Abstracts
Abstract
Oak wilt, which develops in the outer sapwood, is the most destructive disease of oaks in the United States. Species of red oaks are more susceptible to this disease than white oak species and are more likely to facilitate the spread of the pathogen Bretziella fagacearum. To prevent its establishment in new areas, phytosanitary certificates are mandatory for commercial trade, as is the inspection of logs to confirm identification. A literature survey and the results of our assays with seven oak species confirm that it is easy to identify wood of the red and white oak groups using anatomical features. Specifically, earlywood vessels are generally open in red oaks, while they appear occluded with tyloses in white oaks. Such plugs are the consequence of air embolism (cavitation) and not the cause of the wilting process. Although these wide vessels are efficient for water transport, they are vulnerable to cavitation that appears to favour the growth of the oak wilt pathogen. Compartmentalization of infected wood succeeds in restraining cavitation and pathogen spread, allowing some trees to recover from oak wilt.
Keywords:
- microscopy,
- defence reactions,
- sap transport,
- embolism,
- cavitation,
- tyloses
Résumé
Le flétrissement du chêne est la maladie qui affecte le plus les chênes aux États-Unis. Les espèces de chênes rouges sont plus sensibles que le groupe des chênes blancs à cette maladie, et ainsi plus susceptibles de répandre l’agent pathogène Bretziella fagacearum. Pour empêcher l’établissement de la maladie dans de nouveaux territoires, l’exigence de certificats phytosanitaires est nécessaire lors d’échanges commerciaux de même que durant l’inspection des billes pour confirmer l’identification du bois. Une revue de la documentation scientifique et nos essais avec sept espèces de chêne montrent qu’il est aisé de différencier le bois du groupe des chênes rouges de celui des blancs avec quelques critères anatomiques. Un de ces critères est l’apparente absence d’occlusion dans les vaisseaux du bois initial chez les chênes rouges alors qu’ils sont obstrués par des thylles chez les chênes blancs. Ces occlusions sont une conséquence de l’embolie par l’air (cavitation), et non la cause du flétrissement. Ces gros vaisseaux sont efficaces pour transporter la sève, mais vulnérables à la cavitation, cette dernière semblant stimuler la croissance de l’agent pathogène. Le compartimentage du bois infecté réussit à freiner la cavitation et la colonisation par l’agent pathogène, permettant à certains arbres de survivre à cette maladie.
Mots-clés :
- microscopie,
- réactions de défense,
- transport de la sève,
- embolie,
- cavitation,
- thylles
Appendices
References
- Appel, D.N. 1995. The oak wilt enigma: perspectives from the Texas epidemic. Annu. Rev. Phytopathol. 33: 103-118.
- Appel, D.N., R. Peters, and R. Lewis, Jr. 1987. Tree susceptibility, inoculum availability, and potential vectors in a Texas oak wilt center. J. Arboric. 13: 169-173. doi:10.48044/jauf.1987. 037
- Baas, P., E. Werker, and A. Fahn. 1983. Some ecological trends in vessel characters. IAWA J. 4: 141-159. doi:10.1163/ 22941932-90000407
- Baayen, R.P., G.B. Ouellette, and D. Rioux. 1996. Compart-mentalization of decay in carnations resistant to Fusarium oxysporum f. sp. dianthi. Phytopathology 86: 1018-1031.
- Barnett, H.L. 1953. Isolation and identification of the oak wilt fungus. Bulletin No. 359T. West Virginia Agricultural and Forestry Experiment Station Bulletins. Available online [https://researchrepository.wvu.edu/wv_agricultural_and_forestry_experiment_station_bulletins/627].
- Beier, G.L., and R.A. Blanchette. 2018. Defence responses in the xylem of Ulmus americana cultivars after inoculation with Ophiostoma novo-ulmi. For. Pathol. 48: e12453.
- Beier, G.L., B.W. Held, C.P. Giblin, J. Cavender-Bares, and R.A. Blanchette. 2017. American elm cultivars: variation in compartmentalization of infection by Ophiostoma novo-ulmi and its effects on hydraulic conductivity. For. Pathol. 47: e12369.
- Biggs, A.R. 1984. Intracellular suberin: occurrence and detection in tree bark. IAWA J. 5: 243-248.
