Role of Extracellular Hydrolytic and Ligninolytic Enzymes as Virulence Factors of the Dematophora necatrix in the Activation of Basal Resistance of Walnut

Subject Areas : Plant Pathology

Nima Khaledi ^{1 *} , Mahdi Rezaei ² , Farshid Hassani ³

1 - Seed and Plant Certification and Registration Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran
2 - Seed and Plant Certification and Registration Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran
3 - Seed and Plant Certification and Registration Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

Received: 2024-05-10 Accepted : 2024-10-02 Published : 2025-08-29

Keywords: Basal resistance, Defence responses, Phenolics, Soil-borne, Virulence,

Abstract :

Dematophora necatrix is one of the most destructive soil-borne fungal pathogens causing white root rot disease on walnuts in Iran and worldwide. No walnut rootstock genotypes have shown complete resistance to this disease. This study aims to identify and monitor the prevalence of D. necatrix in traditional and commercial walnut orchards as well as to explore extracellular the hydrolytic and ligninolytic enzymes produced by the fungal isolates plus variations in virulence and aggressiveness in vivo. We also examined the role of biochemical mechanisms, including the activities of oxidative enzymes and defensive compounds involved in the basal resistance of walnuts to the necrotrophic D. necatrix. In this study, we investigated the presence of the causal agent of white rot disease in root and soil samples collected from commercial and traditional gardens in 17 regions of Iran. Then, we analysed the relationship between the activity of extracellular hydrolytic and ligninolytic enzymes produced by D. necatrix isolates together with variations in pathogenicity and aggressiveness in vivo. Next, the activity of guaiacol peroxidase (GPX), polyphenol oxidase (PPO), phenylalanine ammonia-lyase (PAL), and level of defensive compounds were studied at various time points after inoculation by different D. necatrix isolates. All fungal isolates were identified as D. necatrix based on their morphological and molecular characteristics. Analysis of the activity of extracellular hydrolytic and ligninolytic enzymes produced by the fungal isolates revealed a higher activity of these enzymes for isolates presenting higher levels of virulence and aggressiveness in walnut seedlings. The current study suggests the critical role of GPX, PPO, and PAL in walnut resistance against D. necatrix, which was associated with lignification and phenolic production. These results provide novel information about the role of metabolism of phenolic compounds in basal resistance of walnut plant after inoculation by D. necatrix, where the level of defence response depends on the level of pathogenicity of isolates.

References:

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
Almeida LC, Araujo Sousa F, Leonardo Mendes B, Duarte DF, Santiago TR, Rodrigues de Souza E, Rios JA (2024) Silver nanoparticles as potential fungicide against rice brown spot: physiological and biochemical responses in plants. Tropical Plant Pathology. 5, 1-13. doi: 10.1007/s40858-024-00653-5
Amin Ghezel M, Ghasemnezhad A, Hemmati K, Sohrabi O (2022) Effect of foliar application of plant extracts on the growth behavior and quality of evening primrose (Oenothera biennis L.). International Journal of Horticultural Science and Technology. 9, 393-404. doi: 10.22059/IJHST.2021.321436.456
Amri R, Font i Forcada C, Giménez R, Pina A, Ángeles Moreno M (2021) Biochemical characterization and differential expression of PAL genes associated with translocated peach/plum graft-incompatibility. Frontiers in Plant Science. 12, 177. doi: 10.3389/fpls.2021.622578
Araji S, Grammer TA, Gertzen R, Anderson SD, Mikulic-Petkovsek M, Veberic R, Phu ML, Solar A, Leslie CA, Dandekar AM, Escobar MA (2014) Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut (Juglans regia). Plant Physiology. 164, 1191-1203. doi: 10.1104/pp.113.228593
Arjona-López JM, Capote N, López-Herrera CJ (2019) Improved real-time PCR protocol for the accurate detection and quantification of Rosellinia necatrix in avocado orchards. Plant and Soil. 443, 605-612. doi: 10.1007/s11104-019-04215-6
Arjona-López J, Capote N, Melero-Vara J, López-Herrera C (2020) Control of avocado white root rot by chemical treatments with fluazinam in avocado orchards. Crop Protection. 131, 105100. doi: 10.1016/j.cropro.2020.105100
Arranz S, Perez-Jimenez J, Saura-Calixto F (2008) Antioxidant capacity of walnut (Juglans regia L.): Contribution of oil and defatted matter. European Food Research and Technology. 27, 425-431. doi: 10.1007/s00217-007-0737-2
Aryapak S, Ziarati P (2014) Nutritive value of Persian walnut (Juglans regia L.) orchards. American-Eurasian Journal of Agriculture and Environmental Science, 14, 1228-1235.
