Bark cankers accompanied by symptoms of decline and dieback are the result of a destructive disease caused by Phytophthora infections in woody plants. Pathogenicity, gas exchange, chlorophyll a fluorescence, and volatile responses to P. cactorum and P. plurivora inoculations were studied in field-grown 10-year-old hybrid poplar plants. The most stressful effects of P. cactorum on photosynthetic behaviour were found at days 30 and 38 post-inoculation (p.-i.), whereas major disturbances induced by P. plurivora were identified at day 30 p.-i. and also belatedly at day 52 p.-i. The spectrum of volatile organic compounds emitted at day 98 p.-i. was richer than that at day 9 p.-i, and the emissions of both sesquiterpenes α-cubebene and germacrene D were induced solely by the Phytophthora inoculations. Significant positive relationships were found between both the axial and the tangential development of bark cankers and the emissions of α-cubebene and β-caryophyllene, respectively. These results show that both α-cubebene and germacrene D are signal molecules for the suppression of Phytophthora hyphae spread from necrotic sites of the bark to healthy living tissues. Four years following inoculations, for the majority of the inoculated plants, the callus tissue had already closed over the bark cankers.

Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 61300 Brno Czech Republic

Faculty of Forestry Technical University in Zvolen T G Masaryka 24 96001 Zvolen Slovakia

Faculty of Wood Sciences and Technology Technical University in Zvolen T G Masaryka 24 96001 Zvolen Slovakia

Phytophthora Research Centre Faculty of Forestry and Wood Technology Mendel University in Brno 61300 Brno Czech Republic

The Chair of Forest Protection Faculty of Forestry University of Belgrade Kneza Višeslava 1 11030 Belgrade Serbia

Zobrazit více v PubMed

Beakes G.W., Thines M., Honda D. eLS. John Wiley and Sons; Chichester, UK: 2015. Straminipile “fungi”—taxonomy; pp. 1–9.

Erwin D.C., Ribeiro O.K. Phytophthora Diseases Worldwide. American Phytopathological Society Press; St. Paul, MN, USA: 1996. p. 562.

Jung T., Pérez–Sierra A., Durán A., Jung M.H., Balci Y., Scanu B. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia. 2018;40:182–220. doi: 10.3767/persoonia.2018.40.08. PubMed DOI PMC

Brasier C.M. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 2008;57:792–808. doi: 10.1111/j.1365-3059.2008.01886.x. DOI

Scott P., Burgess T., Hardy G. Globalization and Phytophthora. In: Lamour K., editor. Phytophthora: A Global Perspective. CAB International; Wallingford, UK: 2013. pp. 226–232.

Hansen E.M., Parke J.L., Sutton W. Susceptibility of Oregon forest trees and shrubs to Phytophthora ramorum: A comparison of artificial inoculation and natural infection. Plant Dis. 2005;89:63–70. doi: 10.1094/PD-89-0063. PubMed DOI

Brasier C., Webber J. Sudden larch death. Nature. 2010;466:824–825. doi: 10.1038/466824a. PubMed DOI

Burgess T.I., Scott J.K., McDougall K.L., Stukely M.J.C., Crane C., Dunstan W.A., Brigg F., Andjic V., White D., Rudman T., et al. Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Global Change Biol. 2017;23:1661–1674. doi: 10.1111/gcb.13492. PubMed DOI

Jung T., Jung M.H., Webber J.F., Kageyama K., Hieno A., Masuya H., Uematsu S., Pérez-Sierra A., Harris A.R., Forster J., et al. The destructive tree pathogen Phytophthora ramorum originates from the laurosilva forests of East Asia. J. Fungi. 2021;7:226. doi: 10.3390/jof7030226. PubMed DOI PMC

Jung T., Orlikowski L., Henricot B., Abad-Campos P., Aday A.G., Aguín Casal O., Bakonyi J., Cacciola S.O., Cech T., Chavarriaga D., et al. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For. Pathol. 2016;46:134–163. doi: 10.1111/efp.12239. DOI

Simamora A.V., Paap T., Howard K., Stukely M.J.C., Hardy G.E.S.J., Burgess T.I. Phytophthora contamination in a nursery and its potential dispersal into the natural environment. Plant Dis. 2018;102:132–139. doi: 10.1094/PDIS-05-17-0689-RE. PubMed DOI

Nassi o Di Nasso N., Guidi W., Ragaglini G., Tozzini C., Bonari E. Biomass production and energy balance of a 12-year-old short-rotation coppice poplar stand under different cutting cycles. GCB Bioenergy. 2010;2:89–97. doi: 10.1111/j.1757-1707.2010.01043.x. DOI

