vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RASvavilov-154Research ArticleСтатьиArticlesPR-БЕЛКИ С РИБОНУКЛЕАЗНОЙ АКТИВНОСТЬЮ И УСТОЙЧИВОСТЬ РАСТЕНИЙ К ПАТОГЕННЫМ ГРИБАМASSOCIATION BETWEEN PR PROTEINS WITH RIBONUCLEASE ACTIVITY AND PLANT RESISTANCE AGAINST PATHOGENIC FUNGIФилипенкоЕ. А.FilipenkoE. A.filipenko@bionet.nsc.ruКочетовА. В.KochetovA. V.filipenko@bionet.nsc.ruKanayamaY.KanayamaY.МалиновскийВ. И.MalinovskyV. I.ШумныйВ. К.ShumnyV. K.filipenko@bionet.nsc.ruФедеральное государственное бюджетное научное учреждение «Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук», Новосибирск, РоссияРоссияInstitute of Cytology and Genetics SB RAS, Novosibirsk, RussiaRussian FederationФедеральное государственное бюджетное учреждение науки Институт цитологии и генетики Сибирского отделения Российской академии наук, Новосибирск, Россия Новосибирский национальный исследовательский государственный университет, Новосибирск, РоссияРоссияInstitute of Cytology and Genetics SB RAS, Novosibirsk, Russia Novosibirsk National Research State University, Novosibirsk, RussiaRussian FederationGraduate School of Agricultural Science, Tohoku University, Aobaku, Sendai 981-8555, JapanЯпонияGraduate School of Agricultural Science, Tohoku University, Aobaku, Sendai 981-8555, JapanJapanФедеральное государственное бюджетное учреждение науки Биолого-почвенный институт Дальневосточного отделения Российской академии наук, Владивосток, РоссияРоссияInstitute of Biology and Soil Science, Far East Branch, Russian Academy of Sciences, Vladivostok, RussiaRussian Federation201327122014172326334Copyright © Филипенко Е.А., Кочетов А.В., Kanayama Y., Малиновский В.И., Шумный В.К., 20142014Филипенко Е.А., Кочетов А.В., Kanayama Y., Малиновский В.И., Шумный В.К.Filipenko E.A., Kochetov A.V., Kanayama Y., Malinovsky V.I., Shumny V.K.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/154

PR-белки (pathogenesis-related proteins) принимают участие в комплексной системе защиты растений от патогенов. Известно, что представители двух семейств PR-белков (PR4 и PR10) в ряде случаев обладают нуклеазной активностью. Установлено, что эти белки способны ингибировать рост патогенных грибов и РНКазная активность необходима для проявления этого эффекта. В обзоре обсуждаются современные данные о молекулярных механизмах фунгицидного действия рибонуклеаз, связанных как с непосредственным цитотоксическим воздействием на клетки патогена, так и с участием в индукции апоптоза и развитии гиперчувствительной реакции.

Pathogenesis-related (PR) proteins participate in complex plant defense response to pathogens. It is known that members of two PR-proteins families (PR-4 and PR-10) exhibit ribonuclease activity in some cases. These proteins were found to be able to inhibit the growth of pathogenic fungi, and the ribonuclease activity is necessary for manifestation of this effect. This paper presents current data on molecular mechanisms governing the antifungal activity of PR-ribonucleases connected both with their direct cytotoxic impact on pathogen cells and with possible participation in induction of plant cell apoptosis and development of the hypersensitive reaction (HR).