Bailey MJ, Biely P, Poutanen K (1992) Interlaboratory testing of methods for assay of xylanase activity. Journal of Biotechnology. 23, 257-270. doi: 10.1016/0168-1656(92)90074-J
Behdad A, Mohsenzadeh S, Azizi M (2020) Comparison of phytochemical compounds of two Glycyrrhiza glabra L. populations and their relationship with the ecological factors. Acta Physiologiae Plantarum. 42, 1-18. doi: 10.1007/s11738-020-03121-0
Behdad E (1975) Morphology, importance and hosts of Rosellinia necatrix (Hart.) Berl., the cause of white root rot in Iran. . Iranian Journal of Plant Pathology. 11, 30-71.
Boeckx T, Winters AL, Webb KJ, Kingston-Smith AH (2015) Polyphenol oxidase in leaves: Is there any significance to the chloroplastic localization? Journal of Experimental Botany. 66, 3571-3579. doi: 10.1093/jxb/erv141
Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry. 72, 248-254. doi: 10.1016/0003-2697(76)90527-3
Carlucci A, Manici LM, Colatruglio L, Caputo A, Frisullo S (2013) Rosellinia necatrix attack according to soil features in the Mediterranean environment. Forest Pathology. 43, 12. doi: 10.1111/j.1439-0329.2012.00787.x
Castro BL, Carreño AJ, Galeano NF, Roux J, Wingfield MJ, Gaitán ÁL (2013) Identification and genetic diversity of Rosellinia spp. associated with root rot of coffee in Colombia. Australasian Plant Pathology. 42, 515-523. doi: 10.1007/s13313-013-0205-3
Chan JC, Paice M, Zhang X (2020) Enzymatic oxidation of lignin: challenges and barriers toward practical applications. ChemCatChem. 12, 401-425. doi: 10.1002/cctc.201901480
Choi SJ, Lee Z, Kim S, Jeong E, Shim JS (2023) Modulation of lignin biosynthesis for drought tolerance in plants. Frontiers in Plant Science. 14, 1116426. doi: 10.3389/fpls.2023.1116426
Das N, Sengupta S, Mukherjee M (1997) Importance of Laccase in vegetative growth of Pleurotus florida. Applied and Environmental Microbiology. 63, 4120-4122. doi: 10.1128/aem.63.10.4120-4122.1997
Di Lella S, La Porta N, Tognetti R, Lombardi F, Nardin T, Larcher R (2022) White rot fungal impact on the evolution of simple phenols during decay of silver fir wood by UHPLC-HQOMS. Phytochemical Analysis. 33, 170-183. doi: 10.1002/pca.3077
FAOSTAT (2023) 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
Fijalkowski KL, Kwarciak-Kozlowska A (2020) Phytotoxicity assay to assess sewage sludge phytoremediation rate using guaiacol peroxidase activity (GPX): a comparison of four growth substrates. Journal of Environmental Management. 263, 110413. doi: 10.1016/j.jenvman.2020.110413
Freeman S, Sztejnberg A, Chet I (1986) Evaluation of Trichoderma as a biocontrol agent for Rosellinia necatrix. Plant and Soil. 94, 163-170. doi: 10.1016/S1049-9644(03)00014-8
Fusco V, Pasciuta V, Lumia V, Matere A, Battaglia V, Bertinelli G, Sansone D, Brunetti A, Pilotti M (2022) Root and stem rot, and wilting of olive tree caused by Dematophora necatrix and associated with Emmia lacerata in Central Italy European. Journal of Plant Pathology. 163, 71-96. doi: 10.1007/s10658-022-02458-1
Gawade DB, Perane RR, Surywanshi AP, Deokar CD (2017) Extracellular enzymes activity determining the virulence of Rhizoctonia bataticola, causing root rot in soybean. Physiological and Molecular Plant Pathology. 100, 49-56. doi: 10.1016/j.pmpp.2017.06.003
Ghatge S, Yang Y, Ahn JH, Hur HG (2020) Biodegradation of polyethylene: a brief review. Applied Biological Chemistry. 63, 1-14. doi: 10.1186/s13765-020-00511-3
Hartley J, Engelbrecht J, van den Berg N (2022) Detection and prevalence of Rosellinia necatrix in South African avocado orchards. European Journal of Plant Pathology. 163, 961-978. doi: 10.1007/s10658-022-02532-8
