Abstract
Sheath rot disease seriously limits rice productivity in several countries. In this study, Fusarium spp. were proven to be major pathogens responsible for sheath rot disease in Indonesia. The disease was initially found in 13 provinces in Indonesia. A total of 287 fungal isolates was obtained from 900 sampled leaf sheaths, and all of them were shown to be pathogenic to rice plants by artificial inoculation. Molecular identification of sheath rot pathogens was performed using the translation elongation factor 1-alpha (TEF1-α) gene sequencing. Morphological characterization was conducted using synthetic low-nutrient agar (SNA) using filter paper. Species within the Fusarium incarnatum-equiseti species complex (FIESC) and the Fusarium fujikuroi species complex (FFSC) were the major taxa found to be associated with the disease. The FIESC included Fusarium bubalinum, F. hainanense, F. sulawesiense and F. tanahbumbuense. The FFSC included F. andiyazi, F. fujikuroi, F. proliferatum, F. pseudocircinatum, and F. sacchari. Fusarium grosmichelii, a member of the Fusarium oxysporum species complex (FOSC), and a species within the Fusarium solani species complex (FSSC) were also found to be associated with the disease. The species in the FIESC and the FFSC are morphologically difficult to distinguish; however, some FFSC species have some diagnostic traits. This is the first study to identify the Fusarium spp. causing sheath rot disease in Indonesia through field survey, fungal isolation, pathogenicity test, molecular identification, and morphological characterization.
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References
Abbas HK, Cartwright RD, Shier WT, Abouzied MM, Bird CB, Rice LG et al (1998) Natural occurrence of fumonisins in rice with Fusarium sheath rot disease. Plant Dis 82:22–25. https://doi.org/10.1094/PDIS.1998.82.1.22
Aoki T, O’Donnell K, Homma Y, Lattanzi AR (2003) Sudden-death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex–F. virguliforme in North America and F. tucumaniae in South America. Mycologia 95:660–684
Badan Informasi Geospasial Republik Indonesia (2015–2019) Peta Rupabumi Digital Indonesia. Bogor, Jawa-Barat. http://tanahair.indonesia.go.id/portal-web/. Accessed 1 Mar 2020
Bashyal BM, Aggarwal R, Sharma S, Gupta S, Rawat K, Singh D, Singh AK, Gopala Krishnan S (2016) Occurrence, identification and pathogenicity of Fusarium species associated with bakanae disease of basmati rice in India. Eur J Plant Pathol 144:457–466. https://doi.org/10.1007/s10658-015-0783-8
Bigirimana VP, Hua GKH, Nyamangyoku OI, Höfte M (2015) Rice sheath rot: An emerging ubiquitous destructive disease complex. Front Plant Sci 6:1–16. https://doi.org/10.3389/fpls.2015.01066
Choi YW, Hyde KD, Ho WH (1999) Single spore isolation of fungi. Fungal Divers 3:29–38
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Duan CX, Du Q, Tang ZL, Li SC, Wang BB (2019) First report of maize ear rot caused by Fusarium sacchari in China. Plant Dis 103:2674. https://doi.org/10.1094/PDIS-04-19-0829-PDN
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Fan J, Yang J, Wang YQ, Li GB, Li Y, Huang F, Wang WM (2016) Current understanding on Villosiclava virens, a unique flower-infecting fungus causing rice false smut disease. Mol Plant Pathol 17:1321–1330. https://doi.org/10.1111/mpp.12362
Fisher PJ, Petrini O (1992) Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L.). New Phytol 120:137–143. https://doi.org/10.1111/j.1469-8137.1992.tb01066.x
