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Физиология растений, 2023, T. 70, № 6, стр. 563-576

Пора неспецифической проницаемости (mPTP) в митохондриях растений и ее роль в гибели клеток

П. А. Буцанец a, *, Н. А. Шугаева a, А. Г. Шугаев a, **

a Федеральное государственное бюджетное учреждение науки Институт физиологии растений им. К.А. Тимирязева Российской академии наук
Москва, Россия

* E-mail: p.corbeau@list.ru
** E-mail: ag_shugaev@ifr.moscow

Поступила в редакцию 01.05.2023
После доработки 29.05.2023
Принята к публикации 29.05.2023

Аннотация

В обзоре изложены современные представления о строении, механизмах регуляции и функциональной роли поры неспецифической проницаемости (mPTP) во внутренней мембране митохондрий животных и растений. Приведены некоторые особенности, характеризующие функционирование mPTP в митохондриях растений и ее регуляцию под влиянием Са2+ и АФК. Суммированы имеющиеся в литературе доказательства, свидетельствующие об участии митохондрий в программируемой гибели клеток растений, в том числе благодаря индукции mPTP. Намечены направления дальнейших исследований mPTP в митохондриях растений.

Ключевые слова: Са2+/АФК-зависимая неспецифическая пора, F0F1-АТФ-синтаза, изменение проницаемости внутренней мембраны, мембранный потенциал, митохондрии, программируемая смерть клеток

Список литературы

  1. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death // Apoptosis. 2007. V. 12. P. 913. https://doi.org/10.1007/s10495-007-0756-2

  2. Giorgi C., Marchi S., Pinton P. The machineries, regulation and cellular functions of mitochondrial calcium // Nat. Rev. Mol. Cell Biol. 2018. V. 19. P. 713. https://doi.org/10.1038/s41580-018-0052-8

  3. Sies H., Jones D.P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents // Nat. Rev. Mol. Cell Biol. 2020. V. 21. P. 363. https://doi.org/10.1038/s41580-020-0230-3

  4. Hansen K.G., Herrmann J.M. Transport of proteins into mitochondria // Protein J. 2019. V. 38. P. 330. https://doi.org/10.1007/s10930-019-09819-6

  5. Giacomello M., Pyakurel A., Glytsou C., Scorrano L. The cell biology of mitochondrial membrane dynamics // Nat. Rev. Mol. Cell Biol. 2020. V. 21. P. 204. https://doi.org/10.1038/s41580-020-0210-7

  6. Rosencrans W.M., Rajendran M., Bezrukov S.M., Rostovtseva T.K. VDAC regulation of mitochondrial calcium flux: from channel biophysics to disease // Cell Calcium. 2021. V. 94:102356. https://doi.org/10.1016/j.ceca.2021.102356

  7. Hunter D.R., Haworth R.A. The Ca2+-induced membrane transition in mitochondria. I. The protective mechanisms // Arch. Biochem. Biophys. 1979. V. 195. P. 453. https://doi.org/10.1016/0003-9861(79)90371-0

  8. Haworth R.A., Hunter D.R. The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site // Arch. Biochem. Biophys. 1979. V. 195. P. 460. https://doi.org/10.1016/0003-9861(79)90372-2

  9. Hunter D.R., Haworth R.A. The Ca2+-induced membrane transition in mitochondria. III. Transitional Ca2+ release // Arch. Biochem. Biophys. 1979. V. 195. P. 468. https://doi.org/10.1016/0003-9861(79)90373-4

  10. Halestrap A.P. What is the mitochondrial permeability transition pore // J. Mol. Cell Cardiol. 2009. V. 46. P. 821. https://doi.org/10.1016/j.yjmcc.2009.02.021

  11. Bernardi P., Krauskopf A., Basso E., Petronilli V., Blalchy-Dyson E., Di Lisa F., Forte M.A. The mitochondrial permeability transition from in vitro artifact to disease target // FEBS J. 2006. V. 273. P. 2077. https://doi.org/10.1111/j.1742-4658.2006.05213.x

  12. Bernardi P., Rassola A., Forte M., Lippe G. The mitochondrial permeability transition pore: channel formation by F-ATP syntase, interaction in signal transduction, and role in pathophysiology // Physiol. Rev. 2015. V. 95. P. 1111. https://doi.org/10.1152/phyrev.00001.2015

