Vol. 62 No. 2 (2023): including 12th Special issue on Grapevine Trunk Diseases
Research papers - 12th Special Issue on Grapevine Trunk Diseases

Unravelling the colonization mechanism of Lasiodiplodia brasiliensis in grapevine plants

Edelweiss A. RANGEL-MONTOYA
Departamento de Microbiología, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada, Baja California, México, 22860
Philippe E. ROLSHAUSEN
Department of Botany and Plant Sciences, University of California Riverside, Riverside, 92521, CA
Rufina HERNANDEZ-MARTINEZ
Departamento de Microbiología, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada, Baja California, México, 22860
Categories

Published 2023-05-12

Keywords

  • carbohydrate metabolism,
  • Botryosphaeria dieback,
  • plant defense

How to Cite

[1]
E. A. RANGEL-MONTOYA, P. E. ROLSHAUSEN, and R. HERNANDEZ-MARTINEZ, “Unravelling the colonization mechanism of Lasiodiplodia brasiliensis in grapevine plants”, Phytopathol. Mediterr., vol. 62, no. 2, pp. 135–149, May 2023.

Abstract

Botryosphaeriaceae cause the degenerative disease Botryosphaeria dieback in many woody hosts, including grapevine. These pathogens penetrate host plants through pruning wounds, and colonize vascular tissues causing necrotic lesions, cankers, and eventually plant death. Colonization processes by Botryosphaeriaceae and their interactions with their hosts has been understudied. The colonization mechanisms were examined for Lasiodiplodia brasiliensis, a common pathogen causing Botryosphaeria dieback in Mexican vineyards. Lasiodiplodia brasiliensis MXBCL28 was inoculated onto grapevine ‘Cabernet Sauvignon’ plants, and after 2 months, infected tissues were observed with microscopy using histological techniques. Lasiodiplodia brasiliensis was also cultured on different carbon sources representing cell walls and non-structural plant components, to complement histology data. The host responded to wounding by developing xylem vessel occlusions with tyloses and deposition of suberin in cambium and ray parenchyma. Infection response also included deposition of suberin in pith tissues, reinforcement of cell walls with phenolic compounds, and lignin deposition in xylem vessels and ray parenchyma. The pathogen could overcome host compartmentalization mechanisms and colonize wood tissue causing extensive necrosis. The fungus was visualized in host cambium, vascular bundles, xylem vessels, and pith, and infected tissues were depleted in starch in the ray parenchyma. Cellulose, hemicellulose, and lignin in cell walls were also degraded, supporting in vitro data.

