Evaluation of some Fungicides for the Control of Armillaria Root Rot of Walnut Trees
Nima Khaledi
1
(
Seed and Plant Certification and Registration Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran
)
Mahdi Rezaei
2
(
Seed and Plant Certification and Registration Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran
)
Keywords: Chemical control, Pathogenicity, Soil-borne, Thiophanate-methyl, Walnut,
Abstract :
Armillaria root rot, primarily caused by the closely related species Armillaria mellea, is a prevalent disease affecting walnut trees globally, leading to stunted growth and plant mortality. Currently, no walnut rootstock genotypes have been identified that offer complete resistance to this disease. The application of chemical fungicides represents the most straightforward and accessible method to mitigate the damage caused by Armillaria root rot in walnut trees. This research aimed to assess the prevalence of Armillaria root rot in both traditional and commercial walnut orchards and to evaluate the efficacy of chemical fungicides, specifically thiophanate-methyl and triazole compounds (propiconazole, cyproconazole, and hexaconazole), in reducing the severity and incidence of root rot. Samples collected from various commercial and traditional orchards in Iran were analyzed for the presence of the causal agent of the disease. Using a combination of morphological and molecular techniques, five isolates of A. mellea were identified. Results indicated variability in pathogenicity among the A. mellea isolates, ranging from pathogenic to weakly pathogenic. Moreover, the fungicides tested were effective in completely inhibiting mycelial growth at the minimum inhibitory concentration (MIC). However, the effectiveness of each fungicide in reducing disease incidence varied. Notably, thiophanate-methyl significantly outperformed the triazole fungicides in inhibiting disease progression. The findings suggest that thiophanate-methyl, when applied at the minimum fungicidal concentration (MFC) upon the initial appearance of disease symptoms, holds promise for the management of Armillaria crown and root rot in walnut orchards.
Aguín O, Mansilla JP, Sainz JM (2006) In vitro selection of an effective fungicide against Armillaria mellea and control of white root rot of grapevine in the field. Pest Management Science. 62, 223-228. doi: 10.1002/ps.1149
Ahmadi K, Ebadzadeh HR, Hatami F, Mohammadnia-Afrozi S, Esfandiarpour E, Abbasi Taleghani R (2021) Agricultural Statistics. Ministry of Agriculture-Jahad. Available at Web site: https://maj.ir/Dorsapax/userfiles/Sub65/amarbaghi1400.pdf
Akca Y, Sahin U (2022) Responses of ‘Chandler’ walnut variety grafted onto different rootstocks to salt stress. International Journal of Horticultural Science and Technology. 9, 1-13. doi: 10.22059/ijhst.2021.319247.444
Amiri A, Bussey KE, Riley MB, Schnabel G (2008) Propiconazole inhibits Armillaria tabescens in vitro and translocates into peach roots following trunk infusion. Plant Disease. 92, 1293-1298. doi: 10.1094/PDIS-92-9-1293
Amiri A, Schnabel G (2012) Persistence of propiconazole in peach roots and efficacy of trunk infusions for Armillaria root rot control. International Journal of Fruit Science. 12, 437-449. doi: 10.1080/15538362.2012.679183
Antonín V, Tomsovsky M, Sedlák P, Májek T, Jankovsky L (2009) Morphological and molecular characterization of the Armillaria cepistipes - A. gallica complex in the Czech Republic and Slovakia. Mycological Progress. 8, 259-271. doi: 10.1007/s11557-009-0597-1
Arab MM, Brown PJ, Abdollahi-Arpanahi R, Sohrabi SS, Askari H, Aliniaeifard S, Mokhtassi-Bidgoli A, Mesgaran MB, Leslie CA, Marrano A, Neale DB, Vahdati K (2022) Genome-wide association analysis and pathway enrichment provide insights into the genetic basis of photosynthetic responses to drought stress in Persian walnut. Horticulture Research, 1-38.
