Чувствительность arp–/– мутантных растений Arabidopsis thaliana к генотоксическим агентам
DOI:
https://doi.org/10.26577/EB-2017-4-1305Ключевые слова:
АП-эндонуклеаза, Arabidopsis thaliana, ДНК гликозилазы, активные формы кислорода.Аннотация
Апуриновые/апиримидиновые (АР) эндонуклеазы являются ключевыми ферментами реализации двух пересекающихся путей репарации ДНК: ДНК-гликозилаза инициированной эксцизионной репарации оснований (BER) и инцизионной репарации нуклеотидов (NIR). В процессе BER, АР-эндонуклеазы специфически гидролизуют фосфодиэфирную связь рядом с АР-сайтом и 3'-блокирующими группами, образующимися в ДНК после удаления окисленного основания ДНК-гликозилазой. Тогда как в NIR механизме АР-эндонуклеазы гидролизуют фосфодиэфирную связь ДНК с 5'-конца от повреждения. Геном широко используемого модельного организма A.thaliana кодирует три предполагаемых гомолога главной человеческой АП-эндонуклеазы 1 (APE1): Arp, Ape1L и Ape2. ARP – это главная АР-эндонуклеаза растений, которая удаляет абазивные сайты. Однако неизвестно, содержат ли АР-эндонуклеазы растений NIR активность. В настоящей работе показано, что гомозиготный arp-/- мутант A. thaliana проявляет высокую чувствительность к метилметансульфонату и трет-бутилгидропероксиду, но не к H2O2, что указывает на то, что ARP-катализируемая NIR активность требуется для восстановления АР-сайтов, генерируемых экзогенными факторами, и специфических окислительных повреждений ДНК, индуцированных t-BuO2H в условиях in vivo. Экстракты растений нокаутных по гену arp не проявляли NIR активность на αdA•T содержащем олигонуклеотидном субстрате. Эти результаты свидетельствуют о том, что ARP является основной АР- и NIR- эндонуклеазой в A. thaliana.
Библиографические ссылки
1 Cadet J., Douki T., Gasparutto D., Ravanat J.L. Oxidative damage to DNA: formation, measurement and biochemical features // Mutat. Res. – 2003. – Vol. 531. – P. 5-23.
2 Krokan H.E., Bjoras M. Base excision repair // Cold Spring Harb. Perspect. Biol. – 2013. – Vol. 5. – P. a012583.
3 Ischenko A.A., Saparbaev M.K. Alternative nucleotide incision repair pathway for oxidative DNA damage // Nature. – 2002. – Vol. 415. – P. 183-187.
4 Hitomi K., Iwai S., Tainer J.A. The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair // DNA Repair (Amst). – 2007. - Vol. 6. – P. 410-428.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway // Nucleic Acids Res. – 2004. – Vol. 32. - P. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA repair and mutagenesis // ASM Press. – 2006.
7 Vanyushin B.F., Ashapkin V.V. DNA methylation in higher plants: past, present and future // Biochim Biophys Acta. – 2011. – Vol. 1809. – P. 360-368.
8 He X.J., Chen T., Zhu J.K. Regulation and function of DNA methylation in plants and animals // Cell Res. – 2011. – Vol. 21. – P. 442-465.
9 Zhu J.K. Active DNA demethylation mediated by DNA glycosylases // Annu. Rev. Genet. – 2009. – Vol. 43. – P. 143-166.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases // Proc. Natl. Acad. Sci. U.S.A. – 2006. – Vol. 103. - P. 6853-6858.
11 Babiychuk E., Kushnir S., Van Montagu M., Inze D. The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun // Proc. Natl. Acad. Sci. U. S. A. – 1994. – Vol. 91. – P. 3299-3303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1 // Plant J. – 2011. – Vol. 68. – P. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L // PLoS One. – 2014. – Vol. 9. – P. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death // Plant Physiol. Biochem. – 2011. – Vol. 49. - P. 1155-1164.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles // Proc. Natl. Acad. Sci. U. S. A. – 2006. - Vol. 103. P. 2564-2569.
