Metabolomic and Physiological Changes in Fagus sylvatica Seedlings Infected with Phytophthora plurivora and the A1 and A2 Mating Types of P. ×cambivora
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
LDF_TP_2019013
Internal Grant Agency (IGA) of Mendel University in Brno (IGA number LDF_TP_2019013, name of the project: Histopathological and physiological characteristics of tree species infected with the pathogen of the genus Phytophthora)
CZ.02.1.01/0.0/0.0/15_003/0000453
Phytophthora Research Centre Reg. No. CZ.02.1.01/0.0/0.0/15_003/0000453, co-financed by the European Regional Development Fund
(1/0450/19)
Slovak scientific grant agency VEGA (1/0450/19)
PubMed
35330301
PubMed Central
PMC8949215
DOI
10.3390/jof8030298
PII: jof8030298
Knihovny.cz E-zdroje
- Klíčová slova
- GABA, chlorophyll fluorescence, gas exchange, mortality, photosynthesis, proline, root pathogens, spectral reflectance, sugars,
- Publikační typ
- časopisecké články MeSH
Phytophthora infections are followed by histological alterations, physiological and metabolomic adjustments in the host but very few studies contemplate these changes simultaneously. Fagus sylvatica seedlings were inoculated with A1 and A2 mating types of the heterothallic P. ×cambivora and with the homothallic P. plurivora to identify plant physiological and metabolomic changes accompanying microscope observations of the colonization process one, two and three weeks after inoculation. Phytophthora plurivora-infected plants died at a faster pace than those inoculated with P. ×cambivora and showed higher mortality than P. ×cambivora A1-infected plants. Phytophthora ×cambivora A1 and A2 caused similar progression and total rate of mortality. Most differences in the physiological parameters between inoculated and non-inoculated plants were detected two weeks after inoculation. Alterations in primary and secondary metabolites in roots and leaves were demonstrated for all the inoculated plants two and three weeks after inoculation. The results indicate that P. plurivora is more aggressive to Fagus sylvatica seedlings than both mating types of P. ×cambivora while P. ×cambivora A1 showed a slower infection mode than P. ×cambivora A2 and led to minor plant metabolomic adjustments.
Department of Agricultural Sciences University of Sassari Viale Italia 39 07100 Sassari Italy
Department of Phytology Technical University in Zvolen 96001 Zvolen Slovakia
Department of Wood Science Technical University in Zvolen 96001 Zvolen Slovakia
Faculty of Forestry University of Belgrade Kneza Višeslava 1 11030 Belgrade Serbia
Institute of Botany Technische Universität Dresden 01062 Dresden Germany
Phytophthora Research and Consultancy Am Rain 9 83131 Nußdorf Germany
Zobrazit více v PubMed
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
Jung T., Blaschke H., Neumann P. Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. Eur. J. For. Pathol. 1996;26:253–272. doi: 10.1111/j.1439-0329.1996.tb00846.x. DOI
Jung T. Phytophthora quercina sp. nov., causing root rot of European oaks. Mycol. Res. 1999;103:785–798. doi: 10.1017/S0953756298007734. DOI
Jung T., Blaschke H., Oßwald W. Involvement of soilborne Phytophthora Species in Central European oak decline and the effect of site factors on the disease. Plant Pathol. 2000;49:706–718. doi: 10.1046/j.1365-3059.2000.00521.x. DOI
Vettraino A.M., Barzanti G.P., Bianco M.C., Ragazzi A., Capretti P., Paoletti E., Luisi N., Anselmi N., Vannini A. Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. For. Pathol. 2002;32:19–28. doi: 10.1046/j.1439-0329.2002.00264.x. DOI
Jung T. Beech decline in Central Europe driven by the interaction between Phytophthora infections and climatic extremes. For. Pathol. 2009;39:73–94. doi: 10.1111/j.1439-0329.2008.00566.x. DOI
Weiland J.E., Nelson A.H., Hudler G.W. Aggressiveness of Phytophthora cactorum, P. citricola I, and P. plurivora from European beech. Plant Dis. 2010;94:1009–1014. doi: 10.1094/PDIS-94-8-1009. PubMed DOI
Jung T., Vettraino A.M., Cech T.L., Vannini A. The Impact of invasive Phytophthora species on European forests. In: Lamour K., editor. Phytophthora: A Global Perspective. CABI; Wallingford, UK: 2013. pp. 146–158.