Hassani D, Sarikhani S, Dastjerdi R, Mahmoudi R, Soleimani A, Vahdati K (2020). Situation and recent trends on cultivation and breeding of Persian walnut in Iran. Scientia Horticulturae, 270, 109369. doi: 10.1016/j.scienta. 2020.109369
Hosseini-Zahani F, Taheri P (2023) The role of oxidative burst, antioxidant genes and enzymes in association with callose in tomato reaction to various taxonomic groups of Rhizoctonia spp. Physiological and Molecular Plant Pathology. 128, 102174. doi: 10.1016/j.pmpp.2023.102174
Huang C, Lai C, Zeng G, Huang D, Xu P, Zhang C, Cheng M, Wan J (2017) Manganese-enhanced degradation of lignocellulosic waste by Phanerochaete chrysosporium: evidence of enzyme activity and gene transcription. Applied Microbiology and Biotechnology. 101, 6541-6549. doi: 10.1007/s00253-017-8371-9
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.
Jahanbani R, Bahramnejad E, Rahimi N, Shafaroodi H, Sheibani N, Moosavi-Movahedi AA, Dehpour A, Vahdati K (2021). Anti-seizure effects of walnut peptides in mouse models of induced seizure: The involvement of GABA and nitric oxide pathways. Epilepsy Research, p.106727.
Jariteh M, Ebrahimzadeh H, Vahdati K, Niknam V and Mirmasoumi M (2011) Antioxidant enzymes activities during secondary somatic embryogenesis in Persian walnut (Juglans regia L.). African Journal of Biotechnology 10(20):4093-4099.
Jiang SJ, Han S, He D, Cao GL, Fang K, Xu X, Yi JM, Wan XQ (2019) The accumulation of phenolic compounds and increased activities of related enzymes contribute to early defense against walnut blight. Physiological and Molecular Plant Pathology. 108, 101433. doi: 10.1016/j.pmpp.2019.101433
Kakueinezhad M, Taheri P, Mahmoudi SB, Tarighi S (2018) Resistance assessment and biochemical responses of sugar beet lines against Pythium aphanidermatum, causing root rot. European Journal of Plant Pathology. 151, 307-319. doi: 10.1007/s10658-017-1373-8.
Kaur SJ, Gupta VK (2017) Production of pectinolytic enzymes pectinase and pectin lyase by Bacillus subtilis SAV-21 in solid state fermentation. Annals of Microbiology. 67, 333-342. doi: 10.1007/s13213-017-1264-4
Khaledi N, Dehshiri A, Hassani F (2021) Effect of seed-borne fungi on seed health of native populations of Iranian cumin (Cuminum cyminum L.). Indian Phytopathology. 74, 659-668. https://doi.org/10.1007/s42360-021-00350-2
Khaledi N, Hassani F (2018) Antifungal activity of Bunium persicum essential oil and its constituents on growth and pathogenesis of Colletotrichum lindemuthianum. Journal of Plant Protection Research. 58, 431-441. doi: 10.24425/jppr.2018.124646
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.
Kim H, Lee SJ, Jo IH, Lee J, Bae W, Kim H, Won K, Hyun TK, Ryu H (2017) Characterization of the Rosellinia necatrix transcriptome and genes related to pathogenesis by single-molecule mRNA sequencing. Plant Pathology Journal. 33, 362-369. doi: 10.5423/PPJ.OA.03.2017.0046.
Kleina HT, dos Santos ÁF, da Silva Silveira Duarte H, Machado EB (2019) Agressiveness and biocontrol of Rosellinia bunodes in Poplar. Floresta. 49, 439-448. doi: 10.5380/rf.v49 i3.59075
Koroljova-Skorobogat’ko OV, Stepanova EV, Gavrilova VP, Morozova OV, Lubimova NV, Dzchafarova AN, Jaropolov AI, Makower A (1998) Purification and characterization of the constitutive form of laccase from the basidiomycete Coriolus hirsutus and effect of inducers on laccase synthesis. Biotechnology and Applied Biochemistry. 28, 47-54. doi: 10.1111/j.1470-8744.1998.tb00511.x.
