Са2+-проницаемые катионные каналы плазматической мембраны клеток высших растений

  • Вера Сергеевна Мацкевич Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь
  • Вероника Валерьевна Самохина Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь
  • Полина Вацлавовна Гриусевич Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь
  • Мария Аркадьевна Войтехович Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь
  • Анатолий Иосифович Соколик Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь
  • Вадим Викторович Демидчик Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь; Ботанический институт им. В. Л. Комарова РАН, ул. Профессора Попова, 2, 197376, г. Санкт-Петербург, Россия

Аннотация

Кальций (Ca2+) является важным структурным элементом, регулятором метаболических процессов, а также универсальным для живых систем сигнальным агентом-посредником, обеспечивающим взаимосвязь между мембранными рецепторами и генетической экспрессией. Важнейшим феноменом, определяющим сигнально-регуляторную функцию Ca2+, выступает его транспорт через плазматическую мембрану и эндомембраны клетки. Ключевую роль в процессах транспорта Са2+ играют катионные каналы, локализованные во всех мембранах растительной клетки. Биоинформационный анализ катионпроницаемых ионных каналов растений не обнаружил в них наличия Ca2+-селективных фильтров, схожих с аналогичными системами у животных. Тем не менее мембраны растений обнаруживают Ca2+-проводимости, т. е. обладают проницаемостью к Са2+. Биофизические характеристики Ca2+-проводимостей растений детально изучены и в последнее время дополнены молекулярно-генетическим анализом. Продемонстрировано, что Ca2+-проводимость растений опосредуется несколькими типами неселективных катионных каналов, кодируемых соответствующими семействами генов, в частности каналами, активируемыми циклическими нуклеотидами, ионотропными глутаматными рецепторами, двупоровым каналом 1, аннексинами и несколькими семействами механочувствительных ионных каналов. Накоплен широкий пласт результатов, указывающих на то, что восприятие внешних факторов среды (температура, гравитация, механическое и химическое воздействие), гормональная сигнализация и везикулярный транспорт связаны с активностью отдельных субъединиц данных ионных каналов.

Биографии авторов

Вера Сергеевна Мацкевич, Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь

аспирантка кафедры клеточной биологии и биоинженерии растений биологического факультета. Научный руководитель – В. В. Демидчик

Вероника Валерьевна Самохина, Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь

аспирантка кафедры клеточной биологии и биоинженерии растений биологического факультета. Научный руководитель – А. И. Соколик

Полина Вацлавовна Гриусевич, Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь

магистрант кафедры клеточной биологии и биоинженерии растений биологического факультета. Научный руководитель – В. В. Демидчик

Мария Аркадьевна Войтехович, Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь

аспирантка кафедры клеточной биологии и биоинженерии растений биологического факультета. Научный руководитель – В. В. Демидчик

Анатолий Иосифович Соколик, Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь

кандидат биологических наук; заведующий научно-исследовательской лабораторией физиологии и биотехнологии растений, доцент кафедры клеточной биологии и биоинженерии растений, заместитель
декана по научно-исследовательской работе биологического факультета

Вадим Викторович Демидчик, Белорусский государственный университет, пр. Независимости, 4, 220030, г. Минск, Республика Беларусь; Ботанический институт им. В. Л. Комарова РАН, ул. Профессора Попова, 2, 197376, г. Санкт-Петербург, Россия

доктор биологических наук, доцент; заведующий кафедрой клеточной биологии и биоинженерии растений биологического факультета БГУ; ведущий научный сотрудник лаборатории молекулярной и экологической физиологии  Ботанического института им. В. Л. Комарова РАН
 