  13. Bernardi P., Carraro M., Lippe G. The mitochondrial permeability transition: resent progress and open questions // FEBS J. 2022. V. 289. P. 7051. https://doi.org/10.1111/febs.162554

  14. Giorgio V., Guo L., Bassot C., Petronilli V., Bernardi P. Calcium and regulation of the mitochondrial permeability transition // Cell Calcium. 2018. V. 70. P. 56. https://doi.org/10.1016/j.ceca.2017.05.004

  15. Baines C.P. Loss of the cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death // Nature. 2005. V. 434. P. 658. https://doi.org/10.1038/nature03434

  16. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death // Physiol. Rev. 2007. V. 87. P. 99. https://doi.org/10.1152/physrev.00013.2006

  17. Tajeddine N. How do reactive oxygen species and calcium trigger mitochondrial membrane permeabilization? // Biochim. Biophys. Acta. 2016. V. 1860 P. 1079. https://doi.org/10.1016/j.bbagen.2016.02.013

  18. Bonora M., Giorgi C., Pinton P. Molecular mechanisms and consequences of mitochondrial permeability transition // Nat. Rev. Mol. Cell Biol. 2022. V. 23. P. 266. https://doi.org/10.1038/s41580-021-00433-y

  19. Kanno T., Sato E.E., Muranaka S., Fujita H., Fujiwara T., Utsumi T., Inoue M., Utsumi K. Oxidative stress underlies the mechanism for Ca2+-induced permeability transition of mitochondria // Free Radic. Res. 2004. V. 38. P. 27. https://doi.org/10.1080/10715760310001626266

  20. Martinez-Reyes I., Cuezva J.M. The H+-ATP synthase: a gate to ROS-mediated cell death ore survival // Biochim. Biophys. Acta. 2004. V. 1837. P. 1099. https://doi.org/10.1016/j.bbabio.2014.03.10

  21. Bernardi P. The mitochondrial permeability transition pore: a mystery solved? // Front. Physiol. 2013. V. 4. P. 95. https://doi.org/10.3389/fphys.2013.00095

  22. Ichas F., Mazat J.P. From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low– to high–conductance state // Biochim. Biophys. Acta. 1998. V. 1366 P. 33. https://doi.org/10.1016/S0005-2728(98)00119-4

  23. Petronilli V., Miotto G., Canton M., Brini M., Colonna R., Bernardi P., Di Lisa F. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence // Biophys. J. 1999. V. 76. P. 725. https://doi.org/10.1016/S0006-3495(99)77239-5

  24. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death // Cell. 2003. V. 112 P. 481. https://doi.org/10.1016/S0092-8674(03)00116-8

  25. Vianello A., Casolo V., Petrussa E., Peresson C., Patui S., Bertolini A., Passamonti S., Braidot E., Zancani M. The mitochondrial permeability transition pore (PTP) — an example of multiple molecular exaptation? // Biochim. Biophys. Acta. 2012. V. 1817. P. 2072. https://doi.org/10.1016/j.bbabio.2012.06.620

  26. Yoon Y., Lee H., Federico M., Sheu S.-S. Non-conventional mitochondrial permeability transition: its regulation by mitochondrial dynamics // Biochim. Biophys. Acta. 2023. V. 1864:148914. https://doi.org/10.1016/j.bbabio.2022.148914

  27. Leung A.W.C., Halestrap A.P. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore // Biochim. Biophys. Acta Bioenerg. 2008. V. 1777. P. 946. https://doi.org/10.1016/j.bbabio.2008.03.009

  28. Boyman L., Coleman A.K., Zhao G., Wescott A.P., Joca H.C., Greiser B.M., Karbowski M., Ward C.W., Lederer W.G. Dynamics of the mitochondrial permeability transition pore: transient and permanent opening events // Arch. Biochem. Biophys. 2019. V. 666. P. 31. https://doi.org/10.1016/j.abb.2019.03.016

  29. Hüser J., Blatter L.A. Fluctuations in mitochondrial membrane potential caused by repetitive gating of the permeability transition pore // Biochem J. 1999. V. 343. P. 311. https://doi.org/10.1042/bj3430311

  30. Bernardi P., Von Stockum S. The permeability transition pore as a Ca2+-release channel: new answers to an old question // Cell Calcium. 2012. V. 52. P. 22. https://doi.org/10.1016/j.ceca.2012.03.004