- Biggs, A.R. 1992a. Anatomical and physiological responses of bark tissues to mechanical injury. Pages 13-40 in R.A. Blanchette and A.R. Biggs (eds.), Defense mechanisms of woody plants against fungi. Springer, Berlin, Germany.
- Biggs, A.R. 1992b. Responses of angiosperm bark tissues to fungi causing cankers and canker rots. Pages 41-61 in R.A. Blanchette and A.R. Biggs (eds.), Defense mechanisms of woody plants against fungi. Springer, Berlin, Germany.
- Blaedow, R.A., J. Juzwik, and B. Barber. 2010. Propiconazole distribution and effects on Ceratocystis fagacearum survival in roots of treated red oaks. Phytopathology 100: 979-985.
- Blanchette, R.A. 1992. Anatomical responses of xylem to injury and invasion by fungi. Pages 76-95 in R.A. Blanchette and A.R. Biggs (eds.), Defense mechanisms of woody plants against fungi. Springer, Berlin, Germany. doi:10. 1007/978-3-662-01642-8_5
- Bonsen, K.J.M., and H.P. Bucher. 1991. What arborists have to know about vessel plugs. Arboric. J. 15: 13-17. doi:10. 1080/03071375.1991.9746864
- Bonsen, K.J.M., and L.J. Kučera. 1990. Vessel occlusions in plants: morphological, functional and evolutionary aspects. IAWA J. 11: 393-399.
- Bonsen, K.J.M., R.J. Scheffer, and D.M. Elgersma. 1985. Barrier zone formation as a resistance mechanism of elms to Dutch elm disease. IAWA J. 6: 71-77. doi:10.1163/ 22941932-90000916
- Brandt, W.H. 1963. Dimorphism and interactions between the oak wilt fungus and associated fungi. Plant Dis. Rep. 47: 579-582.
- Breshears, D.D., N.G. McDowell, K.L. Goddard, K.E. Dayem, S.N. Martens, C.W. Meyer, and K.M. Brown. 2008. Foliar absorption of intercepted rainfall improves woody plant water status most during drought. Ecology 89: 41-47.
- Briggs, L.J. 1950. Limiting negative pressure of water. J. Appl. Phys. 21: 721-722.
- Brodersen, C.R., A.J. McElrone, B. Choat, E.F. Lee, K.A. Shackel, and M.A. Matthews. 2013. In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiol. 161: 1820-1829.
- Brown, A.V., and C.M. Brasier. 2007. Colonization of tree xylem by Phytophthora ramorum, P. kernoviae and other Phytophthora species. Plant Pathol. 56: 227-241. doi:10. 1111/j.1365-3059.2006.01511.x
- Brown, H.R. 2013. The theory of the rise of sap in trees: some historical and conceptual remarks. Phys. Perspect. 15: 320-358.
- Burgess, S.S.O., and T.E. Dawson. 2004. The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant Cell Environ. 27: 1023-1034. doi:10.1111/j.1365-3040. 2004.01207.x
- Canadian Food Inspection Agency. 2020. D-99-03: Phyto-sanitary import requirements to prevent the entry of oak wilt disease (Bretziella fagacearum (Bretz) Hunt) from the Continental United States. Government of Canada. Available online [https://www.inspection.gc.ca/plant-healt h/plant-pests-invasive-species/directives/date/d-99-03/eng /1323852753311/1323852907742] (Accessed in October 2020).
- Castagneri, D., M. Carrer, L. Regev, and E. Boaretto. 2020. Precipitation variability differently affects radial growth, xylem traits and ring porosity of three Mediterranean oak species at xeric and mesic sites. Sci. Total Environ. 699: 134285.
- Cavender-Bares, J. 2019. Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution. New Phytol. 221: 669-692.
- Chatonnet, P., and D. Dubourdieu. 1998. Comparative study of the characteristics of American white oak (Quercus alba) and European oak (Quercus petraea and Q. robur) for production of barrels used in barrel aging of wines. Am. J. Enol. Vitic. 49: 79-85.
- Choat, B., M. Nolf, R. Lopez, J.M.R. Peters, M.R. Carins-Murphy, D. Creek, and T.J. Brodribb. 2019. Non-invasive imaging shows no evidence of embolism repair after drought in tree species of two genera. Tree Physiol. 39: 113-121.
- Cones, W.L. 1967. Oak wilt mats on white oak in West Virginia. Plant Dis. Rep. 51: 430-431.
