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Induced Biochemical Changes in Ganoderma boninense Infected Elaeis guineensis Seedlings in Response to Biocontrol Treatments

Tuan Muhammad Syafiq Tuan Hassan, Nusaibah Syd Ali and Mohd Rafii Yusop

Pertanika Journal of Science & Technology, Volume 46, Issue 1, February 2023

DOI: https://doi.org/10.47836/pjtas.46.1.08

Keywords: Basal stem rot, biological control agents, lignin, metabolites, peroxidase, total phenolic content

Published on: 22 Febuary 2023

Despite massive economic contributions to Malaysia, the oil palm industry faces devastating threats from basal stem rot (BSR) disease. An array of treatments was designed to evaluate the potential of biological control agents (BCAs) as a single and combination of applications in a greenhouse study of six months. Oil palm enzymes, phenolic content, and metabolite induction in BSR-diseased seedlings were also assessed in response to the designed treatments. In the study, seedlings treated with Trichoderma asperellum (UPM16) demonstrated the highest disease reduction (DR) (57.2%). Peroxidase (PO), lignin, and total phenolic content (TPC) were evaluated. Treatments on Ganoderma-infected seedlings treated with Bacillus cereus (UPM15) exhibited the highest reading in all assays. Gas chromatography-mass spectrometry (GC-MS) analysis profiled phenol, 4-2-aminoethyl- as the most abundant metabolite detected in combination treatments with B. cereus and T. asperellum (BT). Both BCAs complimented and demonstrated huge potential in mitigating BSR diseases in oil palm. However, excessive chemical application to control BSRs negatively impacts biodiversity and the human population. In view of this, studies on biological control are crucial in selecting potential BCAs to counter BSR sustainably. Biological control would be an ideal alternative as a sustainable method for controlling oil palm BSR disease.

  • Adaskaveg, J. E., Blanchette, R. A., & Gilbertson, R. L. (1991). Decay of date palm wood by white-rot and brown-rot fungi. Canadian Journal of Botany, 69(3), 615-629. https://doi.org/10.1139/b91-083

  • Alawlaqi, M. M., & Alharbi, A. A. (2014). Impact of acetic acid on controlling tomato fruit decay. Life Science Journal, 11(3s), 114-119. https://doi.org/10.7537/marslsj1103s14.17

  • Alexander, A., Dayou, J., & Chong, K. P. (2015). Morphological changes of Ganoderma boninense mycelia after challenged by Trichoderma and Bacillus. In AIP Conference Proceedings (Vol. 1669, No. 1, p. 020075). AIP Publishing LLC. https://doi.org/10.1063/1.4919213

  • Almeida, J. R., Bertilsson, M., Gorwa-Grauslund, M. F., Gorsich, S., & Lidén, G. (2009). Metabolic effects of furaldehydes and impacts on biotechnological processes. Applied Microbiology and Biotechnology, 82(4), 625-638. https://doi.org/10.1007/s00253-009-1875-1

  • Ashbolt, N. J., Amézquita, A., Backhaus, T., Borriello, P., Brandt, K. K., Collignon, P., Coors, A., Finley, R., Gaze, W. H., Heberer, T., Lawrence, J. R., Larsson, D. G. J., McEwen, S. A., Ryan, J. J., Schönfeld, J., Silley, P., Snape, J. R., Eede, C. V., & Topp, E. (2013). Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environmental Health Perspectives, 121(9), 993-1001. https://doi.org/10.1289/ehp.1206316

  • Avdiushko, S. A., Ye, X. S., & Kuc, J. (1993). Detection of several enzymatic activities in leaf prints of cucumber plants. Physiological and Molecular Plant Pathology, 42(6), 441-454. https://doi.org/10.1006/pmpp.1993.1033

  • Bailey, B. A., Bae, H., Strem, M. D., Crozier, J., Thomas, S. E., Samuels, G. J., Vinyard, B. T., & Holmes, K. A. (2008). Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biological Control, 46(1), 24-35. https://doi.org/10.1016/j.biocontrol.2008.01.003

  • Baydar, N. G., Özkan, G., & Sağdiç, O. (2004). Total phenolic contents and antibacterial activities of grape (Vitis vinifera L.) extracts. Food Control, 15(5), 335-339. https://doi.org/10.1016/S0956-7135(03)00083-5

  • Bennett, A. E., Grussu, D., Kam, J., Caul, S., & Halpin, C. (2015). Plant lignin content altered by soil microbial community. New Phytologist, 206(1), 166-174. https://doi.org/10.1111/nph.13171

  • Bivi, M. R., Noor Farhana, M. S., Khairulmazmi, A., & Idris, A. (2010). Control of Ganoderma boninense: A causal agent of basal stem rot disease in oil palm with endophyte bacteria in vitro. International Journal of Agriculture and Biology, 12(6), 833-839.