Freeman S, Sharon M, Maymon M, Mendel Z, Protasov A, Aoki T et al (2013) Fusarium euwallaceae sp. nov.–a symbiotic fungus of Euwallacea sp., an invasive ambrosia beetle in Israel and California. Mycologia 105:1595–1606. https://doi.org/10.3852/13-066
Gaire SP, Zhou XG, Jo YK, Shi J (2020) First report of Rhizoctonia solani AG-4 causing seedling disease in rice. Plant Dis 104:1546. https://doi.org/10.1094/PDIS-07-19-1570-PDN
Geiser DM, A Al-Hatmi, T Aoki, T Arie, V Balmas, I Barnes (2020) Phylogenomic analysis of a 55.1 kb 19-gene dataset resolves a monophyletic Fusarium that includes the Fusarium solani species complex. Phytopathology Nov 17. https://doi.org/10.1094/PHYTO-08-20-0330
Hofstetter V, Buyck B, Croll D, Viret O, Couloux A, Gindro K (2012) What if esca disease of grapevine were not a fungal disease?. Fungal Divers 54:51–67. https://doi.org/10.1007/s13225-012-0171-z
Hofstetter V, Buyck B, Eyssartier G, Schnee S, Gindro K (2019) The unbearable lightness of sequenced-based identification. Fungal Divers 96:243–284. https://doi.org/10.1007/s13225-019-00428-3
Ibrahim NF, Mohd MH, Nor NIM, Zakaria L (2016) Fusarium fujikuroi causing fusariosis of pineapple in peninsular Malaysia. Australas Plant Dis Notes 11:21. https://doi.org/10.1007/s13314-016-0206-5
Imazaki I, Kadota I (2015) Molecular phylogeny and diversity of Fusarium endophytes isolated from tomato stems. FEMS Microbiol Ecol 91:1–16. https://doi.org/10.1093/femsec/fiv098
IRRI (2013) Standard Evaluation System For Rice, 5th edn. International Rice Research Institute, Manila
Jiang SB, Lin BR, Shen HF, Yang QY, Zhang JX, Sun DY et al (2008) First report of Fusarium fujikuroi causing stem wilt on Canna edulis Ker in China. Plant Dis 102:1177. https://doi.org/10.1094/PDIS-09-17-1479-PDN
Jurado M, Marín P, Callejas C, Moretti A, Vázquez C, González-Jaén MT (2010) Genetic variability and fumonisin production by Fusarium proliferatum. Food Microbiol 27:50–57. https://doi.org/10.1016/j.fm.2009.08.001
Kasson MT, O’Donnell K, Rooney AP, Sink S, Ploetz RC, Ploetz JN et al (2013) An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. Fungal Genet Biol 56:147–157. https://doi.org/10.1016/j.fgb.2013.04.004
Kiyuna T, An KD, Kigawa R, Sano C, Miura S, Sugiyama J (2008) Mycobiota of the Takamatsuzuka and Kitora Tumuli in Japan, focusing on the molecular phylogenetic diversity of Fusarium and Trichoderma. Mycoscience 49:298–311. https://doi.org/10.1007/S10267-008-0427-3
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Laurence MH, Summerell BA, Burgess LW, Liew ECY (2011) Fusarium burgessii sp. nov. representing a novel lineage in the genus Fusarium. Fungal Divers 49:101–112. https://doi.org/10.1007/s13225-011-0093-1
Lei S, Ling W, Lianmeng L, Yuxuan H, Yihua X, Mengqi L, Jian G, Qiqin L, Shiwen H (2019) Infection and colonization of pathogenic fungus Fusarium proliferatum in rice spikelet rot disease. Rice Sci 26:60–68. https://doi.org/10.1016/j.rsci.2018.08.005
Leslie JF, Summerell BA (2006) The Fusarium Laboratory Manual. Blackwell Publishing, Iowa, USA
Lombard L, Sandoval-Denis M, Lamprecht SC, Crous PW (2019) Epitypification of Fusarium oxysporum-clearing the taxonomic chaos. Persoonia 43:1–47. https://doi.org/10.3767/persoonia.2019.43.01
Marasas WFO, Rheeder J, Lamprecht S, Zeller K, Leslie J (2001) Fusarium andiyazi sp. nov., a new species from sorghum. Mycologia 93:1203–1210. https://doi.org/10.2307/3761681
