Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2025-06-11
Page range: 19-34
Abstract views: 97
PDF downloaded: 6

Branch blight and dieback of walnut (Juglans regia L.) caused by Rhytidhysteron juglandis sp. nov. and its endophytic biocontrol agent Granulobasidium vellereum

School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China
School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China
School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China
Intergrated Natural Resources Survey Center, China Geological Survey, Beijing, China
School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China
Rhytidhysteron biological control pathogenicity walnut disease Fungi

Abstract

English walnut (Juglans regia L.) is known for its health benefits and has been widely cultivated in China. Walnut branch blight and dieback are common diseases in walnut plantations. A survey was conducted at walnut plantations in Beijing, China to identify the causal agents of the disease. Six isolates were retrieved from diseased or dead branch samples of English walnut. DNA sequence analyses based on concatenated ITS, LSU, and tef1-α loci, the isolates were identified as a new fungal species, Rhytidhysteron juglandis sp. nov. Endophytic Granulobasidium vellereum isolated from healthy walnut branches, has shown potential as a biological control agent against R. juglandis. Antagonistic assays by dual cultures and walnut branches have demonstrated that G. vellereum significantly inhibits the colony or disease lesion expansion caused by R. juglandis.

References

  1. Bi, S.J., Song, F.H., Zhang, Y.N., Shi, Y.J., Han, H.W. & Bai, J.Y. (2019) Cytospora chrysosperma causing branch dieback and canker of black walnut in China. Canadian Journal of Plant Pathology 42: 203–209. https://doi.org/10.1080/07060661.2019.1637377
  2. Boehm, E.W.A., Mugambi, G.K., Miller, A.N., Huhndorf, S.M., Marincowitz, S., Spatafora, J.W. & Schoch, C.L. (2009) A molecular phylogenetic reappraisal of the Hysteriaceae, Mytilinidiaceae and Gloniaceae (Pleosporomycetidae, Dothideomycetes) with keys to world species. Studies in Mycology 64: 49–83. https://doi.org/10.3114/sim.2009.64.03
  3. Braue, J.A., Larue, R.W., Boyd, A.S. & Fine, J.D. (2020) Phaeohyphomycosis caused by Rhytidhysteron rufulum. Clinical and Experimental Dermatology 45: 524–526. https://doi.org/10.1111/ced.14123
  4. Cao, Y.L. (2022) The development status, problems and countermeasures of Chinese walnut industry in the new period. Henan Agricultural University, China.
  5. Chen, S.F., Morgan, D.P., Hasey, J.K., Anderson, K. & Michailides, T.J. (2014) Phylogeny, morphology, distribution, and pathogenicity of Botryosphaeriaceae and Diaporthaceae from English Walnut in California. Plant Disease 98 (5): 636–652. https://doi.org/10.1094/PDIS-07-13-0706-RE
  6. Chowdhary, A., Guarro, J., Randhawa, H.S., Gene, J., Cano, J., Jain, P.K., Kumar, S. & Khanna, G. (2008) A rare case of chromoblastomycosis in a renal transplant recipient caused by a non-sporulating species of Rhytidhysteron. Medical Mycology 46: 163–166. https://doi.org/10.1080/13693780701630420
  7. Cobos-Villagrán, A., Hernández-Rodríguez, C., Valenzuela, R., Villa-Tanaca, L., Calvillo-Medina, R.P., Mateo-Cid, L.E., Martínez-Pineda, M. & Raymundo, T. (2020) The genus Rhytidhysteron (Dothideomycetes, Ascomycota) in Mexico. Acta Botanica Mexicana 127: e1675. https://doi.org/10.21829/abm127.2020.1675