16 Baker M.A., He S.Q. Elaboration of cellular DNA breaks by hydroperoxides // Free Radic Biol Med. – 1991. - Vol. 11. – P. 563-572.
17 Gros L., Ishchenko A.A., Saparbaev M. Enzymology of repair of etheno-adducts // Mutat. Res. – 2003. – Vol. 531. – P. 219-229.
18 Hix S., Morais Mda S., Augusto O. DNA methylation by tert-butyl hydroperoxide-iron (II) // Free Radic Biol Med. – 1995. – Vol. 19. – P. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies // Chem Res Toxicol. – 2000. – Vol. 13. – P. 1056-1054.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli // DNA Repair (Amst). – 2002. - Vol. 1. P. 437-447.
21 Bradford M. M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding // Anal. Biochem. – 1976. – Vol. 72. – P. 248-254.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. Requirement for abasic endonuclease gene homologues in Arabidopsis seed development // PLoS One. – 2009. – Vol. 4. – P. e4297.
23 Foyer C.H., Noctor G. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiol. Plant. – 2003. – Vol. 119. – P. 355–364.
24 Jaruga P., Dizdaroglu M. 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1413-1425.
25 Brooks P.J. The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1168-1179.
References
1 Cadet J., Douki T., Gasparutto D., Ravanat J.L. (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res., vol. 531, pp. 5-23.
2 Krokan H.E., Bjoras M. (2013) Base excision repair. Cold Spring Harb. Perspect. Biol., vol. 5, pp. a012583.
3 Ischenko A.A., Saparbaev M.K. (2002) Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature, vol. 415, pp. 183-87.
4 Hitomi K., Iwai S., Tainer J.A. (2007) The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst), vol. 6, pp. 410-28.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. (2004) The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res., vol. 32, pp. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. (2006) DNA repair and mutagenesis. ASM Press.
7 Vanyushin B.F., Ashapkin V.V. (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta., vol. 1809, pp. 360-68.
8 He X.J., Chen T., Zhu J.K. (2011) Regulation and function of DNA methylation in plants and animals. Cell Res., vol. 21, pp. 442-65.
9 Zhu J.K. (2009) Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet., vol. 43, pp. 143-66.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. (2006) Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. U.S.A., vol. 103, pp. 6853-58.
11 Babiychuk E., Kushnir S., Van Montagu M., Inze D. (1994) The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun. Proc. Natl. Acad. Sci. U. S. A., vol. 91, pp. 3299-303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. (2011) Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1. Plant J., vol. 68, pp. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. (2014) Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L. PLoS One, vol. 9, pp. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death. Plant Physiol. Biochem., vol. 49, pp. 1155-64.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. (2006) Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles. Proc. Natl. Acad. Sci. U. S. A., vol. 103, pp. 2564-69.
16 Baker M.A., He S.Q. (1991) Elaboration of cellular DNA breaks by hydroperoxides. Free Radic Biol Med., vol. 11, pp. 563-72.
17 Gros L., Ishchenko A.A., Saparbaev M. (2003) Enzymology of repair of etheno-adducts. Mutat. Res. vol. 531, pp. 219-29.
18 Hix S., Morais Mda S., Augusto O. (1995) DNA methylation by tert-butyl hydroperoxide-iron (II). Free Radic Biol Med. vol. 19, pp. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. (2000) In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies. Chem Res Toxicol., vol. 13, pp. 1056-54.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. (2002) Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli. DNA Repair (Amst), vol. 1, pp. 437-47.
21 Bradford M. M. (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem., vol. 72, pp. 248-54.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development. PLoS One, vol. 4, pp. e4297.