  • Breton, F., Hasan, Y., Hariadi, S. S., Lubis, Z., & De Franqueville, H. (2006). Characterization of parameters for the development of an early screening test for basal stem rot tolerance in oil palm progenies. Journal of Oil Palm Research, (Special Issue – April), 24-36.

  • Bruce, R. J., & West, C. A. (1989). Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiology, 91(3), 889-897. https://doi.org/10.1104/pp.91.3.889

  • Burr, G. O., & Burr, M. M. (1930). On the nature and role of the fatty acids essential in nutrition. Journal of Biological Chemistry, 86(2), 587-621. https://doi.org/10.1016/S0021-9258(20)78929-5

  • Campos, L., Lisón, P., López-Gresa, M. P., Rodrigo, I., Zacarés, L., Conejero, V., & Bellés, J. M. (2014). Transgenic tomato plants overexpressing tyramine N-hydroxy cinnamoyl transferase exhibit elevated hydroxycinnamic acid amide levels and enhanced resistance to Pseudomonas syringae. International Society for Molecular Plant-Microbe Interactions, 27(10), 1159-1169. https://doi.org/10.1094/MPMI-04-14-0104-R

  • Chen, P. X., Tang, Y., Zhang, B., Liu, R., Marcone, M. F., Li, X., & Tsao, R. (2014). 5-hydroxymethyl-2-furfural and derivatives formed during acid hydrolysis of conjugated and bound phenolics in plant foods and the effects on phenolic content and antioxidant capacity. Journal of Agricultural and Food Chemistry, 62(20), 4754-4761. https://doi.org/10.1021/jf500518r

  • Coco, F. L., Valentini, C., Novelli, V., & Ceccon, L. (1996). High-performance liquid chromatographic determination of 2-furaldehyde and 5-hydroxymethyl-2-furaldehyde in honey. Journal of Chromatography A, 749(1-2), 95-102. https://doi.org/10.1016/0021-9673(96)00392-5

  • Dean, R. A., & Kuć, J. (1987). Rapid lignification in response to wounding and infection as a mechanism for induced systemic protection in cucumber. Physiological and Molecular Plant Pathology, 31(1), 69-81. https://doi.org/10.1016/0885-5765(87)90007-5

  • Di Francesco, A., Martini, C., & Mari, M. (2016). Biological control of postharvest diseases by microbial antagonists: How many mechanisms of action?. European Journal of Plant Pathology, 145, 711-717. https://doi.org/10.1007/s10658-016-0867-0

  • Doster, M. A., & Bostock, R. M. (1988). Effects of low temperature on resistance of almond trees to Phytophthora pruning wound cankers in relation to lignin and suberin formation in wounded bark tissue. Phytopathology, 78(4), 478-483. https://doi.org/10.1094/Phyto-78-478

  • Fattorusso, E., Lanzotti, V., & Taglialatela‐Scafati, O. (1999). Antifungal N‐feruloyl amides from roots of two Allium species. Plant Biosystem, 133(2), 199-203. https://doi.org/10.1080/11263509909381549

  • Fiehn, O. (2002). Metabolomics – The link between genotypes and phenotypes. Plant Molecular Biology, 48, 155-171. https://doi.org/10.1023/A:1013713905833

  • Giorgio, A., De Stradis, A., Lo Cantore, P., & Iacobellis, N. S. (2015). Biocide effects of volatile organic compounds produced by potential biocontrol rhizobacteria on Sclerotinia sclerotiorum. Frontiers in Microbiology, 6, 1056. https://doi.org/10.3389/fmicb.2015.01056

  • Gomez, K. A., & Gomez, A. A. (1984). Statistical procedures for agricultural research. John Wiley & Sons.