  8. Cobos-Villagrán, A., Valenzuela, R., Hernandez-Rodriguez, C., Calvillo-Medina, R.P., Villa-Tanaca, L., Mateo-Cid, L.E., Perez-Valdespino, A., Martinez-Gonzalez, C.R. & Raymundo, T. (2021) Three new species of Rhytidhysteron (Dothideomycetes, Ascomycota) from Mexico. Mycokeys 83: 123–144. https://doi.org/10.3897/mycokeys.83.68582
  9. Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: More models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
  10. Dayarathne, M.C., Jones, E.B.G., Maharachchikumbura, S.S.N., Devadatha, B., Sarma, V.V., Khongphinitbunjong, K., Chomnunti, P. & Hyde, K.D. (2020) Morpho-molecular characterization of microfungi associated with marine based habitats. Mycosphere 11: 1–188. https://doi.org/10.5943/mycosphere/11/1/1
  11. De Silva, N.I., Tennakoon, D.S., Thambugala, K.M., Karunarathna, S.C., Lumyong, S. & Hyde, K.D. (2019) Morphology and multigene phylogeny reveal a new species and a new record of Rhytidhysteron (Dothideomycetes, Ascomycota) from China. Asian Journal of Mycology 3: 295–306. https://doi.org/10.5943/ajom/3/1/4
  12. Dennis, C. & Webster, J. (1971) Antagonistic properties of species–groups of Trichoderma: III. Hyphal interaction. Transactions of the British Mycological Society 57: 363–369. https://doi.org/10.1016/S0007-1536(71)80050-5
  13. Dervis, S., Turkolmez, S., Ciftci, O., Serce, C.U. & Dikilitas, M. (2019) First report of Neoscytalidium dimidiatum causing black canker and root rot of walnut in Turkey. Plant Disease 103: 2129. https://doi.org/10.1094/PDIS-02-19-0306-PDN
  14. Dingle, T.C., Jansen, B., Walker, C., Sam, M., Verity, B., Purdy, D., Paul, P. & Schwartz, I.S. (2022) Implantation subcutaneous phaeohyphomycosis caused by Rhytidhysteron rufulum: A case report. Medical Mycology Case Report 36: 16–18. https://doi.org/10.1016/j.mmcr.2022.03.002
  15. Doilom, M., Dissanayake, A.J., Wanasinghe, D.N., Boonmee, S., Liu, J.K., Bhat, D.J., Taylor, J.E., Bahkali, A.H., McKenzie, E.H.C. & Hyde, K.D. (2016) Micro fungi on Tectona grandis (teak) in Northern Thailand. Fungal Diversity 82: 107–182. https://doi.org/10.1007/s13225-016-0368-7
  16. Dou, Z.P., He, W. & Zhang, Y. (2017) Does morphology matter in taxonomy of Lasiodiplodia? An answer from Lasiodiplodia hyalina sp. nov. Mycosphere 8: 1014–1027. https://doi.org/10.5943/mycosphere/8/2/5
  17. Du, T.Y., Dai, D.Q., Mapook, A., Lu, L., Stephenson, S.L., Suwannarach, N., Elgorban, A.M., Al-Rejaie, S., Karunarathna, S.C. & Tibpromma, S. (2023) Additions to Rhytidhysteron (Hysteriales, Dothideomycetes) in China. Journal of Fungi 9 (2): 148. https://doi.org/10.3390/jof9020148
  18. Fan, X.L., Hyde, K.D., Liu, M., Liang, Y.M. & Tian, C.M. (2015) Cytospora species associated with walnut canker disease in China, with description of a new species C. gigalocus. Fungal Biology 119: 310–319. https://doi.org/10.1016/j.funbio.2014.12.011
  19. Fraser, J. (2020) Subcutaneous phaeohyphomycosis caused by a black pigmented mould (Rhytidhysteron species) in rural north-western New South Wales, Australia. Rural and Remote Health 20. https://doi.org/10.22605/RRH5903
  20. Guo, R. (2016) Occurrence and control trend of main d es and pests of walnut in Baoji city. Northwest A&F University, China.