  31. Crompton M. The mitochondrial permeability transition pore and its role in cell death // J. Biochem. 1999. V. 341. P. 233. https://doi.org/10.1042/bj3410233

  32. Woodfield K., Rück A., Brdiczka D., Halestrap A.P. Direct demonstration of a specific interaction between cyclophiline-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition // Biochem. J. 1998. V. 336. P. 287. https://doi.org/10.1042/bj3360287

  33. Kokoszka J.E. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore // Nature. 2004. V. 427. P. 461. https://doi.org/10.1038/nature02229

  34. Gutiérrez-Aguilar M. Genetic manipulation of the cardiac mitochondrial phosphate carier does not affect permeability transition // J. Mol. Cell Cardiol. 2014. V. 72. P. 316. https://doi.org/10.1016/j.yjmcc.2014.04.008

  35. Giorgio V., Von Stockum S., Antoniel M., Fabbro A., Fogolari F., Forte M., Glick G.D, Petronilli V., Zoratti M., Szabó I., Lippe G., Bernardi P. Dimers of mitochondrial ATP synthase form the permeability transition pore // Proc. Natl. Acad. Sci. USA. 2013. V. 110. P. 5887. https://doi.org/10.1073/pnas.1217823110

  36. Alavian K.N., Beutner G., Lazrove E., Sacchetti S., Park H.A., Licznerski P., Li H., Nabili P., Hockensmith K., Graham M., Potter G.A. Jr., Jonas E.A. An uncoupling channel with the c–subunit ring of the F1F0–ATP synthase is the mitochondrial permeability transition pore // Proc. Natl. Acad. Sci. USA. 2014. V. 111 P. 10580. https://doi.org/10.1073/pnas.1401591111

  37. Bonora M., Morganti C., Morciano G., Pedriali G., Lebiedzinska-Arciszewska M., Aquila G., Giorgi C., Rizzo P., Campo G., Ferrari R., Kroemer G., Wieckowski M.R., Galluzzi L., Pinton P. Mitochondrial permeability transition involves dissociation of F1FO ATP synthase dimers and C-ring conformation // EMBO Rep. 2017. V. 18. P. 1077. https://doi.org/10.15252/embr.201643602

  38. Galber C., Minervini G., Cannino G., Boldrin F., Petronilli V., Tosatto S., Lippe G., Giorgio V. The f subunit of human ATP synthase is essential for normal mitochondrial morphology and permeability transition // Cell Rep. 2021. V. 35. P. 109. https://doi.org/10.1016/j.celrep.2021.109111

  39. Giorgio V., Burchel V., Schiavone M., Bassot C., Minervini G., Petronilli V., Argenton F., Forte M., Tosatto S., Lippe G., Bernardi P. Ca2+ binding to F- ATP synthase beta subunit triggers the mitochondrial permeability transition // EMBO Rep. 2017. V. 18. P. 1065. https://doi.org/10.15252/embr.201643354

  40. Karch J., Bround M.J., Khalil H., Sargent M.A., Latchman N., Terada N., Peixoto P.M., Molkentin J.D. Inhibition of mitochondrial permeability transition by deletion of the ANT family and CypD // Sci. Adv. 2019. V. 5. eaaw4597. https://doi.org/10.1126/sciadv.aaw4597

  41. Neginskaya M.A., Solesio M.E., Berezhnaya E.V., Amodeo G.F., Mnatsakanyan N., Jonas E.A., Pavlov E.V. ATP synthase c-subunit-deficient mitochondria have a small cyclosporine a-sensitive channel, but lack the permeability transition pore // Cell Rep. 2019. V. 26. P. 11. https://doi.org/10.1016/j.celrep.2018.12.033

  42. Carrer A., Tommasin L., Šileikytė J., Ciscato F., Filadi R., Urbani A., Forte M., Rasola A., Szabò I., Carraro M., Bernardi P. Defining the molecular mechanisms of the mitochondrial permeability transition through genetic manipulation of F-ATP synthase // Nat. Commun. 2019. V. 12:4835. https://doi.org/10.1038/s41467-021-25161-x

  43. Vianello A., Macri F., Braidot E., Mokhova E.N. Effect of cyclosporin A on energy coupling in pea stem mitochondria // FEBS Lett. 1995. V. 371. P. 258. https://doi.org/10.1016/0014-5793(95)00897-i

