Sains Malaysiana 51(11)(2022): 3591-3605
http://doi.org/10.17576/jsm-2022-5111-07
Characterisation
and Pathogenicity of Fusarium Species
Associated with Yellowing Disease in Black Pepper (Piper nigrum L.)
(Pencirian dan Kepatogenan Spesies Fusarium Berkaitan dengan Penyakit Kuning pada Lada Hitam (Piper nigrum L.))
SHUN
HUI CHEONG1, FRANKLIN RAGAI KUNDAT1, MUI YUN
WONG2 & YEE MIN KWAN1,3,*
1Department of
Crop Science, Faculty of Agricultural Science and Forestry, Universiti Putra Malaysia Bintulu Sarawak Campus, 97008 Bintulu, Sarawak, Malaysia
2Institute of Plantation
Studies, Universiti Putra Malaysia, 43000 UPM Serdang, Selangor Darul Ehsan,
Malaysia
3Institute
of Ecosystem Science Borneo (IEB), Universiti Putra Malaysia Bintulu Sarawak
Campus, 97008 Bintulu, Sarawak, Malaysia
Diserahkan: 13 Disember 2021/Diterima: 17 Jun 2022
Abstract
Yellowing
disease has become one of the main threats to black pepper (Piper nigrum L.) production. This study was conducted to
isolate and characterize Fusarium species
associated with yellowing disease based on morphological and molecular
characteristics, and to evaluate their pathogenicity on black pepper. Fungal isolates were recovered from symptomatic black
pepper plants located in major growing areas in Sarawak. Based on morphological
characteristics, a total of 73 Fusarium isolates were identified. Genomic DNA sequence analysis of nuclear ribosomal
DNA internal transcribed spacer (ITS) and translation elongation factor-1 alpha
(EF-1α) had confirmed the identity of the Fusarium isolates. The four identified Fusarium species were F. solani (90.4%), F. oxysporum (5.5%), F. concentricum (2.7%), and F. mangiferae (1.4%). Based
on morphological characterisation, F. solani isolates were grouped into two distinct morphotypes, morphotype I
and II. Phylogenetic analysis of F. solani has shown a high level of
intraspecific variation among the isolates. The two major clades formed were
found to correspond to the morphotype grouping.
Pathogenicity test showed that all four Fusariumspecies
are pathogenic to black pepper based on disease incidence and severity. This
study provides new insights into the Fusarium species associated with yellowing disease in black pepper, and highlights the
high genetic variability among the Fusarium isolates. This result calls for a critical revision of the current strategies
in disease management, and resistance breeding programs in black pepper.
Keywords: Fusarium solanispecies
complex; phylogeography; population genetic; root rot
disease; slow wilt
Abstrak
Penyakit kuning telah menjadi salah satu ancaman utama kepada pengeluaran lada hitam (Piper nigrum L.). Kajian ini dijalankan untuk memencil dan mencirikan spesies Fusarium yang dikaitkan dengan penyakit kuning berdasarkan ciri morfologi dan molekul serta menilai sifat kepatogenannya ke atas lada hitam. Pencilan kulat diperoleh daripada pokok lada hitam bergejala yang terdapat di kawasan penanaman utama Sarawak. Berdasarkan ciri morfologi, sebanyak 73 pencilan Fusarium telah dikenal pasti. Analisis jujukan DNA genom bagipenjarak dalaman yang ditranskripsikan (ITS) DNA ribosom nuklear dan faktor pemanjangan translasi-1 alfa (EF-1α) telah mengesahkan identiti pencilan Fusarium. Sebanyak empat spesies Fusarium yang dikenal pasti iaitu F. solani (90.4%), F. oxysporum (5.5%), F. concentricum (2.7%) dan F. mangiferae (1.4%). Berdasarkan pencirian morfologi, pencilan F. solani telah dikelaskan kepada dua morfotip yang berbeza iaitu morfotip I dan II. Analisis filogenetik F. solani telah menunjukkan tahap variasi intrakhusus yang tinggi dalam kalangan pencilan. Dua klad utama yang terbentuk didapati sepadan dengan kumpulan morfotip. Kajian kepatogenan mendedahkan bahawa kesemua empat spesies Fusarium adalah patogen kepada lada hitam berdasarkan kejadian dan keterukan penyakit. Kajian ini memberikan pandangan baharu tentang spesies Fusarium yang dikaitkan dengan penyakit kuning pada lada hitam dan menyerlahkan kebolehubahan genetik yang tinggi dalam kalangan pencilan Fusarium. Hasil kajian ini mencadangkan semakan kritikal dibuat terhadap strategi semasa dalam pengurusan penyakit dan program pembiakan kerintangan bagi lada hitam.
