The role of ion disequilibrium in induction of root cell death and autophagy by environmental stresses
Vadim Demidchik A B C , Elena V. Tyutereva A and Olga V. Voitsekhovskaja A C
+ Author Affiliations
- Author Affiliations
A Laboratory of Plant Ecological Physiology, Komarov Botanical Institute, Russian Academy of Sciences, ul. Professora Popova 2, 197376 St Petersburg, Russia.
B Department of Plant Cell Biology and Bioengineering, Biological Faculty, Belarusian State University, Independence Avenue 4, 220030, Minsk, Belarus.
C Corresponding authors. Emails: ovoitse@binran.ru; dzemidchyk@bsu.by
This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 19–23 June 2016.
Functional Plant Biology 45(2) 28-46 https://doi.org/10.1071/FP16380
Submitted: 31 October 2016 Accepted: 9 December 2016 Published: 28 February 2017
Abstract
Environmental stresses such as salinity, drought, oxidants, heavy metals, hypoxia, extreme temperatures and others can induce autophagy and necrosis-type programmed cell death (PCD) in plant roots. These reactions are accompanied by the generation of reactive oxygen species (ROS) and ion disequilibrium, which is induced by electrolyte/K+ leakage through ROS-activated ion channels, such as the outwardly-rectifying K+ channel GORK and non-selective cation channels. Here, we discuss mechanisms of the stress-induced ion disequilibrium and relate it with ROS generation and onset of morphological, biochemical and genetic symptoms of autophagy and PCD in roots. Based on our own data and that in the literature, we propose a hypothesis on the induction of autophagy and PCD in roots by loss of cytosolic K+. To support this, we present data showing that in conditions of salt stress-induced autophagy, gork1–1 plants lacking root K+ efflux channel have fewer autophagosomes compared with the wild type. Overall, literature analyses and presented data strongly suggest that stress-induced root autophagy and PCD are controlled by the level of cytosolic potassium and ROS.
Additional keywords: abiotic stress, autophagy, ion fluxes, programmed cell death, reactive oxygen species.
References
Adamakis IDS, Panteris E, Eleftheriou EP (2011) The fatal effect of tungsten on Pisum sativum L. root cells: indications for endoplasmic reticulum stress-induced programmed cell death. Planta 234, 21–34.| The fatal effect of tungsten on Pisum sativum L. root cells: indications for endoplasmic reticulum stress-induced programmed cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotVeltrw%3D&md5=8fc3094fab00a2a36366b4ea69ef58efCAS |
Andersen MN, Rasmussen HB (2012) AMPK, a regulator of ion channels. Communicative & Integrative Biology 5, 480–484.
| AMPK, a regulator of ion channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1SitrbK&md5=6c7deb8a2d17377264165b665849e5dcCAS |
Atkinson MM, Huang JS, Knopp JA (1985) The hypersensitive reaction of tobacco to Pseudomonas syringae pv. pisi: activation of a plasmalemma K+/H+ exchange mechanism. Plant Physiology 79, 843–847.
| The hypersensitive reaction of tobacco to Pseudomonas syringae pv. pisi: activation of a plasmalemma K+/H+ exchange mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XjtF2jug%3D%3D&md5=f38091fbaa6ab563a82484bef7f41741CAS |
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Deckert J, Rucińska-Sobkowiak R, Gzyl J, Pawlak-Sprada S, Abramowski D, Jelonek T, Gwóźdź EA (2012) Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiology and Biochemistry 58, 124–134.
| Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1emsrrK&md5=fe47731560c357f30a9cb2394e96f95bCAS |
Atkinson MM, Midland SL, Sims JJ, Keen NT (1996) Syringolide 1 triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiology 112, 297–302.
| Syringolide 1 triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvFKht74%3D&md5=e59f54ee7ef1a2f2b0a3616a23e5a304CAS |
Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942.
| A central integrator of transcription networks in plant stress and energy signalling.Crossref | GoogleScholarGoogle Scholar |
Bajji M, Kinet JM, Lutts S (2002) Osmotic and ionic effects of NaCl on germination, early seedling growth and ion content of Atriplex halimus (Chenopodiaceae). Canadian Journal of Botany 80, 297–304.
| Osmotic and ionic effects of NaCl on germination, early seedling growth and ion content of Atriplex halimus (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlCjtr4%3D&md5=4b2326624f4fcc91690f2fad4eef0f80CAS |
Becker D, Geiger D, Dunkel M, Roller A, Bertl A, Latz A, Carpaneto A, Dietrich P, Roelfsema MRG, Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K, Hedrich R (2004) AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 101, 15621–15626.
| AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWisLrF&md5=454eadb72ecfbe1844024dce8a75351eCAS |
Behboodi BS, Samadi L (2004) Detection of apoptotic bodies and oligonucleosomal DNA fragments in cadmium-treated root apical cells of Allium cepa L. Plant Science 167, 411–416.