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References

Adler T., 1977. Lignin chemistry-past, present and future. Wood Science and Technology 11: 69–218.
Adrian M., Trouvelot S., Gamm M., Poinssot B., Héloir M.C., Daire X., 2012. Activation of grapevine defense mechanisms: theoretical and applied approaches. In: Plant Defence: Biological Control (J. Mérillon, K. Ramawat, ed.), Springer, Dordrecht, 313–331. doi:10.1007/978-94-007-1933-0_13
Amponsah N.T., Jones E.E., Ridgway H.J., Jaspers M.V., 2012. Microscopy of some interactions between Botryosphaeriaceae species and grapevine tissues. Australasian Plant Pathology 41: 665–673.
Armijo G., Schlechter R., Agurto M., Muñoz D., Nuñez C., Arce-Johnson P., 2016. Grapevine pathogenic microorganisms: Understanding infection strategies and host response scenarios. Frontiers in plant science 7: 382. doi:10.3389/fpls.2016.00382
Batista E., Lopes A., Alves A., 2021. What do we know about Botryosphaeriaceae? An overview of a worldwide cured dataset. Forests 12: 313. doi:10.3390/f12030313
Bertsch C., Ramírez‐Suero M., Magnin‐Robert M., Larignon P., Chong J., … Fontaine F., 2013. Grapevine trunk diseases: Complex and still poorly understood. Plant Pathology 62: 243–265. doi:10.1111/j.1365-3059.2012.02674
Călugăr A., Cordea M.I., Babeş A., Fejer M., 2019. Dynamics of starch reserves in some grapevine varieties (Vitis vinifera L.) during dormancy. Bulletin UASVM Horticulture 76:185–192. doi:10.15835/buasvmcn-hort: 2019.0008
Claverie M., Notaro M., Fontaine F., Wéry J., 2020. Current knowledge on Grapevine Trunk Diseases with complex etiology: A systemic approach. Phytopathologia Mediterranea 59: 29–53. doi:10.14601/Phyto-11150
De Micco V., Balzano A., Wheeler E.A., Baas P., 2016. Tyloses and gums: A review of structure, function and occurrence of vessel occlusions. IAWA journal 37: 186–205. doi:10.1163/22941932-20160130
Eisenman H.C., Casadevall A., 2012. Synthesis and assembly of fungal melanin. Applied Microbiology and Biotechnology 93: 931–940. doi:10.1007/s00253-011-3777-2
Eisenman H.C., Greer E.M., McGrail C.W., 2020. The role of melanins in melanotic fungi for pathogenesis and environmental survival. Applied Microbiology and Biotechnology 104: 4247–4257. doi:10.1007/s00253-020-10532-z
Félix C., Meneses R., Gonçalves M.F., Tilleman L., Duarte A.S., … Alves A., 2019. A multi-omics analysis of the grapevine pathogen Lasiodiplodia theobromae reveals that temperature affects the expression of virulence-and pathogenicity-related genes. Scientific Reports 9: 1–12. doi:10.1038/s41598-019-49551-w
Ferreira R.B., Monteiro S.A.R.A., Freitas R., Santos C.N., Chen Z., … Teixeira A.R., 2007. The role of plant defence proteins in fungal pathogenesis. Molecular Plant Pathology 8: 677-700. doi: 10.1111/j.1364-3703.2007.00419.x
Fleurat-Lessard P., Bourbouloux A., Thibault F., Ménard E., Béré E., … Roblin, G., 2013. Differential occurrence of suberized sheaths in canes of grapevines suffering from black dead arm, esca or Eutypa dieback. Trees 27: 1087–1100. doi: 10.1007/s00468-013-0859-z
Fontaine F., Pinto C., Vallet J., Clément C., Gomes A.C., Spagnolo A., 2016. The effects of grapevine trunk diseases (GTDs) on vine physiology. European Journal of Plant Pathology 144: 707–721. doi:10.1007/s10658-015-0770-0
Freeman B.C., Beattie G.A., 2008. An overview of plant defenses against pathogens and herbivores. Plant Health Instructor 94: 1–12. doi:10.1094/PHI-I-2008-0226-01
Galarneau E.R., Lawrence D.P., Wallis C.M., Baumgartner K., 2021. A comparison of the metabolomic response of grapevine to infection with ascomycete wood-infecting fungi. Physiological and Molecular Plant Pathology 113: 101596. doi: 10.1016/j.pmpp.2020.101596
Garcia J.F., Lawrence D.P., Morales-Cruz A., Travadon R., Minio A., … Cantu D., 2021. Phylogenomics of plant-associated Botryosphaeriaceae species. Frontiers in Microbiology 12: 587. doi:10.3389/fmicb.2021.652802
Gispert C., Kaplan, J.D., Deyett E., Rolshausen P.E., 2020. Long-term benefits of protecting table grape vineyards against Trunk Diseases in the California desert. Agronomy 10: 1895. doi: 10.3390/agronomy10121895