- Cruiziat, P., H. Cochard, and T. Améglio. 2002. Hydraulic architecture of trees: main concepts and results. Ann. For. Sci. 59: 723-752.
- Dashko, S., N. Zhou, C. Compagno, and J. Piškur. 2014. Why, when, and how did yeast evolve alcoholic fermentation? FEMS Yeast Res. 14: 826-832.
- Davis, S.D., J.S. Sperry, and U.G. Hacke. 1999. The relationship between xylem conduit diameter and cavitation caused by freezing. Am. J. Bot. 86: 1367-1372.
- Dawson, T.E. 1998. Fog in the California redwood forest: eco-system inputs and use by plants. Oecologia 117: 476-485.
- de Beer, Z.W., S. Marincowitz, T.A. Duong, and M.J. Wingfield. 2017. Bretziella, a new genus to accommodate the oak wilt fungus, Ceratocystis fagacearum (Microascales, Ascomycota). MycoKeys 27: 1-19.
- De Micco, V., A. Balzano, E.A. Wheeler, and P. Baas. 2016. Tyloses and gums: a review of structure, function and occurrence of vessel occlusions. IAWA J. 37: 186-205.
- DiGasparro, M. 2020. Oak wilt eDNA detected in Ontario. Available online [https://www.invasivespeciescentre.ca/oa k-wilt-edna-detected-in-ontario] (Accessed in August 2022).
- Dimond, A.E. 1970. Biophysics and biochemistry of the vascular wilt syndrome. Annu. Rev. Phytopathol. 8: 301-322.
- Dixon, H.H., and J. Joly. 1895. XII. On the ascent of sap. Phil. Trans. R. Soc. Lond. B 186: 563-576.
- Eames, A.J. 1910. On the origin of the broad ray in Quercus. Bot. Gaz. 49: 161-167. doi:10.1086/33014
- Ellmore, G.S., and F.W. Ewers. 1986. Fluid flow in the outermost xylem increment of a ring-porous tree, Ulmus americana. Am. J. Bot. 73: 1771-1774.
- Et-Touil, A., D. Rioux, F.M. Mathieu, and L. Bernier. 2005. External symptoms and histopathological changes following inoculation of elms putatively resistant to Dutch elm disease with genetically close strains of Ophiostoma. Can. J. Bot. 83: 656-667.
- Farrar, J.L. 1995. Trees in Canada. Canadian Forest Service, and Fitzhenry and Whiteside Limited, Ottawa/Markham, ON, Canada. 502 pp.
- Farrar, J.L. 2017. Trees in Canada. Canadian Forest Service, and Fitzhenry and Whiteside Limited, Ottawa/Markham, ON, Canada. 512 pp.
- French, D.W., and W.C. Stienstra. 1980. Oak wilt. Report No. 310. University of Minnesota, Agricultural Extension Service, MN, USA. 6 pp.
- Gerry, E. 1914. Tyloses: their occurrence and practical signi-ficance in some American woods. J. Agric. Res. 1: 445-470.
- Goldman, D.H. 2017. Plant guide for live oak (Quercus virginiana). USDA-Natural Resources Conservation Service, National Plant Data Team. Greensboro, NC, USA. Available online [http://gulfcoastswcd.org/wp-content/uploads/2 020/01/PG-Live-Oak.pdf].
- Government of Canada. 2019. 440391 - Logs, of oak, not treated - Canadian Importers Database (CID). Available online [https://www.ic.gc.ca/app/scr/ic/sbms/cid/produ ctReportHS10.html?hsCode=4403910010] (Accessed in March 2021).
- Graf, I., M. Ceseri, and J.M. Stockie. 2015. Multiscale model of a freeze–thaw process for tree sap exudation. J. R. Soc. Interface 12: 20150665.
- Haight, R.G., F.R. Homans, T. Horie, S.V. Mehta, D.J. Smith, and R.C. Venette. 2011. Assessing the cost of an invasive forest pathogen: a case study with oak wilt. Environ. Manage. 47: 506-517.
- Hargrave, K.R., K.J. Kolb, F.W. Ewers, and S.D. Davis. 1994. Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytol. 126: 695-705.
- Harlow, W.M., E.S. Harrar, and F.M. White. 1979. Textbook of dendrology: covering the important forest trees of the United States and Canada. McGraw-Hill, New York, NY, USA. 510 pp.