Литература

  1. Marschner H. Marschner’s Mineral Nutrition of Higher Plants. 3rd edn. London: Academic Press; 2012.
  2. Demidchik V, Maathuis FJ. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. Tansley Review. New Phytologist. 2007;175(3):387– 404. DOI: 10.1111/j.1469-8137.2007.02128.x.
  3. Dodd AN, Kudla J, Sanders D. The language of calcium signalling. Annual Review of Plant Biology. 2010;61:593– 620. DOI: 10.1146/annurev-arplant-070109-104628.
  4. Hedrich R. Ion channels in plants. Physiological Reviews. 2012;92(4):1777–1811. DOI: 10.1152/physrev.00038.2011.
  5. Swarbreck SM, Colaço R, Davies JM. Plant calcium-permeable channels. Plant Physiology. 2013;163(2):514–522. DOI: 10.1104/pp.113.220855.
  6. Demidchik V, Shabala S. Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated «ROS-Ca2+ Hub». Functional Plant Biology. 2018;45:9–27. DOI: 10.1071/FP16420.
  7. Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM. The evolution of calcium-based signalling in plants. Current Biology. 2017;27(13):667–679. DOI: 10.1016/j.cub.2017.05.020.
  8. White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM. Genes for calcium-permeable channels in the plasma membrane of lant root cells. Biochimica et Biophysica Acta Biomembranes. 2002;1564(2):299 –309. DOI: 10.1016/S0005-2736(02)00509-6.
  9. Demidchik V, Davenport RJ, Tester MA. Nonselective cation channels in plants. Annual Review of Plant Biology. 2002;53:67–107. DOI: 10.1146/annurev.arplant.53.091901.161540.
  10. Demidchik V. Characterisation of root plasma membrane Ca2+-permeable cation channels: techniques and basic concepts. In: Volkov AG (ed.) Plant Electrophysiology. Heidelberg: Springer; 2012.
  11. Miedema H, Demidchik V, Véry AA, Bothwell JH, Brownlee C, Davies JM. Two voltage-dependent calcium channels coexist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytologist. 2008;179(2):378–385. DOI: 10.1111/j.1469-8137.2008.02465.x.
  12. Straltsova D, Chykun P, Subramaniam S, Sosan A, Kolbanov D, Sokolik A, et al. Cation channels are involved in brassinosteroid signalling in higher plants. Steroids. 2015;97:98–106. DOI: 10.1016/j.steroids.2014.10.008.
  13. Gao QF, Gu LL, Wang HQ, Fei CF, Fang X, Hussain J, et al. Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proceedings of the National Academy Sciences of the United States of America. 2016;113(11):3096 –3101. DOI: 10.1073/pnas.1524629113.
  14. Tapken D, Anschütz U, Liu LH, Huelsken T, Seebohm G, Becker D, et al. A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids. Science Signaling. 2013;6(279):ra47. DOI: 10.1126/scisignal.2003762.
  15. Davenport R. Glutamate receptors in plants. Annals of Botany. 2002;90(5):549–557. DOI: 10.1093/aob/mcf228.
  16. Demidchik V, Adobea P, Tester MA. Glutamate activates sodium and calcium currents in the plasma membrane of Arabidopsis root cells. Planta. 2004;219:167–175.
  17. Carraretto L, Checchetto V, De Bortoli S, Formentin E, Costa A, Szabó I, et al. Calcium flux across plant mitochondrial membranes: possible molecular players. Frontiers in Plant Science. 2016;7:354. DOI: 10.3389/fpls.2016.00354.
  18. Zhang WH, Walker NA, Tyerman SD, Patrick JW. Fast activation of a time-dependent outward current in protoplasts derived from coats of developing Phaseolus vulgaris seeds. Planta. 2000;211(6):894 – 898. DOI: 10.1007/s004250000391.
  19. Sosan A, Svistunenko D, Straltsova D, Tsiurkina K, Smolich I, Lawson T, et al. Engineered silver nanoparticles are sensed at the plasma membrane and dramatically modify physiology of Arabidopsis thaliana plants. The Plant Journal. 2016;85(2):245–257. DOI: 10.1111/tpj.13105.
  20. Arranz-Tagarro JA, de los Ríos C, García AG, Padín JF. Recent patents on calcium channel blockers: emphasis on CNS diseases. Expert Opinion on Therapeutic Patents. 2014;24(9):959 – 977. DOI: 10.1517/13543776.2014.940892.