Gómez P., Báidez A.G., Ortuño A., Del Río J.A., 2016. Grapevine xylem response to fungi involved in trunk diseases. Annals of Applied Biology 169: 116–124. doi:10.1111/aab.1228
Gonçalves M.F., Nunes R.B., Tilleman L., Van de Peer Y., Deforce D., … Alves A., 2019. Dual RNA Sequencing of Vitis vinifera during Lasiodiplodia theobromae infection unveils host–pathogen interactions. International Journal of Molecular Sciences 20: 6083. doi:10.3390/ijms20236083
Gubler W.D., Rolshausen P.E., Trouillase F.P., Úrbez-Torres J.R., Voegel T., 2005. Grapevine Trunk Diseases in California. Practical Winery & Vineyard Jan/Feb: 6-25.
Hrycan J., Hart M., Bowen P., Forge T., Úrbez-Torres J.R., 2020. Grapevine Trunk Disease fungi: Their roles as latent pathogens and stress factors that favour disease development and symptom expression. Phytopathologia Mediterranea 59: 395–424. doi:10.14601/Phyto-11275
Joshi V., Joshi N., Vyas A., Jadhav S.K., 2021. Pathogenesis-related proteins: Role in plant defense. In Biocontrol agents and secondary metabolites (pp. 573-590). Woodhead Publishing.
Kaplan J., Travadon R., Cooper M., Hillis V., Lubell M., Baumgartner K., 2016. Identifying economic hurdles to early adoption of preventative practices: the case of trunk diseases in California winegrape vineyards. Wine Economics and Policy 5: 127-141. doi: 10.1016/j.wep.2016.11.001
Kaur S., Samota M.K., Choudhary M., Choudhary M., Pandey A.K., … Thakur J.,2022. How do plants defend themselves against pathogens-Biochemical mechanisms and genetic interventions. Physiology and Molecular Biology of Plants 28: 485–504. doi:10.1007/s12298-022-01146-y
Kim S.J., Lee C.M., Han B.R., Kim M.Y., Yeo Y.S., … Jun H.K., 2008. Characterization of a gene encoding cellulase from uncultured soil bacteria. FEMS Microbiology Letters 282: 44–51. doi:10.1111/j.1574-6968.2008.01097.x
Labois C., Wilhelm K., Laloue H., Tarnus C., Bertsch C., … Chong J., 2020. Wood metabolomic responses of wild and cultivated grapevine to infection with Neofusicoccum parvum, a trunk disease pathogen. Metabolites 10: 232. doi: 10.3390/metabo10060232
Lambert C., Bisson J., Waffo-Téguo P., Papastamoulis Y., Richard T., … Cluzet S., 2012. Phenolics and their antifungal role in grapevine wood decay: focus on the Botryosphaeriaceae family. Journal of Agricultural and Food Chemistry 60: 11859–11868. doi: 10.1021/jf303290g
Lewis N.G., Yamamoto E., Wooten J.B., Just G., Ohashi H., Towers G.H.N., 1987. Monitoring biosynthesis of wheat cell-wall phenylpropanoids in situ. Science 237: 1344–1346. doi: 10.1126/science.237.4820.1344
Liljegren S., 2010. Phloroglucinol stain for lignin. Cold Spring Harbor Protocols 2010: pdb-prot4954. doi:10.1101/pdb.prot4954
Lillie R.D., 1965. Histopathologic technique and practical histochemistry. 3rd ed. McGraw Hill, New York, USA, 942 pp.
Ling‐Lee M., Chilvers G.A., Ashford A.E., 1977. A histochemical study of phenolic materials in mycorrhizal and uninfected roots of Eucalyptus fastigata Deane and Maiden. New Phytologist 78: 313–328.
Magnin-Robert M., Spagnolo A., Boulanger A., Joyeux C., Clément C., … Fontaine F., 2016. Changes in plant metabolism and accumulation of fungal metabolites in response to esca proper and apoplexy expression in the whole grapevine. Phytopathology 106: 541–553. doi:10.1094/PHYTO-09-15-0207-R
Mehl J., Wingfield M.J., Roux J., Slippers B., 2017. Invasive everywhere? Phylogeographic analysis of the globally distributed tree pathogen Lasiodiplodia theobromae. Forests 8: 1–22. doi:10.3390/f8050145
Meshitsuka C., Nakano J., 1977. Studies on the mechanism of lignin color reaction, XI. Mäule color reaction (7). Journal of the Japan Wood Research Society 23: 232–236.
Mithöfer A., Boland W., 2012. Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology 63: 431–450. doi:10.1146/annurev-arplant-042110-103854
Mitra P.P., Loqué D., 2014. Histochemical staining of Arabidopsis thaliana secondary cell wall elements. Journal of Visualized Experiments: JoVE 87: 51381. doi:10.3791/51381