Zhang Y., Tian Y., Ding S., Lv Y., Samjhana W., Fang S. Growth, carbon storage, and optimal rotation in poplar plantations: A case study on clone and planting spacing effects. Forests. 2020;11:842. doi: 10.3390/f11080842. DOI

Milenković I., Keča N., Karadžić D., Radulović Z., Nowakowska J.A., Oszako T., Sikora K., Corcobado T., Jung T. Isolation and pathogenicity of Phytophthora species from poplar plantations in Serbia. Forests. 2018;9:330. doi: 10.3390/f9060330. DOI

Cerny K., Strnadova V., Gregorova B., Holub V., Tomsovsky M., Mrazkova M., Gabrielova S. Phytophthora cactorum causing bleeding canker of common beech, horse chestnut, and white poplar in the Czech Republic. Plant Pathol. 2009;58:394. doi: 10.1111/j.1365-3059.2008.01970.x. DOI

Pernek M., Županić M., Diminić D., Cech T. Phytophthora species on beech and poplars in Croatia. Šumarski List. 2011;135:130–137. (In Croatian)

Keča N., Milenković I., Keča L. Mycological complex of poplars in Serbia. J. For. Sci. 2015;61:169–174. doi: 10.17221/13/2014-JFS. DOI

Hartmann H., Ziegler W., Trumbore S. Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct. Ecol. 2013;27:413–427. doi: 10.1111/1365-2435.12046. DOI

Zvereva E.L., Kozlov M.V. Sources of variation in plant responses to belowground insect herbivory: A meta-analysis. Oecologia. 2012;169:441–452. doi: 10.1007/s00442-011-2210-y. PubMed DOI

Flower C.E., Lynch D.J., Knight K.S., Gonzalez-Meler M.A. Biotic and abiotic drivers of sap flux in mature green ash trees (Fraxinus pennsylvanica) experiencing varying levels of emerald ash borer (Agrilus planipennis) infestation. Forests. 2018;9:301. doi: 10.3390/f9060301. DOI

Kurjak D., Konôpková A., Kmeť J., Macková M., Frýdl J., Živčák M., Palmroth S., Ditmarová Ľ., Gömöry D. Variation in the performance and thermostability of photosystem II in European beech (Fagus sylvatica L.) provenances is influenced more by acclimation than by adaptation. Eur. J. For. Res. 2019;138:79–92. doi: 10.1007/s10342-018-1155-7. DOI

Kubov M., Fleischer P., Jr., Rozkošný J., Kurjak D., Konôpková A., Galko J., Húdoková H., Lalík M., Rell S., Pittner J., et al. Drought or severe drought? Hemiparasitic yellow mistletoe (Loranthus europaeus) amplifies drought stress in sessile oak trees (Quercus petraea) by altering water status and physiological responses. Water. 2020;12:2985. doi: 10.3390/w12112985. DOI

Iqbal Z., Iqbal M.S., Hashem A., Abd_Allah E.F., Ansari M.I. Plant defense responses to biotic stress and its interplay with fluctuating dark/light conditions. Front. Plant Sci. 2021;12:631810. doi: 10.3389/fpls.2021.631810. PubMed DOI PMC

Lu Y., Yao J. Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense. Int. J. Mol. Sci. 2018;19:3900. doi: 10.3390/ijms19123900. PubMed DOI PMC

McDowell N., Pockman W.T., Allen C.D., Breshears D.D., Cobb N., Kolb T., Plaut J., Sperry J., West A., Williams D.G., et al. Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytol. 2008;178:719–739. doi: 10.1111/j.1469-8137.2008.02436.x. PubMed DOI

Bricchi I., Leitner M., Foti M., Mithöfer A., Boland W., Maffei M.E. Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: Early signaling and volatile emission in lima bean (Phaseolus lunatus L.) Planta. 2010;232:719–729. doi: 10.1007/s00425-010-1203-0. PubMed DOI

McCartney M.M., Roubtsova T.V., Yamaguchi M.S., Kasuga T., Ebeler S.E., Davis C.E., Bostock R.M. Effects of Phytophthora ramorum on volatile organic compound emissions of Rhododendron using gas chromatography–mass spectrometry. Anal. Bioanal. Chem. 2018;410:1475–1487. doi: 10.1007/s00216-017-0789-5. PubMed DOI