  • Gotor-Vila, A., Teixidó, N., Di Francesco, A., Usall, J., Ugolini, L., Torres, R., & Mari, M. (2017). Antifungal effect of volatile organic compounds produced by Bacillus amyloliquefaciens CPA-8 against fruit pathogen decays of cherry. Food Microbiology, 64, 219-225. https://doi.org/10.1016/j.fm.2017.01.006

  • Gottfried, J. L., De Lucia Jr, F. C., & Miziolek, A. W. (2009). Discrimination of explosive residues on organic and inorganic substrates using laser-induced breakdown spectroscopy. Journal of Analytical Atomic Spectrometry, 24(3), 288-296. https://doi.org/10.1039/B818481J

  • Hagel, J. M., & Facchini, P. J. (2005). Elevated tyrosine decarboxylase and tyramine hydroxy cinnamoyl transferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta, 221(6), 904-914. https://doi.org/10.1007/s00425-005-1484-x

  • Halász, A., Baráth, A., Simon-Sarkadi, L., & Holzapfel, W. (1994). Biogenic amines and their production by microorganisms in food. Trends in Food Science and Technology, 5(2), 42-49. https://doi.org/10.1016/0924-2244(94)90070-1

  • Halfeld-Vieira, B. D. A., Vieira Júnior, J. R., Romeiro, R. D. S., Silva, H. S. A., & Baracat-Pereira, M. C. (2006). Induction of systemic resistance in tomato by the autochthonous phylloplane resident Bacillus cereus. Pesquisa Agropecuaria Brasileira, 41(8), 1247-1252. https://doi.org/10.1590/S0100-204X2006000800006

  • Hermosa, R., Rubio, M. B., Cardoza, R. E., Nicolás, C., Monte, E., & Gutiérrez, S. (2013). The contribution of Trichoderma to balancing the costs of plant growth and defense. International Microbiology, 16(2), 69-80. https://doi.org/10.2436/20.1501.01.181

  • Hu, C., & Kitts, D. D. (2001). Evaluation of antioxidant activity of epigallocatechin gallate in biphasic model systems in vitro. Molecular and Cellular Biochemistry, 218, 147-155. https://doi.org/10.1023/A:1007220928446

  • Huang, C. B., & Ebersole, J. L. (2010). A novel bioactivity of omega‐3 polyunsaturated fatty acids and their ester derivatives. Molecular Oral Microbiology, 25(1), 75-80. https://doi.org/10.1111/j.2041-1014.2009.00553.x

  • Huang, Z., Cui, Q., Xiong, L., Wang, Z., Wang, K., Zhao, Q., Bi, F., & Wang, Q. (2009). Synthesis and insecticidal activities and SAR studies of novel benzoheterocyclic diacylhydrazine derivatives. Journal of Agricultural and Food Chemistry, 57(6), 2447-2456. https://doi.org/10.1021/jf8036193

  • Idris, A. S., Kushairi, D., Ariffin, D., & Basri, M. W. (2006). Technique for inoculation of oil palm germinated seeds with Ganoderma. http://palmoilis.mpob.gov.my/TOTV3/wp-content/uploads/2020/02/TT-314.pdf

  • Izzati, M. Z. N. A., & Abdullah, F. (2008). Disease suppression in Ganoderma-infected oil palm seedlings treated with Trichoderma harzianum. Plant Protection Science, 44(3), 101-107. https://doi.org/10.17221/23/2008-PPS

  • Jang, J. H., Kanoh, K., Adachi, K., & Shizuri, Y. (2006). New dihydrobenzofuran derivative, awajanoran, from marine-derived Acremonium sp. AWA16-1. The Journal of Antibiotics, 59, 428-431. https://doi.org/10.1038/ja.2006.60

  • Katritzky, A. R., & Rees, C. W. (Eds.). (1984). Comprehensive heterocyclic chemistry. Pergamon Press.