Mounguengui S., Saha Tchinda J.B., Ndikontar M.K., Dumarçay S., Attéké C., ... Gérardin P., 2016. Total phenolic and lignin contents, phytochemical screening, antioxidant and fungal inhibition properties of the heartwood extractives of ten Congo Basin tree species. Annals of Forest Science 73: 287–296. doi: 10.1007/s13595-015-0514-5
Morales-Cruz A., Amrine K.C., Blanco-Ulate B., Lawrence D.P., Travadon R., ... Cantu D., 2015. Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens. BMC Genomics 16: 1–22. doi: 10.1186/s12864-015-1624-z
Nagel J.H., Wingfield M.J., Slippers B., 2021. Abundant secreted hydrolytic enzymes and secondary metabolite gene clusters in genomes of the Botryosphaeriaceae reflect their role as important plant pathogens. bioRxiv. doi:10.1101/2021.01.22.427741
Nakano J., Meshitsuka G., 1992. The detection of lignin. In: Methods in lignin chemistry (S.Y. Lin, C.W. Dence, ed.), Springer, Berlin, Heidelberg, 23–32.
Nardini A, Lo Gullo M, Salleo S., 2011. Refilling embolized xylem conduits: Is it a matter of phloem unloading? Plant Science 180: 604–611. doi: 10.1016/j.plantsci.2010.12.011
Noronha H., Silva A., Dai Z., Gallusci P., Rombolà A.D., … Gerós H., 2018. A molecular perspective on starch metabolism in woody tissues. Planta 248: 559–568. doi:10.1007/s00425-018-2954-2
Obrador-Sánchez J.A., Hernandez-Martinez R., 2020. Microscope observations of Botryosphaeriaceae spp. in the presence of grapevine wood. Phytopathologia Mediterranea 59: 119–129. doi:10.14601/Phyto-11040
Paolinelli-Alfonso M., Villalobos-Escobedo J.M., Rolshausen P., Herrera-Estrella A., Galindo-Sanchez C., … Hernandez-Martinez R., 2016. Global transcriptional analysis suggests Lasiodiplodia theobromae pathogenicity factors involved in modulation of grapevine defensive response. BMC Genomics 17: 615. doi:10.1186/s12864-016-2952-3
Pearce R.B., 1996. Antimicrobial defences in the wood of living trees. New Phytologist 132: 203–233. doi:10.1111/j.1469-8137.1996.tb01842.x
Pearce R.B., 2000. Decay development and its restriction in trees. Journal of Arboriculture 26: 1–11.
Phillips A.J.L., Alves A., Abdollahzadeh J., Slippers B., Wingfield, M.J., … Crous P.W., 2013. The Botryosphaeriaceae: genera and species known from culture. Studies in Mycology 76: 51–167. doi:10.3114/sim0021
Pouzoulet J., Jacques A., Besson X., Dayde J., Mailhac N., 2013. Histopathological study of response of Vitis vinifera cv. Cabernet Sauvignon to bark and wood injury with and without inoculation by Phaeomoniella chlamydospora. Phytopathologia Mediterranea 52: 313–323.
Pouzoulet J., Scudiero E., Schiavon M., Rolshausen P.E., 2017. Xylem vessel diameter affects the compartmentalization of the vascular pathogen Phaeomoniella chlamydospora in grapevine. Frontiers in Plant Science 8: 1442. doi:10.3389/fpls.2017.01442
Pouzoulet J., Yelle D.J., Theodory B., Nothnagel E.A., Bol S., Rolshausen P.E., 2022. Biochemical and histological insights into the interaction between the canker pathogen Neofusicoccum parvum and Prunus dulcis. Phytopathology 112: 345–354. doi: 10.1094/PHYTO-03-21-0107-R
Rangel-Montoya E.A., Paolinelli M., Rolshausen P., Hernandez-Martinez R., 2020. The role of melanin in the grapevine trunk disease pathogen Lasiodiplodia gilanensis. Phytopathologia Mediterranea 59: 549–563. doi: 10.14601/Phyto-11685
Rangel-Montoya E.A., Paolinelli M., Rolshausen P., Hernandez-Martinez R., 2021. Characterization of Lasiodiplodia species associated with grapevines in Baja California and Sonora, Mexico. Phytopathologia Mediterranea 60: 237-251. doi: 10.36253/phyto-12576
Rolshausen P.E., Greve L.C., Labavitch J.M., Mahoney N.E., Molyneux R.J., Gubler W.D., 2008 Pathogenesis of Eutypa lata in grapevine: identification of virulence factors and biochemical characterization of cordon dieback. Phytopathology 98: 222–229. doi:10. 1094/PHYTO-98-2-0222.
Rolshausen P.E., Úrbez-Torres J.R., Rooney-Latham S., Eskalen A., Smith R. J., Gubler W.D. 2010. Evaluation of pruning wound susceptibility and protection against fungi associated with grapevine trunk diseases. American Journal of Enology and Viticulture 61: 113–119. doi: 10.5344/ajev.2010.61.1.113