РНКазаPR-белкифитопатогенапоптозRNasePR proteinsPR-10PR-4plant pathogenapoptosisинтеграционый проект СО РАН – ДВО РАН, программа РАН «Живая природа: современное состояние и проблемы развития», грант РФФИ (12-04-01478)ReferencesМалиновский В.И. PR-белки и фитовирусы // Усп. соврем. биологии. 2009. Т. 129. № 3. С. 1–9.Малиновский В.И. PR-белки и фитовирусы // Усп. соврем. биологии. 2009. Т. 129. № 3. С. 1–9.Сангаев С.С., Кочетов А.В., Ибрагимова С.С. и др. Роль экстраклеточных рибонуклеаз в физиологических процессах высших растений // Информ. вестник ВОГиС. 2010. Т. 14. № 1. С. 232–242.Сангаев С.С., Кочетов А.В., Ибрагимова С.С. и др. Роль экстраклеточных рибонуклеаз в физиологических процессах высших растений // Информ. вестник ВОГиС. 2010. Т. 14. № 1. С. 232–242.Трифонова Е.А., Кочетов А.В., Шумный В.К. Роль нуклеаз в физиологических процессах высших растений // Усп. соврем. биологии. 2000. Т. 120. № 4. С. 395–405.Трифонова Е.А., Кочетов А.В., Шумный В.К. Роль нуклеаз в физиологических процессах высших растений // Усп. соврем. биологии. 2000. Т. 120. № 4. С. 395–405.Agrawal G.K., Rakwal R., Tamogami S. et al. Chitosan activates defense/stress response(s) in the leaves of Oryza sativa seedlings // Plant Physiol. Biochem. 2002. V. 40. P. 1061–1069.Agrawal G.K., Rakwal R., Tamogami S. et al. Chitosan activates defense/stress response(s) in the leaves of Oryza sativa seedlings // Plant Physiol. Biochem. 2002. V. 40. P. 1061–1069.Bai S., Dong C., Li B., Dai H. A PR-4 gene identifi ed from Malus domestica is involved in the defense responses against Botryosphaeria dothidea // Plant Physiol. Biochem. 2013. V. 62. P. 23–32.Bai S., Dong C., Li B., Dai H. A PR-4 gene identifi ed from Malus domestica is involved in the defense responses against Botryosphaeria dothidea // Plant Physiol. Biochem. 2013. V. 62. P. 23–32.Bantignies B., Se’guin J., Muzac I. et al. Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots // Plant Mol. Biol. 2000. V. 42. P. 871–881.Bantignies B., Se’guin J., Muzac I. et al. Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots // Plant Mol. Biol. 2000. V. 42. P. 871–881.Bahramnejad B., Goodwin P.H., Zhang J. et al. A comparison of two class 10 pathogenesis-related genes from alfalfa and their activation by multiple stresses and stress-related signaling molecules // Plant Cell Rep. 2010. V. 29. P. 1235–1250.Bahramnejad B., Goodwin P.H., Zhang J. et al. A comparison of two class 10 pathogenesis-related genes from alfalfa and their activation by multiple stresses and stress-related signaling molecules // Plant Cell Rep. 2010. V. 29. P. 1235–1250.Bertini L., Caporale C., Testa M. et al. Structural basis of the antifungal activity of wheat PR4 proteins // FEBS Letters. 2009. V. 583. P. 2865–2871.Bertini L., Caporale C., Testa M. et al. Structural basis of the antifungal activity of wheat PR4 proteins // FEBS Letters. 2009. V. 583. P. 2865–2871.Bertini L., Proietti S., Aleandri M.P. et al. Modular structure of HEL protein from Arabidopsis reveals new potential functions for PR-4 proteins // Biol. Chem. 2012. V. 393. Nо. 12. P. 1533–1546.Bertini L., Proietti S., Aleandri M.P. et al. Modular structure of HEL protein from Arabidopsis reveals new potential functions for PR-4 proteins // Biol. Chem. 2012. V. 393. Nо. 12. P. 1533–1546.Borsics T., Lados M. Dodder infection induces the expression of a pathogenesis-related gene of the family PR-10 in alfalfa // J. Exp. Bot. 2002. V. 53. P. 1831–1832.Borsics T., Lados M. Dodder infection induces the expression of a pathogenesis-related gene of the family PR-10 in alfalfa // J. Exp. Bot. 2002. V. 53. P. 1831–1832.Bravo J.M., Campo S., Murillo I. et al. B. Fungus- and woundinduced accumulation of mRNA containing a class II chitinase of the pathogenesis-related protein 4 (PR-4) family of maize // Plant Mol. Biol. 2003. V. 52. P. 745–759.Bravo J.M., Campo S., Murillo I. et al. B. Fungus- and woundinduced accumulation of mRNA containing a class II chitinase of the pathogenesis-related protein 4 (PR-4) family of maize // Plant Mol. Biol. 2003. V. 52. P. 745–759.Breda C., Sallaud C., El-Turk J. et al. Defense reaction in Medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles // Mol. Plant Microbe Interact. 