Konieczny R, Banaś AK, Surówka E, Michalec Ż, Miszalski Z, Libik-Konieczny M (2014) Pattern of antioxidant enzyme activities and hydrogen peroxide content during developmental stages of rhizogenesis from hypocotyl explants of Mesembryanthemum crystallinum L. Plant Cell Reports. 33, 165-177. doi: 10.1007/s00299-013-1520-4
Kubicek CP, Starr TL, Glass NL (2014) Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annual Review of Phytopathology. 52, 427-451. doi: 10.1146/annurev-phyto-102313-045831
Kuvalekar A, Redkar A, Gandhe K, Harsulkar A (2011) Peroxidase and polyphenol oxidase activities in compatible host-pathogen interaction in Jasminum officinale and Uromyces hobsoni: Insights into susceptibility of host. New Zealand Journal of Botany. 3, 351-359. doi: 10.1080/0028825X. 2011. 569727.
Kuwahara M, Glenn JK, Morgan MA, Gold MH (1984) Separation and characterization of two extracelluar H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Letters. 169, 247-250. doi: 10.1016/0014-5793(84)80327-0
Lin D, Xiao M, Zhao J, Li Z, Xing B, Li X, Kong M, Li L, Zhang Q, Liu Y, Cheng H, Qin W, Wu H, Chen S (2016) An overview of plant phenolic compounds and their importance in human nutrition and management of type 2 diabetes. Molecules. 21, 1374-1393. doi: 10.3390/molecules21101374
López M, Ruano-Rosa D, López-Herrera CJ, Monte E, Hermosa R (2008) Intraspecific diversity within avocado field isolates of Rosellinia necatrix from south-east Spain. European Journal of Plant Pathology. 121, 201-205. doi: 10.1007/s10658-007-9253-2
Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signaling & Behavior. 5, 359-368. doi: 10.4161/psb. 5.4.10871
Martínez AT (2002) Molecular biology and structure-function of lignin degrading heme peroxidases. Enzyme and Microbial Technology. 30, 425-444. doi: 10.1016/S0141-0229(01)00521-X
Mayer AM, Harel E, Shaul RB (1965) Assay of catechol oxidase, a critical comparison of methods. Phytochemistry. 5, 783-789. doi: 10.1016/S0031-9422(00)83660-2.
Nikraftar F, Taheri P, Rastegar FM, Tarighi S (2013) Tomato partial resistance to Rhizoctonia solani involves antioxidative defense mechanisms. Physiological and Molecular Plant Pathology. 81, 74-83. doi: 10.1016/j.pmpp.2012.11.004.
Nowogórska A, Patykowski J (2015) Selected reactive oxygen species and antioxidant enzymes in common bean after Pseudomonas syringae pv. phaseolicola and Botrytis cinerea infection. Acta Physiologiae Plantarum. 37, 1725. doi: 10.1007/s11738-014-1725-3
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.
Pasini L, Prodorutti D, Pastorelli S, Pertot I (2016) Genetic diversity and biocontrol of Rosellinia necatrix infecting apple in northern Italy. Plant Disease. 100, 444-452. doi: 10.1094/PDIS-04-15-0480-RE
Pérez-Jiménez RM (2006) A review of the biology and pathogenicity of Rosellinia necatrix-the cause of white root rot disease of fruit trees and other plants. Journal of Phytopathology. 154, 257-266. doi: 10.1111/j.1439-0434.2006.01101.x
Pliego C, Kanematsu S, Ruano-Rosa D, de Vicente A, López-Herrera C, Cazorla FM, Ramos C (2009) GFP sheds light on the infection process of avocado roots by Rosellinia necatrix. Fungal Genetics and Biology. 46, 137-145. doi: 10.1016/j.fgb.2008.11.009.