- Henry, B.W., C.S. Moses, C.A. Richards, and A.J. Riker. 1944. Oak wilt, its significance, symptoms and cause. Phytopa-thology 34: 636-647.
- Hoadley, R.B. 1990. Identifying wood: accurate results with simple tools. The Taunton Press, Newtown, CT, USA. 223 pp.
- Jacobi, W.R., and W.L. MacDonald. 1980. Colonization of resistant and susceptible oaks by Ceratocystis fagacearum. Phytopathology 70: 618-623.
- Jansen, S., B. Choat, and A. Pletsers. 2009. Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am. J. Bot. 96: 409-419.
- Jensen, W.A. 1962. Botanical histochemistry: principles and practice. W.H. Freeman, San Francisco, CA, USA. 408 pp.
- Juzwik, J., D.N. Appel, W.L. MacDonald, and S. Burks. 2011. Challenges and successes in managing oak wilt in the United States. Plant Dis. 95: 888-900.
- Juzwik, J., T.C. Harrington, W.L. MacDonald, and D.N. Appel. 2008. The origin of Ceratocystis fagaceaum, the oak wilt fungus. Annu. Rev. Phytopathol. 46: 13-26.
- Juzwik, J., J. O’Brien, C. Evenson, P. Castillo, and G. Mahal. 2010. Controlling spread of the oak wilt pathogen (Ceratocystis fagacearum) in a Minnesota urban forest park reserve. Arboric. Urban For. 36: 171-178.
- Kashyap, A., M. Planas-Marquès, M. Capellades, M. Valls, and N.S. Coll. 2021. Blocking intruders: inducible physico-chemical barriers against plant vascular wilt pathogens. J. Exp. Bot. 72: 184-198.
- Kim, Y.S., and A.P. Singh. 2000. Micromorphological charac-teristics of wood biodegradation in wet environments: a review. IAWA J. 21: 135-155.
- Kitin, P., and R. Funada. 2016. Earlywood vessels in ring-porous trees become functional for water transport after bud burst and before the maturation of the current-year leaves. IAWA J. 37: 315-331.
- Kulkarni, R.K., and K.W. Nickerson. 1981. Nutritional control of dimorphism in Ceratocystis ulmi. Exp. Mycol. 5: 148-154. doi:10.1016/0147-5975(81)90015-3
- Langan, S.J., F.W. Ewers, and S.D. Davis. 1997. Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs. Plant Cell Environ. 20: 425-437.
- Lev-Yadun, S. 1994. Radial fibres in aggregate rays of Quercus calliprinos Webb. – evidence for radial signal flow. New Phytol. 128: 45-48.
- Limm, E.B., K.A. Simonin, A.G. Bothman, and T.E. Dawson. 2009. Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia 161: 449-459.
- Lovisolo, C., and A. Schubert. 1998. Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. J. Exp. Bot. 49: 693-700. doi:10.1093/jxb/49.321.693
- Lowe, A.J., E.E. Dormontt, M.J. Bowie, B. Degen, S. Gardner, D. Thomas, C. Clarke, A. Rimbawanto, A. Wiedenhoeft, Y. Yin, and N. Sasaki. 2016. Opportunities for improved transparency in the timber trade through scientific verification. BioScience 66: 990-998.
- Manos, P.S., J.J. Doyle, and K.C. Nixon. 1999. Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Mol. Phylogenet. Evol. 12: 333-349.
- Martin, C.W., R.C. Maggio, and D.N. Appel. 1989. The contributory value of trees to residential property in the Austin, Texas metropolitan area. J. Arboric. 15: 72-76.
- Martín, J.A., A. Solla, T. Oszako, and L. Gil. 2021. Characterizing offspring of Dutch elm disease-resistant trees (Ulmus minor Mill.). Forestry 94: 374-385.
- Martin-StPaul, N., S. Delzon, and H. Cochard. 2017. Plant resistance to drought depends on timely stomatal closure. Ecol. Lett. 20: 1437-1447.
- McShea, W.J., W.M. Healy, P. Devers, T. Fearer, F.H. Koch, D. Stauffer, and J. Waldon. 2007. Forestry matters: decline of oaks will impact wildlife in hardwood forests. J. Wildl. Manage. 71: 1717-1728.