  21. Zepeda-Jazo I, Velarde-Buendia AM, Enriquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, et al. Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiology. 2011;157(4):2167–2180. DOI: 10.1104/pp.111.179671.
  22. Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O. Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. Journal of experimental botany. 2014;65(5):1271–1283. DOI: 10.1093/jxb/ert423.
  23. Görlach A, Bertram K, Hudecova S, Krizanova O. Calcium and ROS: a mutual interplay. Redox BiolOGY. 2015;6:260 –271. DOI: 10.1016/j.redox.2015.08.010.
  24. Demidchik V, Shabala SN, Davies JM. Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. The Plant Journal. 2007;49(3):377–386. DOI: 10.1111/j.1365-313X.2006.02971.x.
  25. Véry AA, Davies JM. Hyperpolarisation-activated calcium channels at the tip of Arabidopsis root hairs. Proceedings of the National Academy Sciences of the United States of America. 2000;97(17):9801– 9806. DOI: 10.1073/pnas.160250397.
  26. Jammes F, Hu HC, Villiers F, Bouten R, Kwak JM. Calcium-permeable channels in plant cells. The FEBS Journal. 2011;278(22):4262– 4276. DOI: 10.1111/j.1742-4658.2011.08369.x.
  27. DeFalco TA, Moeder W, Yoshioka K. Opening the gates: insights into cyclic nucleotide-gated channel-mediated signalling. Trends in Plant Science. 2016;21(11):903–906. DOI: 10.1016/j.tplants.2016.08.011.
  28. Jha SK, Sharma M, Pandey GK. Role of cyclic nucleotide gated channels in stress management in plants. Current Genomics. 2016;17(4):315–329. DOI: 10.2174/1389202917666160331202125.
  29. Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJ. Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a nonselective ion transporter involved in germination and cation transport. Journal of Experimental Botany. 2006:57(4):791– 800.
  30. Charpentier M, Sun J, Vaz Martins T, Radhakrishnan GV, Findlay K, Soumpourou E, et al. Nuclear-localized cyclic nucleotidegated channels mediate symbiotic calcium oscillations. Science. 2016;352(6289):1102–1105. DOI: 10.1126/science.aae0109.
  31. Gao QF, Fei CF, Dong JY, Gu Li-Li, Wang Y.-F. Arabidopsis CNGC18 is a Ca2+-permeable channel. Molecular Plant. 2014;7:739 –743. DOI: 10.1093/mp/sst174.
  32. Zhou L, Lan W, Jiang Y, Fang W, Luan S. A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Molecular Plant. 2014;7(2):369–376. DOI: 10.1093/mp/sst125.
  33. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, et al. Death don’t have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel 2 and innate immunity. The Plant Cell. 2007;19(3):1081–1095. DOI: 10.1105/tpc.106.045096.
  34. Lu M, Zhang Y, Tang S, Pan J, Yu Y, Han J, et al. AtCNGC2 is involved in jasmonic acid-induced calcium mobilisation. Journal of Experimental Botany. 2016;67(3):809–819. DOI: 10.1093/jxb/erv500.
  35. Gao F, Han X, Wu J, Zheng S, Shang Z, Sun D, et al. A heat-activated calcium-permeable channel – Arabidopsis cyclic nucleotide-gated ion channel 6 – is involved in heat shock responses. The Plant Journal. 2012;70(6):1056 –1069. DOI: 10.1111/j.1365-313X.2012.04969.x.
  36. Shih HW, DePew CL, Miller ND, Monshausen GB. The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana. Current Biology. 2015;25(23):3119–3125. DOI: 10.1016/j.cub.2015.10.025.
  37. Wang YF, Munemasa S, Nishimura N, Ren HM, Robert N, Han M, et al. Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. Plant Physiology. 2013;163(2):578–590. DOI: 10.1104/pp.113.225045.
  38. Ben-Johny M, Dick IE, Sang L, Limpitikul WB, Kang PW, Niu J, et al. Towards a unified theory of calmodulin regulation of voltage-gated calcium and sodium channels. Current Molecular Pharmacology. 2015;8(2):188–205. PMCID: PMC4960983.
  39. Mori IC, Schroeder JI. Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiology. 2004;135(2):702–708. DOI: 0.1104/pp.104.042069.
  40. Linse S, Helmersson A, Forsén S. Calcium binding to calmodulin and its globular domains. Journal of Biological Chemistry.1991;266(13):8050 – 8054. PMID: 1902469.