Rudelle J., Octave S., Kaid-Harche M., Roblin G., Fleurat-Lessard P., 2005. Structural modifications induced by Eutypa lata in the xylem of trunk and canes of Vitis vinifera. Functional plant biology 32: 537–547. doi: 10.1071/FP05012
Rusjan D., Persic M., Likar M., Biniari K., Mikulic-Petkovsek M., 2017. Phenolic responses to esca-associated fungi in differently decayed grapevine woods from different trunk parts of ‘Cabernet Sauvignon’. Journal of Agricultural and Food Chemistry 65: 6615–6624. doi:10.1021/acs.jafc.7b02188
Ruzin S.E., 1999. Plant microtechnique and microscopy (Vol. 198). New York: Oxford University Press, 322 pp.
Schmaler-Ripcke J., Sugareva V., Gebhardt P., Winkler R., Kniemeyer O., … Brakhage A.A., 2009. Production of pyomelanin, a second type of melanin, via the tyrosine degradation pathway in Aspergillus fumigatus. Applied and Environmental Microbiology 75: 493–503. doi:10.1128/AEM.02077-08
Shigo A.L., Marx H.G., 1977. Compartmentalization of decay in trees (No. 405). Department of Agriculture, Forest Service, 73 pp.
Shigo A.L., Tippett J.T., 1981. Compartmentalization of decayed wood associated with Armillaria mellea in several tree species (Vol. 488). US Department of Agriculture, Forest Service 20 pp.
Shigo A.L., 1984. Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Annual Review of Phytopathology 22: 189–214. doi: 10.1146/annurev.py.22.090184.001201
Skyba O., Douglas C.J., Mansfield S.D., 2013. Syringyl-rich lignin renders poplars more resistant to degradation by wood decay fungi. Applied and environmental microbiology 79 2560–2571. doi: 10.1128/AEM.03182-12
Slippers B., Wingfield M., 2007. Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews 21: 90–106. doi: 10.1016/j.fbr.2007.06.002.
Spagnolo A., Larignon P., Magnin-Robert M., Hovasse A., Cilindre C., … Fontaine F., 2014. Flowering as the most highly sensitive period of grapevine (Vitis vinifera L. cv Mourvèdre) to the Botryosphaeria dieback agents Neofusicoccum parvum and Diplodia seriata infection. International Journal of Molecular Sciences 15: 9644–9669.
Stempien E., Goddard M.L., Wilhelm K., Tarnus C., Bertsch C., Chong, J., 2017. Grapevine Botryosphaeria dieback fungi have specific aggressiveness factor repertory involved in wood decay and stilbene metabolization. PloS One 12: e0188766. doi:10.1371/journal.pone.0188766
Tippett J.T., Shigo A.L., 1981. Barrier zone formation: a mechanism of tree defense against vascular pathogens. IAWA Journal 2: 163–168. doi:10.1163/22941932-90000724
Úrbez-Torres J.R., Gubler W.D., 2009. Pathogenicity of Botryosphaeriaceae Species Isolated from Grapevine Cankers in California. Plant Disease 93: 584–592. doi:10.1094 /PDIS-93-6-0584
Úrbez-Torres J.R., 2011. The status of Botryosphaeriaceae species infecting grapevines. Phytopathologia Mediterranea 50: S5–S45.
Yamashita D., Kimura S., Wada M., Takabe K., 2016. Improved Mäule color reaction provides more detailed information on syringyl lignin distribution in hardwood. Journal of Wood Science 62: 131–137. doi:10.1007/s10086-016-1536-9
Yan J.Y., Zhao W.S., Chen Z., Xing Q.K., Zhang W., … Li X.H., 2018. Comparative genome and transcriptome analyses reveal adaptations to opportunistic infections in woody plant degrading pathogens of Botryosphaeriaceae. DNA Research 25: 87–102. doi:10.1093/dnares/dsx040
Yeung E.C., 2015. A guide to the study of plant structure with emphasis on living specimens. In: Plant Microtechniques and Protocols (E.C.T. Yeung, C. Stasolla, M.J. Sumner, B.Q. Huang, ed.), Springer, Cham, Switzerland, 3–22. doi:10.1007/978-3-319-19944-3_1
Zhang W., Groenewald J.Z., Lombard L., Schumacher R.K., Phillips A.J.L., Crous P.W., 2021. Evaluating species in Botryosphaeriales. Persoonia 46: 63–115. doi:10.3767/persoonia.2021.46.03
Zhao X.H., Liu L.Y., Nan L.J., Wang H., Li H., 2014. Development of tyloses in the xylem vessels of Meili grapevine and their effect on water transportation. Russian Journal of Plant Physiology 61: 194–203. doi: 10.1134/S1021443714020198