- Milburn, J.A., and P.E.R. O’Malley. 1984. Freeze-induced sap absorption in Acer pseudoplatanus: a possible mechanism. Can. J. Bot. 62: 2101-2106.
- Miller, R.B., J.T. Quirk, and D.J. Christensen. 1985. Identifying white oak logs with sodium nitrite. For. Prod. J. 35: 33-38.
- Morris, H., and S. Jansen. 2016. Secondary xylem parenchyma – From classical terminology to functional traits. IAWA J. 37: 1-15.
- Morris, H., L. Plavcová, M. Gorai, M.M. Klepsch, M. Kotowska, H. Jochen Schenk, and S. Jansen. 2018. Vessel-associated cells in angiosperm xylem: highly specialized living cells at the symplast-apoplast boundary. Am. J. Bot. 105: 151-160.
- Murmanis, L. 1975. Formation of tyloses in felled Quercus rubra L. Wood Sci. Technol. 9: 3-14.
- Nair, V.M.G., and J.E. Kuntz. 1963. Mat formation in bur oaks infected with Ceratocystis fagacearum. Note No. 95. University of Wisconsin, College of Agricultural and Forest Research, Madison, WI, USA.
- Naruzawa, E.S., and L. Bernier. 2014. Control of yeast-mycelium dimorphism in vitro in Dutch elm disease fungi by mani-pulation of specific external stimuli. Fungal Biol. 118: 872-884.
- Newbanks, D., A. Bosch, and M.H. Zimmermann. 1983. Evidence for xylem dysfunction by embolization in Dutch elm disease. Phytopathology 73: 1060-1063.
- Newcombe, G., and J. Robb. 1989. The chronological deve-lopment of a lipid-to-suberin response at Verticillium trapping sites in alfalfa. Physiol. Mol. Plant Pathol. 34: 55-73. doi:10.1016/0885-5765(89)90016-7
- Nixon, K.C. 1993. Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Ann. Sci. For. 50: 25s-34s (Suppl.).
- O’Brien, J.G., M.E. Mielke, D. Starkey, and J. Juzwik. 2011. How to identify, prevent, and control oak wilt. Publication No. NA-FR-01-11. United States Department of Agriculture, Forest Service, Northeastern Area State and Private Forestry, Newton Square, PA, USA. 38 pp. Available online [https://arborcareandconsulting.com/sites/arbor/files/oak_wilt_usda.pdf].
- Ontario Government. 2016. Red oak – Quercus rubra. Forest Resources of Ontario. Available online [https://www.ont ario.ca/document/forest-resources-ontario-2016/red-oak-quercus-rubra] (Accessed in August 2022).
- Orlowski, M. 1991.Mucor dimorphism. Microbiol. Mol. Biol. Rev. 55: 234-258.
- Osterbauer, N.K., and D.W. French. 1992. Propiconazole as a treatment for oak wilt in Quercus rubra and Q. ellipsoidalis. J. Arboric. 18: 221-226.
- Oswalt, S.N., W.B. Smith, P.D. Miles, and S.A. Pugh. 2019. Forest Resources of the United States, 2017: a technical document supporting the Forest Service 2020 RPA Assessment. General technical report No. WO-97. US Department of Agriculture, Forest Service, Washington, DC, USA. 237 pp.
- Ouellette, G.B. 1962. Morphological characteristics of Ceratocytis ulmi (Buism.) C. Moreau in American elm trees. Can. J. Bot. 40: 1463-1466.
- Ouellette, G.B. 1980. Occurrence of tyloses and their ultra-structural differentiation from similarly configured structures in American elm infected by Ceratocystis ulmi. Can. J. Bot. 58: 1056-1073.
- Ouellette, G.B. 1981a. Ultrastructural cell wall modifications in secondary xylem of American elm surviving the acute stage of Dutch elm disease: fibres. Can. J. Bot. 59: 2425-2438.
- Ouellette, G.B. 1981b. Ultrastructural cell wall modifications in secondary xylem of American elm surviving the acute stage of Dutch elm disease: vessel members. Can. J. Bot. 59: 2411-2424.
- Panshin, A.J., and C. de Zeeuw. 1980. Textbook of wood technology: structure, identification, properties, and uses of the commercial woods of the United States and Canada. McGraw-Hill, New York, NY, USA. 722 pp.
- Peacher, P.H., M.J. Weiss, and J.F. Wolf. 1975. Southward spread of oak wilt remains static. Plant Dis. Rep. 59: 303-304.