  41. Liang H, DeMaria CD, Erickson MG, Mori MX, Alseikhan BA, Yue DT. Unified mechanisms of Ca2+ regulation across the Ca2+ channel family. Neuron. 2003;39(6):951–960. DOI: 10.1016/S0896-6273(03)00560-9.
  42. Demidchik V, Bowen HC, Maathuis FJM, Shabala SN, Tester MA, White PJ, et al. Arabidopsis thaliana root nonselective cation channels mediate calcium uptake and are involved in growth. The Plant Journal. 2002;32(5):799–808. DOI: 10.1046/j.1365-313X.2002.01467.x.
  43. Köhler C, Merkle T, Neuhaus G. Characterisation of a novel gene family of putative cyclic nucleotide- and calmodulin-regulated ion channels in Arabidopsis thaliana. The Plant Journal. 1999;18(1):97–104. DOI: 10.1046/j.1365-313X.1999.00422.x.
  44. Köhler C, Neuhaus G. Characterisation of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. FEBS Letters. 2000;471(2–3):133–136. DOI: 10.1016/S0014-5793(00)01383-1.
  45. Fischer C, DeFalco TA, Karia P, Snedden WA, Moeder W, Yoshioka K, et al. Calmodulin as a Ca2+-sensing subunit of Arabidopsis cyclic nucleotide-gated channel complexes. Plant and Cell Physiology. 2017;58(7):1208 –1221. DOI: 10.1093/pcp/pcx052.
  46. Fischer C, Kugler A, Hoth S, Dietrich P. An IQ domain mediates the interaction with calmodulin in a plant cyclic nucleotide-gated channel. Plant and Cell Physiology. 2013;54(4):573–584. DOI: 10.1093/pcp/pct021.
  47. DeFalco TA, Marshall CB, Munro K, Kang HG, Moeder W, Ikura M, et al. Multiple calmodulin-binding sites positively and negatively regulate Arabidopsis cyclic nucleotide-gated channel. The Plant Cell. 2016;28(7):1738 –1751. DOI: 10.1105/tpc.15.00870.
  48. Forde BG, Roberts MR. Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defence? F1000Prime Reports. 2014;6:37. DOI: 10.12703/P6-37.
  49. Forde BG. Glutamate signalling in roots. Journal of Experimental Botany. 2014;65(3):779–787. DOI: 10.1093/jxb/ert335.
  50. Weiland M, Mancuso S, Baluska F. Signalling via glutamate and GLRs in Arabidopsis thaliana. Functional Plant Biology. 2015;43(1):1–25. DOI: 0.1071/FP15109.
  51. Lam H-M, Chiu J, Hsieh M-H, Meisel L, Oliveira IC, Shin M, et al. Glutamate receptor genes in plants. Nature. 1998;396(6707):125–126. DOI: 10.1038/24066.
  52. Aouini A, Matsukura C, Ezura H, Asamizu E. Characterisation of 13 glutamate receptor-like genes encoded in the tomato genome by structure, phylogeny and expression profiles. Gene. 2012;493(1):36 – 43. DOI: 10.1016/j.gene.2011.11.037.
  53. Ni J, Yu Z, Du G, Zhang Y, Taylor JL, Shen C, et al. Heterologous expression and functional analysis of rice glutamate receptor-like family indicates its role in glutamate triggered calcium flux in rice roots. Rice. 2016;9(1):9. DOI: 10.1186/s12284-016-0081-x.
  54. Chiu J, Desalle R, Lam HM, Meisel L, Coruzzi G. Molecular evolution of glutamate receptors: a primitive signaling mechanism that existed before plants and animals diverged. Molecular biology and evolution. 1999;16(6):826 – 838. DOI: 10.1093/oxfordjournals.molbev.a026167.
  55. Price MB, Kong D, Okumoto S. Inter-subunit interactions between glutamate-like receptors in Arabidopsis. Plant Signaling & ehavior. 2013;8(12):27–34. DOI: 10.4161/psb.27034.
  56. Roy SJ, Gilliham M, Berger B, Essah PA, Cheffings C, Miller AJ, et al. Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant, Cell & Environment. 2008;31(6):861– 871. DOI: 10.1111/j.1365-3040.2008.01801.x.
  57. Lohaus G, Winter H, Riens B, Heldt HW. Further studies of the phloem loading process in leaves of barley and spinach – the comparison of metabolite concentrations in the apoplastic compartment with those in the cytosolic compartment and in the sieve tubes. Botanica Acta. 1995;108(3):270 –275. DOI: 10.1111/j.1438-8677.1995.tb00860.x.
  58. Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Hermann Muehling K. Is the infiltration-centrifugation technique appropriate for the isolation of apoplastic fluid? A critical evaluation with different plant species. Physiologia Plantarum. 2001;111(4):457– 465. DOI: 10.1034/j.1399-3054.2001.1110405.x.