Avis TJ (2007) Antifungal compounds that target fungal membranes: applications in plant disease control. Canadian Journal of Plant Pathology. 29, 323-329. doi: 10.1080/07060660709507478
Baumgartner K (2004) Root collar excavation for postinfection control of Armillaria root disease of grapevine. Plant Disease. 88, 1235-1240. doi: 10.1094/PDIS.2004.88.11.1235
Baumgartner K, Coetzee MPA, Hoffmeister D (2011) Secrets of the subterranean pathosystem of Armillaria. Molecular Plant Pathology. 12, 515-534. doi: 10.1111/j.1364-3703.2010.00693.x
Chatrabnous N, Yazdani N, Vahdati K (2018) Determination of nutritional value and oxidative stability of fresh walnut. Journal of Nuts. 9(1), 11-20.
Chauhan C, Namdev S (2022) Spectrophotometric method development for thiophante methyl based systemic fungicide, Roko formulation. Materials Today: Proceedings. 68, 1106-1109. doi: 10.1016/j.matpr.2022.08.481
Chen L, Heng J, Qin S, Bian K (2018) A comprehensive understanding of the biocontrol potential of Bacillus velezensis LM2303 against Fusarium head blight. Plos One, 13(6), e0198560. doi: 10.1371/journal.pone.0198560
Coetzee MPA, Wingfield BD, Bloomer P, Ridley GS, Wingfield MJ (2003) Molecular identification and phylogeny of Armillaria isolates from South America and Indo-Malaysia. Mycologia. 95, 285-293.
Dalili SAR, Nanagulyan SG, Alavi SV (2008) Identification of Armillaria species on different hosts from Iran. Mycologia Balcanica. 5, 119-122. doi: 10.2307/3762039
Devkota P, Hammerschmidt R (2020) The infection process of Armillaria mellea and Armillaria solidipes. Physiological and Molecular Plant Pathology. 112, 101543. doi: 10.1016/j.pmpp.2020.101543
Elias-Roman RD, Galderon-Zavala G, Guzman-Mendoza R, Vallejo-Perez MR, Klopfenstein NB, Mora-Aguilera JA (2019) ‘Mondragon’: a clonal plum rootstock to enhance management of Armillaria root disease in peach orchards of Mexico. Crop Protection. 121, 89-95. doi: 10.1016/j. cropro. 2019.03.011
FAOSTAT (2022) FAOSTAT Database. Food and Agriculture Organization of the United Nations, Statistics Division. https://www.fao.org/faostat/en/#data/QCL
Farsi M, Fatahi Moghadam M, Zamani Z, Hassani D (2018) Effects of scion cultivar, rootstock age and hormonal treatment on minigrafting of persian walnut. International Journal of Horticultural Science and Technology. 5, 185-197. doi; 10.22059/ijhst. 2018.255460. 233
Freeman S, Sztejnberg A, Chet I (1986) Evaluation of Trichoderma as a biocontrol agent for Rosellinia necatrix. Plant and Soil. 94, 163-170.
Gohet E, Van Canh T, Louanchi M, Despreaux D (1991) New developments in chemical control of white root disease of Hevea brasiliensis in Africa. Crop Protection. 10, 234-238. doi: 10.1016/0261-2194(91)90049-W
Hoopen GMT, Krauss U (2006) Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: A review. Crop Protection. 25, 89-107. doi: 10.1016/j.cropro.2005.03.009
Jahanbani R, Ghaffari SM, Vahdati K, Salami M, Khalesi MR, Sheibani N, Moosavi-Movahedi AA (2018) Kinetics study of protein hydrolysis and inhibition of angiotensin converting enzyme by peptides hydrolysate extracted from walnut. International Journal of Peptide Research and Therapeutics. 24(1), 77-85.
Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L, Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens. 10(1), 76. doi: 10.3390/pathogens10010076
Khodadadi F, Tohidfar M, Mohayeji M, Dandekar AM, Leslie CA, Kluepfel D, Butterfield T, Vahdati K (2016) Induction of polyphenol oxidase in walnut and its relationship to the pathogenic response to bacterial blight. Journal of the American Society for Horticultural Science. 141(2), 119-124.