| Detection of apoptotic bodies and oligonucleosomal DNA fragments in cadmium-treated root apical cells of Allium cepa L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFOqtrc%3D&md5=356c5d1ed890124958fc1b8498b0d95dCAS |
Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Science 21, 43–47.
| Cell membrane stability as a measure of drought and heat tolerance in wheat.Crossref | GoogleScholarGoogle Scholar |
Bortner CD, Gómez-Angelats M, Cidlowski JA (2001) Plasma membrane depolarization without repolarization is an early molecular event in anti-Fas-induced apoptosis. Journal of Biological Chemistry 276, 4304–4314.
| Plasma membrane depolarization without repolarization is an early molecular event in anti-Fas-induced apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXht1GnsL0%3D&md5=8d7f3eba4f25beeb4f7c8c3e080473dcCAS |
Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L, Fernie AR, Willmitzer L, Giavalisco P (2013) Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. The Plant Journal 73, 897–909.
| Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFWrs7s%3D&md5=7f9b3d6b9807e2b27c12cfd0c0ac9e4aCAS |
Canu N, Tufi R, Serafino AL, Amadoro G, Ciotti MT, Calissano P (2005) Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. Journal of Neurochemistry 92, 1228–1242.
| Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitlehsr0%3D&md5=4bfbfc7ddd7b698c3f2872839f25c330CAS |
Cardaci S, Desideri E, Ciriolo MR (2012) Targeting aerobic glycolysis: 3-bromopyruvate as a promising anticancer drug. Journal of Bioenergetics and Biomembranes 44, 17–29.
| Targeting aerobic glycolysis: 3-bromopyruvate as a promising anticancer drug.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xktlehtbo%3D&md5=0dad3ba68e18b7aa35c7f121e0258048CAS |
Chen L, Liao B, Qi H, Xie LJ, Huang L, Tan WJ, Zhai N, Yuan LB, Zhou Y, Yu LJ, Chen QF, Shu W, Xiao S (2015) Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana. Autophagy 11, 2233–2246.
| Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnvFGlsw%3D%3D&md5=36ee10e3a17a81bf976c1be9fbd95947CAS |
Cheng JH, Kodama I (2004) Two components of delayed rectifier K+ current in heart: molecular basis, functional diversity, and contribution to repolarization. Acta Pharmacologica Sinica 25, 137–145.
Cox CD, Nomura T, Ziegler CS, Campbell AK, Wann KT, Martinac B (2013) Selectivity mechanism of the mechanosensitive channel MscS revealed by probing channel subconducting states. Nature Communications 4, 2137
| Selectivity mechanism of the mechanosensitive channel MscS revealed by probing channel subconducting states.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sjpvVeitQ%3D%3D&md5=bb2ecb35670bfefdc9943e1c5f53ac22CAS |
Crozet P, Margalha L, Confraria A, Rodrigues A, Martinho C, Adamo M, Elias CA, Baena-González E (2014) Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Frontiers in Plant Science
| Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases.Crossref | GoogleScholarGoogle Scholar |
Czarny P, Pawlowska E, Bialkowska-Warzecha J, Kaarniranta K, Blasiak J (2015) Autophagy in DNA damage response. International Journal of Molecular Sciences 16, 2641–2662.
| Autophagy in DNA damage response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXktlaksr0%3D&md5=882abeb056b747b454c6c02841afe0c2CAS |
De Vos C, Schat H, De Waal M, Vooijs R, Ernst W (1991) Increased resistance to copper induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiologia Plantarum 82, 523–528.
| Increased resistance to copper induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlslKqurc%3D&md5=4e9118f25f9ef04d2f60ce223c991271CAS |
Deb S, Sankaranarayanan S, Wewala G, Widdup E, Samuel MA (2014) The S-domain receptor kinase, Arabidopsis receptor Kinase 2 and the U Box/Armadillo repeat-containing E3 ubiquitin ligase 9 module mediates lateral root development under phosphate starvation in Arabidopsis. Plant Physiology 165, 1647–1656.
| The S-domain receptor kinase, Arabidopsis receptor Kinase 2 and the U Box/Armadillo repeat-containing E3 ubiquitin ligase 9 module mediates lateral root development under phosphate starvation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlKntbnP&md5=c989ca4d0305394b6f1327940c6e98b4CAS |
Demidchik V (2014) Mechanisms and physiological roles of K+ efflux from root cells. Journal of Plant Physiology 171, 696–707.
| Mechanisms and physiological roles of K+ efflux from root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlt1Cjsb8%3D&md5=a469d2a79ba8a70aa64f63f6cf3c2ba8CAS |
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109, 212–228.
| Mechanisms of oxidative stress in plants: from classical chemistry to cell biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaiur%2FM&md5=f8db8a141307c54edb23849b86ec517bCAS |
Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175, 387–404.
| Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFSqs7w%3D&md5=523effe247b9d3f5e8663a91091fd2a4CAS |
Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+-and K+-permeable channels in plant root cells. Journal of Cell Science 116, 81–88.