  21. Gusella, G., Giambra, S., Conigliaro, G., Burruano, S. & Polizzi, G. (2021) Botryosphaeriaceae species causing canker and dieback of English walnut (Juglans regia) in Italy. Forest Pathology 51 (1). https://doi.org/10.1111/efp.12661
  22. Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182. https://doi.org/10.1093/sysbio/42.2.182
  23. Horst, K.R. (2013) Blights. In: Westcott’s Plant Disease Handbook. Springer, Netherlands, pp. 135–186. https://doi.org/10.1007/978-94-007-2141-8_20
  24. Iqbal, S., Hernandez, Y., Lolas, M.A., Elfar, K., Eskalen, A., Latorre, B.A. & Diaz, G.A. (2022) Dothiorella sarmentorum causing branch dieback of English walnut in Maule Region, Chile. Plant Disease 112 (11): 103. https://doi.org/10.1094/PDIS-03-22-0636-PDN
  25. Jimenez Luna, I., Besoain, X., Saa, S., Peach–Fine, E., Cadiz Morales, F., Riquelme, N., Larach, A., Morales, J., Ezcurra, E., Ashworth, V.E. & Rolshausen, P.E. (2022) Identity and pathogenicity of Botryosphaeriaceae and Diaporthaceae from Juglans regia in Chile. Phytopathologia Mediterranea 61: 79–94. https://doi.org/10.36253/phyto-12832
  26. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
  27. Keche, A., Tigga, R., Satyaki, G., Chhabra, N. & Gupta, R. (2022) Rare isolates from subcutaneous mycotic lesions; A study from tertiary care center in Chhattisgarh, India. Medical Mycology 60: 140. https://doi.org/10.1093/mmy/myac072.P216
  28. Kokubun, T., Scott-Brown, A., Kite, G.C. & Simmonds, M.S.J. (2016) Protoilludane, Illudane, Illudalane, and Norilludane Sesquiterpenoids from Granulobasidium vellereum. Journal of Natural Products 79 (6): 1698–1701. https://doi.org/10.1021/acs.jnatprod.6b00325
  29. Kumar, V., Cheewangkoon, R., Thambugala, K.M., Jones, G.E.B., Brahmanage, R.S., Doilom, M., Jeewon, R. & Hyde, K.D. (2019) Rhytidhysteron mangrovei (Hysteriaceae), a new species from mangroves in Phetchaburi Province, Thailand. Phytotaxa 401: 166–178. https://doi.org/10.11646/phytotaxa.401.3.2
  30. Lopez-Moral, A., Lovera, M., Raya, M.D., Cortes-Cosano, N., Arquero, O., Trapero, A. & Agusti-Brisach, C. (2020) Etiology of branch dieback and shoot blight of English Walnut caused by Botryosphaeriaceae and Diaporthe species in Southern Spain. Plant Disease 104: 533–550. https://doi.org/10.1094/PDIS-03-19-0545-RE
  31. Mapook, A., Hyde, K.D., McKenzie, E.H.C., Jones, E.B.G., Bhat, D.J., Jeewon, R., Stadler, M., Samarakoon, M.C., Malaithong, M., Tanunchai, B., Buscot, F., Wubet, T. & Purahong, W. (2020) Taxonomic and phylogenetic contributions to fungi associated with the invasive weed Chromolaena odorata (Siam weed). Fungal Diversity 101: 1–175. https://doi.org/10.1007/s13225-020-00444-8
  32. Meng, J., Fang, X.P., Shi, X.M., Zhang, Y. & Liu, J. (2023) Situation, problems and suggestions on the development of walnut industry in China. China oils and fats 48 (1).
  33. Mudhigeti, N., Patnayak, R., Kalawat, U. & Yeddula, S.R.C. (2018) Subcutaneous Rhytidhysteron Infection: A Case Report from South India with Literature Review. Cureus Journal of Medical Science 10. https://doi.org/10.7759/cureus.2406
  34. Mugambi, G.K. & Huhndorf, S.M. (2009) Parallel evolution of hysterothecial ascomata in ascolocularous fungi (Ascomycota, Fungi). Systematics and Biodiversity 7: 453–464. https://doi.org/10.1017/S147720000999020X
  35. Mulero-Aparicio, A., Agusti-Brisach, C., Raya, M.D., Lovera, M., Arquero, O. & Trapero, A. (2019) First report of Fusarium solani causing stem canker in English walnut in Spain. Plant Disease 103: 3281. https://doi.org/10.1094/PDIS-06-19-1163-PDN
  36. Nord, C. (2014) Secondary metabolites from the saprotrophic fungus Granulobasidium vellereum. Swedish University of Agricultural Sciences, Swedish.