Maryani N, Sandoval-Denis M, Lombard L, Crous PW, Kemal GHJ (2019a) New endemic Fusarium species hitch-hiking with pathogenic Fusarium strains causing Panama disease in small-holder banana plots in Indonesia. Persoonia 43:48–69. https://doi.org/10.3767/persoonia.2019.43.02
Maryani N, Lombard L, Poerba YS, Subandiyah S, Crous PW, Kema GHJ (2019b) Phylogeny and genetic diversity of the banana Fusarium wilt pathogen Fusarium oxysporum f. sp. cubense in the Indonesian centre of origin. Stud Mycol 92:155–194. https://doi.org/10.1016/j.simyco.2018.06.003
Miyajima K, Tanii A, Akita T (1983) Pseudomonas fuscovaginae sp. nov., nom. rev. Int J Syst Bacteriol 33:656–657. https://doi.org/10.1099/00207713-33-3-656
Moussa TAA, Al-Zahrani HS, Kadasa NMS, Ahmed SA, de Hoog GS, Al-Hatmi AMS (2017) Two new species of the Fusarium fujikuroi species complex isolated from the natural environment. Antonie Van Leeuwenhoek 110:819–832. https://doi.org/10.1007/s10482-017-0855-1
Muraosa Y, Oguchi M, Yahiro M, Watanabe A, Yaguchi T, Kamei K (2017) Epidemiological study of Fusarium species causing invasive and superficial fusariosis in Japan. Med Mycol J 58:E5–E13. https://doi.org/10.3314/mmj.16-00024
Nakata N, Yokoyama T, Nakamura K (2018) Multiplex PCR for detecting Fusarium oxysporum, F. solani and Pythium sulcatum present in blot-like lesions of carrots. Ann Rep Kanto-Tosan Plant Protec Soc 65:39–43. https://doi.org/10.11337/ktpps.2018.39
Nalim F, Samuels G, Wijesundera R, Geiser D (2011) New species from the Fusarium solani species complex derived from perithecia and soil in the Old World tropics. Mycologia 103:1302–1330. https://doi.org/10.3852/10-307
Narayanasamy P, Viswanathan R (1990) A new scoring system for sheath rot of rice. Madras Agric J 7:256–257
Nirenberg H, O’Donnell K (1998) New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia 90:434–458. https://doi.org/10.2307/3761403
Nuryanti S, Hakim DB, Siregar H, Sawit MH (2017) Political economic analysis of rice self-sufficiency in Indonesia. Indones J Agric Sci 18:77–86. https://doi.org/10.21082/ijas.v.18.n2.2017
O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493. https://doi.org/10.2307/3761407
O'Donnell K (2000) Molecular Phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 92:919–938. https://doi.org/10.2307/3761588
O'Donnell K, Sarver BA, Brandt M, Chang DC, Noble-Wang J, Park BJ et al (2007) Phylogenetic diversity and microsphere array-based genotyping of human pathogenic Fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. J Clin Microbiol 45(7):2235–2248. https://doi.org/10.1128/JCM.00533-07
O’Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME et al (2008) Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 46:2477–1184. https://doi.org/10.1128/JCM.02371-07
O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A et al (2009a) A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Gen Biol 46:936–48. https://doi.org/10.1016/j.fgb.2009.08.006
O’Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM (2009b) Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-equiseti and F. chlamydosporum species complexes within the United States. J Clin Microbiol 47:3851–3861. https://doi.org/10.1128/JCM.01616-09
O’Donnell K, Ward TJ, Robert VARG, Crous PW, Geiser DM, Kang S (2015) DNA sequence-based identification of Fusarium: Current status and future directions. Phytoparasitica 43:583–595. https://doi.org/10.1007/s12600-015-0484-z
Ou SH (1985) Rice Diseases. 2nd Ed. The Cambrian News, United Kingdom
