/43581714.
Syazwan SA, Mohd-Farid A, Wan-Muhd-Azrul WA, Syahmi HM, Mohd Zaki A, Ong SP, Mohamed R. 2021. Survey, identification, and pathogenicity of Ceratocystis fimbriata complex associated with wilt disease on Acacia mangium in Malaysia. Forests 12(12): 1782. DOI: 10.3390/f12121782.
Tamura K, Stecher G, Kumar S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38(7):3022–3027. DOI: 10.1093/molbev/msab120.
Tarigan M, Roux J, Van Wyk M, Tjahjono B, Wingfield MJ. 2011a. A new wilt and dieback disease of Acacia mangium associated with Ceratocystis manginecans and C. acaciivora sp. nov. in Indonesia. South African Journal of Botany 77(2):292–304. DOI: 10.1016/j.sajb.2010.08.006.
Tarigan M, Wingfield MJ, van Wyk M, Tjahjono B, Roux J. 2011b. Pruning quality affects infection of Acacia mangium and A. crassicarpa by Ceratocystis acaciivora and Lasiodiplodia theobromae. Southern Forests 73(3–4):187–191. DOI: 10.2989/20702620.2011.639498.
Thu PQ, Qynh DN, Dell B. 2012. Ceratocystis sp. causes crown wilt of Acacia spp. planted in some ecological zones of Vietnam. In C. Mohammed C, Beadle J, Roux S, Rahayu (eds.) Proceeding of International Conference on The Impact of Climate Change to Forest Pests and Diseases in The Tropics (pp. 38–44). Vienna: International Union of Forest Research Organizations (IUFRO).
Trang TT, Eyles A, Davies N, Glen M, Ratkowsky D, Mohammed C. 2018. Screening for host responses in Acacia to a canker and wilt pathogen, Ceratocystis manginecans. Forest Pathology, 48(1), e12390. DOI: 10.1111/efp.12390.
Udarbe MP, Hepburn AJ. 1986. Development of Acacia mangium as a plantation species in Sabah. In J. W. Turnbull (ed.), Australian Acacias in Developing Countries. Proceedings of an International Workshop held at The Forestry Training Centre, Gympie, Qld., Australia. ACIAR Proceedings No. 16 (pp. 157–159) Canberra: Australian Centre for International Agricultural Research (ACIAR).
Unchi S. 2010. A three-decade Acacia mangium. Sepilok Bulletin 12:57–61.
Van Wyk M, Al Adawi AO, Khan IA, Deadman ML, Al Jahwari AA, Wingfield BD, Ploetz R, Wingfield MJ. 2007. Ceratocystis manginecans sp. nov., causal agent of a destructive mango wilt disease in Oman and Pakistan. Fungal Diversity 27:213–230.
Wingfield M, Wingfield B, Warburton P, Japarudin Y, Lapammu M, Rauf MA, Boden D, Barnes I. 2023. Ceratocystis wilt of Acacia mangium in Sabah: understanding the disease and reducing its impact. Journal of Tropical Forest Science 35:51–66. https://www.jstor.org/stable/48731000.
Wingfield MJ, Barnes I, de Beer ZW, Roux J, Wingfield BD, Taerum SJ. 2017. Novel associations between ophiostomatoid fungi, insects and tree hosts: current status—future prospects. Biological Invasions 19(11):3215–3228. DOI: 10.1007/s10530-017-1468-3.
Yadeta KA, Thomma BPHJ. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Frontiers in Plant Science 4:97. DOI: 10.3389/fpls.2013.00097. Kashyap A, Planas-Marquès M, Capellades M, Valls M, Coll NS. 2021. Blocking intruders: inducible physico-chemical barriers against plant vascular wilt pathogens. Journal of Experimental Botany, 72(2), 184-198. DOI: 10.1093/jxb/eraa444.

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