Pliego C, López-herrera C, Ramos C, Cazorla FM (2012) Developing tools to unravel the biological secrets of Rosellinia necatrix, an emergent threat to woody crops. Molecular Plant Pathology. 13, 226-239. doi: 10.1111/j.1364-3703.2011.00753.x
Pointing SB, Parungao MM, Hyde KD (2003) Production of wood-decay enzymes, mass loss and lignin solubilization in woody by tropical Xylariaceae. Mycological Research. 107, 231-235. doi: 10.1017/S0953756203007329
Pourmoghaddam MJ, Ekiz G, Lambert C, Surup F, Primahana G, Wittstein K, Khodaparast SA, Voglmayr H, Krisai-Greilhuber I, Stradal TEB (2022) Studies on the secondary metabolism of Rosellinia and Dematophora strains (Xylariaceae) from Iran. Mycological Progress, 21(8), 65. doi: 10.1007/s11557-022-01816-x
Pourmoghaddam MJ, Petrini LE, Khodaparast SA (2023) Morphological and molecular study of Dematophora buxi (Xylariaceae) on Buxus sempervirens as a new record from Asia. Mycologia Iranica. 10, 93-101. doi: 10.22043/MI.2023.360801.1243
Praveen K, Viswanath B, Usha KY, Pallavi H, Venkata SRG, Naveen M, Rajasekhar RB (2011) Lignolytic enzymes of a mushroom Stereum ostrea isolated from wood logs. Enzyme Research. 1-6. doi: 10.4061/2011/749518
Ramamoorthy V, Raguchander T, Samiyappan R (2002) Enhancing resistance of tomato and hot pepper to Pythium diseases by seed treatment with fluorescent pseudomonads. European Journal of Plant Pathology. 108, 429-441. doi: 10.1023/A:1016062702102
Rasool F, Uzair M, Naeem MK, Rehman N, Afroz A, Shah H, Khan MR (2021) Phenylalanine ammonia-lyase (PAL) genes family in wheat (Triticum aestivum L.): genome-wide characterization and expression profiling. Agronomy. 11, 2511. doi: 10.3390/ agronomy11122511
Ruano-Rosa D, Schena L, Ippolito A, López-Herrera CJ (2007) Comparison of conventional and molecular methods for the detection of Rosellinia necatrix in avocado orchards in southern Spain. Plant Pathology. 56, 251-256. doi: 10.1111/j.1365-3059.2006.01546.x
Ruiz-Dueñas FJ, Ludell T, Floudas D, Nagy LG, Barrasa JM, Hibbett DS, Martínez AT (2013) Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes. Mycologia. 105, 1428-1444. doi: 10.3852/13-059
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
Schena L, Nigro F, Ippolito A (2002) Identification and detection of Rosellinia necatrix by conventional and real-time Scorpion-PCR. European Journal of Plant Pathology. 108, 355-366. doi: 10.1023/A:1015697813352
Schwarze FWMR (2007) Wood decay under the microscope. Fungal Biology Reviews. 21, 133-170. doi: 10.1016/j.fbr.2007.09.001
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany. 217037, 1-26. doi: 10.1155/2012/217037
Shimizu T, Kanematsu S, Yaegashi H (2018) Draft genome sequence and transcriptional analysis of Rosellinia necatrix infected with a virulent Mycovirus. Phytopathology. 108, 1206-1211. doi: 10.1094/PHYTO-11-17-0365-R
Solekha R, Susanto FA, Joko T, Nuringtyas TR, Purwestri YA (2020) Phenylalanine ammonia lyase (PAL) contributes to the resistance of black rice against Xanthomonas oryzae pv. oryzae. Journal of Plant Pathology. 102, 359-365. doi: 10.1007/s42161-019-00426-z
Song L, Pan L, Jiang N, Fu J, Wan L, Wei S (2022) Effects of endophytic fungi on parasitic process of Taxillus chinensis. Scientific Reports. 12, 1-11. doi: 10.1038/s41598-022-11940-z
Sousa MA, Costa LMAS, Pereira TS, Zied DC, Rinker DL, Dias ES (2019) Enzyme activity and biochemical changes during production of Lentinula edodes (Berk.) Pegler. Food Science and Technology. 39, 774-780. doi: 10.1590/fst.38517
Sun EJ, Lin HS, Hsieh HJ (2008) Study on Rosellinia necatrix isolates causing white root rot disease in Taiwan. Journal of Phytopathology. 156, 104-111. doi: 10.1111/j14390434