1996. V. 9. P. 713–719.Breda C., Sallaud C., El-Turk J. et al. Defense reaction in Medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles // Mol. Plant Microbe Interact. 1996. V. 9. P. 713–719.Broekaert W., Lee H.H., Kush A. et al. Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis) // Proc. Natl Acad. Sci. USA. 1990. V. 87. P. 7633–7637.Broekaert W., Lee H.H., Kush A. et al. Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis) // Proc. Natl Acad. Sci. USA. 1990. V. 87. P. 7633–7637.Bufe A., Spangfort M.D., Kahlert H. et al. The major birch pollen allergen, bet v1, shows ribonuclease activity // Planta. 1996. V. 199. P. 413–415.Bufe A., Spangfort M.D., Kahlert H. et al. The major birch pollen allergen, bet v1, shows ribonuclease activity // Planta. 1996. V. 199. P. 413–415.Caporale C., Di Bernardino I., Leonardi L. et al. Wheat pathogenesis–related proteins of class 4 have ribonuclease activity // FEBS Letters. 2004. V. 575. P. 71–76.Caporale C., Di Bernardino I., Leonardi L. et al. Wheat pathogenesis–related proteins of class 4 have ribonuclease activity // FEBS Letters. 2004. V. 575. P. 71–76.Caruso C., Caporale C., Poerio C. et al. The amino acid sequence of a protein from wheat kernels closely related to proteins involved in the mechanism of plant defense // J. Protein Chem. 1993. V. 12. P. 379–386.Caruso C., Caporale C., Poerio C. et al. The amino acid sequence of a protein from wheat kernels closely related to proteins involved in the mechanism of plant defense // J. Protein Chem. 1993. V. 12. P. 379–386.Chadha P., Das R.H. A pathogenesis related protein, AhPR10, from peanut: an insight of its mode of antifungal activity // Planta. 2006. V. 225. P. 213–222.Chadha P., Das R.H. A pathogenesis related protein, AhPR10, from peanut: an insight of its mode of antifungal activity // Planta. 2006. V. 225. P. 213–222.Chen Z.Y., Brown R.L., Damann K.E., Cleveland T.E. PR10 expression in maize and its effect on host resistance against Aspergillus fl avus infection and afl atoxin production // Mol. Plant Pathol. 2010. V. 11. No. 1. P. 69–81.Chen Z.Y., Brown R.L., Damann K.E., Cleveland T.E. PR10 expression in maize and its effect on host resistance against Aspergillus fl avus infection and afl atoxin production // Mol. Plant Pathol. 2010. V. 11. No. 1. P. 69–81.Choi D.S., Hwang I.S., Hwang B.K. Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper // Plant Cell. 2012. V. 24. No. 4. P. 1675–1690.Choi D.S., Hwang I.S., Hwang B.K. Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper // Plant Cell. 2012. V. 24. No. 4. P. 1675–1690.Chung K.M., Igari K., Uchida N., Tasaka M. New perspectives on plants defense responses through modulation of developmental pathways // Mol. Cells. 2008. V. 26. P. 107–112.Chung K.M., Igari K., Uchida N., Tasaka M. New perspectives on plants defense responses through modulation of developmental pathways // Mol. Cells. 2008. V. 26. P. 107–112.Crowell D., John M.E., Russell D., Amasino R.M. Characterization of a stress-induced developmentally regulated gene family from soybean // Plant Mol. Biol. 1992. V. 18. P. 459–466.Crowell D., John M.E., Russell D., Amasino R.M. Characterization of a stress-induced developmentally regulated gene family from soybean // Plant Mol. Biol. 1992. V. 18. P. 459–466.Fernandes H., Pasternak O., Bujacz G. et al. Lupinus luteus pathogenesis-related protein as a reservoir for cytokinin // J. Mol. Biol. 2008. V. 378. P. 1040–1051.Fernandes H., Pasternak O., Bujacz G. et al. Lupinus luteus pathogenesis-related protein as a reservoir for cytokinin // J. Mol. Biol. 2008. V. 378. P. 1040–1051.Fristensky B., Horovitz D., Hadwiger L.A. cDNA sequences for pea disease response genes // Plant Mol. Biol. 1988. V. 11. P. 713–715.Fristensky B., Horovitz D., Hadwiger L.A. cDNA sequences for pea disease response genes // Plant Mol. Biol. 1988. V. 11. P. 713–715.Gonzalez-Teuber M., Eilmus S., Muck A. et al. Pathogenesisrelated proteins protect extrafl oral nectar from microbial infestation // Plant J. 2009. V. 58. P. 464–473.Gonzalez-Teuber M., Eilmus S., Muck A. et al. Pathogenesisrelated proteins protect extrafl oral nectar from microbial infestation // Plant J. 2009. V. 58. P. 464–473.Gu Y.Q., Wildermuth M.C., Chakravarthy S. et al. Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis // Plant Cell. 2002. V. 14. P. 817–831.Gu Y.Q., Wildermuth M.C., Chakravarthy S. et al. Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis // Plant Cell. 2002. V. 14. P. 817–831.Guevara-Morato M.A., de Lacoba M.G., García-Luque I., Serra M.T. Characterization of a pathogenesis-related protein 4 (PR-4) induced in Capsicum chinense L3 plants with dual RNase and DNase activities // J. Exp. Bot. 2010. V. 61. No. 12. P. 3259–3271.Guevara-Morato M.A., de Lacoba M.G., García-Luque I., Serra M.T. Characterization of a pathogenesis-related protein 4 (PR-4) induced in Capsicum chinense L3 plants with dual RNase and DNase activities // J. Exp. Bot. 2010. V. 61. No. 12. P. 3259–3271.Hadwiger L.A., Polashock J. Fungal mitochondrial DNases: effectors with the potential to activate plant defenses in nonhost resistance // Phytopathology. 2013. V. 103. No. 1. P. 81–90.Hadwiger L.A., Polashock J. Fungal mitochondrial DNases: effectors with the potential to activate plant defenses in nonhost resistance // Phytopathology. 2013. V. 103. No. 1. P. 81–90.Hawes M.C., Curlango-Rivera G., Wen F. et al. Extracellular DNA: the tip of root defenses? // Plant Sci. 2011. V. 180. No. 6. P. 741–745.Hawes M.C., Curlango-Rivera G., Wen F. et al. Extracellular DNA: the tip of root defenses? // Plant Sci. 2011. V. 180. No. 6. P. 741–745.He M., Xu Y., Cao J. et al. Subcellular localization and functional analyses of a PR10 protein gene from Vitis pseudoreticulata in response to Plasmopara viticola infection // Protoplasma. 2013. V. 250. No. 1. P. 129–1240.He M., Xu Y., Cao J. et al. Subcellular localization and functional analyses of a PR10 protein gene from Vitis pseudoreticulata in response to Plasmopara viticola infection // Protoplasma. 2013. V. 250. No. 1. P. 129–1240.Hillwig M.S., Liu X., Liu G. et al. Petunia nectar proteins have ribonuclease activity // J. Exp. Bot. 2010. V. 61. No. 11. P. 2951–2965.Hillwig M.S., Liu X., Liu G. et al. Petunia nectar proteins have ribonuclease activity // J. Exp. Bot. 2010. V. 61. No. 11. P. 2951–2965.Huang J.C., Chang F.C., Wang C.S. Characterization of a lily tapetal transcript that shares sequence similarity with a class of intracellular pathogenesis-related (IPR) proteins // Plant Mol. Biol. 1997. V. 34. P. 681–686.Huang J.C., Chang F.C., Wang C.S. Characterization of a lily tapetal transcript that shares sequence similarity with a class of intracellular pathogenesis-related (IPR) proteins // Plant Mol. Biol. 1997. V. 34. P. 681–686.Hugot K., Ponchet M., Marais A. et al. A tobacco S-like RNase inhibits hyphal elongation of plant pathogens // Mol. Plant Microbe Interact. 2002. V. 15. No. 3. P. 243–250.Hugot K., Ponchet M., Marais A. et al. A tobacco S-like RNase inhibits hyphal elongation of plant pathogens // Mol. Plant Microbe Interact. 2002. V. 15. No. 3. P. 243–250.Hwang S.H., Lee I.A., Yie S.W., Hwang D.J. Identifi cation of an OsPR10a promoter region responsive to salicylic acid // Planta. 2008. V. 227. P. 1141–1150.Hwang S.H., Lee I.A., Yie S.W., Hwang D.J. Identifi cation of an OsPR10a promoter region responsive to salicylic acid // Planta. 2008. V. 227. P. 1141–1150.Kim S.T., Yu S., Kang Y.H. et al. The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity // Plant Cell Rep. 2008. V. 27. P. 593–603.Kim S.T., Yu S., Kang Y.H. et al. The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity // Plant Cell Rep. 2008. V. 27. P. 593–603.Kim S.G., Kim S.T., Wang Y. et al. The RNase activity of rice probenazole-induced protein1 (PBZ1) plays a key role in cell death in plants // Mol. Cells. 2011. V. 31. No. 1. P. 25–31.Kim S.G., Kim S.T., Wang Y. et al. The RNase activity of rice probenazole-induced protein1 (PBZ1) plays a key role in cell death in plants // Mol. Cells. 