  37. Nord, C.L., Menkis, A., Lendel, C., Vasaitis, R. & Broberg, A. (2014) Sesquiterpenes from the saprotrophic fungus Granulobasidium vellereum (Ellis & Cragin) Jülich. Phytochemistry 102: 197–204. https://doi.org/10.1016/j.phytochem.2014.03.012
  38. Nord, C.L., Menkis, A., Vasaitis, R. & Broberg, A. (2013) Protoilludane sesquiterpenes from the wood decomposing fungus Granulobasidium vellereum (Ellis & Cragin) Jülich. Phytochemistry 90: 128–134. https://doi.org/10.1016/j.phytochem.2014.03.012
  39. Polat, Z., Gultekin, M.A., Palacioglu, G., Bayraktar, H., Ozer, N. & Yilmaz, S. (2020) First report of Neocosmospora solani causing stem canker on Juglans regia in Turkey. Plant Disease 102: 1289. https://doi.org/10.1007/s42161-020-00570-x
  40. Posada, D. & Buckley, T.R. (2004) Model selection and model averaging inphylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793–808. https://doi.org/10.1080/10635150490522304
  41. Rashmi, M., Kushveer, J.S. & Sarma, V.V. (2019) A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10: 798–1079. https://doi.org/10.5943/mycosphere/10/1/19
  42. Rehner, S.A. & Buckley, E. (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97: 84–98. https://doi.org/10.1080/15572536.2006.11832842
  43. Ren, G.C., Wanasinghe, D.N., Jeewon, R., Monkai, J., Mortimer, P.E., Hyde, K.D., Xu, J.C. & Cui, H. (2022) Taxonomy and phylogeny of the novel Rhytidhysteron-like collections in the Greater Mekong Subregion. Mycokeys 86: 65–85. https://doi.org/10.3897/mycokeys.86.70668
  44. Robles, C.A., Ceriani-Nakamurakare, E., Slodowicz, M., Gonzalez-Audino, P. & Carmaran, C.C. (2018) Granulobasidium vellereum (Ellis & Cragin) Jülich a promising biological control agent. Biological Contro 117: 99–108. https://doi.org/10.1016/j.biocontrol.2017.10.012
  45. Ronquist, F., Teslenko, M., Mark, P., Avres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
  46. Samuels, G.J. & Müller, E. (1979) Life-history studies of Brazilian Ascomycetes. 7. Rhytidhysteron rufulum and the genus Eutryblidiella. Sydowia 32: 277–292.
  47. Seta, S., Gonzalez, M. & Lori, G. (2004) First report of walnut canker caused by Fusarium incarnatum in Argentina. Plant Pathology 53: 248. https://doi.org/10.1111/j.0032-0862.2004.00968.x
  48. Shen, D.Y., Wu, S.T., Zheng, Y.W., Han, Y.X., Ni, Z.L., Li, S.L., Tang, F.B., Mo, R.H. & Liu, Y.H. (2021) Characterization of iron walnut in different regions of China based on phytochemical composition. Journal of Food Science and Technology-mysore 58: 1358–1367. https://doi.org/10.1007/s13197-020-04647-4
  49. Singh, B., Kalha, C.S., Razdan, V.K. & Verma, V.S. (2011) First report of walnut canker caused by Fusarium incarnatum from India. Plant Disease 95: 1587. https://doi.org/10.1094/PDIS-04-11-0352
  50. Spegazzini, C. (1881) Fungi argentini additis nonnullis brasiliensibus montevideensibusque. Pugillus quartus (Continuacion). An Soc Cient Argent 12: 174–189.
  51. Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  52. Swofford, D.L. (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, Massachusetts.