Van Doan C., Züst T., Maurer C., Zhang X., Machado R.A.R., Mateo P., Ye M., Schimmel B.C.J., Glauser G., Robert C.A.M. Herbivore-induced plant volatiles mediate defense regulation in maize leaves but not in maize roots. Plant Cell Environ. 2021;44:2672–2686. doi: 10.1111/pce.14052. PubMed DOI PMC

Arimura G.-I., Huber D.P.W., Bohlmann J. Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (–)-germacrene D synthase, PtdTPS1. Plant J. 2004;37:603–616. PubMed

Peñuelas J., Asensio D., Tholl D., Wenke K., Rosenkranz M., Piechulla B., Schnitzler J.P. Biogenic volatile emissions from the soil. Plant Cell Environ. 2014;37:1866–1891. doi: 10.1111/pce.12340. PubMed DOI

Liu H., Brettell L.E. Plant defense by VOC-induced microbial priming. Trends Plant Sci. 2019;24:187–189. doi: 10.1016/j.tplants.2019.01.008. PubMed DOI

Meents A.K., Mithöfer A. Plant–plant communication: Is there a role for volatile damage-associated molecular patterns? Front. Plant Sci. 2020;11:583275. doi: 10.3389/fpls.2020.583275. PubMed DOI PMC

Block A.K., Vaughan M.M., Schmelz E.A., Christensen S.A. Biosynthesis and function of terpenoid defense compounds in maize (Zea mays) Planta. 2019;249:21–30. doi: 10.1007/s00425-018-2999-2. PubMed DOI

Ďurkovič J., Husárová H., Javoříková L., Čaňová I., Šuleková M., Kardošová M., Lukáčik I., Mamoňová M., Lagaňa R. Physiological, vascular and nanomechanical assessment of hybrid poplar leaf traits in micropropagated plants and plants propagated from root cuttings: A contribution to breeding programs. Plant Physiol. Biochem. 2017;118:449–459. doi: 10.1016/j.plaphy.2017.07.012. PubMed DOI

Ďurkovič J., Kačík F., Husárová H., Mamoňová M., Čaňová I. Cell wall compositional and vascular traits of hybrid poplar wood in micropropagated plants and plants propagated from root cuttings. New For. 2020;51:119–135. doi: 10.1007/s11056-019-09723-y. DOI

Campbell D.R., Galen C., Wu C.A. Ecophysiology of first and second generation hybrids in a natural plant hybrid zone. Oecologia. 2005;144:214–225. doi: 10.1007/s00442-005-0064-x. PubMed DOI

Ďurkovič J., Čaňová I., Priwitzer T., Biroščíková M., Kapraľ P., Saniga M. Field assessment of photosynthetic characteristics in micropropagated and grafted wych elm (Ulmus glabra Huds.) trees. Plant Cell Tissue Organ Cult. 2010;101:221–228. doi: 10.1007/s11240-010-9680-1. DOI

Bubeníková T., Bednár M., Gergeľ T., Igaz R. Adsorption effect of added powder graphite on reduction of volatile organic compounds emissions from expanded polystyrene. BioResources. 2019;14:9729–9738.

Evans C.K., Hunger R.M., Siegerist W.C. Comparison of greenhouse and field testing to identify wheat resistant to tan spot. Plant Dis. 1999;83:269–273. doi: 10.1094/PDIS.1999.83.3.269. PubMed DOI

Twizeyimana M., Ojiambo P.S., Ikotun T., Paul C., Hartman G.L., Bandyopadhyay R. Comparison of field, greenhouse, and detached-leaf evaluations of soybean germplasm for resistance to Phakopsora pachyrhizi. Plant Dis. 2007;91:1161–1169. doi: 10.1094/PDIS-91-9-1161. PubMed DOI

Quencez C., Desprez-Loustau M.-L., Bastien C. Reliability of field, greenhouse and cut-shoot screening procedures for evaluating susceptibility of Scots pine to Melampsora pinitorqua. For. Pathol. 2001;31:193–256. doi: 10.1046/j.1439-0329.2001.00240.x. DOI

Karadžić D., Radulović Z., Sikora K., Stanivuković Z., Golubović Ćurguz V., Oszako T., Milenković I. Characterisation and pathogenicity of Cryphonectria parasitica on sweet chestnut and sessile oak trees in Serbia. Plant Protect. Sci. 2019;55:191–201. doi: 10.17221/38/2018-PPS. DOI

Karadžić D., Stanivuković Z., Milanović S., Sikora K., Radulović Z., Račko V., Kardošová M., Ďurkovič J., Milenković I. Development of Neonectria punicea pathogenic symptoms in juvenile Fraxinus excelsior trees. Front. Plant Sci. 2020;11:592260. doi: 10.3389/fpls.2020.592260. PubMed DOI PMC