2011. V. 31. No. 1. P. 25–31.Krishnaswamy S., Baral P.K., James M.N., Kav N.N. Site-directed mutagenesis of histidine 69 and glutamic acid 148 alters the ribonuclease activity of pea ABR17 (PR10.4) // Plant Physiol. Biochem. 2011. V. 49. No. 9. P. 958–962.Krishnaswamy S., Baral P.K., James M.N., Kav N.N. Site-directed mutagenesis of histidine 69 and glutamic acid 148 alters the ribonuclease activity of pea ABR17 (PR10.4) // Plant Physiol. Biochem. 2011. V. 49. No. 9. P. 958–962.Krishnaswamy S.S., Srivastava S., Mohammadi M. et al. Transcriptional profi ling of pea ABR17 mediated changes in gene expression in Arabidopsis thaliana // BMC Plant Biol. 2008. DOI: 10.1186/1471-2229-8-91.Krishnaswamy S.S., Srivastava S., Mohammadi M. et al. Transcriptional profi ling of pea ABR17 mediated changes in gene expression in Arabidopsis thaliana // BMC Plant Biol. 2008. DOI: 10.1186/1471-2229-8-91.Lebel S., Schellenbaum P., Walter B., Maillot P. Characterisation of the Vitis vinifera PR10 multigene family // BMC Plant Biol. 2010. DOI: 10.1186/1471-2229-10-184.Lebel S., Schellenbaum P., Walter B., Maillot P. Characterisation of the Vitis vinifera PR10 multigene family // BMC Plant Biol. 2010. DOI: 10.1186/1471-2229-10-184.LeBrasseur N.D., MacIntosh G.C., Pérez-Amador M.A. et al. Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway // Plant J. 2002. V. 29. No. 4. P. 393–403.LeBrasseur N.D., MacIntosh G.C., Pérez-Amador M.A. et al. Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway // Plant J. 2002. V. 29. No. 4. P. 393–403.Linthorst H.J.M., Danhash N., Brederode F.T. et al. Tobacco and tomato PR proteins homologous to win and pro-hevein lack the «hevein» domain // Mol. Plant Microbe Interact. 1991. V. 4. P. 586–592.Linthorst H.J.M., Danhash N., Brederode F.T. et al. Tobacco and tomato PR proteins homologous to win and pro-hevein lack the «hevein» domain // Mol. Plant Microbe Interact. 1991. V. 4. P. 586–592.Liu J.-J., Ekramoddoullah A.K.M., Yu X. Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening // Physiol. Plant. 2003. V. 119. P. 544–553.Liu J.-J., Ekramoddoullah A.K.M., Yu X. Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening // Physiol. Plant. 2003. V. 119. P. 544–553.Ludvigsen S., Poulsen F.M. Three-dimensional structure in solution of Barwin, a protein from barley seed // Biochemistry. 1992. V. 31. P. 8783–8789.Ludvigsen S., Poulsen F.M. Three-dimensional structure in solution of Barwin, a protein from barley seed // Biochemistry. 1992. V. 31. P. 8783–8789.Lu H.C., Lin J.H., Chua A.C. et al. Cloning and expression of pathogenesis-related protein 4 from jelly fi g (Ficus awkeotsang Makino) achenes associated with ribonuclease, chitinase and anti-fungal activities // Plant Physiol. Biochem. 2012. V. 56. P. 1–13.Lu H.C., Lin J.H., Chua A.C. et al. Cloning and expression of pathogenesis-related protein 4 from jelly fi g (Ficus awkeotsang Makino) achenes associated with ribonuclease, chitinase and anti-fungal activities // Plant Physiol. Biochem. 2012. V. 56. P. 1–13.McGee J.D., Hamer J.E., Hodges T.K. Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea // Mol. Plant Microbe Interact. 2001. V. 14. P. 877–886.McGee J.D., Hamer J.E., Hodges T.K. Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea // Mol. Plant Microbe Interact. 2001. V. 14. P. 877–886.MacIntosh G.C., Bariola P.A., Newbigin E., Green P.J. Characterization of Rny1, the Saccharomyces cerevisiae member of the T2 RNase family of RNases: Unexpected functions for ancient enzymes? // Proc. Natl Acad. Sci. USA. 2001. V. 98. P. 1018–1023.MacIntosh G.C., Bariola P.A., Newbigin E., Green P.J. Characterization of Rny1, the Saccharomyces cerevisiae member of the T2 RNase family of RNases: Unexpected functions for ancient enzymes? // Proc. Natl Acad. Sci. USA. 2001. V. 98. P. 1018–1023.MacIntosh G.C., Hillwig M.S., Meyer A., Flagel L. RNase T2 genes from rice and the evolution of secretory ribonucleases in plants // Mol. Genet. Genomics. 