- Pearce, R.B. 1996. Antimicrobial defences in the wood of living trees. New Phytol. 132: 203-233.
- Pedlar, J.H., D.W. McKenney, E. Hope, S. Reed, and J. Sweeney. 2020. Assessing the climate suitability and potential economic impacts of Oak wilt in Canada. Sci. Rep. 10: 19391.
- Pegg, G.F. 1985. Life in a black hole – The micro-environment of the vascular pathogen. Trans. Br. Mycol. Soc. 85: 1-20. doi:10.1016/S0007-1536(85)80151-0
- Piao, S., Q. Liu, A. Chen, I.A. Janssens, Y. Fu, J. Dai, L. Liu, X. Lian, M. Shen, and X. Zhu. 2019. Plant phenology and global climate change: current progresses and challenges. Glob. Change Biol. 25: 1922-1940.
- Poiré, T., and E. Appleton. 2018. CFIA plant health surveillance update: eastern Ontario forest health review. Govern-ment of Canada, Canadian Food Inspection Agency. Available online [https://www.eomf.on.ca/media/k2/att achments/CFIA_-RFHN_Review_November_2018.pdf] (Accessed in September 2021).
- Popkin, G. 2021. Forest fight. Science 374: 1184-1189.
- Rabaey, D., S. Huysmans, F. Lens, E. Smets, and S. Jansen. 2008. Micromorphology and systematic distribution of pit membrane thickenings in Oleaceae: tori and pseudo-tori. IAWA J. 29: 409-424.
- Rioux, D., and R.P. Baayen. 1997. A suberized perimedullary reaction zone in Populus balsamifera novel for compart-mentalization in trees. Trees 11: 389-403.
- Rioux, D., M. Blais, N. Nadeau-Thibodeau, M. Lagacé, P. DesRochers, K. Klimaszewska, and L. Bernier. 2018. First extensive microscopic study of butternut defense mecha-nisms following inoculation with the canker pathogen Ophiognomonia clavigignenti-juglandacearum reveals compartmentalization of tissue damage. Phytopathology 108: 1237-1252.
- Rioux, D., H. Chamberland, M. Simard, and G.B. Ouellette. 1995. Suberized tyloses in trees: an ultrastructural and cytochemical study. Planta 196: 125-140.
- Rioux, D., M. Nicole, M. Simard, and G.B. Ouellette. 1998. Immunocytochemical evidence that secretion of pectin occurs during gel (gum) and tylosis formation in trees. Phytopathology 88: 494-505. doi:10.1094/PHYTO.1998.8 8.6.494
- Rioux, D., and G.B. Ouellette. 1989. Light microscope obser-vations of histological changes induced by Ophiostoma ulmi in various nonhost trees and shrubs. Can. J. Bot. 67: 2335-2351.
- Rioux, D., and G.B. Ouellette. 1991a. Barrier zone formation in host and nonhost trees inoculated with Ophiostoma ulmi. I. Anatomy and histochemistry. Can. J. Bot. 69: 2055-2073.
- Rioux, D., and G.B. Ouellette. 1991b. Barrier zone formation in host and nonhost trees inoculated with Ophiostoma ulmi. II. Ultrastructure. Can. J. Bot. 69: 2074-2083.
- Rizzo, D.M., M. Garbelotto, J.M. Davidson, G.W. Slaughter, and S.T. Koike. 2002.Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis. 86: 205-214. doi:10.10 94/PDIS.2002.86.3.205
- Robert, E.M.R., M. Mencuccini, and J. Martínez-Vilalta. 2017. The anatomy and functioning of the xylem in oaks. Pages 261-302 in E. Gil-Pelegrín, J.J. Peguero-Pina, and D. Sancho-Knapik (eds.), Oaks physiological ecology. Exploring the functional diversity of genus Quercus L. Springer Interna-tional Publishing, Cham, Switzerland.
- Sachs, I.B., V.M.G. Nair, and J.E. Kuntz. 1970. Penetration and degradation of cells walls in oaks infected with Ceratocystis fagacearum. Phytopathology 60: 1399-1404.
- Sander, I.L., and H.N. Rosen. 1985. Oak, an American wood. Publication No. FS-247. US Department of Agriculture, Forest Service, Washington, DC, USA. 11 pp. Available online [https://www.fpl.fs.usda.gov/documnts/usda/am wood/247oak.pdf] (Accessed in September 2021).
