{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T10:36:09Z","timestamp":1787567769619,"version":"build-2736575974"},"reference-count":51,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32501656"],"award-info":[{"award-number":["32501656"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["32501656"],"award-info":[{"award-number":["32501656"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Chinese hickory (Carya cathayensis Sarg.) is an economically important tree species widely cultivated in southeastern China, where trunk canker disease caused by Botryosphaeria dothidea poses a serious threat to tree health and production. Pectin-degrading enzymes are important virulence-associated factors that facilitate fungal colonization and host tissue maceration, but their evolutionary diversification and functional roles in B. dothidea during woody host infection remain poorly understood. Comparative genomic analysis revealed lineage-specific variation in the GH28 glycoside hydrolase family among the examined Botryosphaeriaceae species, with B. dothidea exhibiting an expanded GH28 repertoire relative to the analyzed species. Expression analysis and functional assays revealed that BdGH28_3 showed the highest transcript abundance during infection stage and contributed to the full virulence of B. dothidea. A predicted protein\u2013protein interaction (PPI) network suggested potential associations between BdGH28_3 and other pectinolytic enzymes, including polygalacturonases, pectin lyases, and pectinesterases. Collectively, these findings identify GH28 diversification as a distinctive feature of the B. dothidea genome and establish BdGH28_3 as a virulence-associated member, providing a foundation for investigating GH28-mediated pathogenicity in woody hosts.<\/jats:p>","DOI":"10.3390\/plants15162547","type":"journal-article","created":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T09:20:02Z","timestamp":1787563202000},"page":"2547","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genome-Wide Characterization of the Botryosphaeria dothidea GH28 Family Reveals BdGH28_3 Contributes to Virulence on Chinese Hickory"],"prefix":"10.3390","volume":"15","author":[{"given":"Dong","family":"Liang","sequence":"first","affiliation":[{"name":"College of Advanced Agricultural Sciences, Zhejiang Agriculture and Forest University, Hangzhou 311300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Ai","sequence":"additional","affiliation":[{"name":"College of Advanced Agricultural Sciences, Zhejiang Agriculture and Forest University, Hangzhou 311300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi-Ru","family":"Jiang","sequence":"additional","affiliation":[{"name":"College of Advanced Agricultural Sciences, Zhejiang Agriculture and Forest University, Hangzhou 311300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"943","DOI":"10.32604\/phyton.2022.023225","article-title":"Effects of Different Chinese Hickory Husk Returning Modes on Soil Nutrition and Microbial Community in Acid Forest Soil","volume":"92","author":"Liu","year":"2023","journal-title":"Phyton"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1186\/s13068-021-02076-9","article-title":"Valorization of Chinese Hickory Shell as Novel Sources for the Efficient Production of Xylooligosaccharides","volume":"14","author":"Wang","year":"2021","journal-title":"Biotechnol. Biofuels"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1094\/PDIS-05-11-0457","article-title":"First Report of Canker on Pecan (Carya cathayensis) Caused by Botryosphaeria dothidea in China","volume":"95","author":"Zhang","year":"2011","journal-title":"Plant Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s13313-017-0465-4","article-title":"Management of Chinese Hickory (Carya cathayensis) Trunk Canker through Effective Fungicide Application Programs and Baseline Sensitivity of Botryosphaeria dothidea to Trifloxystrobin","volume":"46","author":"Dai","year":"2017","journal-title":"Australas. Plant Pathol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1111\/mpp.12495","article-title":"Botryosphaeria dothidea: A Latent Pathogen of Global Importance to Woody Plant