Kata kunci: Filogeografi; genetik populasi; kelayuan perlahan; penyakit akar reput; spesies kompleks Fusarium solani
RUJUKAN
Biju, C.N., Ishwara, B.A., Praveena, R., Senthil, K.C.M.
& Suseela, B.R. 2019. Pests and Diseases of
Black Pepper. International Pepper Community,
Jakarta, Indonesia. pp. 11-13.
Chen,
Y.S., Dayod, M. & Tawan,
C.S. 2018. Phenetic analysis of cultivated black
pepper (Piper nigrum L.) in Malaysia. International Journal of Agronomy 2018: Article ID.
3894924.
Department
of Agriculture Sarawak (DOA). 2020. Pepper. https://doa.sarawak.gov.my/page-0-0-138-Pepper.html. Accessed on November 2020
.
Doyle,
J.J. & Doyle, J.L. 1990. Isolation of plant DNA from fresh tissue. Focus 12: 13-15.
Duarte,
M.L.R. & Archer, S.A. 2003. In vitro toxin production by Fusarium solani f.
sp. piperis. Fitopatologia Brasileira 28(3).
Fang,
X.L., Phillips, D., Li, H., Verheyen, G., Sivasithamparam, K. & Barbetti,
M.J. 2012. Yields and resistance of strawberry cultivars to crown and root
diseases in the field, and variety responses to pathogens under controlled
environment conditions. Phytopathologia Mediterranea 51(1): 69-84.
Gouy, M., Guindon, S. & Gascuel, O. 2010. SeaView version
4: A multiplatform graphical user interface for sequence alignment and
phylogenetic tree building. Molecular Biology and Evolution 27(2):
221-224.
Hafizi, R., Salleh, B. & Latiffah, Z. 2013. Morphological and molecular
characterization of Fusarium solani and F. oxysporum associated with crown disease of oil palm. Brazilian Journal of Microbiology 44(3): 959-968.
Hamedi, A., Ghanati, F. & Vahidi, H. 2012. Study on the effects of different culture
conditions on the morphology of Agaricus blazei and the relationship between morphology and
biomass or EPS production. Annals of Microbiology 62: 699-707.
Kho,
P.E. & Chen, Y.S. 2017. Novel farming innovation for high production of
black pepper (Piper nigrum L.) planting
materials. Journal of Agricultural Science and Technology B7: 301-308.
Klix, M.B., Beyer, M. & Verreet,
J.A. 2008. Effects of cultivar, agronomic practices, geographic location, and
meteorological conditions on the composition of selected Fusarium species on wheat heads. Canadian
Journal of Plant Pathology 30(1): 46-57.
Leslie,
J.F. & Summerell, B.A. 2006. Species
descriptions. The Fusarium Laboratory Manual, 1st ed. Hoboken: Blackwell Publishing. pp.
212-255.
Malz, S., Grell, M.N., Thrane, C., Maier,
F.J., Rosager, P., Felk,
A., Albertsen, K.S., Salomon, S., Bohn, L., Schafer,
W. & Giese, H. 2005. Identification of a gene cluster responsible for the
biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genetics and Biology 42(5): 420-433.