  44. Curtis M.J., Wolpert T.J. The victorine induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs witgout of membrane integrity // Plant J. 2004. V. 38. P. 244. https://doi.org/10.1111/j.1365-313X.2004.02040.x

  45. Fortes F., Castilho R.F., Catisti R., Carnieri E.G.S., Vercesi A.E. Ca2+ -induces a cyclosporin A-insensitive permeability transition pore in isolated potato tuber mitochondria mediated by reactive oxygen species // J. Bioenerg. Biomembr. 2001. V. 33. P. 43. https://doi.org/10.1023/a:1005672623709

  46. Arpagaus S., Rawyler A., Braendle R. Occurrence and characteristics of the mitochondrial permeability transition in plants // J. Biol. Chem. 2002. V. 277. P. 1780. https://doi.org/10.1074/jbc.M109416200

  47. Virolainen E., Blokhina O., Fagerstedt K. Ca2+-induced high amplitude swelling and cytochrome c release from wheat (Triticum aestivum L.) mitochondria under anoxic stress // Ann. Bot. 2002. V. 90. P. 509. https://doi.org/:10.1093/aob/mcf221

  48. Tiwari B.S., Belenghi B., Levine A. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death // Plant Physiol. 2002. V. 128. P. 1271. https://doi.org//10.1104/pp.010999

  49. Morimoto S., Tanaka Y., Sasaki K., Tanaka H., Fukamizu T., Shoyama Y., Shoyama Sh., Taura F. Identification and characterization of cannabinoids that induce cell death through mitochondrial permeability transition in Cannabis leaf cells // J. Biol. Chem. 2007. V. 282. P. 20739. https://doi.org/10.1074/jbc.M700133200

  50. Shugaev A.G., Butsanets P.A., Shugaeva N.A. Salicylic acid induces the proton conductance in the inner mitochondrial membrane of lupine cotyledons // Russ. J. Plant Physiol. 2016. V. 63. P. 727. https://doi.org/10.1134/S1021443716060091

  51. Romano P.G.N., Horton P., Gray J. The Arabidopsis cyclophilin gene family // Plant Physiol. 2004. V. 134. P. 1268. https://doi.org/10.1104/pp.103022160

  52. Mainali H.R., Chapman P., Dhaubhadel S. Genome-wide analysis of cyclophilin gen family in soybean (Glycine max) // BMC Plant Biol. 2014. V. 14. P. 282. https://doi.org/10.1186/s12870-014-0282-7

  53. De Coll V., Petrussa E., Casolo U., Braidot E., Filippi A., Peresson C., Patui S., Bertolini A., Giorgio V., Checchetto V., Vianello A., Bernardi P., Zancani M. Properties of the permeability transition of pea stem mitochondria // Front. Physiol. 2018. V. 9:1626. .https://doi.org/10.3389/fphys.2018.01626

  54. Shugaev A.G., Butsanets P.A., Shugaeva N.A. Ca2+-dependent regulation of proton permeability of the inner membrane in the mitochondria of lupine cotyledons // Russ. J. Plant Physiol. 2023. V. 70: 73. https://doi.org/10.1134/S1021443723700127

  55. Zancani M., Casolo V., Petrussa E.,Peresson C., Patui S., Bertolini A., De Coll V., Draidot E., Boscutti., Vianello A. The permeability transition in plant mitochondria: the missing link // Front. Plant. Sci. 2015. V. 6. P. 1120. https://doi.org/10.3389/fpls.2015.01120

  56. Vlot C.A., Depsey D.A., Klessig D.F. Salicylic acid a multifaceted hormone to combat disease // Annu. Rev. Phytopathol. 2009. V. 47. P. 177. https://doi.org/10.1146/annualrev.phyto.050908.135202

  57. Nie S., Yue H., Zhou J., Xing D. Mitochondrial-derived reactive oxygen species play a pivotal role in the salicylic acid signaling in Arabidopsis thaliana // Plos One. 2015. V. 10. e0119853. https://doi.org/10.1371/journal.pone.0119853

  58. Belt K., Huang S., Thatcher L.F., Casarotto H., Singh K.B., Van Aken O., Millar A.H. Salicylic acid-dependent plant stress signaling via mitochondrial succinate dehydrogenase // Plant Physiol. 2017. V. 173. P. 2029. https://doi.org/10.1104/pp.1600060