Corcobado T., Cech T.L., Brandstetter M., Daxer A., Hüttler C., Kudláček T., Jung M.H., Jung T. Decline of European Beech in Austria: Involvement of Phytophthora spp. and contributing biotic and abiotic factors. Forests. 2020;11:895. doi: 10.3390/f11080895. DOI
Gibbs J., Lipscombe M., Peace A. The impact of Phytophthora disease on riparian populations of Common alder (Alnus glutinosa) in Southern Britain. Eur. J. For. Pathol. 1999;29:39–50. doi: 10.1046/j.1439-0329.1999.00129.x. DOI
Streito J.C., Legrand P., Tabary F., Jarnouen De Villartay G. Phytophthora disease of alder (Alnus glutinosa) in France: Investigations between 1995 and 1999. For. Pathol. 2002;32:179–191. doi: 10.1046/j.1439-0329.2002.00282.x. DOI
Brasier C.M., Kirk S.A., Delcan J., Cooke D.E.L., Jung T., Man In’t Veld W.A. Phytophthora alni sp. nov. and its variants: Designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol. Res. 2004;108:1172–1184. doi: 10.1017/S0953756204001005. PubMed DOI
Jung T., Blaschke M. Phytophthora root and collar rot of alders in Bavaria: Distribution, modes of spread and possible management strategies. Plant Pathol. 2004;53:197–208. doi: 10.1111/j.0032-0862.2004.00957.x. DOI
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
Jung T., Nechwatal J., Cooke D.E.L., Hartmann G., Blaschke M., Oßwald W.F., Duncan J.M., Delatour C. Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. Mycol. Res. 2003;107:772–789. doi: 10.1017/S0953756203008074. PubMed DOI
Jung T., Hudler G.W., Jensen-Tracy S.L., Griffiths H.M., Fleischmann F., Osswald W. Involvement of Phytophthora species in the decline of European beech in Europe and the USA. Mycologist. 2005;19:159–166. doi: 10.1017/S0269915X05004052. DOI
Jung T., Jung M.H., Scanu B., Seress D., Kovács G.M., Maia C., Pérez-Sierra A., Chang T.T., Chandelier A., Heungens K., et al. Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia. 2017;38:100–135. doi: 10.3767/003158517X693615. PubMed DOI PMC
Jung T., La Spada F., Pane A., Aloi F., Evoli M., Jung M.H., Scanu B., Faedda R., Rizza C., Puglisi I., et al. Diversity and distribution of Phytophthora Species in protected natural areas in Sicily. Forests. 2019;10:259. doi: 10.3390/f10030259. DOI
Schmitz S., Zini J., Chandelier A. Involvement of Phytophthora species in the decline of beech (Fagus sylvatica) in the southern part of Belgium. In: Goheen E., Frankel S., editors. Phytophthoras in Forests and Natural Ecosystems: Fourth Meeting of the International Union of Forest Research Organizations (IUFRO) Working Party S07.02.09. USDA Forest Service, Pacific Southwest Research Station; Albany, CA, USA: 2009. p. 320.
Nechwatal J., Hahn J., Schönborn A., Schmitz G. A twig blight of understorey European beech (Fagus sylvatica) caused by soilborne Phytophthora spp. For. Pathol. 2011;41:493–500. doi: 10.1111/j.1439-0329.2011.00711.x. DOI
Telfer K.H., Brurberg M.B., Herrero M.L., Stensvand A., Talgø V. Phytophthora cambivora found on beech in Norway. For. Pathol. 2015;45:415–425. doi: 10.1111/efp.12215. DOI
Vettraino A.M., Morel O., Perlerou C., Robin C., Diamandis S., Vannini A. Occurrence and distribution of Phytophthora Species in European chestnut stands, and their association with Ink disease and crown decline. Eur. J. Plant Pathol. 2005;111:169–180. doi: 10.1007/s10658-004-1882-0. DOI
Saavedra A., Hansen E.M., Goheen D.J. Phytophthora cambivora in Oregon and its pathogenicity to Chrysolepis Chrysophylla. For. Pathol. 2007;37:409–419. doi: 10.1111/j.1439-0329.2007.00515.x. DOI
Reeser P., Sutton W., Hansen E. Phytophthora species associated with stem cankers on tanoak in Southwestern Oregon. In: Frankel S.J., Kliejunas J.T., Palmieri K.M., editors. Proceedings of the Sudden Oak Death Third Science Symposium. US Department of Agriculture, Forest Service, Pacific Southwest Research Station; Albany, CA, USA: 2008. pp. 227–229.