Khodadadi F, Tohidfar M, Vahdati K, Dandekar AM, Leslie CA. (2020). Functional analysis of walnut polyphenol oxidase gene (JrPPO1) in transgenic tobacco plants and PPO induction in response to walnut bacterial blight. Plant Pathology. 69, 756-764.
Liao TZ, Chen YH, Tsai JN, Chao C, Huang TP, Hong CF, Wu ZC, Tsai IJ, Lee HH, Klopfenstein, NB, Kim MS, Stewart JE, Atibalentja N, Brooks FE, Cannon P, Mohd Farid A, Hattori T, Kwan HS, Lam YCR, Ota Y, Sahashi N, Schlub RL, Shuey LS, Tang AMC, Chung CL (2023) Translocation of fungicides and their efficacy in controlling Phellinus noxius, the cause of brown root rot disease. Plant Disease. 107, 2039-2053. doi: 10.1094/PDIS-06-22-1285-RE
Lee SH, Shin H, Chang WB, Ryu KY, Kim HT, Cha B, Cha JS (2020) Dieback reality of apple trees resulting from soil-borne fungal pathogens in South Korea from 2016 to 2019. Research in Plant Disease. 26, 8-94. doi: 10.5423/RPD.2020.26.2.88
Liu XJ, Meng PP, Yang GY, Zhang MY, Peng SB, Zhai MZ (2020) Genome-wide identification and transcript profiles of walnut heat stress transcription factor involved in abiotic stress. BMC Genomics. 21, 474. doi: 10.1186/s12864-020-06879-2.
Lochman J, Serý O, Jankovský L, Mikes V (2004a) The rapid identification of European Armillaria species from soil samples by nested PCR. FEMS Microbiology Letters. 237, 105-110. doi: 10.1016/j.femsle.2004.06.019
Lochman J, Serý O, Jankovský L, Mikes V (2004b) Variations in ITS of ribosomal DNA of Czech Armillaria species determined by PCR and high performance liquid chromatography. Mycological Research. 108, 1-9. doi: 10.1017/s0953756204000644
Mahmoudian M, Rahemi M, Karimi S, Yazdani N, Tajdini Z, Sarikhani S, Vahdati K (2021) Role of kaolin on drought tolerance and nut quality of Persian walnut, Journal of the Saudi Society of Agricultural Sciences, 20(6), 409-416.
Metaliaj R, Sicoli G, Luisi N (2006) Pathogenicity of Armillaria isolates inoculated on five Quercus species at different watering regimes. Phytopathologia Mediterranea. 45, 3-9.
Mohammadi AH, Haghdel M, Mirabolfathy M, Alaei H (2022) Armillaria root and crown rot disease in pistachio orchards. Plant Pathology Science. 11, 92-102. doi: 10.52547/pps.11.2.92
Mwenje E, Wingfield BD, Coetzee MPA, Wingfield MJ (2003) Molecular characterisation of Armillaria species from Zimbabwe. Mycological Research. 107, 291-296.
Najafi S, Jafary, H, Nazer Kakhki SH (2018) Chemical management of Armillaria rot diseases of olive trees in Tarom region of Zanjan province. In Proceedings of the 23rd Iranian Plant Protection Congress, Gorgan, Iran 27-30 August.
Nourbakhsh S (2022) List of important pests, diseases and weeds of major agricultural products, chemicals and recommended ways for their control. Plant Protection organization, Ministry of Jihad-e Agriculture.
Pakrah S, Rahemi M, Nabipour A, Zahedzadeh F, Kakavand F, Vahdati K (2021) Sensory and nutritional attributes of Persian walnut kernel influenced by maturity stage, drying method, and cultivar. Journal of Food Processing and Preservation, e15513.