  59. Butsanets P.A., Shugaeva N.A., Shugaev A.G. Effect of melatonin and salicylic acid on ROS generation by mitochondria of lupine seedlings // Russ. J. Plant Physiol. 2021. V. 68. P. 745. https://doi.org/10.1134/S1021443721040038

  60. Alvares M.E. Salicylic acid in the machinery of hypersensitive cell death and disease resistance // Mol. Cell Biol. 2000. V. 44. P. 499. https://doi.org/10.1023/a:1026561029533

  61. Poore P. Effects of salicylic acid on the metabolism of mitochondrial reactive oxygen species in plants // Biomolecules. 2020. V. 10. P. 341. https://doi.org/10.3390/biom10020341

  62. Battaglia V., Salvi M., Toninello A. Oxidative stress is resposible for mitochondrail permeability tsansition induction by salicylate in liver mitochondria // J. Biol. Chem. 2005. V. 280. P. 33864. https://doi.org/10.1074/jbc.M502391200

  63. Arnao M.B., Hernandes-Ruis J. Functions of melatonin in plants: a review //J. Pineal. Res. 2015. V. 59. P. 133. https://doi.org/10.1111/jpi.12253

  64. Khanna K., Bhardwaj R., Ahmad P., Reiter R. Phytomelatonin: a master regulator for plant oxidative stress management // Plant Physiol. Biochem. 2023. V. 196. P. 260. https://doi.org/10.1016/j.plaphy.2023.01.035

  65. Hu C.-H., Zheng Y., Tong C.-L., Zhang D.-J. Effects of exogenous melatonin on plant growth, root hormones and photosynthetic characteristics of trifoliate orange subjected to salt stress // Plant Growth Regul. 2022. V. 97. P. 551. https://doi.org/10.1007/s10725-022-00814-z

  66. Kobylinska A., Reiter R., Postmyk M. Melatonin protects cultured tobacco cells against lead-induced cell death via inhibition of cytochrome c translocation // Front. Plant Sci. 2017. V. 14: 1560. https://doi.org/10.3389/fpls.2017.01560

  67. Wang P., Sun X., Wang N., Tan D.-X., Ma F. Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings // J. Pineal. Res. 2015. V. 58. P. 479. https://doi.org/10.1111/jpi.12233

  68. Hibaoui Y., Roulet E., Ruegg U.T. Melatonin prevents oxidative stress-mediated mitochondrial permeability transition and death in skeletal muscle cells // J. Pineal Res. 2009. V. 47. P. 238. https://doi.org/j.1600-079X.2009.00707

  69. Jou M.-J., Peng T.-I., Reiter R.J. Protective stabilization of mitochondrial permeability transition and mitochondrial oxidation during mitochondrial Ca2+ stress by melatonin’s cascade metabolites C3-OHM and AFMK in RBA1 astrocytes // J. Pineal Res. 2018. V. 66. e12538. https://doi.org/10.1111/jpi.12538

  70. Van Doom W.G., Woltering E. Many ways to exit? Cell death categories in plants // Trends Plant Sci. 2005. V. 10. P. 117. https://doi.org/10.1016/j.tplants.2005.01.006

  71. Wang P., Mugume Y., Bassman D.C. New advaces in autophagy in plants: regulation, selectivity and function // Sem. Cell Develop. Biol. 2018. V. 80. P. 133. https://doi.org/10.1016/j.semcdb.2017.07.018

  72. Bock F.J., Tait S.W. Mitochondria as multifaceted regulator of cell death // Nat. Rev. Mol. Cell Biol. 2020. V. 21. P. 85. https://doi.org/10.1038/s41580-019-0173-8

  73. Chu Q., Gu X., Zheng Q., Wang J., Zhu H. Mitochondrial mechanisms of apoptosis and necrosis in liver diseases // Anal. Cell. Pathol. 2021. V. 2021: 8900122. https://doi.org/10.1155/2021/8900122

  74. Minina E.A., Dauphinee A.N., Ballhaus F., Gogvadze V., Stemenko A.P., Bozhkov P.V. Apoptosis is not conserved in plants as revealed by critical examination of model for plant apoptosis-like cell death // BMC Biology. 2021. V. 19: 100. https://doi.org/10.1185/s12915-021-01018-z