Fleischmann F., Koehl J., Portz R., Beltrame A.B., Oßwald W. Physiological changes of Fagus sylvatica seedlings infected with Phytophthora citricola and the contribution of its elicitin “citricolin” to pathogenesis. Plant Biol. 2005;7:650–658. doi: 10.1055/s-2005-872891. PubMed DOI

Reeksting B.J., Taylor N.J., van den Berg N. Flooding and Phytophthora cinnamomi: Effects on photosynthesis and chlorophyll fluorescence in shoots of non-grafted Persea americana (Mill.) rootstocks differing in tolerance to Phytophthora root rot. South Afr. J. Bot. 2014;95:40–53. doi: 10.1016/j.sajb.2014.08.004. DOI

Cahill D.M., Weste G.M., Grant B.R. Changes in cytokinin concentrations in xylem extrudate following infection of Eucalyptus marginata Donn ex Sm with Phytophthora cinnamomi Rands. Plant Physiol. 1986;81:1103–1109. doi: 10.1104/pp.81.4.1103. PubMed DOI PMC

Clemenz C., Fleischmann F., Häberle K.-H., Matyssek R., Oßwald W. Photosynthetic and leaf water potential responses of Alnus glutinosa saplings to stem-base inoculation with Phytophthora alni subsp. alni. Tree Physiol. 2008;28:1703–1711. doi: 10.1093/treephys/28.11.1703. PubMed DOI

Oßwald W., Fleischmann F., Rigling D., Coelho A.C., Cravador A., Diez J., Dalio R.J., Jung M.H., Pfanz H., Robin C., et al. Strategies of attack and defence in woody plant–Phytophthora interactions. For. Pathol. 2014;44:169–190. doi: 10.1111/efp.12096. DOI

Dinis L.-T., Peixoto F., Zhang C., Martins L., Costa R., Gomes-Laranjo J. Physiological and biochemical changes in resistant and sensitive chestnut (Castanea) plantlets after inoculation with Phytophthora cinnamomi. Physiol. Mol. Plant Pathol. 2011;75:146–156. doi: 10.1016/j.pmpp.2011.04.003. DOI

Umami M., Parker L.M., Arndt S.K. The impacts of drought stress and Phytophthora cinnamomi infection on short-term water relations in two year-old Eucalyptus obliqua. Forests. 2021;12:109. doi: 10.3390/f12020109. DOI

Fleischmann F., Göttlein A., Rodenkirchen H., Lütz C., Oßwald W. Biomass, nutrient and pigment content of beech (Fagus sylvatica) saplings infected with Phytophthora citricola, P. cambivora, P. pseudosyringae and P. undulata. For. Pathol. 2004;34:79–92. doi: 10.1111/j.1439-0329.2004.00349.x. DOI

Bate N.J., Rothstein S.J. C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J. 1998;16:561–569. doi: 10.1046/j.1365-313x.1998.00324.x. PubMed DOI

Schaub A., Blande J.D., Graus M., Oksanen E., Holopainen J.K., Hansel A. Real-time monitoring of herbivore induced volatile emissions in the field. Physiol. Plant. 2010;138:123–133. doi: 10.1111/j.1399-3054.2009.01322.x. PubMed DOI

Danner H., Boeckler G.A., Irmisch S., Yuan J.S., Chen F., Gershenzon J., Unsicker S.B., Köllner T.G. Four terpene synthases produce major compounds of the gypsy moth feeding-induced volatile blend of Populus trichocarpa. Phytochemistry. 2011;72:897–908. doi: 10.1016/j.phytochem.2011.03.014. PubMed DOI

Das A., Lee S.-H., Hyun T.K., Kim S.-W., Kim J.-Y. Plant volatiles as method of communication. Plant Biotechnol. Rep. 2013;7:9–26. doi: 10.1007/s11816-012-0236-1. DOI

Quintana-Rodriguez E., Morales-Vargas A.T., Molina-Torres J., Ádame-Alvarez R.M., Acosta-Gallegos J.A., Heil M. Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J. Ecol. 2015;103:250–260. doi: 10.1111/1365-2745.12340. DOI

Chen Y., Gu F., Li J., He S., Xu F., Fang Y. Involvement of colonizing Bacillus isolates in glucovanillin hydrolysis during the curing of Vanilla planifolia Andrews. Appl. Environ. Microbiol. 2015;81:4947–4954. doi: 10.1128/AEM.00458-15. PubMed DOI PMC