- Schmitt, U., and W. Liese. 1994. Wound tyloses in Robinia pseudoacacia L. IAWA J. 15: 157-160.
- Schoeneweiss, D.F. 1959. Xylem formation as a factor in oak wilt resistance. Phytopathology 49: 335-337.
- Scholander, P.F., W. Flagg, R.J. Hock, and L. Irving. 1953. Studies on the physiology of frozen plants and animals in the Arctic. J. Cell. Physiol. 42: 1-56 (Suppl.).
- Scholander, P.F., E.D. Bradstreet, E.A. Hemmingsen, and H.T. Hammel. 1965. Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148: 339-346.
- Schultz, H.R., and M.A. Matthews. 1988. Vegetative growth distribution during water deficits in Vitis vinifera L. Aust. J. Plant Physiol. 15: 641-656.
- Shigo, A.L. 1984. Compartmentalization: a conceptual frame-work for understanding how trees grow and defend themselves. Annu. Rev. Phytopathol. 22: 189-214. doi:10. 1146/annurev.py.22.090184.001201
- Shigo, A.L., and H.G. Marx. 1977. Compartmentalization of decay in trees. Bulletin No. 405. US Department of Agriculture, Forest Service, Washington, DC, USA. 73 pp. Available online [https://www.nrs.fs.usda.gov/pubs/mis c/ne_aib405.pdf].
- Shigo, A.L., and J.T. Tippett. 1981. Compartmentalization of American elm tissues infected by Ceratocystis ulmi. Plant Dis. 65: 715-718.
- Sillett, S.C., and R. Van Pelt. 2000. A redwood tree whose crown may be the most complex on Earth. Pages 11-18 in M. Labrecque (ed.), L’Arbre 2000. Isabelle Quentin, Montréal, QC, Canada.
- Sinclair, W.A., and H.H. Lyon. 2005. Oak wilt. Pages 238-239 in W.A. Sinclair, and H.H. Lyon (eds.), Diseases of trees and shrubs. Cornell University Press, Ithaca, NY, USA.
- Skelton, R.P., L.D.L. Anderegg, J. Diaz, M.M. Kling, P. Papper, L.J. Lamarque, S. Delzon, T.E. Dawson, and D.D. Ackerly. 2021. Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks. Proc. Natl. Acad. Sci. 118: e2008987118. doi:10.1073/pnas.200898711
- Smith, D.R., and G.R. Stanosz. 2018. Occurrence of Diplodia corticola, including new oak host records, in Wisconsin, USA. For. Pathol. 48: e12427.
- Solla, A., and L. Gil. 2002. Xylem vessel diameter as a factor in resistance of Ulmus minor to Ophiostoma novo-ulmi. For. Pathol. 32: 123-134.
- Sperry, J.S., J.R. Donnelly, and M.T. Tyree. 1988. Seasonal occurrence of xylem embolism in sugar maple (Acer saccharum). Am. J. Bot. 75: 1212-1218.
- Sperry, J.S., and J.E.M. Sullivan. 1992. Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiol. 100: 605-613.
- Sperry, J.S. and M.T. Tyree. 1990. Water-stress-induced xylem embolism in three species of conifers. Plant Cell Environ. 13: 427-436.
- Stein, J.D., D. Binion, and R.E. Acciavatti. 2003. Field guide to native oak species of eastern North America. US Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV, USA. 161 pp.
- Steudle, E. 1995. Trees under tension. Nature 378: 663-664.
- Struckmeyer, B.E., J.E. Kuntz, and A.J. Riker. 1958. Histology of certain oaks infected with the oak fungus. Phytopa-thology 48: 556-561.
- Tainter, F.H., and F.A. Baker. 1996. Oak wilt. Pages 673-682 in F.H. Tainter, and F.A. Baker (eds.), Principles of forest pathology. John Wiley & Sons, New York, NY, USA. 832 pp.
- Tainter, F.H., and S.W. Fraedrich. 1986. Compartmentali-zation of Ceratocystis fagacearum in Turkey oak in South Carolina. Phytopathology 76: 698-701.
- Tainter, F.H., and D.L. Ham. 1983. The survival of Ceratocystis fagacearum in South Carolina. Eur. J. For. Pathol. 13: 102-109.