  • Kokkinakis, D. M., & Brooks, J. L. (1979). Hydrogen peroxide-mediated oxidation of indole-3-acetic acid by tomato peroxidase and molecular oxygen. Plant Physiology, 64(2), 220-223. https://doi.org/10.1104/pp.64.2.220

  • Lin, A. S., Qian, K., Usami, Y., Lin, L., Itokawa, H., Hsu, C., Morris-Natschke, S. L., & Lee, K. H. (2008). 5-hydroxymethyl-2-furfural, a clinical trials agent for sickle cell anemia, and its mono/di-glucosides from classically processed steamed Rehmanniae Radix. Journal of Natural Medicines, 62, 164-167. https://doi.org/10.1007/s11418-007-0206-z

  • Małolepsza, U., & Różalska, S. (2005). Nitric oxide and hydrogen peroxide in tomato resistance: Nitric oxide modulates hydrogen peroxide level in o-hydroxyethylorutin-induced resistance to Botrytis cinerea in tomato. Plant Physiology and Biochemistry, 43(6), 623-635. https://doi.org/10.1016/j.plaphy.2005.04.002

  • Mari, M., Bautista-Baños, S., & Sivakumar, D. (2016). Decay control in the postharvest system: Role of microbial and plant volatile organic compounds. Postharvest Biology and Technology, 122, 70-81. https://doi.org/10.1016/j.postharvbio.2016.04.014

  • Musa, H., Nusaibah, S. A., & Khairulmazmi, A. (2018). Assessment on Trichoderma spp. mixture as a potential biocontrol agent of Ganoderma boninense infected oil palm seedlings. Journal of Oil Palm Research, 30(3), 403-415. https://doi.org/10.21894/jopr.2018.0035

  • Naher, L., Yusuf, U. K., Tan, S. G., Siddiquee, S., & Islam, M. R. (2014). In vitro and in vivo biocontrol performance of Trichoderma harzianum Rifai on Ganoderma boninense Pat. related to pathogenicity on oil palm (Elaeis guineensis Jacq.). Journal of Pure and Applied Microbiology, 8(2), 973-978.

  • Newman, M. A., von Roepenack-Lahaye, E., Parr, A., Daniels, M. J., & Dow, J. M. (2001). Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defense response activated by hrp gene-dependent and hrp gene-independent mechanisms. International Society for Molecular Plant-Microbe Interactions, 14(6), 785-792. https://doi.org/10.1094/MPMI.2001.14.6.785

  • Nikraftar, F., Taheri, P., Rastegar, M. F., & Tarighi, S. (2013). Tomato partial resistance to Rhizoctonia solani involves antioxidative defence mechanisms. Physiological and Molecular Plant Pathology, 81, 74-83. https://doi.org/10.1016/j.pmpp.2012.11.004

  • Nusaibah, S. A., Akmar, A. S. N., Idris, A. S., Sariah, M., & Pauzi, Z. M. (2016). Involvement of metabolites in early defence mechanism of oil palm (Elaeis guineensis Jacq.) against Ganoderma disease. Plant Physiology and Biochemistry, 109, 156-165. https://doi.org/10.1016/j.plaphy.2016.09.014

  • Nusaibah, S. A., Saad, G., & Hun, T. G. (2017). Antagonistic efficacy of Trichoderma harzianum and Bacillus cereus against Ganoderma disease of oil palm via dip, place and drench (DPD) artificial inoculation technique. International Journal of Agriculture and Biology, 19(2), 299-306. https://doi.org/10.17957/IJAB/15.0280

  • Ramarathnam, R., Fernando, W. D., & de Kievit, T. (2011). The role of antibiosis and induced systemic resistance, mediated by strains of Pseudomonas chlororaphis, Bacillus cereus and B. amyloliquefaciens, in controlling blackleg disease of canola. BioControl, 56, 225-235. https://doi.org/10.1007/s10526-010-9324-8

  • Richardson, S. N., Nsiama, T. K., Walker, A. K., McMullin, D. R., & Miller, J. D. (2015). Antimicrobial dihydrobenzofurans and xanthenes from a foliar endophyte of Pinus strobus. Phytochemistry, 117, 436-443. https://doi.org/10.1016/j.phytochem.2015.07.009

  • Samatha, T., Shyamsundarachary, R., Srinivas, P., & Swamy, N. R. (2012). Quantification of total phenolic and total flavonoid contents in extracts of Oroxylum indicum L. Kurz. Asian Journal of Pharmaceutical and Clinical Research, 5(4), 177-179.