  59. Dennison KL, Spalding EP. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiology. 2000;124(4):1511–1514. PMID: 11115867.
  60. Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM. A role for glycine in the gating of plant NMDA-like receptors. The Plant Journal. 2003;35(6):800 – 810. DOI: 10.1046/j.1365-313X.2003.01849.x.
  61. Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho J, et al. Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science. 2011;332(6028):434 – 437. DOI: 10.1126/science.1201101.
  62. Vincill ED, Bieck AM, Spalding EP. Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiology. 2012;159(1):40 – 46. DOI: 10.1104/pp.112.197509.
  63. Qi Z, Stephens NR, Spalding EP. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiology. 2006;142(3):963–971. DOI: 10.1104/pp.106.088989.
  64. Singh SK, Chien CT, Chang IF. The Arabidopsis glutamate receptor-like gene GLR3.6 controls root development by repressing the Kip-related protein gene KRP4. Journal of Experimental Botany. 2016;67(6):1853–1869. DOI: 10.1093/jxb/erv576.
  65. Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, et al. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature. 2005;434(7031):404 – 408. DOI: 10.1038/nature03381.
  66. Hedrich R, Marten I. TPC1-SV channels gain shape. Molecular Plant. 2011;4(3):428– 441. DOI: 10.1093/mp/ssr017.
  67. Dadacz-Narloch B, Kimura S, Kurusu T, Farmer EE, Becker D, Kuchitsu K, et al. On the cellular site of two-pore channel TPC1 action in the Poaceae. New Phytologist. 2013;200(3):663– 674. DOI: 10.1111/nph.12402.
  68. Patel S, Cai X. Evolution of acidic Ca2+ stores and their resident Ca2+-permeable channels. Cell Calcium. 2015;57(3):222–230. DOI: 10.1016/j.ceca.2014.12.005.
  69. Pottosin I, Wherrett T, Shabala S. SV channels dominate the vacuolar Ca2+ release during intracellular signalling. FEBS Letters. 2009;583(5):921– 926. DOI: 10.1016/j.febslet.2009.02.009.
  70. Gilliham M, Anthman A, Tyerman SD, Conn SJ. Cell-specific compartmentation of mineral nutrients is an essential mechanism for optimal plant productivity – another role for TPC1? Plant Signaling & Behavior. 2011;6(11):1656 –1661. DOI: 10.4161/psb.6.11.17797.
  71. Pottosin I, Dobrovinskaya O. Non-selective cation channels in plasma and vacuolar membranes and their contribution to K+ transport. Journal of Plant Physiology. 2014;171(9):732–742. DOI: 10.1016/j.jplph.2013.11.013.
  72. Guo J, Zeng W, Jiang Y. Tuning the ion selectivity of two-pore channels. PNAS. 2017;114(5):1009 –1014. DOI: 10.1073/pnas.1616191114.
  73. Johannes E, Sanders D. Lumenal calcium modulates unitary conductance and gating of a plant vacuolar calcium release channel. Journal of Membrane Biology. 1995;146(2):211–224. DOI: 10.1007/BF00238010.
  74. Pottosin II, Dobrovinskaya OR, Muñiz J. Conduction of monovalent and divalent cations in the slow vacuolar channel. Journal of Membrane Biology. 2001;181(1):55 – 65. DOI: 10.1007/s0023200100073.
  75. Guo J, Zeng W, Chen Q, Lee C, Chen L, Yang Y, et al. Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature. 2016;531:196 –201.
  76. Pottosin II, Schönknecht G. Vacuolar calcium channels. Journal of Experimental Botany. 2007;58(7):1559 –1569. DOI: 10.1093/jxb/erm035.
  77. Lizarbe MA, Barrasa JI, Olmo N, Gavilanes F, Turnay J. Annexin-phospholipid interactions. Functional implications. International Journal of Molecular Sciences. 2013;14(2):2652–2683. DOI: 10.3390/ijms14022652.
  78. Konopka-Postupolska D, Clark G. Annexins as overlooked regulators of membrane trafficking in plant cells. International Journal of Molecular Sciences. 2017;18(4):863. DOI: 10.3390/ijms18040863.
  79. Brazier SP, Telezhkin V, Kemp PJ. Functional Interactions between BKCaa-subunit and annexin A5: implications in apoptosis. Oxidative Medicine and Cellular Longevity. 2016;2016:1–9. DOI: 10.1155/2016/1607092.