- Takahashi, S., N. Okada, and T. Nobuchi. 2015. Relationship between vessel porosity and leaf emergence pattern in ring- and diffuse-porous deciduous trees in a temperate hardwood forest. Botany 93: 31-39. doi:10.1139/cjb-201 4-0129
- Tchernoff, V. 1965. Methods for screening and for the rapid selection of elms for resistance to Dutch elm disease. Acta Bot. Neerl. 14: 409-452.
- The Wood Database. n.d.-a. Chestnut Oak sealed. Available online [https://www.wood-database.com/wp-content/uploads/chestnut-oak-sealed.jpg] (Accessed in August 2022).
- The Wood Database. n.d.-b. Distinguishing red and white oak. Available online [https://www.wood-database.com /wood-articles/distinguishing-red-oak-from-white-oak/] (Accessed in August 2022).
- Tippett, J.T., and A.L. Shigo. 1981a. Barrier zone formation: a mechanism of tree defense against vascular pathogens. IAWA J. 2: 163-168.
- Tippett, J.T., and A.L. Shigo. 1981b. Barriers to decay in conifer roots. Eur. J. For. Pathol. 11: 51-59.
- Trouy, M.-C. 2015. Anatomie du bois : formation, fonctions et identification. Éditions Quae, Versailles, France. 151 pp.
- Tyree, M.T., and M.H. Zimmermann. 2002. Xylem structure and the ascent of sap. Springer, Berlin, Germany. 283 pp.
- US Forest Service-Forest Products Laboratory. 1921. Identification of oak woods. Technical note No. 125. Madison, WI, USA. 2 pp. Available online [https://www.fpl.fs.usda.gov/documnts/fpltn/fpltn-125.pdf].
- Utsumi, Y., Y. Sano, J. Ohtani, and S. Fujikawa. 1996. Seasonal changes in the distribution of water in the outer growth rings in Fraxinus mandshurica var. japonica: a study by cryo-scanning electron microscopy. IAWA J. 17: 113-124.
- Van Alfen, N.K., B.D. McMillan, V. Turner, and W.M. Hess. 1983. Role of pit membranes in macromolecule-induced wilt of plants. Plant Physiol. 73: 1020-1023.
- Wheeler, E.A., P. Baas, and S. Rodgers. 2007. Variations in dicot wood anatomy: a global analysis based on the InsideWood database. IAWA J. 28: 229-258.
- Wheeler, E.A., C.A. LaPasha, and R.B. Miller. 1989. Wood anatomy of elm (Ulmus) and hackberry (Celtis) species native to the United States. IAWA J. 10: 5-26.
- Wheeler, J.K., J.S. Sperry, U.G. Hacke, and N. Hoang. 2005. Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ. 28: 800-812.
- Wikimedia Foundation. n.d. Hyperion (tree). Wikipedia. Available online [https://en.wikipedia.org/wiki/Hyperion _(tree)] (Accessed in August 2022).
- Williams, S. 1939. Secondary vascular tissues of the oaks indigenous to the United States - I. The importance of secondary xylem in delimiting Erythrobalanus and Leucobalanus. Bull. Torrey Bot. Club 66: 353-365.
- Woodcock, D.W. 1989. Distribution of vessel diameter in ring-porous trees. Aliso 12: 287-293. doi:10.5642/aliso.19891 202.05
- Zimmermann, M.H. 1979. The discovery of tylose formation by a Viennese lady in 1845. IAWA Bull. 2-3: 51-56.
- Zimmermann, M.H., and A.A. Jeje. 1981. Vessel-length distri-bution in stems of some American woody plants. Can. J. Bot. 59: 1882-1892.
- Zimmermann, M.H., and J. McDonough. 1978. Dysfunction in the flow of food. Pages 117-140 in J.G. Horsfall and E.B. Cowling (eds.), Plant disease: an advanced treatise. Vol III: How plants suffer from disease. Academic Press, New York, NY, USA.
- Zucchino, D. 2014. 1800s-era sunken logs are now treasure; here are the men who find them. Los Angeles Times. Available online [https://www.latimes.com/nation/la-na-si nker-wood-20140713-story.html] (Accessed in July 2021).
- Zwieniecki, M.A., and Holbrook, N.M. 1998. Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L,) and red spruce (Picea rubens Sarg.). Plant Cell Environ. 21: 1173-1180.