  75. Dickman M., Williams B., Li Y., Figuieiredo P., Wolpert T. Reassessing apoptosis in plant // Nat. Plants. 2017. V. 3. P. 773. https://doi.org/10/1038/s4147-017-0020-x

  76. Jones A. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? // Trends Plant Sci. 2000. V. 5. P. 225. https://doi.org/10.1016/s1360-1380(00)01605-8

  77. Vianello A., Zancani M., Peresson C., Petrussa E., Casolo V., Krajnakova J., Patui S., Braidot E., Macri F. Plant mitochondrial pathway leading to programmed cell death // Physiol. Plant. 2007. V. 129. P. 242. https://doi.org/10.1111/j.1399-3054.2006.00767.x

  78. Reape T.J., McCabe P.F. Apoptotic-like regulation of programmed cell death in plants // Apoptosis. 2010. V. 15. P. 249. https://doi.org/10.1007/s10495-009-0447-2

  79. Van Aken O., Van Breusegem F. Licensed to kill: mitochondria, chloroplasts, and cell death // Trends Plant Sci. 2015. V. 20. P. 754. https://doi.org/10.1016/j.tplants.2015.08.002

  80. Gutierrez-Aguilar M. Mitochondrial calcium transport and permeability transition as rational targets for plant protection // Biochim. Biophys. Acta. 2020. V. 1861. P. 148. https://doi.org/10.1016/j.bbabio.2020.148288

  81. Yu X.H., Perdue T.D., Heimer Y.M., Jones A.M. Mitochondrial involvement in tracheary element programmed cell death // Cell Death Differ. 2002. V. 9. P. 189. https://doi.org/10.1038/sj.cdd.4400940

  82. Vacca R.A., Valenti D., Bobba A., Merafina R.S., Passarella S., Marra E. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Brigth-Yellow 2 cells en route to heat shock-induced cell death // Plant Physiol. 2006. V. 141. P. 208. https://doi.org/10.1104/pp.106.078683

  83. Lin J., Wang Y., Wang G. Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive by reactive oxygen species and mitochondrial permeability transition pore status // J. Plant Physiol. 2006. V. 163. P. 731. https://doi.org/10.1016/j.jplph.2005.06.016

  84. Gao C., Xing D., Li L., Zang L. Implication of reactive oxygen species and mitochondrial disfunction in the early stages of programmed cell death induced by ultraviolet-C overexposure // Planta. 2008. V. 227. P. 755. https://doi.org/10.1007/s00425-007-0654-4

  85. Stein J.C., Hansen G.M. Mannose induces an endonuclease responsible for DNA laddering in plant cells // Plant Physiol. 1999. V. 121. P. 71. https://doi.org/1104/pp.121.1.71

  86. Yao N., Eisfelder B.J., Marvin J., Greenberg J.T. The mitochondria: an organelle commonly involved in programmed cell death in Arabidopsis thaliana // Plant J. 2004. V. 40. P. 1803. https://doi.org/10.1111/j.1365-313X.2004.02239.x

  87. Garcia-Heredia L.M., Hervas M., De la Rosa M.A., Navaro J.A. Acetylsalicylic acid induced programmed death in Arabidopsis cell cultures // Planta. 2008. V. 228. P. 89. https://doi.org/10.1007/s00425-008-0721-5

  88. Krause M., Durner J. Harpin inactivates mitochondria in Arabidopsis suspension cells // Mol. Plant Microbe Interact. 2004. V. 17. P. 131. https://doi.org/10.1094/MPMI.2004.17.2.131

  89. Amirsadeghi S., Robson C., Vanlerberghe G.C. The role of the mitochondria in plant responses to biotic stress // Physiol. Plant. 2007. V. 129. P. 253. https://doi.org/10.1111/j.1399-3054.2006.00775.x

  90. Mur L.A., Kenton P., Lloyd A.J., Ougham H., Prats E. The hypersensitive response: the centenary is upon us but much do me know? // J. Exp. Bot. 2008. V. 59. P. 501. https://doi.org/10.1093/jxb/erm239

  91. Colombatti F., Gonzales D.H., Welchen E. Plant mitochondria under pathogen attack: a sigh of relief or a last breath? // Mitochondrion. 2014. V. 19. P. 238. https://doi.org/10/1016/j.mito.2014.03.006