  80. Xu L, Tang Y, Gao S, Su S, Hong L, Wang W, et al. Comprehensive analyses of the annexin gene family in wheat. BMC Genomics. 2016;17:415. DOI: 10.1186/s12864-016-2750-y.
  81. Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, et al. Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+-permeable conductance. The Plant Cell. 2009;21(2):479– 493. DOI: 10.1105/tpc.108.059550.
  82. Laohavisit A, Richards SL, Shabala L, Chen C, Colaço RD, Swarbreck SM, et al. Salinity-induced calcium signaling and root adaptation in Arabidopsis require the calcium regulatory protein annexin1. Plant Physiology. 2013;163(1):253–262. DOI: 10.1104/pp.113.217810.
  83. Isayenkov S, Isner JC, Maathuis FJ. Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Letters. 2010;584(10):1982–1988. DOI: 10.1016/j.febslet.2010.02.050.
  84. Isayenkov S, Isner JC, Maathuis FJ. Membrane localisation diversity of TPK channels and their physiological role. Plant Signaling & Behavior. 2011;6(8):1201–1204. DOI: 10.4161/psb.6.8.15808.
  85. Hamilton ES, Schlegel AM, Haswell ES. United in diversity: mechanosensitive ion channels in plants. Annual Review of Plant Biology. 2015;66:113–137. DOI: 10.1146/annurev-arplant-043014-114700.
  86. Hamilton ES, Haswell ES. The tension-sensitive ion transport activity of MSL8 is critical for its function in pollen hydration and germination. Plant & Cell Physiology. 2017;58(7):1222–1237. DOI: 10.1093/pcp/pcw230.
  87. Maksaev G, Haswell ES. MscS-Like10 is a stretch-activated ion channel from Arabidopsis thaliana with a preference for anions. PNAS. 2012;109(46):19015 –19020. DOI: 10.1073/pnas.1213931109.
  88. Veley KM, Maksaev G, Frick EM, January E, Kloepper SC, Haswell ES. Arabidopsis MSL10 has a regulated cell death signaling activity that is separable from its mechanosensitive ion channel activity. The Plant Cell. 2014;26(7):3115–3131. DOI: 10.1105/tpc.114.128082.
  89. Lee CP, Maksaev G, Jensen GS, Murcha MW, Wilson ME, Fricker M, et al. MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress. The Plant Journal. 2016;88(5):809 – 825. DOI: 10.1111/tpj.13301.
  90. Peyronnet R, Haswell ES, Barbier-Brygoo H, Frachisse JM. AtMSL9 and AtMSL10: sensors of plasma membrane tension in Arabidopsis roots. Plant Signaling & Behavior. 2008;3(9):726 –729. DOI: 10.4161/psb.3.9.6487.
  91. Kamano S, Kume S, Iida K, Lei KJ, Nakano M, Nakayama Y, et al. Transmembrane topologies of Ca2+-permeable mechanosensitive channels MCA1 and MCA2 in Arabidopsis thaliana. Journal of Biological Chemistry. 2015;290(52):30901–30909. DOI: 10.1074/jbc.M115.692574.
  92. Furuichi T, Iida H, Sokabe M, Tatsumi H. Expression of Arabidopsis MCA1 enhanced mechanosensitive channel activity in the Xenopus laevis oocyte plasma membrane. Plant Signaling & Behavior. 2012;7(8):1022–1026. DOI: 10.4161/psb.20783.
  93. Kurusu T, Nishikawa D, Yamazaki Y, Gotoh M, Nakano M, Hamada H, et al. Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2+ influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biology. 2012;12(1):11. DOI: 10.1186/1471-2229-12-11.
  94. Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, et al. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature. 2014;514(7522):367–371. DOI: 10.1038/nature13593.
Опубликован
2019-01-18
Ключевые слова: кальций, катионные каналы, Ca2 -проводимость, каналы, активируемые циклическими нуклеотидами, ионотропные глутаматные рецепторы, механочувствительные каналы, высшие растения
Как цитировать
Мацкевич, В. С., Самохина, В. В., Гриусевич, П. В., Войтехович, М. А., Соколик, А. И., & Демидчик, В. В. (2019). Са2+-проницаемые катионные каналы плазматической мембраны клеток высших растений. Экспериментальная биология и биотехнология, 2, 11-26. Доступно по https://journals.bsu.by/index.php/biology/article/view/2505
Раздел
Клеточная биология и биотехнология растений