Prabhukarthikeyan SR, Keerthana U, Nagendran K, Yadav MK, Parameswaran C, Panneerselvam P et al (2020) First report of Fusarium proliferatum causing sheath rot disease of rice in Eastern India. Plant Dis. https://doi.org/10.1094/PDIS-08-20-1846-PDN
Pramunadipta S, Widiastuti A, Wibowo A, Priyatmojo, A (2017) Characterization of sheath rot disease in rice and environmental facors that influence the disease. Bachelor thesis, Universitas Gadjah Mada
Pramunadipta S, Widiastuti A, Wibowo A, Suga H, Priyatmojo A (2020) Short Communication : Sarocladium oryzae associated with sheath rot disease of rice in Indonesia. Biodiversitas 21:1243–1249. https://doi.org/10.13057/biodiv/d210352
Reeb V, Lutzoni F, Roux C (2004) Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32:1036–1060. https://doi.org/10.1016/j.ympev.2004.04.012
Ronquist F, Teslenko M, Van Der Mark K, Ayres DL, Darling A, Hohna S et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choise across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Sakthivel N, Gnanamanickam S (1987) Evaluation of Pseudomonas fluorescens for suppression of Sheath Rot disease and for enhancement of grain yields in rice (Oryza sativa L.). Appl Environ Microbiol 53:2056–2059. https://doi.org/10.1128/AEM.53.9.2056-2059.1987
Sakthivel N (2001) Sheath rot disease of rice: current status and control strategies. In: Sreenivasaprasad S, Johnson R (eds) Major Fungal Diseases of Rice. Springer, Dordrecht, pp 271–283
Sandoval-Denis M, Lombard L, Crous PW (2019) Back to the roots: A reappraisal of Neocosmospora. Persoonia 43:90–185. https://doi.org/10.3767/persoonia.2019.43.04
Santillan-Mendoza R, Fernandez-Pavia SP, O’Donnell K, Ploetz RC, Ortega-Arreola R, Vazquez-Marrufo G et al (2018) A novel disease of big-leaf mahogany caused by two Fusarium species in Mexico. Plant Dis 102:1965–1972. https://doi.org/10.1094/PDIS-01-18-0060-RE
Schroers HJ, Samuels GJ, Zhang N, Short DP, Juba J, Geiser DM (2016) Epitypification of Fusisporium (Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia 108:806–819. https://doi.org/10.3852/15-255
Suga H, Karugia GW, Ward T, Gale LR, Tomimura K, Nakajima T et al (2008) Molecular characterization of Fusarium graminearum species complex in Japan. Phytopathology 98:159–166. https://doi.org/10.1094/PHYTO-98-2-0159
Suga H, Kitajima M, Nagumo R, Tsukiboshi T, Uegaki R, Nakajima T et al (2014) A single nucleotide polymorphism in the translation elongation factor 1α gene correlates with the ability to produce fumonisin in Japanese Fusarium fujikuroi. Fungal Biol 118:402–412. https://doi.org/10.1016/j.funbio.2014.02.005
Summerell BA (2019) Resolving Fusarium: current status of the genus. Annu Rev Phytopathol 57:323–339. https://doi.org/10.1146/annurev-phyto-082718-100204
Stielow JB, Lévesque CA, Seifert KA, Meyer W, Iriny L, Smits D et al (2015) One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes. Persoonia 35:242–263. https://doi.org/10.3767/003158515X689135
Stöver BC, Müller KF (2010) TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinf 11:1–9. https://doi.org/10.1186/1471-2105-11-7
Swofford DL (2003) Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland. Sinauer Associates, MA, USA
Venturini G, Toffolatti SL, Quaglino F, Casati P (2017) First report of Fusarium andiyazi causing ear rot on maize in Italy. Plant Dis 101:839. https://doi.org/10.1094/PDIS-10-16-1525-PDN
Verma SK, Kingsley KL, Bergen MS, Kowalski KP, White JF (2018) Fungal disease prevention in seedlings of rice (Oryza sativa) and other grasses by growth-promoting seed-associated endophytic bacteria from invasive Phragmites australis. Microorganisms 6:1–13. https://doi.org/10.3390/microorganisms6010021