| Free oxygen radicals regulate plasma membrane Ca2+-and K+-permeable channels in plant root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtF2lsA%3D%3D&md5=eede4b7865478d7d00a7ac9b79d5f2d2CAS |
Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123, 1468–1479.
| Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1KmtL0%3D&md5=1ea5171aa64a36e614598240e5e6d344CAS |
Demidchik V, Shang Z, Shin R, Shabala S, Davies JM (2011) Receptor-like activity evoked by extracellular ADP in Arabidopsis thaliana root epidermal plasma membrane. Plant Physiology 156, 1375–1385.
| Receptor-like activity evoked by extracellular ADP in Arabidopsis thaliana root epidermal plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWks7g%3D&md5=63b4f9215c220c8a15086e2e519a63e5CAS |
Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany 65, 1259–1270.
| Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htb4%3D&md5=bf101b7b23972cc5786358931a472e29CAS |
Dexter ST, Tottingham WE, Graber LF (1932) Investigation of the hardiness of plants by measurement of electrical conductivity. Plant Physiology 7, 63–78.
| Investigation of the hardiness of plants by measurement of electrical conductivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA38XhvVGjtw%3D%3D&md5=e8aed66341e051ee2731b342055e502eCAS |
Díaz-Troya S, Pérez-Pérez ME, Florencio FJ, Crespo JL (2008) The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4, 851–865.
| The role of TOR in autophagy regulation from yeast to plants and mammals.Crossref | GoogleScholarGoogle Scholar |
Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. Journal of Biological Chemistry 277, 33105–33114.
| The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnt1Slsbw%3D&md5=03a87994621d251e74de5c7b17812483CAS |
Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends in Plant Science 5, 123–127.
Duan Y, Zhang W, Li B, Wang Y, Li K, Sodmergen , Han C, Zhang Y, Li X (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytologist 186, 681–695.
| An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVejt7g%3D&md5=7c6d50491d9c51e90ad61c69027cfdc0CAS |
Dubbs JB, Mongkolsuk S (2012) Peroxide-sensing transcriptional regulators in bacteria. Journal of Bacteriology 194, 5495–5503.
| Peroxide-sensing transcriptional regulators in bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2itbjN&md5=9962bcbd86757b8a17b1b9b8cc1f8a22CAS |
Dunkel M, Latz A, Schumacher K, Müller T, Becker D, Hedrich R (2008) Targeting of vacuolar membrane localized members of the TPK channel family. Molecular Plant 1, 938–949.
| Targeting of vacuolar membrane localized members of the TPK channel family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotValuw%3D%3D&md5=e089f77dc80d10006052c6c345ddc5c9CAS |
Escamez S, Tuominen H (2014) Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal. Journal of Experimental Botany 65, 1313–1321.
| Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htbs%3D&md5=18e95130fb89e3c3b78cadaecc0ecf30CAS |
Faget M, Blossfeld S, Jahnke S, Huber G, Schurr U, Nagel KA (2013) Temperature effects on root growth. In: ‘Plant roots: the hidden half, fourth edition’. (CRC Press)
Finka A, Cuendet AF, Maathuis FJ, Saidi Y, Goloubinoff P (2012) Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. The Plant Cell 24, 3333–3348.
| Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFeku7vM&md5=24f20e1a5e2d10da486555a51132bd36CAS |
Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.
| Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlGgtLg%3D&md5=dc90ce6dd130e8a7fd34100cf7f77cd1CAS |
Fulcher N, Sablowski R (2009) Hypersensitivity to DNA damage in plant stem cell niches. Proceedings of the National Academy of Sciences of the United States of America 106, 20984–20988.
| Hypersensitivity to DNA damage in plant stem cell niches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFygtw%3D%3D&md5=7782b5c6af8314df0b4506927e23994aCAS |
Galluzzi L, Pietrocola F, Levine B, Kroemer G (2014) Metabolic control of autophagy. Cell 159, 1263–1276.
| Metabolic control of autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFOrt7bN&md5=1aa641cebffff23be748b88aaaae8f84CAS |
Gamalei YuV (1971) Autolysis in differentiating tracheids. Tsitologiya 13, 278–285. [in Russian]
Garcia-Mata C, Wang J, Gajdanowicz P, Gonzalez W, Hills A, Donald N, Riedelsberger J, Amtmann A, Dreyer I, Blatt MR (2010) A minimal cysteine motif required to activate the SKOR K+ channel of Arabidopsis by the reactive oxygen species H2O2. Journal of Biological Chemistry 285, 29286–29294.
| A minimal cysteine motif required to activate the SKOR K+ channel of Arabidopsis by the reactive oxygen species H2O2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFCns7nN&md5=681d1ba697248708bd5766827eef93ebCAS |
Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655.
| Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVWksrs%3D&md5=9b6371bc40175e163eebf070bcf120dfCAS |
Ge Y, Cai Y-M, Bonneau L, Rotari V, Danon A, McKenzie EA, McLellan H, Mach L, Gallois P (2016) Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis. Cell Death and Differentiation 23, 1493–1501.
| Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlvVamsrw%3D&md5=117ee2513e427212071e8016adfa3475CAS |
Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJ (2006) Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport. Journal of Experimental Botany 57, 791–800.
| Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVOqsbc%3D&md5=771d3cc4b430460be26c584440948c12CAS |
Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cellular Microbiology 6, 201–211.
| The role and regulation of programmed cell death in plant-pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Knu70%3D&md5=549b4004bb7c81927d89ff6c5a480a70CAS |
Gunawardena AH, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212, 205–214.
| Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Kkuw%3D%3D&md5=5f768ecc24a2f078678a335d78330e49CAS |
Halliwell B, Gutteridge JMC (1999) ‘Free radicals in biology and medicine.’ (Oxford University Press: Oxford)
Han S, Wang Y, Zheng X, Jia Q, Zhao J, Bai F, Hong Y, Liu Y (2015) Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana. The Plant Cell 27, 1316–1331.
| Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosV2rtrk%3D&md5=cd8d9b8ec1af1baeeafac8d9b78eda4dCAS |
Hatsugai N, Yamada K, Goto-Yamada S, Hara-Nishimura I (2015) Vacuolar processing enzyme in plant programmed cell death. Frontiers in Plant Science 6, 234
| Vacuolar processing enzyme in plant programmed cell death.Crossref | GoogleScholarGoogle Scholar |
Hedrich R (2012) Ion channels in plants. Physiological Reviews 92, 1777–1811.
| Ion channels in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2lsbnF&md5=76478592f0e1f84cb75a00b3a2520fffCAS |
Henry E, Fung N, Liu J, Drakakaki G, Coaker G (2015) Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLOS Genetics 11, e1005199
| Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses.Crossref | GoogleScholarGoogle Scholar |
Huang WJ, Oo TL, He HY, Wang AQ, Zhan J, Li CZ, Wei SQ, He LF (2014) Aluminum induces rapidly mitochondria dependent programmed cell death in Al-sensitive peanut root tips. Botanical Studies (Taipei, Taiwan) 55, 67
| Aluminum induces rapidly mitochondria dependent programmed cell death in Al-sensitive peanut root tips.Crossref | GoogleScholarGoogle Scholar |
Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiology 171, 1551–1559.
| The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVaqtL%2FI&md5=532c0bda987ad1c7297e3ee7e564cf94CAS |
Hughes T, Rusten TE (2007) Origin and evolution of self-consumption: autophagy. Advances in Experimental Medicine and Biology 607, 111–118.
| Origin and evolution of self-consumption: autophagy.Crossref | GoogleScholarGoogle Scholar |
Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. The Plant Journal 29, 649–659.
| Salt causes ion disequilibrium-induced programmed cell death in yeast and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XislOhtr8%3D&md5=95b72e9153f68863b2c5bc677a3e130eCAS |
Inoue Y, Suzuki T, Hattori M, Yoshimoto K, Ohsumi Y, Moriyasu Y (2006) AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant & Cell Physiology 47, 1641–1652.
| AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFWlsw%3D%3D&md5=a6c51430f46d606d8840b46096979686CAS |
Izumi M, Hidema J, Wada S, Kondo E, Kurusu T, Kuchitsu K, Makino A, Ishida H (2015) Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation. Plant Physiology 167, 1307–1320.
| Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlvVKlu7k%3D&md5=5cf9d6ece2c5a66cf3e21afdd88ff625CAS |
Jiménez-Quesada MJ, Traverso JÁ, Alché Jde D (2016) NADPH oxidase-dependent superoxide production in plant reproductive tissues. Frontiers in Plant Science 7, 359
| NADPH oxidase-dependent superoxide production in plant reproductive tissues.Crossref | GoogleScholarGoogle Scholar |
Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide gated channels in plants. FEBS Letters 581, 2237–2246.
| Cyclic nucleotide gated channels in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1aiurg%3D&md5=71f6e1b05a94902f2e658fb65f2622cbCAS |
Katsuhara M, Shibasaka M (2000) Cell death and growth recovery of barley after transient salt stress. Journal of Plant Research 113, 239–243.
| Cell death and growth recovery of barley after transient salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFOksbg%3D&md5=63318644852e95473080ab9079a6ae42CAS |
Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiological Reviews 82, 769–824.
| Cyclic nucleotide-gated ion channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslCmt70%3D&md5=2f98c4cf3445791366c89a57574d36feCAS |
Kiedrowski L, Mienville JM (2001) Kainate-induced K+ efflux and plasma membrane depolarization in cultured cerebellar granule cells. Neuroreport 12, 59–62.
| Kainate-induced K+ efflux and plasma membrane depolarization in cultured cerebellar granule cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFCntQ%3D%3D&md5=cff3942646a7edf9ee2f8e608595380eCAS |
Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nature Cell Biology 13, 132–141.
| AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlamtb0%3D&md5=3646260f88c6bf5e5443c6af62b1f1a8CAS |
Kim S-H, Kwon C, Lee J-H, Chung T (2012) Genes for plant autophagy: functions and interactions. Molecules and Cells 34, 413–423.