  • Sariah, M. C., Coo, C. W., Zakaria, H., & Norihan, M. S. (2005). Quantification and characterization of Trichoderma spp. from different ecosystems. Mycopathologia, 159, 113-117. https://doi.org/10.1007/s11046-004-4432-6

  • Shaner, G., & Finney, R. E. (1977). The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat. Phytopathology, 67(8), 1051-1056. https://doi.org/10.1094/Phyto-67-1051

  • Singleton, V. L., Orthofer, R., & Lamuela-Raventós, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. In L. Packer (Ed.), Methods in enzymology (Vol. 299, pp. 152-178). Academic press. https://doi.org/10.1016/S0076-6879(99)99017-1

  • Subramenium, G. A., Swetha, T. K., Iyer, P. M., Balamurugan, K., & Pandian, S. K. (2018). 5-hydroxymethyl-2-furaldehyde from marine bacterium Bacillus subtilis inhibits biofilm and virulence of Candida albicans. Microbiological Research, 207, 19-32. https://doi.org/10.1016/j.micres.2017.11.002

  • Sundram, S., Sariah, M., Idris, A. S., & Radziah, O. (2011). Symbiotic interaction of endophytic bacteria with arbuscular mycorrhizal fungi and its antagonistic effect on Ganoderma boninense. Journal Microbiology, 49(4), 551–557. https://doi.org/10.1007/s12275-011-0489-3

  • Surekha, C. H., Neelapu, N. R. R., Kamala, G., Prasad, B. S., & Ganesh, P. S. (2013). Efficacy of Trichoderma viride to induce disease resistance and antioxidant responses in legume Vigna mungo infested by Fusarium oxysporum and Alternaria alternata. International Journal of Agricultural Science Research, 3(2), 285-294.

  • Syafiq, T. H. T. M., Nusaibah, S. A., & Rafii, M. Y. (2021). Effectiveness of bioinoculants Bacillus cereus and Trichoderma asperellum as oil palm seedlings growth promoters. Pertanika Journal of Tropical Agricultural Science, 44(1), 157-170. https://doi.org/10.47836/pjtas.44.1.09

  • Tarig, S. A., Sariah, M., Sijam, K., & Marziah, M. (1998). Enhancements of growth and disease suppression by PGPF isolate, Fusarium oxysporum (Foc4), in banana seedlings. In Z. Wahab (Ed.), Proceedings of the First National Banana Seminar (pp. 261-268). Malaysian Agricultural Information Portal.

  • Treutter, D. (2006). Significance of flavonoids in plant resistance: A review. Environmental Chemistry Letters, 4, 147-157. https://doi.org/10.1007/s10311-006-0068-8

  • Usall, J., Teixidó, N., Fons, E. & Viñas, I. (2000). Biological control of blue mould on apple by a strain of Candida sake under several controlled atmosphere conditions. International Journal of Food Microbiology, 58(1-2), 83-92. https://doi.org/10.1016/S0168-1605(00)00285-3

  • Walters, D., Raynor, L., Mitchell, A., Walker, R., & Walker, K. (2004). Antifungal activities of four fatty acids against plant pathogenic fungi. Mycopathologia, 157(1),87-90. https://doi.org/10.1023/B:MYCO.0000012222.68156.2c

  • Weisskopf, L. (2013). The potential of bacterial volatiles for crop protection against phytopathogenic fungi. In A. Méndez-Vilas (Ed.), Microbial pathogens and strategies for combating them: Science, technology and education (pp. 1352-1363). Formatex.

  • Xu, L., Zhu, L., Tu, L., Liu, L., Yuan, D., Jin, L., & Zhang, X. (2011). Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. Journal of Experimental Botany, 62(15), 5607-5621. https://doi.org/10.1093/jxb/err245

  • Yang, C. A., Cheng, C. H., Lo, C. T., Liu, S. Y., Lee, J. W., & Peng, K. C. (2011). A novel L-amino acid oxidase from Trichoderma harzianum ETS 323 associated with antagonism of Rhizoctonia solani. Journal of Agricultural and Food Chemistry, 59(9), 4519-4526. https://doi.org/10.1021/jf104603w

  • Zaiton, S., Sariah, M., & Ahmad, Z. A. M. (2008). Effect of endophytic bacteria on growth and suppression of Ganoderma infection in oil palm. International Journal of Agricultural and Biology, 10(2), 127-132.

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