Health","volume":"18","author":"Marsberg","year":"2017","journal-title":"Mol. Plant Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3869","DOI":"10.1094\/PDIS-02-21-0289-RE","article-title":"Diversity of Botryosphaeriaceae Species Associated with Chinese Hickory Tree (Carya cathayensis) Trunk Cankers","volume":"105","author":"Zhuang","year":"2021","journal-title":"Plant Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"51","DOI":"10.3114\/sim0021","article-title":"The Botryosphaeriaceae: Genera and Species Known from Culture","volume":"76","author":"Phillips","year":"2013","journal-title":"Stud. Mycol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"105500","DOI":"10.1016\/j.pestbp.2023.105500","article-title":"Sensitivity and Resistance Risk of Botryosphaeria dothidea Causing Chinese Hickory Trunk Canker to Fludioxonil","volume":"194","author":"Li","year":"2023","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Liang, D., Jiang, Y., Zhang, Y., Mao, C., Ma, T., and Zhang, C. (2024). The Comparative Genomics of Botryosphaeriaceae Suggests Gene Families of Botryosphaeria dothidea Related to Pathogenicity on Chinese Hickory Tree. J. Fungi, 10.","DOI":"10.3390\/jof10040299"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"D490","DOI":"10.1093\/nar\/gkt1178","article-title":"The Carbohydrate-Active Enzymes Database (CAZy) in 2013","volume":"42","author":"Lombard","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Zhao, Z., Liu, H., Wang, C., and Xu, J.R. (2013). Comparative Analysis of Fungal Genomes Reveals Different Plant Cell Wall Degrading Capacity in Fungi. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-274"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1094\/MPMI-02-12-0043-R","article-title":"Cellulases Belonging to Glycoside Hydrolase Families 6 and 7 Contribute to the Virulence of Magnaporthe oryzae","volume":"25","author":"Itoh","year":"2012","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/s12284-022-00584-2","article-title":"Magnaporthe oryzae Chloroplast Targeting Endo-\u03b2-1,4-Xylanase I MoXYL1A Regulates Conidiation, Appressorium Maturation and Virulence of the Rice Blast Fungus","volume":"15","author":"Shabbir","year":"2022","journal-title":"Rice"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1007\/s00294-018-0814-z","article-title":"Two Genes Encoding GH10 Xylanases Are Essential for the Virulence of the Oomycete Plant Pathogen Phytophthora parasitica","volume":"64","author":"Lai","year":"2018","journal-title":"Curr. Genet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1146\/annurev-arplant-083023-034055","article-title":"The Dynamics, Degradation, and Afterlives of Pectins: Influences on Cell Wall Assembly and Structure, Plant Development and Physiology, Agronomy, and Biotechnology","volume":"76","author":"Anderson","year":"2025","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1186\/s13068-021-02045-2","article-title":"Revalorization of Sunflower Stalk Pith as Feedstock for the Coproduction of Pectin and Glucose Using a Two-Step Dilute Acid Pretreatment Process","volume":"14","author":"Zhang","year":"2021","journal-title":"Biotechnol. Biofuels"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3219","DOI":"10.1105\/tpc.105.037473","article-title":"Pectin Methylesterases and Pectin Dynamics in Pollen Tubes","volume":"17","author":"Bosch","year":"2005","journal-title":"Plant Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.pbi.2008.03.006","article-title":"Pectin Structure and Biosynthesis","volume":"11","author":"Mohnen","year":"2008","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/BF02198762","article-title":"Production of a Toxic Metabolite and Pectolytic Enzyme by Pythium butleri","volume":"52","author":"Janardhanan","year":"1974","journal-title":"Mycopathol. Mycol. Appl."