| Genes for plant autophagy: functions and interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWqsrbI&md5=3846bbbe9bbc3727107bd940c4ee570aCAS |
Kim J, Lee H, Lee HN, Kim SH, Shin KD, Chung T (2013) Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. The Plant Cell 25, 4956–4966.
| Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFars7s%3D&md5=8d9a2c408f5769bd686d06235aa0c706CAS |
Kim Y, Wang M, Bai Y, Zeng Z, Guo F, Pan J, Han N, Bian H, Wang J, Pan J, Zhu M (2014) Bcl-2 suppresses activation of VPEs by inhibiting cytosolic Ca2+ level with elevated K+ efflux in NaCl-induced PCD in rice. Plant Physiology and Biochemistry 80, 168–175.
| Bcl-2 suppresses activation of VPEs by inhibiting cytosolic Ca2+ level with elevated K+ efflux in NaCl-induced PCD in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpsl2mt7k%3D&md5=0768c32fe24a8400b8a3bf67c6887755CAS |
Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al (2016) Guidelines for the use and interpretation of assays for monitoring autophagy. (3rd edn). Autophagy 12, 1–222.
Kollist H, Jossier M, Laanemets K, Thomine S (2011) Anion channels in plant cells. The FEBS Journal 278, 4277–4292.
| Anion channels in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFaksrbN&md5=b927bdb7d9cf49cc85c910cce63e3ff7CAS |
Kondratskyi A, Yassine M, Kondratska K, Skryma R, Slomianny C, Prevarskaya N (2013) Calcium-permeable ion channels in control of autophagy and cancer. Frontiers in Physiology 4, 272
| Calcium-permeable ion channels in control of autophagy and cancer.Crossref | GoogleScholarGoogle Scholar |
Kugler A, Köhler B, Palme K, Wolff P, Dietrich P (2009) Salt-dependent regulation of a CNG channel subfamily in Arabidopsis. BMC Plant Biology 9, 140
| Salt-dependent regulation of a CNG channel subfamily in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Kupis W, Pałyga J, Tomal E, Niewiadomska E (2016) The role of sirtuins in cellular homeostasis. Journal of Physiology and Biochemistry 72, 371–380.
| The role of sirtuins in cellular homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnvVGgtbg%3D&md5=abb407a5ac3b96a56b3bc9fe74b8186aCAS |
Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, Brownlee C, Hofmann A, Webb AA, Miedema H, Battey NH, Davies JM (2009) Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+-permeable conductance. The Plant Cell 21, 479–493.
| Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+-permeable conductance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKrtro%3D&md5=e949ba7b950a92ac2ff9c378c1cde550CAS |
Laohavisit A, Shang Z, Rubio L, Cuin TA, Véry AA, Wang A, Mortimer JC, Macpherson N, Coxon KM, Battey NH, Brownlee C, Park OK, Sentenac H, Shabala S, Webb AA, Davies JM (2012) Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+- and K+-permeable conductance in root cells. The Plant Cell 24, 1522–1533.
| Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+- and K+-permeable conductance in root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XoslCrtLk%3D&md5=8f46feb0614c986ab02ef6a23d5fa111CAS |
Le Bars R, Marion J, Satiat-Jeunemaitre B, Bianchi MW (2014) Folding into an autophagosome: ATG5 sheds light on how plants do it. Autophagy 10, 1861–1863.
| Folding into an autophagosome: ATG5 sheds light on how plants do it.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjvFGisL0%3D&md5=2f6357a16f4ff3c4d898bffca018e6e4CAS |
Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell. New Phytologist 97, 1–13.
| A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXksFequrY%3D&md5=b9badba96f12ef29ec4c2606f1b6de3eCAS |
Leopold AC, Musgrave ME, Williams KM (1981) Solute leakage resulting from leaf desiccation. Plant Physiology 68, 1222–1225.
| Solute leakage resulting from leaf desiccation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjtFyntw%3D%3D&md5=5bd6dd6b870546d07684e32bb827ce63CAS |
Li JY, Jiang AL, Zhang W (2007) Salt stress-induced programmed cell death in rice root tip cells. Journal of Integrative Plant Biology 49, 481–486.
| Salt stress-induced programmed cell death in rice root tip cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFOhtrw%3D&md5=df49d672d67d947de77504f33dcbc77cCAS |
Liu Y, Bassham DC (2010) TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One 5, e11883
| TOR is a negative regulator of autophagy in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology 63, 215–237.
| Autophagy: pathways for self-eating in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1ams7g%3D&md5=ddbd4b444e0d81bf166c5ea3120372c6CAS |
Liu XZ, Huang BR (2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Science 40, 503–510.
| Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsF2mt7k%3D&md5=5ad6ba695da0a57e3d4cfd0fe8c24fe6CAS |
Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5, 954–963.
| Autophagy is required for tolerance of drought and salt stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmt1Chtw%3D%3D&md5=9c1bbb22e76cb4bcd8618f9a8e077bd0CAS |
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Annals of Botany 84, 123–133.