2010. V. 283. No. 4. P. 381–396.MacIntosh G.C., Hillwig M.S., Meyer A., Flagel L. RNase T2 genes from rice and the evolution of secretory ribonucleases in plants // Mol. Genet. Genomics. 2010. V. 283. No. 4. P. 381–396.Matton D.P., Brisson N. Cloning, expression and sequence conservation of pathogenesis-related gene transcripts of potato // Mol. Plant Microbe. Interact. 1989. V. 2. P. 325–331.Matton D.P., Brisson N. Cloning, expression and sequence conservation of pathogenesis-related gene transcripts of potato // Mol. Plant Microbe. Interact. 1989. V. 2. P. 325–331.Midoh N., Iwata M. Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis related protein in rice // Plant Cell Physiol. 1996. V. 37. P. 9–18.Midoh N., Iwata M. Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis related protein in rice // Plant Cell Physiol. 1996. V. 37. P. 9–18.Neuhaus J.M, Sticher L., Meins F.Jr., Boller T. A short C-terminal sequence is necessary and suffi cient for the targeting of chitinases to the plant vacuole // Proc. Natl Acad. Sci. USA. 1991. V. 88. P. 10362–10366.Neuhaus J.M, Sticher L., Meins F.Jr., Boller T. A short C-terminal sequence is necessary and suffi cient for the targeting of chitinases to the plant vacuole // Proc. Natl Acad. Sci. USA. 1991. V. 88. P. 10362–10366.Neudecker P., Schweimer K., Nerkamp J. et al. Allergic Crossreactivity made visible solution structure of the major cherry allergen Pru av 1 // J. Biol. Chem. 2001. V. 276. P. 22756–22763.Neudecker P., Schweimer K., Nerkamp J. et al. Allergic Crossreactivity made visible solution structure of the major cherry allergen Pru av 1 // J. Biol. Chem. 2001. V. 276. P. 22756–22763.Park C.-J., Kim K.-J., Shin R. et al. Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway // Plant J. 2004. V. 37. P. 186–198.Park C.-J., Kim K.-J., Shin R. et al. Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway // Plant J. 2004. V. 37. P. 186–198.Park Y.S., Jeon M.H., Lee S.H. et al. Activation of defense responses in chinese cabbage by a nonhost pathogen, Pseudomonos syringae pv. tomato // J. Biochem. Mol. Biol. 2005. V. 538. P. 748–754.Park Y.S., Jeon M.H., Lee S.H. et al. Activation of defense responses in chinese cabbage by a nonhost pathogen, Pseudomonos syringae pv. tomato // J. Biochem. Mol. Biol. 2005. V. 538. P. 748–754.Pasternak O., Biesiadka J., Dolot R. et al. Structure of a yellow lupin pathogenesis-related PR-10 protein belonging to novel subclass // Acta Crystallogr. Sect. D Biol. Crystallogr. 2005. V. 61. P. 99–107.Pasternak O., Biesiadka J., Dolot R. et al. Structure of a yellow lupin pathogenesis-related PR-10 protein belonging to novel subclass // Acta Crystallogr. Sect. D Biol. Crystallogr. 2005. V. 61. P. 99–107.Potter S., Uknes S., Lawton K. et al. Regulation of a heveinlike gene in Arabidopsis // Mol. Plant Microbe Interact. 1993. V. 6. P. 680–685.Potter S., Uknes S., Lawton K. et al. Regulation of a heveinlike gene in Arabidopsis // Mol. Plant Microbe Interact. 1993. V. 6. P. 680–685.Poupard P., Parisi L., Campion C. et al. A wound- and ethephon-inducible PR-10 gene subclass from apple is differentially expressed during infection with a compatible and an incompatible race of Venturia inaequalis // Physiol. Mol. Plant Pathol. 2003. V. 62. P. 3–12.Poupard P., Parisi L., Campion C. et al. A wound- and ethephon-inducible PR-10 gene subclass from apple is differentially expressed during infection with a compatible and an incompatible race of Venturia inaequalis // Physiol. Mol. Plant Pathol. 2003. V. 62. P. 3–12.Puehringer H., Zinoecker I., Mazban G. et al. MdAP, a novel protein in apple, is associated with the major allergen Mal d 1 // Gene. 2003. V. 321. P. 173–183.Puehringer H., Zinoecker I., Mazban G. et al. MdAP, a novel protein in apple, is associated with the major allergen Mal d 1 // Gene. 2003. V. 321. P. 173–183.Rakwal R., Agrawal G.K., Yonekura M. Separation of proteins from stressed rice Oryza sativa L. leaf tissues by twodimensional polyacrylamide gel electrophoresis, induction of pathogenesis-related and cellular protectant proteins by jasmonic acid, UV irradiation and copper chloride // Electrophoresis. 