  53. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
  54. Thambugala, K.M., Hyde, K.D., Eungwanichayapant, P.D., Romero, A.I. & Liu, Z.Y. (2016) Additions to the Genus Rhytidhysteron in Hysteriaceae. Cryptogamie, Mycologie 37: 99–116. https://doi.org/10.7872/crym/v37.iss1.2016.99
  55. Thiyagarajan, M., Gopal, M., Rangasamy, G. & Ranganathan, U. (2019) Subcutaneous Phaeohyphomycosis caused by Rhytidhysteron rufulum-A case report and review of literature. Journal of Clinical and Diagnostic Research 13: DD01–DD02. https://doi.org/10.7860/JCDR/2019/42460.13141
  56. Vahdati, K., Arab, M.M., Sarikhani, S., Sadat-Hosseini, M., Leslie, C.A. & Brown, P.J. (2019) Advances in Persian Walnut (Juglans regia L.) Breeding Strategies. In Advances in Plant Breeding Strategies: Nut and Beverage Crops. https://doi.org/10.1007/978-3-030-23112-5_11
  57. Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172: 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  58. Wanasinghe, D.N., Mortimer, P.E. & Xu, J.C. (2021) Insight into the systematics of microfungi colonizing dead woody twigs of Dodonaea viscosa in Honghe (China). Journal of Fungi 7 (3). https://doi.org/10.3390/jof7030180
  59. Wang, F.H., Zeng, Q., Lv, Y.C., Xu, X.L., Han, S., Yang, H., Li, S.J., Lin, T.T., Yang, H.B. & Yang, C.L. (2022) Branch Blight of Juglans regia Caused by Palmiascoma qujingense in China. Plant Disease 106: 2292. https://doi.org/10.1094/PDIS-01-22-0010-PDN
  60. White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gefand, D.H., Sninsky, J.J. & White, T.J. (Eds.) PCR Protocols: a guide to methods and applications. Academic Press, San Diego. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  61. Xu, S.S., Zang, R., Sun, D.Y., Zhu, T.S., Chen, X.W. & Chen, X.F. (2023) First report of Cytospora tritici causing branch canker on English walnut in China. Plant Disease 105 (2): 595. https://doi.org/10.1007/s42161-023-01306-3
  62. Xu, X.L., Xiao, Q.G., Yang, C.L., Jeewon, R. & Liu, Y.G. (2022) Multigene phylogenetic support for novel Rhytidhysteron Speg. species (Hysteriaceae) from Sichuan Province, China. Cryptogamie Mycologie 43: 63–79. https://doi.org/10.5252/cryptogamie-mycologie2022v43a3
  63. Yildiz, A., Benlioglu, S., Benlioglu, K. & Korkom, Y. (2022) Occurrence of twig blight and branch dieback of walnut caused by Botryosphaeriaceae species in Turkey. Journal of Plant Disease and Protection 129: 687–693. https://doi.org/10.1007/s41348-022-00591-x
  64. Zhang, M., Zhang, Y.K., Geng, Y.H., Zang, R. & Wu, H.Y. (2017) First report of Diplodia seriata causing twig dieback of English walnut in China. Plant Disease 101 (6): 1036. https://doi.org/10.1094/PDIS-04-16-0458-PDN
  65. Zhang, Y., Wang, H.K., Fournier, J., Crous, P.W., Jeewon, R., Pointing, S.B. & Hyde, K.D. (2009) Towards a phylogenetic clarification of Lophiostoma Msarina and morphologically similar genera in the Pleosporales. Fungal Diversity 38: 225–251. https://doi.org/10.1094/PDIS-01-19-0079-RE
  66. Zhao, L.L., Sun, W., Zhang, L., Yin, Y.Q., Xie, Y.Q. & Zhang, Y. (2024) Heart rot disease caused by Nothophoma juglandis sp. nov. and its endophytic biocontrol agent. Plant Disease 108 (3): 746–756. https://doi.org/10.1094/PDIS-11-22-2660-RE

How to Cite

Zhao, L.-L., Zhang, L., Jiao, N., Li, M. & Zhang, Y. (2025) Branch blight and dieback of walnut (Juglans regia L.) caused by Rhytidhysteron juglandis sp. nov. and its endophytic biocontrol agent Granulobasidium vellereum. Phytotaxa 705 (1): 19–34. https://doi.org/10.11646/phytotaxa.705.1.2