| K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVCgtL4%3D&md5=548f98e32e45539f42e5300515dcf755CAS |
Marschner H, Handley R, Overstreet R (1966) Potassium loss and changes in the fine structure of corn root tips induced by H-ion. Plant Physiology 41, 1725–1735.
| Potassium loss and changes in the fine structure of corn root tips induced by H-ion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXmt1KksA%3D%3D&md5=4bb82c962fd9899b8c7b2fe87ccb2462CAS |
McLellan H, Gilroy EM, Yun BW, Birch PRJ, Loake GJ (2009) Functional redundancy in the Arabidopsis Cathepsin B gene family contributes to basal defence, the hypersensitive response and senescence. New Phytologist 183, 408–418.
| Functional redundancy in the Arabidopsis Cathepsin B gene family contributes to basal defence, the hypersensitive response and senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptlSjs7c%3D&md5=da373837fdbdcc18b78f11cd30a95668CAS |
Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. Journal of Experimental Botany 58, 2297–2306.
| Nitrate transport and signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1ykt7s%3D&md5=00be2e9d2c8dbb8da5238c5677591fdbCAS |
Minibayeva F, Dmitrieva S, Ponomareva A, Ryabovol V (2012) Oxidative stress-induced autophagy in plants: the role of mitochondria. Plant Physiology and Biochemistry 59, 11–19.
| Oxidative stress-induced autophagy in plants: the role of mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWltr3N&md5=957d8c4454f89c9b81718ed44d1ac409CAS |
Minina E, Filonova L, Fukada K, Savenkov EI, Gogvadye G, Clapham D, Sanez-Vera V, Suarez MF, Zhivotovsky B, Daniel G, Smertenko A, Bozhkov PV (2013) Autophagy and metacaspase determine the mode of cell death in plants. Journal of Cell Biology 203, 917–927.
| Autophagy and metacaspase determine the mode of cell death in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFKnsw%3D%3D&md5=0daba940a70e9298e2bd2ea4a2753334CAS |
Minina EA, Stael S, Van Breusegem F, Bozhkov PV (2014) Plant metacaspase activation and activity. Methods in Molecular Biology 1133, 237–253.
| Plant metacaspase activation and activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXns1yktrk%3D&md5=41d0c5b13cb8276be83a81531d3e311aCAS |
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15–19.
| Abiotic stress, the field environment and stress combination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVKjsw%3D%3D&md5=d8d6673f6a864bec474abd7d7b9d3bd6CAS |
Monastyrska I, Rieter E, Klionsky DJ, Reggiori F (2009) Multiple roles of the cytoskeleton in autophagy. Biological Reviews of the Cambridge Philosophical Society 84, 431–448.
| Multiple roles of the cytoskeleton in autophagy.Crossref | GoogleScholarGoogle Scholar |
Moreau K, Renna M, Rubinsztein DC (2013) Connections between SNAREs and autophagy. Trends in Biochemical Sciences 38, 57–63.
| Connections between SNAREs and autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVehsA%3D%3D&md5=785ab1c0dc5f41a56faddeed804b03beCAS |
Munafó DB, Colombo MI (2001) A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. Journal of Cell Science 114, 3619–3629.
Murphy A, Taiz L (1997) Correlation between potassium efflux and copper sensitivity in ten Arabidopsis ecotypes. New Phytologist 136, 211–222.
| Correlation between potassium efflux and copper sensitivity in ten Arabidopsis ecotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltlKgtLY%3D&md5=e850d4c8b2ba75f85b30e2dd5c74ccb3CAS |
Murphy AS, Eisinger WR, Shaff JE, Kochian LV, Taiz L (1999) Early copper-induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiology 121, 1375–1382.
| Early copper-induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFyis7k%3D&md5=732e845187186eba7514b65bab347aefCAS |
Nassery H (1972) The loss of potassium and sodium from excised barley and bean roots. New Phytologist 71, 269–274.
| The loss of potassium and sodium from excised barley and bean roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XktlWls7g%3D&md5=ea4deeea509a5cdd5b157872dd87e080CAS |
Nassery H (1975) The effects of salt and osmotic stress on the retention of potassium by excised barley and bean roots. New Phytologist 75, 63–67.
| The effects of salt and osmotic stress on the retention of potassium by excised barley and bean roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlslGlsbk%3D&md5=4e6d3ea54b30147588d9ee9e222b790fCAS |
Ning SB, Song YC, van Damme P (2002) Characterization of the early stages of programmed cell death in maize root cells by using comet assay and the combination of cell electrophoresis with annexin binding. Electrophoresis 23, 2096–2102.
| Characterization of the early stages of programmed cell death in maize root cells by using comet assay and the combination of cell electrophoresis with annexin binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVegtbg%3D&md5=d1ac39b54075656a3b741afe263f5fa2CAS |
Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant, Cell & Environment 39, 1140–1160.
| Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlvVaitb8%3D&md5=0e603b0b2baec30cb81ddd32b2c2f76dCAS |
Orlov SN, Thorin-Trescases N, Kotelevtsev SV, Tremblay J, Hamet P (1999) Inversion of the intracellular Na+/K+ ratio blocks apoptosis in vascular smooth muscle at a site upstream of caspase 3. Journal of Biological Chemistry 274, 16545–16552.
| Inversion of the intracellular Na+/K+ ratio blocks apoptosis in vascular smooth muscle at a site upstream of caspase 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1OntLw%3D&md5=551feef2c0c8ce3c7c00c962a60b27f4CAS |
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany 64, 445–458.
| Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVGluw%3D%3D&md5=2d1409cad3d21987365d45f41824ef25CAS |
Osterhaut WJV (1922) ‘Injury, recovery, and death, in relation to conductivity and permeability.’ (JB Lippincott: Philadelphia, PA, USA)
Palta J, Levitt J, Stadelmann EJ (1977) Freezing injury in onion bulb cells. I. Evaluation of the conductivity method and analysis of ion and sugar efflux. Plant Physiology 60, 393–397.
| Freezing injury in onion bulb cells. I. Evaluation of the conductivity method and analysis of ion and sugar efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXls1Cnu7k%3D&md5=b14aa6f31d663339ae0d05c2a12ebd45CAS |
Pan JW, Zhu MY, Chen H (2001) Aluminum-induced cell death in root-tip cells of barley. Environmental and Experimental Botany 46, 71–79.
| Aluminum-induced cell death in root-tip cells of barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvV2gtbw%3D&md5=c7f06ba1e484021b00407083286fa954CAS |
Perez-Neut M, Haar L, Rao V, Santha S, Lansu K, Rana B, Jones WK, Gentile S (2016) Activation of hERG3 channel stimulates autophagy and promotes cellular senescence in melanoma. Oncotarget 7, 21991–22004.
Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science 6, 69
| ROS-mediated abiotic stress-induced programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar |
Price MB, Jelesko J, Okumoto S (2012) Glutamate receptor homologs in plants: functions and evolutionary origins. Frontiers in Plant Science 3, 235
| Glutamate receptor homologs in plants: functions and evolutionary origins.Crossref | GoogleScholarGoogle Scholar |
Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M (2011) Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytologist 190, 351–368.
| Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1GktLc%3D&md5=7a2c0b02efddf66f4b1cda907406b873CAS |
Remillard CV, Yuan JXJ (2004) Activation of K+ channels: an essential pathway in programmed cell death. The American Journal of Physiology 286, 49–67.
Reumann S, Voitsekhovskaja O, Lillo C (2010) From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247, 233–256.
| From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features.Crossref | GoogleScholarGoogle Scholar |
Rybaczek D, Musiałek MW, Balcerczyk A (2015) Caffeine-induced premature chromosome condensation results in the apoptosis-like programmed cell death in root meristems of Vicia faba. PLoS One 10, e0142307
| Caffeine-induced premature chromosome condensation results in the apoptosis-like programmed cell death in root meristems of Vicia faba.Crossref | GoogleScholarGoogle Scholar |
Sandalio LM, Romero-Puertas MC (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Annals of Botany 116, 475–485.
| Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MbivFeqsQ%3D%3D&md5=d7bf1b5fb7176fa1d54972ae1478ae64CAS |
Sarkar P, Gladish DK (2012) Hypoxic stress triggers a programmed cell death pathway to induce vascular cavity formation in Pisum sativum roots. Physiologia Plantarum 146, 413–426.
| Hypoxic stress triggers a programmed cell death pathway to induce vascular cavity formation in Pisum sativum roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKlurrI&md5=fedb373ac620e2cc7f8d7760c1df65bcCAS |
Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO Journal 26, 1749–1760.
| Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjslOmtLs%3D&md5=e537e2c0c8ce3bd7287ecebef338fd8aCAS |
Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytologist 190, 289–298.
| Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1GktLg%3D&md5=1870a3095896d70bf8ac085e350612ecCAS |
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiology 141, 1653–1665.
| Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKitbo%3D&md5=1583ba00794bbed3e82f390e3c0d4f41CAS |
Shabala S, Cuin TA, Pottosin II (2007a) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Letters 581, 1993–1999.
| Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFGlur8%3D&md5=d22fc6faba93f94f81fe5ddfef0c40f4CAS |
Shabala S, Cuin TA, Prismall L, Nemchinov LG (2007b) Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta 227, 189–197.
| Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyku7zF&md5=4d1e8fec9d499fa7c9c94fa479736102CAS |
Shin JH, Yoshimoto K, Ohsumi Y, Jeon JS, An G (2009) OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Molecular Cell 27, 67–74.
| OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVCmsr8%3D&md5=c0a82bc08b3dab4c3d78720329ba2268CAS |
Simon F, Varela D, Eguiguren AL, Díaz LF, Sala F, Stutzin A (2004) Hydroxyl radical activation of a Ca2+-sensitive nonselective cation channel involved in epithelial cell necrosis. American Journal of Physiology. Cell Physiology 287, C963–C970.