Menezes,
B.S., Solidade, L.S., Conceição,
A.A., Santos Junior, M.N., Leal, P.L., de Brito, E.S., Canuto,
K.M., Mendonça, S., de Siqueira,
F.G. & Marques, L.M. 2020. Pigment production by Fusarium solani BRM054066 and determination of antioxidant
and anti-inflammatory properties. AMB Express 10(1): 117.
O'Donnell,
K., Sutton, D.A., Rinaldi, M.G., Gueidan, C., Crous, P.W. & Geiser, D.M.
2009. Novel multilocus sequence typing scheme reveals
high genetic diversity of human pathogenic members of the Fusarium incarnatum-equiseti and Fusarium chlamydosporum species complexes within the
United States. Journal of Clinical Microbiology 47: 3851-3861.
Perwara, G. & Munggaran,
B. 2020. Pepper Statistical Yearbook 2019. International Pepper
Community, Jakarta, Indonesia. pp. 5-9.
Ramana, K.V. & Eapen, S.J. 2000.
Nematode induced diseases of black pepper. In Black Pepper: Piper nigrum (Medicinal and Aromatic Plants - Industrial
Profiles), edited by Ravindran, P.N. Amsterdam: Harwood
Academic. pp. 269-296.
Rampersad, S.N. & Teelucksingh,
L.D. 2011. First report of Fusarium proliferatum infecting pimento chili peppers in
Trinidad. Plant Disease 95(10): 1313.
Schuller, D., Cardoso, F., Sousa, S.,
Gomes, P., Gomes, A.C., Santos, M.A.S. & Casal,
M. 2012. Genetic diversity and population structure of Saccharomyces cerevisiae strains
isolated from different grape varieties and winemaking regions. PLoS ONE 7(2): e32507.
Shahnazi, S., Meon,
S., Vadamalai, G., Yazdani,
D. & Shabani, M.R. 2014.
Genetic diversity of Fusarium solani isolates from black pepper (Piper nigrum L.) in Malaysia by ISSR marker. Journal
of Tropical Agricultural Science 37(3): 359-370.
Shahnazi, S., Meon,
S., Vadamalai, G., Ahmad, K. & Nejat, N. 2012.
Morphological and molecular characterization of Fusarium spp. associated with
yellowing disease of black pepper (Piper nigrum L.) in Malaysia. Journal of General Plant
Pathology 78(3): 160-169.
Sisic,
A., Bacanovic-Sisic, J., Al-Hatmi,
A.M.S., Karlovsky, P., Ahmed, S.A., Maier, W., de
Hong, G.S. & Finckh, M.R. 2018. The 'forma specialis' issue in Fusarium:
A case study in Fusarium solani f. sp. pisi. Scientific
Reports 8(1): 1252.
Summerell,
B.A. 2019. Resolving Fusarium: Current status
of the genus. Annual Review of Phytopathology 57: 323-339.
Thuy, T.T.T., Yen, N.T., Tuyet,
N.T.A., Te, L.L. & Waele,
D.D. 2012. Plant-parasitic nematodes and yellowing of leaves associated with
black pepper plants in Vietnam. Archives of Phytopathology and Plant
Protection 45(10): 1183-1200.
Wong,
M.H. 2010. Diseases of Pepper (Part 1). Department of Agriculture
Sarawak (DOA). https://doa.sarawak.gov.my/page-0-270-283-ARC-ARTICLES-Archives.html.
Accessed on November 2020.
Zhu,
Z., Zheng, L., Pan, L., Hsiang, T. & Huang, J. 2014. Identification and
characterization of Fusarium species associated with
wilt of Eleocharis dulcis (Chinese water chestnut) in China. Plant Disease 98(7): 977-987.
*Pengarang untuk surat-menyurat; email: yeemink@upm.edu.my