Greslebin A.G., Hansen E.M., Winton L.M., Rajchenberg M. Phytophthora species from declining Austrocedrus chilensis forests in Patagonia, Argentina. Mycologia. 2005;97:218–228. doi: 10.1080/15572536.2006.11832855. PubMed DOI
Jung T., Durán A., Sanfuentes von Stowasser E., Schena L., Mosca S., Fajardo S., González M., Navarro Ortega A.D., Bakonyi J., Seress D., et al. Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. For. Pathol. 2018;48:e12443. doi: 10.1111/efp.12443. DOI
Suzui T., Hoshino Y. Collar rot of apple caused by Phytophthora cambivora (Petri) Buism. Jpn. J. Phytopathol. 1979;45:344–352. doi: 10.3186/jjphytopath.45.344. DOI
Jung T., Jung M.H., Cacciola S.O., Cech T., Bakonyi J., Seress D., Mosca S., Schena L., Seddaiu S., Pane A., et al. Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus. 2017;8:219–244. doi: 10.5598/imafungus.2017.08.02.02. PubMed DOI PMC
Jung T., Burgess T.I. Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia. 2009;22:95–110. doi: 10.3767/003158509X442612. PubMed DOI PMC
Fleischmann F., Schneider D., Matyssek R., Oßwald W.F. Investigations on net CO2 assimilation, transpiration and root growth of Fagus sylvatica infested with four different Phytophthora species. Plant Biol. 2002;4:144–152. doi: 10.1055/s-2002-25728. 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
Jung T., Chang T.T., Bakonyi J., Seress D., Pérez-Sierra A., Yang X., Hong C., Scanu B., Fu C.H., Hsueh K.L., et al. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathol. 2017;66:194–211. doi: 10.1111/ppa.12564. DOI
Jung T., Scanu B., Brasier C.M., Webber J., Milenković I., Corcobado T., Tomšovský M., Pánek M., Bakonyi J., Maia C., et al. A survey in natural forest ecosystems of Vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests. 2020;11:93. doi: 10.3390/f11010093. DOI
Vélez M.L., Silva P.V., Troncoso O.A., Greslebin A.G. Alteration of physiological parameters of Austrocedrus chilensis by the pathogen Phytophthora austrocedrae. Plant Pathol. 2012;61:877–888. doi: 10.1111/j.1365-3059.2011.02585.x. DOI
Angay O., Fleischmann F., Recht S., Herrmann S., Matyssek R., Oßwald W., Buscot F., Grams T.E.E. Sweets for the foe—effects of nonstructural carbohydrates on the susceptibility of Quercus robur against Phytophthora quercina. New Phytol. 2014;203:1282–1290. doi: 10.1111/nph.12876. 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. S. Afr. J. Bot. 2014;95:40–53. doi: 10.1016/j.sajb.2014.08.004. DOI
Gold K.M., Townsend P.A., Larson E.R., Herrmann I., Gevens A.J. Contact reflectance spectroscopy for rapid, accurate, and nondestructive Phytophthora infestans clonal lineage discrimination. Phytopathology. 2020;110:851–862. doi: 10.1094/PHYTO-08-19-0294-R. PubMed DOI
Newby Z., Murphy R.J., Guest D.I., Ramp D., Liew E.C.Y. Detecting symptoms of Phytophthora cinnamomi infection in Australian native vegetation using reflectance spectrometry: Complex effects of water stress and species susceptibility. Australas. Plant Pathol. 2019;48:409–424. doi: 10.1007/s13313-019-00642-2. DOI
Manter D.K., Kelsey R.G., Karchesy J.J. Photosynthetic declines in Phytophthora ramorum-infected plants develop prior to water stress and in response to exogenous application of elicitins. Phytopathology. 2007;97:850–856. doi: 10.1094/PHYTO-97-7-0850. PubMed DOI
Abu-Nada Y., Kushalappa A.C., Marshall W.D., Al-Mughrabi K., Murphy A. Temporal dynamics of pathogenesis-related metabolites and their plausible pathways of induction in potato leaves following inoculation with Phytophthora infestans. Eur. J. Plant Pathol. 2007;118:375–391. doi: 10.1007/s10658-007-9150-8. DOI
Zhu L., Zhou Y., Li X., Zhao J., Guo N., Xing H. Metabolomics analysis of soybean hypocotyls in response to Phytophthora sojae infection. Front. Plant Sci. 2018;9:1530. doi: 10.3389/fpls.2018.01530. PubMed DOI PMC
Rouse J.W., Hass R.H., Schell J.A., Deering D.W. Monitoring vegetation systems in the Great Plains with ERTS. Third ERTS Symp. 1974;1:309–317.