Pildain M, Coetzee M, Rajchenberg M, Petersen R, Wingfield M, Wingfield B (2009) Molecular phylogeny of Armillaria from the Patagonian Andes. Mycological Progress. 8, 181-194. doi: 10.1007/s11557-009-0590-8
Plodpai P, Chuenchitt S, Petcharat V, Chakthong S, Voravuthikunchai SP (2013) Anti-Rhizoctonia solani activity by Desmos chinensis extracts and its mechanism of action. Crop Protection. 43, 65-71. doi: 10.1016/j.cropro.2012.09.004
Porter DL, Bradshaw AJ, Nielsen RH, Newell P, Dentinger BTM, Naleway SE (2022) The melanized layer of Armillaria ostoyae rhizomorphs: its protective role and functions. Journal of the Mechanical Behavior of Biomedical Materials. 125, 104934. doi: 10.1016/j.jmbbm.2021.104934
Rees HJ, Drakulic J, Cromey MG, Bailey AM, Foster GD (2022) Endophytic Trichoderma spp. can protect strawberry and privet plants from infection by the fungus Armillaria mellea. Plos One. 17(8), e0271622. doi: 10.1371/journal.pone.0271622
Sarikhani S, Vahdati K, Ligterink W (2021) Biochemical properties of superior persian walnut genotypes originated from southwest of Iran. International Journal of Horticultural Science and Technology. 8, 13-24. doi: 10.22059/ijhst.2020.309363.392
Sipos G, Prasanna AN, Walter MC, O'Connor E, Bálint B, Krizsán K, Kiss B, Hess J, Varga T, Slot J, Riley R, Bóka B, Rigling D, Barry K, Lee J, Mihaltcheva S, LaButti K, Lipzen A, Waldron R, Moloney NM, Sperisen C, Kredics L, Vágvölgyi C, Patrignani A, Fitzpatrick D, Nagy I, Doyle S, Anderson JB, Grigoriev IV, Güldener U, Münsterkötter M, Nagy LG (2017) Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria. Nature Ecology & Evolution. 1(12), 1931-1941. doi: 10.1038/s41559-017-0347-8
Soltantoyeh R, Dalili A, Borhani A (2014) Evaluation of some important woody plant species against wood destroying activity of honey fungus. Australian Journal of Crop Science. 8(6), 881-886.
Thomidis T, Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection. 36, 49-51. doi: 10.1016/j.cropro.2012.02.003
Thompson DP (1989) Fungitoxic activity of essential oil components on food storage fungi. Mycologia. 81, 151-153. doi: 10.2307/3759462
Vahdati K, Sarikhani S, Arab MM, Leslie CA, Dandekar AM, Aletà N, Bielsa B, Gradziel TM, Montesinos Á, Rubio-Cabetas MJ, Sideli GM, Serdar Ü, Akyüz B, Beccaro GL, Donno D, Rovira M, Ferguson L, Akbari M, Sheikhi A, Sestras AF, Kafkas S, Paizila A, Roozban MR, Kaur A, Panta S, Zhang L, Sestras RE, Mehlenbacher S (2021) Advances in rootstock breeding of nut trees: objectives and strategies. Plants 10 (11), 2234.
Volk TJ (2005). Key to North American Armillaria species. Retrieved May 18, 2017 from the Tom Volk's Fungi Web site: http://botit.botany.wisc.edu/toms_fungi/armkey.html
West JS, Fox RTV (2002) Stimulation of Armillaria mellea by phenolic fungicides. Annals of Applied Biology - AAB. 140, 291-295. doi: 10.1111/j.1744-7348.2002.tb00184.x
Woodward JE, Brenneman TB (2008) Development of an inoculation method for quantifying fungicide residues on peanut foliage. Peanut Science. 35, 25-31. doi: 10.3146/PS06-045.1
Worrall JJ (1991) Media for selective isolation of hymenomycetes. Mycologia. 83, 296-302. doi: 10.1080/00275514.1991.12026013
Yousefi Hamedani E, Sharifnabi B, Bahar M (2012) Application of classical and molecular techniques in detection of Armillaria mellea the causal agent of root and crown rot disease from soil and wood. Iranian Journal of Plant Pathology. 48, 223-235.