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1128\/MMBR.00038-07","article-title":"Structural Biology of Pectin Degradation by Enterobacteriaceae","volume":"72","author":"Abbott","year":"2008","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Sharma, V., Salwan, R., and Al-Ani, L.K.T. (2020). The Effect of Incompatible Plant Pathogens on the Host Plant. Molecular Aspects of Plant Beneficial Microbes in Agriculture, Elsevier.","DOI":"10.1016\/B978-0-12-818469-1.00004-3"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Zhang, F., Liu, N., Chen, T., Xu, H., Li, R., Wang, L., Zhou, S., Cai, Q., Hou, X., and Wang, L. (2024). Genome-Wide Identification of GH28 Family and Insight into Its Contributions to Pod Shattering Resistance in Brassica napus L.. BMC Genom., 25.","DOI":"10.1186\/s12864-024-10406-y"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1111\/mpp.13366","article-title":"The Glycoside Hydrolase 28 Member VdEPG1 Is a Virulence Factor of Verticillium dahliae and Interacts with the Jasmonic Acid Pathway-Related Gene GhOPR9","volume":"24","author":"Liu","year":"2023","journal-title":"Mol. Plant Pathol."},{"key":"ref_24","unstructured":"Rastegari, A.A., Yadav, A.N., Awasthi, A.K., and Yadav, N. (2020). The Role of Microbial Signals in Plant Growth and Development: Current Status and Future Prospects. New and Future Developments in Microbial Biotechnology and Bioengineering, Elsevier."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1094\/MPMI.1998.11.10.1009","article-title":"The Endopolygalacturonase Gene Bcpg1 Is Required for Full Virulence of Botrytis cinerea","volume":"11","author":"Mulder","year":"1998","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Nagel, J.H., Wingfield, M.J., and Slippers, B. (2021). Increased Abundance of Secreted Hydrolytic Enzymes and Secondary Metabolite Gene Clusters Define the Genomes of Latent Plant Pathogens in the Botryosphaeriaceae. BMC Genom., 22.","DOI":"10.1186\/s12864-021-07902-w"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Liang, D., Jiang, Y., Ai, W., Zhang, Y., Mao, C., Ma, T., and Zhang, C. (2025). Co-Expression Network Analysis Suggests PacC Transcriptional Factor Involved in Botryosphaeria dothidea Pathogenicity in Chinese Hickory. J. Fungi, 11.","DOI":"10.3390\/jof11080580"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.pbi.2008.03.003","article-title":"Wood Cell Walls: Biosynthesis, Developmental Dynamics and Their Implications for Wood Properties","volume":"11","author":"Mellerowicz","year":"2008","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Zhao, N., Li, D., Guo, B.J., Tao, X., Lin, X., Yan, S.Z., and Chen, S.L. (2020). Genome Sequencing and Analysis of the Hypocrellin-Producing Fungus Shiraia bambusicola S4201. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.00643"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1111\/mpp.13108","article-title":"Target of Rapamycin Controls Hyphal Growth and Pathogenicity through FoTIP4 in Fusarium oxysporum","volume":"22","author":"Li","year":"2021","journal-title":"Mol. Plant Pathol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1093\/protein\/14.9.615","article-title":"Pectin Degrading Glycoside Hydrolases of Family 28: Sequence-Structural Features, Specificities and Evolution","volume":"14","year":"2001","journal-title":"Protein Eng."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Villarreal, F., Stocchi, N., and Ten Have, A. (2022). Functional Classification and Characterization of the Fungal Glycoside Hydrolase 28 Protein Family. J. Fungi, 8.","DOI":"10.3390\/jof8030217"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1111\/j.1365-313X.2005.02436.x","article-title":"Necrotizing Activity of Five Botrytis cinerea Endopolygalacturonases Produced in Pichia pastoris","volume":"43","author":"Kars","year":"2005","journal-title":"Plant J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.gene.2011.02.009","article-title":"Evolutionary Analysis of Glycosyl Hydrolase Family 28 (GH28) Suggests Lineage-Specific Expansions in Necrotrophic Fungal Pathogens","volume":"479","author":"Sprockett","year":"2011","journal-title":"Gene"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1094\/MPMI.2002.15.9.907","article-title":"Characterization and Evolutionary Analysis of a Large Polygalacturonase Gene Family in the Oomycete Plant Pathogen Phytophthora cinnamomi","volume":"15","author":"Marshall","year":"2002","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1038\/nchembio.439","article-title":"Heterogeneity in the Chemistry, Structure and Function of Plant Cell Walls","volume":"6","author":"Burton","year":"2010","journal-title":"Nat. Chem. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Blanco-Ulate, B., Morales-Cruz, A., Amrine, K.C., Labavitch, J.M., Powell, A.L.T., and Cantu, D. (2014). Genome-Wide Transcriptional Profiling of Botrytis cinerea Genes Targeting Plant Cell Walls during Infections of Different Hosts. Front. Plant Sci., 5.","DOI":"10.3389\/fpls.2014.00435"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Le Normand, M., Rietzler, B., Vilaplana, F., and Ek, M. (2021). Macromolecular Model of the Pectic Polysaccharides Isolated from the Bark of Norway Spruce (Picea abies). Polymers, 13.","DOI":"10.3390\/polym13071106"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1007\/BF00201825","article-title":"Pectin Changes in Samples Containing Poplar Cambium and Inner Bark in Relation to the Seasonal Cycle","volume":"193","author":"Goldberg","year":"1994","journal-title":"Planta"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1007\/s004250050104","article-title":"Pectin Methylesterases from Poplar Cambium and Inner Bark: Localization, Properties and Seasonal Changes","volume":"202","author":"Guglielmino","year":"1997","journal-title":"Planta"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3871","DOI":"10.1021\/acssuschemeng.6b00641","article-title":"Morphology and Overall Chemical Characterization of Willow (Salix sp.) Inner Bark and Wood: Toward Controlled Deconstruction of Willow Biomass","volume":"4","author":"Dou","year":"2016","journal-title":"ACS Sustain. Chem. Eng."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1094\/PD-77-0170","article-title":"Role of Botryosphaeria Species in Peach Tree Gummosis on the Basis of Differential Isolation from Outer and Inner Bark","volume":"77","author":"Pusey","year":"1993","journal-title":"Plant Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1821","DOI":"10.1094\/PDIS-03-12-0275-PDN","article-title":"First Report of Botryosphaeria dothidea Causing Canker and Dieback Disease of Helwingia chinensis in China","volume":"96","author":"Yu","year":"2012","journal-title":"Plant Dis."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.scienta.2016.03.002","article-title":"Cytological and Histological Studies of the Interaction between Botryosphaeria dothidea and Apple Twigs","volume":"202","author":"Han","year":"2016","journal-title":"Sci. Hortic."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Yang, Y., Yu, Y., Liang, Y., Anderson, C.T., and Cao, J. (2018). A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases. Front. Plant Sci., 9.","DOI":"10.3389\/fpls.2018.01208"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"S170","DOI":"10.1016\/j.fgb.2008.07.021","article-title":"Assessment of the Pectin Degrading Enzyme Network of Aspergillus niger by Functional Genomics","volume":"46","author":"Schaap","year":"2009","journal-title":"Fungal Genet. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"W95","DOI":"10.1093\/nar\/gky418","article-title":"dbCAN2: A Meta Server for Automated Carbohydrate-Active Enzyme Annotation","volume":"46","author":"Zhang","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"6968","DOI":"10.1038\/s41467-022-34630-w","article-title":"MUSCLE5: High-Accuracy Alignment Ensembles Enable Unbiased Assessments of Sequence Homology and Phylogeny","volume":"13","author":"Edgar","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e49","DOI":"10.1093\/nar\/gkr1293","article-title":"MCScanX: A Toolkit for Detection and Evolutionary Analysis of Gene Synteny and Collinearity","volume":"40","author":"Wang","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e239","DOI":"10.1002\/imt2.239","article-title":"ImageGP 2 for Enhanced Data Visualization and Reproducible Analysis in Biomedical Research","volume":"3","author":"Chen","year":"2024","journal-title":"iMeta"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/16\/2547\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T09:43:03Z","timestamp":1787564583000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/16\/2547"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,21]]},"references-count":51,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["plants15162547"],"URL":"https:\/\/doi.org\/10.3390\/plants15162547","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,21]]}}}