Suwannasai N, Sangvichien E, Phosri C, McCloskey S, Wangsawat N, Thamvithayakorn P, Ruchikachorn N, Thienhirun S, Mekkamol S, Sihanonth P, Whalley MA, Whalley AJS (2023) Exploring the Xylariaceae and its relatives. Botanical Studies. 64, 15. doi: 10.1186/s40529-023-00389-6
Suzuki S, Suzuki Y, Yamamoto N, Hattori T, Sakamoto M, Umezawa T (2009) High-throughput determination of thioglycolic acid lignin from rice. Plant Biotechnology Journal. 26, 337-340. doi: 10.5511/ plantbiotechnology.26.337
Takemoto S, Nakamura H, Sasaki A, Shimane T (2011) Species-specific PCRs differentiate Rosellinia necatrix from R. compacta as the prevalent cause of white root rot in Japan. Journal of General Plant Pathology. 77, 107-111. doi: 10.1007/s10327-011-0297-y
Tomás-Barberán FA, Espín JC (2001) Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. Journal of the Science of Food and Agriculture. 81, 853-876. doi: 10.1002/jsfa.885
Treutter D (2006) Significance of flavonoids in plant resistance: A review. Environmental Chemistry Letters. 4, 147-157. doi: 10.1007/s10311-006-0068-8
Urbanek AK, Rymowicz W, Mirończuk AM (2018) Degradation of plastics and plasticdegrading bacteria in cold marine habitats. Applied microbiology and biotechnology. 102, 7669- 7678. doi: 10.1007/s00253-018-9195-y
Vahdati K, Arab MM, Sarikhani S, Sadat Hosseini M, Leslie CA, Brown PJ (2019) Advances in Persian walnut (Juglans regia L.) breeding strategies. In: JM Al-Khayri, SM Jain and DV Johnson (eds.) Advances in plant breeding strategies, Vol 4. pp. 401-472. Nut and Beverage Crops. Springer, Switzerland.
Villavicencio EV, Mali T, Mattila HK, Lundell T (2020) Enzyme activity profiles produced on wood and straw by four fungi of different decay strategies. Microorganisms. 8, 73. doi: 10.3390/microorganisms8010073
Wang X, Wang D, Wang H, Jiao S, Wu J, Hou Y, Sun J, Yuan J (2022) Chemical Profile and Antioxidant Capacity of Kombucha Tea by the Pure Cultured Kombucha. Lebensmittel-Wissenschaft & Technologie. 168, 113931. doi: 10.1016/j.lwt.2022.113931
Waksman SA (1922) A method for counting the number of fungi in the soil. Journal of Bacteriology. 7, 339-341. doi: 10.1128/jb. 7.3.339-341.1922
Williamson-Benavides BA, Dhingra A (2021). Understanding root rot disease in agricultural crops. Horticulturae. 7, 33. doi: 10.3390/horticulturae7020033
Wittstein K, Cordsmeier A, Lambert C, Wendt L, Sir EB, Weber J, Wurzler N, Petrini LE, Stadler M (2020) Identification of Rosellinia species as producers of cyclodepsipeptide PF1022A and resurrection of the genus Dematophora as inferred from polythetic taxonomy. Studies in Mycology, 96, 1-16. doi: 10.1016/j. simyco.2020.01.001
Wood TM, Bhat M (1988) Methods for measuring cellulase activities. Methods in Enzymology. 160, 87-112. doi: 10.1016/0076-6879(88)60109-1
Yan F, Li H, Zhao P (2019) Genome-wide identification and transcriptional expression of the PAL gene family in common walnut (Juglans regia l.). Genes. 10, 46. doi: 10.3390/genes10010046.
Zhang YG, Kan H, Chen SX, Thakur K, Wang S, Zhang JG, Shang YF, Wei ZJ (2020) Comparison of phenolic compounds extracted from Diaphragma juglandis fructus, walnut pellicle, and flowers of Juglans regia using methanol, ultrasonic wave, and enzyme assisted-extraction. Food Chemistry. 321, 126672. doi: 10.1016/j.foodchem. 2020.126672
Zhang Q, Li M, Yang G, Liu X, Yu Z, Peng S (2022) Protocatechuic acid, ferulic acid and relevant defense enzymes correlate closely with walnut resistance to Xanthomonas arboricola pv. Juglandis. BMC Plant Biology. 22, 598. doi: 10.1186/s12870-022-03997-9