Peñuelas J., Filella I., Gamon J.A. Assessment of photosynthetic radiation-use efficiency with spectral reflectance. New Phytol. 1995;131:291–296. doi: 10.1111/j.1469-8137.1995.tb03064.x. DOI
Gitelson A.A., Zur Y., Chivkunova O.B., Merzlyak M.N. Assessing carotenoid content in plant leaves with reflectance spectroscopy. Photochem. Photobiol. 2002;75:272–281. doi: 10.1562/0031-8655(2002)075<0272:ACCIPL>2.0.CO;2. PubMed DOI
Berka M., Luklová M., Dufková H., Berková V., Novák J., Saiz-Fernández I., Rashotte A.M., Brzobohatý B., Černý M. Barley root proteome and metabolome in response to cytokinin and abiotic stimuli. Front. Plant Sci. 2020;11:1647. doi: 10.3389/fpls.2020.590337. PubMed DOI PMC
Therneau T. A Package for Survival Analysis in S. [(accessed on 16 February 2022)];2015 Volume 2 R Package Version. Available online: https://sites.google.com/site/statsr4us/docs/SurvivalanalysisinR_package.pdf.
Kassambara A., Kosinski M. Survminer: Drawing Survival Curves Using ‘Ggplot2’. 2017. [(accessed on 16 February 2022)]. R Package Version 0.3. Available online: https://rpkgs.datanovia.com/survminer/
R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2019.
Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008;50:346–363. doi: 10.1002/bimj.200810425. PubMed DOI
Zeileis A. Econometric computing with HC and HAC covariance matrix estimators. J. Stat. Softw. 2004;11:1–17. doi: 10.18637/jss.v011.i10. DOI
Zeileis A. Object-oriented computation of sandwich estimators. J. Stat. Softw. 2006;16:1–16. doi: 10.18637/jss.v016.i09. DOI
Herberich E., Sikorski J., Hothorn T. A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS ONE. 2010;5:e9788. doi: 10.1371/journal.pone.0009788. PubMed DOI PMC
Gu Z., Eils R., Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 2016;32:2847–2849. doi: 10.1093/bioinformatics/btw313. PubMed DOI
Wickham H. Ggplot2: Elegant Graphics for Data Analysis. Springer; Berlin/Heidelberg, Germany: 2016.
Inkscape Project Inkscape. 2020. [(accessed on 16 February 2022)]. Available online: https://inkscape.org/news/2020/
Zarco-Tejada P.J., González-Dugo M.V., Fereres E. Seasonal stability of chlorophyll fluorescence quantified from airborne hyperspectral imagery as an indicator of net photosynthesis in the context of precision agriculture. Remote Sens. Environ. 2016;179:89–103. doi: 10.1016/j.rse.2016.03.024. DOI
Sanogo S., El-Sebai O.I., Sanderson R. Severity of Verticillium wilt, plant growth, and spectral reflectance indices of Chile pepper under periodic flooding and no-flooding conditions. HortScience. 2008;43:414–419. doi: 10.21273/HORTSCI.43.2.414. DOI
Sankaran S., Ehsani R., Inch S.A., Ploetz R.C. Evaluation of visible-near infrared reflectance spectra of avocado leaves as a non-destructive sensing tool for detection of laurel wilt. Plant Dis. 2012;96:1683–1689. doi: 10.1094/PDIS-01-12-0030-RE. PubMed DOI
Jansen M., Bergsträsser S., Schmittgen S., Müller-Linow M., Rascher U. Non-invasive spectral phenotyping methods can improve and accelerate Cercospora disease scoring in sugar beet breeding. Agriculture. 2014;4:147–158. doi: 10.3390/agriculture4020147. DOI
Dalio R.J.D., Fleischmann F., Chambery A., Eichmann R., Massola N.S., Pascholati S.F., Osswald W. Immunodepletion of α-Plurivorin effector leads to loss of virulence of Phytophthora plurivora towards Fagus sylvatica. For. Pathol. 2017;47:e12362. doi: 10.1111/efp.12362. DOI