1999. V. 20. P. 3472–3478.Rakwal R., Agrawal G.K., Yonekura M. Separation of proteins from stressed rice Oryza sativa L. leaf tissues by twodimensional polyacrylamide gel electrophoresis, induction of pathogenesis-related and cellular protectant proteins by jasmonic acid, UV irradiation and copper chloride // Electrophoresis. 1999. V. 20. P. 3472–3478.Rakwal R., Agrawal G.K., Yonekura M. Lightdependent induction of OsPR10 in rice (Oryza sativa L.) seedlings by the global stress signaling molecule jasmonic acid and protein phosphatase 2A inhibitors // Plant Sci. 2001. V. 61. P. 469–479.Rakwal R., Agrawal G.K., Yonekura M. Lightdependent induction of OsPR10 in rice (Oryza sativa L.) seedlings by the global stress signaling molecule jasmonic acid and protein phosphatase 2A inhibitors // Plant Sci. 2001. V. 61. P. 469–479.Rao M.V., Lee H., Davis K.R. Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death // Plant Cell. 2002. V. 32. P. 447–456.Rao M.V., Lee H., Davis K.R. Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death // Plant Cell. 2002. V. 32. P. 447–456.Robert N., Ferran J., Breda C. et al. Molecular characterization of the incompatible interaction of Vitis vinifera leaves with Pseudomonas syringae pv pisi, expression of genes coding for stilbene synthase and class 10 PR protein // Eur. J. Plant. Pathol. 2001. V. 7. P. 249–261.Robert N., Ferran J., Breda C. et al. Molecular characterization of the incompatible interaction of Vitis vinifera leaves with Pseudomonas syringae pv pisi, expression of genes coding for stilbene synthase and class 10 PR protein // Eur. J. Plant. Pathol. 2001. V. 7. P. 249–261.Ruperti B., Cattivelli L., Pagni S., Ramina A. Ethyleneresponsive genes are differentially regulated during abscission, organ senescence and wounding in peach (Prunus persica) // J. Exp. Bot. 2002. V. 53. P. 429–437.Ruperti B., Cattivelli L., Pagni S., Ramina A. Ethyleneresponsive genes are differentially regulated during abscission, organ senescence and wounding in peach (Prunus persica) // J. Exp. Bot. 2002. V. 53. P. 429–437.Sikorski M.M., Biesiadka J., Kasperska A.E. et al. Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules // Plant Sci. 1999. V. 149. P. 125–137.Sikorski M.M., Biesiadka J., Kasperska A.E. et al. Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules // Plant Sci. 1999. V. 149. P. 125–137.Somssich I.E., Schmelzer E., Bollmann J., Hahlbrock K. Rapid activation by fungal elicitor of genes encoding «pathogenesisrelated » proteins in cultured parsley cells // Proc. Natl Acad. Sci. USA. 1986. V. 83. No. 8. P. 2427–2430.Somssich I.E., Schmelzer E., Bollmann J., Hahlbrock K. Rapid activation by fungal elicitor of genes encoding «pathogenesisrelated » proteins in cultured parsley cells // Proc. Natl Acad. Sci. USA. 1986. V. 83. No. 8. P. 2427–2430.Somssich I.E., Schmelzer E., Kawalleck P., Hahlbrock K. Gene structure and in situ transcript localization of pathogenesisrelated protein 1 in parsley // Mol. Gen. Genet. 1988. V. 213. No. 1. P. 93–98.Somssich I.E., Schmelzer E., Kawalleck P., Hahlbrock K. Gene structure and in situ transcript localization of pathogenesisrelated protein 1 in parsley // Mol. Gen. Genet. 1988. V. 213. No. 1. P. 93–98.Srivastava S., Emery R.J.N., Kurepin L.V. et al. Pea PR 10.1 is a ribonuclease and its transgenic expression elevates cytokinin levels // Plant Growth Regul. 2006. V. 49. P. 17–25.Srivastava S., Emery R.J.N., Kurepin L.V. et al. Pea PR 10.1 is a ribonuclease and its transgenic expression elevates cytokinin levels // Plant Growth Regul. 2006. V. 49. P. 17–25.Stanford A., Bevan M., Northcote D. Differential expression within a family of novel wound-induced genes in potato // Mol. Gen. Genet. 1989. V. 215. P. 200–208.Stanford A., Bevan M., Northcote D. Differential expression within a family of novel wound-induced genes in potato // Mol. Gen. Genet. 