Park S.Y., Park S.J., Park N.J., Joo W.H., Lee S.-J., Choi Y.-W. α-iso-cubebene exerts neuroprotective effects in amyloid beta stimulated microglia activation. Neurosci. Lett. 2013;555:143–148. doi: 10.1016/j.neulet.2013.09.053. PubMed DOI

Park S.Y., Jung W.J., Kang J.S., Kim C.-M., Park G., Choi Y.-W. Neuroprotective effects of α-iso-cubebene against glutamate-induced damage in the HT22 hippocampal neuronal cell line. Int. J. Mol. Med. 2015;35:525–532. doi: 10.3892/ijmm.2014.2031. PubMed DOI

Lee S.K., Kim S.D., Lee H.Y., Baek S.-H., Ko M.J., Son B.G., Park S., Choi Y.W., Bae Y.-S. α-iso-cubebene, a natural compound isolated from Schisandra chinensis fruit, has therapeutic benefit against polymicrobial sepsis. Biochem. Biophys. Res. Commun. 2012;426:226–231. doi: 10.1016/j.bbrc.2012.08.070. PubMed DOI

Könen P.P., Wüst M. Analysis of sesquiterpene hydrocarbons in grape berry exocarp (Vitis vinifera L.) using in vivo-labeling and comprehensive two-dimensional gas chromatography–mass spectrometry (GC×GC–MS) Beilstein J. Org. Chem. 2019;15:1945–1961. doi: 10.3762/bjoc.15.190. PubMed DOI PMC

Adio A.M. Germacrenes A–E and related compounds: Thermal, photochemical and acid induced transannular cyclizations. Tetrahedron. 2009;65:1533–1552. doi: 10.1016/j.tet.2008.11.050. DOI

Pazouki L., Memari H.R., Kännaste A., Bichele R., Niinemets Ü. Germacrene A synthase in yarrow (Achillea millefolium) is an enzyme with mixed substrate specificity: Gene cloning, functional characterization and expression analysis. Front. Plant Sci. 2015;6:111. doi: 10.3389/fpls.2015.00111. PubMed DOI PMC

Bamoniri A., Mazoochi A. Determination of bioactive and fragrant molecules from leaves and fruits of Ferula assa-foetida L. growing in central Iran by nano scale injection. Digest J. Nanomater. Biostruct. 2009;4:323–328.

Noge K., Shimizu N., Becerra J.X. (R)-(–)-linalyl acetate and (S)-(–)-germacrene D from the leaves of Mexican Bursera linanoe. Nat. Prod. Commun. 2010;5:351–354. doi: 10.1177/1934578X1000500301. PubMed DOI

Schnee C., Köllner T.G., Held M., Turlings T.C.J., Gershenzon J., Degenhardt J. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. USA. 2006;103:1129–1134. doi: 10.1073/pnas.0508027103. PubMed DOI PMC

McCormick A.C., Irmisch S., Reinecke A., Boeckler G.A., Veit D., Reichelt M., Hansson B.S., Gershenzon J., Köllner T.G., Unsicker S.B. Herbivore-induced volatile emission in black poplar: Regulation and role in attracting herbivore enemies. Plant Cell Environ. 2014;37:1909–1923. doi: 10.1111/pce.12287. PubMed DOI

Sabulal B., Dan M., John A.J., Kurup R., Pradeep N.S., Valsamma R.K., George V. Caryophyllene-rich rhizome oil of Zingiber nimmonii from South India: Chemical characterization and antimicrobial activity. Phytochemistry. 2006;67:2469–2473. doi: 10.1016/j.phytochem.2006.08.003. PubMed DOI

Singh G., Marimuthu P., de Heluani C.S., Catalan C.A.N. Antioxidant and biocidal activities of Carum nigrum (seed) essential oil, oleoresin, and their selected components. J. Agric. Food Chem. 2006;54:174–181. doi: 10.1021/jf0518610. PubMed DOI

Rather M.A., Dar B.A., Dar M.Y., Wani B.A., Shah W.A., Bhat B.A., Ganai B.A., Bhat K.A., Anand R., Qurishi M.A. Chemical composition, antioxidant and antibacterial activities of the leaf essential oil of Juglans regia L. and its constituents. Phytomedicine. 2012;19:1185–1190. doi: 10.1016/j.phymed.2012.07.018. PubMed DOI

Defense mechanisms promoting tolerance to aggressive Phytophthora species in hybrid poplar