Sghaier-Hammami B., Valero-Galvàn J., Romero-Rodríguez M.C., Navarro-Cerrillo R.M., Abdelly C., Jorrín-Novo J. Physiological and proteomics analyses of Holm Oak (Quercus ilex subsp. ballota [Desf.] Samp.) responses to Phytophthora cinnamomi. Plant Physiol. Biochem. 2013;71:191–202. doi: 10.1016/j.plaphy.2013.06.030. PubMed DOI
Saiz-Fernández I., Milenković I., Berka M., Černý M., Tomšovský M., Brzobohatý B., Kerchev P. Integrated proteomic and metabolomic profiling of Phytophthora cinnamomi attack on Sweet chestnut (Castanea sativa) reveals distinct molecular reprogramming proximal to the infection site and away from it. Int. J. Mol. Sci. 2020;21:8525. doi: 10.3390/ijms21228525. PubMed DOI PMC
Saiz-Fernández I., De Diego N., Brzobohatý B., Muñoz-Rueda A., Lacuesta M. The imbalance between C and N metabolism during high nitrate supply inhibits photosynthesis and overall growth in maize (Zea mays L.) Plant Physiol. Biochem. 2017;120:213–222. doi: 10.1016/j.plaphy.2017.10.006. PubMed DOI
Clemenz C., Fleischmann F., Häberle K.H., Matyssek R., Oßwald W. Photosynthetic and leaf water potential responses of Alnus glutinosa saplings to stem-base inoculaton with Phytophthora alni subsp. alni. Tree Physiol. 2008;28:1703–1711. doi: 10.1093/treephys/28.11.1703. PubMed DOI
Tauzin A.S., Giardina T. Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front. Plant Sci. 2014;5:293. doi: 10.3389/fpls.2014.00293. PubMed DOI PMC
Sperdouli I., Moustakas M. Differential response of photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress. Acta Physiol. Plant. 2012;34:1267–1276. doi: 10.1007/s11738-011-0920-8. DOI
Maurel M., Robin C., Simonneau T., Loustau D., Dreyer E., Desprez-Loustau M.L. Stomatal conductance and root-to-shoot signalling in chestnut saplings exposed to Phytophthora cinnamomi or partial soil drying. Funct. Plant Biol. 2004;31:41–51. doi: 10.1071/FP03133. PubMed DOI
Oßwald W., Fleischmann F., Rigling D., Coelho A.C., Cravador A., Diez J., Dalio R.J., Horta Jung M., 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
Ruiz Gómez F.J., Navarro-Cerrillo R.M., Sánchez-Cuesta R., Pérez-de-Luque A. Histopathology of infection and colonization of Quercus ilex fine roots by Phytophthora cinnamomi. Plant Pathol. 2015;64:605–616. doi: 10.1111/ppa.12310. PubMed DOI PMC
Ruiz-Gómez F.J., Pérez-de-Luque A., Navarro-Cerrillo R.M. The involvement of Phytophthora root rot and drought stress in holm oak decline: From ecophysiology to microbiome influence. Curr. For. Rep. 2019;5:251–266. doi: 10.1007/s40725-019-00105-3. DOI
Vandana V.V., Suseela Bhai R., Ramakrishnan Nair R., Azeez S. Role of cell wall and cell membrane integrity in imparting defense response against Phytophthora capsici in black pepper (Piper nigrum L.) Eur. J. Plant Pathol. 2019;154:359–375. doi: 10.1007/s10658-018-01661-3. DOI
Parker D., Beckmann M., Zubair H., Enot D.P., Caracuel-Rios Z., Overy D.P., Snowdon S., Talbot N.J., Draper J. Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J. 2009;59:723–737. doi: 10.1111/j.1365-313X.2009.03912.x. PubMed DOI
Draper J., Rasmussen S., Zubair H. Metabolite analysis and metabolomics in the study of biotrophic interactions between plants and microbes. Annu. Plant Rev. 2018;43:25–59. doi: 10.1002/9781119312994.apr0462. DOI