1989. V. 215. P. 200–208.van Loon L.C., Pierpoint W.S., Boller T., Conejero V. Recommendation for naming plant pathogenesis-related proteins // Plant Mol. Biol. Rep. 1994. V. 12. P. 245–264.van Loon L.C., Pierpoint W.S., Boller T., Conejero V. Recommendation for naming plant pathogenesis-related proteins // Plant Mol. Biol. Rep. 1994. V. 12. P. 245–264.van Loon L.C., van Strien E.A. The family of pathogenesis related proteins // Physiol. Mol. Plant Pathol. 1999. V. 55. P. 85–97.van Loon L.C., van Strien E.A. The family of pathogenesis related proteins // Physiol. Mol. Plant Pathol. 1999. V. 55. P. 85–97.van Loon L.C., Rep M., Pietersen C.M.J. Signifi cance of inducible defense-related proteins in infected plants // Annu. Rev. Phytopathol. 2006. V. 44. P. 135–162.van Loon L.C., Rep M., Pietersen C.M.J. Signifi cance of inducible defense-related proteins in infected plants // Annu. Rev. Phytopathol. 2006. V. 44. P. 135–162.Walter M.H., Liu J.W. et al. Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental, dark-induced and exogenousstimulus-dependent expression // Eur. J. Biochem. 1996. V. 239. P. 281–293.Walter M.H., Liu J.W. et al. Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental, dark-induced and exogenousstimulus-dependent expression // Eur. J. Biochem. 1996. V. 239. P. 281–293.Wang N., Xiao B., Xiong L. Identifi cation of a cluster of PR4-like genes involved in stress responses in rice // J. Plant Physiol. 2011. V. 168. P. 2212–2224.Wang N., Xiao B., Xiong L. Identifi cation of a cluster of PR4-like genes involved in stress responses in rice // J. Plant Physiol. 2011. V. 168. P. 2212–2224.Warner S.A.J., Scott R., Draper J. Characterization of a woundinduced transcript from the monocot asparagus that shares similarity with a class of intracellular pathogenesis-related (PR) proteins // Plant Mol. Biol. 1992. V. 19. P. 555–561.Warner S.A.J., Scott R., Draper J. Characterization of a woundinduced transcript from the monocot asparagus that shares similarity with a class of intracellular pathogenesis-related (PR) proteins // Plant Mol. Biol. 1992. V. 19. P. 555–561.Wen F., White G.J., VanEtten H.D. et al. Extracellular DNA is required for root tip resistance to fungal infection // Plant Physiol. 2009. V. 151. No. 2. P. 820–829.Wen F., White G.J., VanEtten H.D. et al. Extracellular DNA is required for root tip resistance to fungal infection // Plant Physiol. 2009. V. 151. No. 2. P. 820–829.Xie Y.R., Chen Z.Y., Brown R.L., Bhatnagar D. Expression and functional characterization of two pathogenesis-related protein 10 genes from Zea mays // J. Plant Physiol. 2010. V. 167. P. 121–130.Xie Y.R., Chen Z.Y., Brown R.L., Bhatnagar D. Expression and functional characterization of two pathogenesis-related protein 10 genes from Zea mays // J. Plant Physiol. 2010. V. 167. P. 121–130.Yamamoto M., Torikai S., Oeda K. A major root protein of carrots with high homology to intracellular pathogenesisrelated (PR) proteins and pollen allergens // Plant Cell Physiol. 1997. V. 38. P. 1080–1086.Yamamoto M., Torikai S., Oeda K. A major root protein of carrots with high homology to intracellular pathogenesisrelated (PR) proteins and pollen allergens // Plant Cell Physiol. 1997. V. 38. P. 1080–1086.Zhang N., Zhang S., Borchert S. et al. High levels of a fungal superoxide dismutase and increased concentration of a PR-10 plant protein in associations between the endophytic fungus Neotyphodium lolii and ryegrass // Mol. Plant Microbe Interact. 2011. V. 24. No. 8. P. 984–992.Zhang N., Zhang S., Borchert S. et al. High levels of a fungal superoxide dismutase and increased concentration of a PR-10 plant protein in associations between the endophytic fungus Neotyphodium lolii and ryegrass // Mol. Plant Microbe Interact. 2011. V. 24. No. 8. P. 984–992.Zhou X.J., Lu S., Xu Y.H. et al. A cotton cDNA (GaPR-10) encoding a pathogenesis-related 10 protein with in vitro ribonuclease activity // Plant Sci. 2002. V. 162. No. 4. P. 629–636.Zhou X.J., Lu S., Xu Y.H. et al. A cotton cDNA (GaPR-10) encoding a pathogenesis-related 10 protein with in vitro ribonuclease activity // Plant Sci. 2002. V. 162. No. 4. P. 629–636.

The authors declare that there are no conflicts of interest present.