Wang MM, Chen Q, Diao YZ, Duan WJ, Ca L (2019) Fusarium incarnatum-equiseti complex from China. Persoonia 43:70–89. https://doi.org/10.3767/persoonia.2019.43.03
Wiraswati SM, Rusmana I, Nawangsih AA, Wahyudi AT (2019) Antifungal activities of bacteria producing bioactive compounds isolated from rice phyllosphere against Pyricularia oryzae. J Plant Prot Res 59:86–94. https://doi.org/10.24425/jppr.2019.126047
Wollenweber HW, Reinking OA (1935) Die Fusarien, ihre Beschreibung, Schadwirkung, und Bekämpfung. Paul Parey, Berlin
Xia JW, Sandoval-Denis M, Crous PW, Zhang XG, Lombard L (2019) Numbers to names – restyling the Fusarium incarnatum-equiseti species complex. Persoonia 43:186–221. https://doi.org/10.3767/persoonia.2019.43.05
Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA et al (2006) Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 44:2186–2190. https://doi.org/10.1128/JCM.00120-06
Zhang H, Luo W, Pan Y, Xu J, Xu JS, Chen WQ et al (2014) First report of Fusarium ear rot of maize caused by Fusarium andiyazi in China. Plant Dis 98:1428. https://doi.org/10.1094/PDIS-01-14-0038-PDN
Zhang J, Pan Y, Li Y, Ren T, Cong R, Lu J et al (2019) Low grain sink activity imposed by potassium deficiency aggravates loss in quality of rice (Oryza sativa L.) infected with natural sheath rot disease. J Cereal Sci 87:31–38. https://doi.org/10.1016/j.jcs.2019.02.010
Acknowledgements
This study has been funded by the Ministry of Research, Technology and Higher Education of the Republic of Indonesia through PMDSU number 5829/UN1.DITLIT/DIT-LIT/LT/2018. The authors thank Sri Giyanti (Universitas Gadjah Mada, Indonesia), Tomomi Katsu, and Ayako Usui (Gifu University, Japan) for their technical supports.
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42161_2021_988_MOESM1_ESM.tif
Supplementary file1 (TIF 1038 KB) The Maximum Likelihood consensus tree based on RPB2 sequence alignments of Fusarium grosmichelii, F. hexaseptatum, F. callistephi, F. cugenangense, F. duoseptatum, F tardichlamydosporum, and F. oxysporum. Bootstrap values ≥ 60% (maximum parsimony and maximum likelihood) and posterior probability ≥ 95% (Bayesian inference) are in the internodes, respectively. Acremonium sp. was used as the outgroup taxon (a). Comparison of the RPB2 sequences among Fusarium grosmichelii JBR A (OK324964), F. grosmichelii InaCC F833 (LS479295), InaCC F848 (LS479338), and InaCC F852 (LS479342) as confirmed spesies of Fusarium grosmichelii and F. hexaseptatum InaCC F866 (LS479359) (b)
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Supplementary file3 (DOCX 27 KB) a TEF1-α reference sequences to generate phylogenetic tree used in this study. b RPB2 reference sequences to generate phylogenetic tree used in this study
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Supplementary file4 (DOCX 25 KB) a The TEF1-α sequence alignments used to generate phylogenetic tree. b RPB2 sequence alignments used to generate phylogenetic tree
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Pramunadipta, S., Widiastuti, A., Wibowo, A. et al. Identification and pathogenicity of Fusarium spp. associated with the sheath rot disease of rice (Oryza sativa) in Indonesia. J Plant Pathol 104, 251–267 (2022). https://doi.org/10.1007/s42161-021-00988-x
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DOI: https://doi.org/10.1007/s42161-021-00988-x