Ahanger M.A., Bhat J.A., Siddiqui M.H., Rinklebe J., Ahmad P. Integration of silicon and secondary metabolites in plants: A significant association in stress tolerance. J. Exp. Bot. 2020;71:6758–6774. doi: 10.1093/jxb/eraa291. PubMed DOI
Tenenboim H., Brotman Y. Omic relief for the biotically stressed: Metabolomics of plant biotic interactions. Trends Plant Sci. 2016;21:781–791. doi: 10.1016/j.tplants.2016.04.009. PubMed DOI
Judelson H.S., Tani S., Narayan R.D. Metabolic adaptation of Phytophthora infestans during growth on leaves, tubers and artificial media. Mol. Plant Pathol. 2009;10:843–855. doi: 10.1111/j.1364-3703.2009.00570.x. PubMed DOI PMC
Rodenburg S.Y., Seidl M.F., Judelson H.S., Vu A.L., Govers F., de Ridder D. Metabolic model of the Phytophthora infestans-tomato interaction reveals metabolic switches during host colonization. MBio. 2019;10:e00454-19. doi: 10.1128/mBio.00454-19. PubMed DOI PMC
Dumschott K., Richter A., Loescher W., Merchant A. Post photosynthetic carbon partitioning to sugar alcohols and consequences for plant growth. Phytochemistry. 2017;144:243–252. doi: 10.1016/j.phytochem.2017.09.019. PubMed DOI
Lee D.K., Ahn S., Cho H.Y., Yun H.Y., Park J.H., Lim J., Lee J., Kwon S.W. Metabolic response induced by parasitic plant-fungus interactions hinder amino sugar and nucleotide sugar metabolism in the host. Sci. Rep. 2016;6:37434. doi: 10.1038/srep37434. PubMed DOI PMC
Williamson J.D., Jennings D.B., Guo W.W., Pharr D.M., Ehrenshaft M. Sugar alcohols, salt stress, and fungal resistance: Polyols—multifunctional plant protection? J. Am. Soc. Hortic. Sci. 2002;127:467–473. doi: 10.21273/JASHS.127.4.467. DOI
Calmes B., Guillemette T., Teyssier L., Siegler B., Pigné S., Landreau A., Iacomi B., Lemoine R., Richomme P., Simoneau P. role of mannitol metabolism in the pathogenicity of the necrotrophic fungus Alternaria brassicicola. Front. Plant Sci. 2013;4:131. doi: 10.3389/fpls.2013.00131. PubMed DOI PMC
Eshel G., Shaked R., Kazachkova Y., Khan A., Eppel A., Cisneros A., Acuna T., Gutterman Y., Tel-Zur N., Rachmilevitch S., et al. Anastatica hierochuntica, an Arabidopsis desert relative, is tolerant to multiple abiotic stresses and exhibits species-specific and common stress tolerance strategies with its halophytic relative, Eutrema (Thellungiella) salsugineum. Front. Plant Sci. 2017;7:1992. doi: 10.3389/fpls.2016.01992. PubMed DOI PMC
Ohkama-Ohtsu N., Oikawa A., Zhao P., Xiang C., Saito K., Oliver D.J. A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol. 2008;148:1603–1613. doi: 10.1104/pp.108.125716. PubMed DOI PMC
Gullner G., Komives T., Király L., Schröder P. Glutathione S-transferase enzymes in plant-pathogen interactions. Front. Plant Sci. 2018;9:1836. doi: 10.3389/fpls.2018.01836. PubMed DOI PMC
Vasyukova N.I., Chalenko G.I., Gerasimova N.G., Ozeretskovskaya O.L. Wound repair in plant tissues (review) Appl. Biochem. Microbiol. 2011;47:229–233. doi: 10.1134/S0003683811030161. PubMed DOI
Pietryczuk A., Czerpak R. Effect of traumatic acid on antioxidant activity in Chlorella vulgaris (Chlorophyceae) Plant Growth Regul. 2011;65:279–286. doi: 10.1007/s10725-011-9599-5. DOI
Szabados L., Savouré A. Proline: A multifunctional amino acid. Trends Plant Sci. 2010;15:89–97. doi: 10.1016/j.tplants.2009.11.009. PubMed DOI