23 Foyer C.H., Noctor G. (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant, vol. 119, pp. 355–64.
24 Jaruga P., Dizdaroglu M. (2008) 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst), vol. 7, pp. 1413-25.
25 Brooks P.J. (2008) The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair. DNA Repair (Amst), vol. 7, pp. 1168-79.
2 Krokan H.E., Bjoras M. Base excision repair // Cold Spring Harb. Perspect. Biol. – 2013. – Vol. 5. – P. a012583.
3 Ischenko A.A., Saparbaev M.K. Alternative nucleotide incision repair pathway for oxidative DNA damage // Nature. – 2002. – Vol. 415. – P. 183-187.
4 Hitomi K., Iwai S., Tainer J.A. The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair // DNA Repair (Amst). – 2007. - Vol. 6. – P. 410-428.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway // Nucleic Acids Res. – 2004. – Vol. 32. - P. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA repair and mutagenesis // ASM Press. – 2006.
7 Vanyushin B.F., Ashapkin V.V. DNA methylation in higher plants: past, present and future // Biochim Biophys Acta. – 2011. – Vol. 1809. – P. 360-368.
8 He X.J., Chen T., Zhu J.K. Regulation and function of DNA methylation in plants and animals // Cell Res. – 2011. – Vol. 21. – P. 442-465.
9 Zhu J.K. Active DNA demethylation mediated by DNA glycosylases // Annu. Rev. Genet. – 2009. – Vol. 43. – P. 143-166.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases // Proc. Natl. Acad. Sci. U.S.A. – 2006. – Vol. 103. - P. 6853-6858.
11 Babiychuk E., Kushnir S., Van Montagu M., Inze D. The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun // Proc. Natl. Acad. Sci. U. S. A. – 1994. – Vol. 91. – P. 3299-3303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1 // Plant J. – 2011. – Vol. 68. – P. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L // PLoS One. – 2014. – Vol. 9. – P. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death // Plant Physiol. Biochem. – 2011. – Vol. 49. - P. 1155-1164.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles // Proc. Natl. Acad. Sci. U. S. A. – 2006. - Vol. 103. P. 2564-2569.
16 Baker M.A., He S.Q. Elaboration of cellular DNA breaks by hydroperoxides // Free Radic Biol Med. – 1991. - Vol. 11. – P. 563-572.
17 Gros L., Ishchenko A.A., Saparbaev M. Enzymology of repair of etheno-adducts // Mutat. Res. – 2003. – Vol. 531. – P. 219-229.
18 Hix S., Morais Mda S., Augusto O. DNA methylation by tert-butyl hydroperoxide-iron (II) // Free Radic Biol Med. – 1995. – Vol. 19. – P. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies // Chem Res Toxicol. – 2000. – Vol. 13. – P. 1056-1054.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli // DNA Repair (Amst). – 2002. - Vol. 1. P. 437-447.
21 Bradford M. M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding // Anal. Biochem. – 1976. – Vol. 72. – P. 248-254.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. Requirement for abasic endonuclease gene homologues in Arabidopsis seed development // PLoS One. – 2009. – Vol. 4. – P. e4297.
23 Foyer C.H., Noctor G. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiol. Plant. – 2003. – Vol. 119. – P. 355–364.
24 Jaruga P., Dizdaroglu M. 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1413-1425.
25 Brooks P.J. The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair // DNA Repair (Amst). – 2008. – Vol. 7. – P. 1168-1179.
References
1 Cadet J., Douki T., Gasparutto D., Ravanat J.L. (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res., vol. 531, pp. 5-23.
2 Krokan H.E., Bjoras M. (2013) Base excision repair. Cold Spring Harb. Perspect. Biol., vol. 5, pp. a012583.
3 Ischenko A.A., Saparbaev M.K. (2002) Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature, vol. 415, pp. 183-87.
4 Hitomi K., Iwai S., Tainer J.A. (2007) The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst), vol. 6, pp. 410-28.