  92. Salvesen G.S., Hempel A., Coll N.S. Protease signaling in animal and plant-regulated cell death // FEBS J. 2016. V. 238. P. 2577. https://doi.org/10.1111/febs.13616

  93. Buono A.R., Hudecek R., Nowack M.K. The roles of proteases during developmental programmed cell death in plant // J. Exp. Bot. 2019. V. 70. P. 2097. https://doi.org/10.1093/jxb/erz072

  94. Martinez-Fabregas J., Diaz-Moreno I., Gonzales-Arzola K., Janocha S., Navarro J.A., Hervás M., Bernhardt R., Díaz-Quintana A., De la Rosa M.Á. New Arabidopsis thaliana cytochrome c partners: a look into the elusive role of cytochrome c in Programmed Cell Death in plants // Mol. Cell Proteomics. 2013. V. 12. P. 3666. https://doi.org/10.1074/mcp.M113.030692

  95. Elena-Real C.A., Gonzalez-Arzola K., Peres-Mejias G., Diaz-Quintana A., Velazquez-Campoy A., Desvoyes B., Gutierez C., De la Rosa M.A., Diaz-Moreno I. Proposed mechanism for regulation of H2O2-induced programmed cell death in plants by binding cytochrome c to 14-3-3 proteins // Plant J. 2021. V. 106. P. 74. https://doi.org/10.1111/tpj.15146

  96. Kawai-Yamada M., Ohori Y., Uchimiya H. Dissection of Arabidopsis Bax inhibitor -1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death // Plant Cell. 2004. V. 16. P. 21. https://doi.org/10.1105/tpc.014613

  97. Watanabe N., Lam E. Recent advance in the study of caspase- ike proteases and Bax inhibitor 1 in plants: their possible role as regulator of programmed cell death // Mol. Plant Patol. 2004. V. 5. P. 65. https://doi.org/10.1111/1364-3703-2004-00206

  98. Lord C.E.N., Gunawardena A.H.L.A.N. Programmed cell death in C. elegans, mammals and plants // Eur. J. Cell Biol. 2012. V. 91. P. 603. https://doi.org/10.1016/j.ejcb.2012.02.002

  99. De Marchi E., Bonora M., Giorgi C., Pinton P. The mitochondrial permeability transition pore is a dispensable element for mitochondrial calcium efflux // Cell Calcium. 2014. V. 56. P. 1. https://doi.org/10.1016/j.ceca.2014.03.004

  100. Carraretto L., Checchetto V., De Bortoli S., Formentin E., Costa A., Szabo I., Teardo E. Calcium flux across plant mitochondrial membranes: possible molecular players // Front. Plant Sci. 2016. V. 7: 354. https://doi.org/10.3389/fpls.2016.00354

  101. Bozhkov P.V. Plant autophagy mechanisms and function // J. Exp. Bot. 2018. V. 69. P. 1281. https://doi.org/10.1093/jxb/ery070

  102. Broda M., Millar A. H., Van Aken O. Mitophagy: a mechanism for plant growth and survival // Trend Plant Sci. 2018. V. 23. P. 434. https://doi.org/10.1016/j.plants.2018.02.010

  103. Ren K., Feng L., Sun S., Zhuang X. Plant mitophagy in comparison to mammals: what is still missing? // Int. J. Mol. Sci. 2021. V. 22. P. 1236. https://doi.org/10.3390/ijms22031236

  104. Kumar R., Reichert A.S. Common principles and specific mechanisms of mitophagy from yeast to humans // Int. J. Mol. Sci. 2021. V. 22. P. 4363. https://doi.org/10.3390/ijms22094363

  105. Ye C., Zheng S., Jiang D., Lu J., Huang Z., Liu Z., Zhou H., Zhuang H., Li J. Initiation and execution of programmed cell death and regulation of reactive oxygen species in plants // Int. J. Mol. Sci. 2021. V. 22. P. 12942. https://doi.org/10.3390/ijms.222312942

  106. Lord C.E.N., Weitman J.N., Lane S., Gunawardena A.H. Do mitochondria play a role in remodeling lace plant leaves during programmed cell death? // BMC Plant Biol. 2011. V. 11. P. 102. https://doi.org/10.1186/1471-2229-11-102

  107. Weitman J., Lord E.N., Dauphinee, Gunawardena A.H. The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves // BMC Plant Biol. 2012. V. 12. P. 115. https://doi.org/10.1186/1471-2229-12-115

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