5 Gros L., Ishchenko A.A., Ide H., Elder R.H., Saparbaev M.K. (2004) The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res., vol. 32, pp. 73-81.
6 Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. (2006) DNA repair and mutagenesis. ASM Press.
7 Vanyushin B.F., Ashapkin V.V. (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta., vol. 1809, pp. 360-68.
8 He X.J., Chen T., Zhu J.K. (2011) Regulation and function of DNA methylation in plants and animals. Cell Res., vol. 21, pp. 442-65.
9 Zhu J.K. (2009) Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet., vol. 43, pp. 143-66.
10 Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marin M.I., Martinez-Macias M.I., Ariza R.R., Roldan-Arjona T. (2006) Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. U.S.A., vol. 103, pp. 6853-58.
11 Babiychuk E., Kushnir S., Van Montagu M., Inze D. (1994) The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun. Proc. Natl. Acad. Sci. U. S. A., vol. 91, pp. 3299-303.
12 Cordoba-Canero D., Roldan-Arjona T., Ariza R.R. (2011) Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed by LIG1. Plant J., vol. 68, pp. 693-702.
13 Joldybayeva B., Prorok P., Grin I.R., Zharkov D.O., Ishenko A.A., Tudek B., Bissenbaev A.K., Saparbaev M. (2014) Cloning and Characterization of a Wheat Homologue of Apurinic/Apyrimidinic Endonuclease Ape1L. PLoS One, vol. 9, pp. e92963.
14 Bissenbaev A.K., Ishchenko A.A., Taipakova S.M., Saparbaev M.K. (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death. Plant Physiol. Biochem., vol. 49, pp. 1155-64.
15 Ishchenko A.A., Deprez E., Maksimenko A., Brochon J.C., Tauc P., Saparbaev M.K. (2006) Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles. Proc. Natl. Acad. Sci. U. S. A., vol. 103, pp. 2564-69.
16 Baker M.A., He S.Q. (1991) Elaboration of cellular DNA breaks by hydroperoxides. Free Radic Biol Med., vol. 11, pp. 563-72.
17 Gros L., Ishchenko A.A., Saparbaev M. (2003) Enzymology of repair of etheno-adducts. Mutat. Res. vol. 531, pp. 219-29.
18 Hix S., Morais Mda S., Augusto O. (1995) DNA methylation by tert-butyl hydroperoxide-iron (II). Free Radic Biol Med. vol. 19, pp. 293-301.
19 Hix S., Kadiiska M.B., Mason R.P., Augusto O. (2000) In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin trapping and DNA methylation studies. Chem Res Toxicol., vol. 13, pp. 1056-54.
20 Gasparutto D., Dherin C., Boiteux S., Cadet J. (2002) Excision of 8-methylguanine site-specifically incorporated into oligonucleotide substrates by the AlkA protein of Escherichia coli. DNA Repair (Amst), vol. 1, pp. 437-47.
21 Bradford M. M. (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem., vol. 72, pp. 248-54.
22 Murphy T.M., Belmonte M., Shu S., Britt A.B., Hatteroth J. (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development. PLoS One, vol. 4, pp. e4297.
23 Foyer C.H., Noctor G. (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant, vol. 119, pp. 355–64.
24 Jaruga P., Dizdaroglu M. (2008) 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst), vol. 7, pp. 1413-25.
25 Brooks P.J. (2008) The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair. DNA Repair (Amst), vol. 7, pp. 1168-79.
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Как цитировать
Taipakova, S. M., Smekenov, I. T., Kuanbay, A. K., Saparbayev, M. K., & Bissenbaev, A. K. (2018). Чувствительность arp–/– мутантных растений Arabidopsis thaliana к генотоксическим агентам. Вестник КазНУ. Серия биологическая, 73(4), 90–101. https://doi.org/10.26577/EB-2017-4-1305
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МОЛЕКУЛЯРНАЯ БИОЛОГИЯ И ГЕНЕТИКА