| Hydroxyl radical activation of a Ca2+-sensitive nonselective cation channel involved in epithelial cell necrosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVyitr0%3D&md5=f7eef371fad660877dc53d554d435614CAS |
Suttangkakul A, Li F, Chung T, Vierstra RD (2011) The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. The Plant Cell 23, 3761–3779.
| The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1eku7rE&md5=3eeb3277af47c34a5ed6a04450b877bcCAS |
Tamás L, Budíková S, Huttová J, Mistrík I, Simonovicová M, Siroká B (2005) Aluminum-induced cell death of barley-root border cells is correlated with peroxidase- and oxalate oxidase-mediated hydrogen peroxide production. Plant Cell Reports 24, 189–194.
| Aluminum-induced cell death of barley-root border cells is correlated with peroxidase- and oxalate oxidase-mediated hydrogen peroxide production.Crossref | GoogleScholarGoogle Scholar |
Vaid N, Pandey P, Srivastava VK, Tuteja N (2015) Pea lectin receptor-like kinase functions in salinity adaptation without yield penalty, by alleviating osmotic and ionic stresses and upregulating stress-responsive genes. Plant Molecular Biology 88, 193–206.
| Pea lectin receptor-like kinase functions in salinity adaptation without yield penalty, by alleviating osmotic and ionic stresses and upregulating stress-responsive genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmsVWrsLc%3D&md5=d803a459fdd2b41a1e7425dd00eef871CAS |
van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. Journal of Experimental Botany 62, 4749–4761.
| Classes of programmed cell death in plants, compared to those in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejsrfK&md5=58ce881f50a20cf154f11d0a47fec26dCAS |
van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death and Differentiation 18, 1241–1246.
| Morphological classification of plant cell deaths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1Gku7w%3D&md5=5ccfca0193b5f3ba603066df3cce6b81CAS |
Velarde-Buendía AM, Shabala S, Cvikrova M, Dobrovinskaya O, Pottosin I (2012) Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiology and Biochemistry 61, 18–23.
| Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines.Crossref | GoogleScholarGoogle Scholar |
Voitsekhovskaja OV, Schiermeyer A, Reumann S (2014) Plant peroxisomes are degraded by starvation-induced and constitutive autophagy in tobacco BY-2 suspension-cultured cells. Frontiers in Plant Science 5, 629
| Plant peroxisomes are degraded by starvation-induced and constitutive autophagy in tobacco BY-2 suspension-cultured cells.Crossref | GoogleScholarGoogle Scholar |
Wang P, Sun X, Wang N, Tan DX, Ma F (2015) Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. Journal of Pineal Research 58, 479–489.
| Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlvVGkur8%3D&md5=90997e42f213f9b1692eac96d9fd12afCAS |
Wang F, Chen ZH, Liu X, Colmer TD, Shabala L, Salih A, Zhou M, Shabala S (2016a) Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis. Journal of Experimental Botany
| Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Wang P, Richardson C, Hawes C, Hussey PJ (2016b) Arabidopsis NAP1 regulates the formation of autophagosomes. Current Biology 26, 2060–2069.
| Arabidopsis NAP1 regulates the formation of autophagosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1eju7bE&md5=59092f94445ee5e750e3c90824defd5fCAS |
Xiao AY, Homma M, Wang XQ, Wang X, Yu SP (2001) Role of K+ efflux in apoptosis induced by AMPA and kainate in mouse cortical neurons. Neuroscience 108, 61–67.
| Role of K+ efflux in apoptosis induced by AMPA and kainate in mouse cortical neurons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVelu7c%3D&md5=a68131229609b06b249892d4a04574a5CAS |
Xiong Y, Sheen J (2012) Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. Journal of Biological Chemistry 287, 2836–2842.
| Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpslOnsg%3D%3D&md5=c5fbe307bf9f40734ad6613ce703346fCAS |
Xiong Y, Sheen J (2014) The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiology 164, 499–512.
| The role of target of rapamycin signaling networks in plant growth and metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks1Sms7Y%3D&md5=bf1b3df38f62d5841a7adbebf739df4aCAS |
Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiology 143, 291–299.
| Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Omsg%3D%3D&md5=fe8c48005b230517a43c722d81d8cec4CAS |
Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose-TOR signalling reprograms the trascriptome and activates meristems. Nature 496, 181–186.
| Glucose-TOR signalling reprograms the trascriptome and activates meristems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkvFOksbw%3D&md5=5ea4ca0be0b4d6d3c3763b76396a254aCAS |
Yamashita K, Matsumoto H (1996) Salt stress-induced enhancement of anion efflux and anion transport activity in plasma membrane of barley roots. Soil Science and Plant Nutrition 42, 209–213.
| Salt stress-induced enhancement of anion efflux and anion transport activity in plasma membrane of barley roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVyksL0%3D&md5=a8809b1af954dcb46a45f33e41a16f26CAS |
Yu SP (2003) Regulation and critical role of potassium homeostasis in apoptosis. Progress in Neurobiology 70, 363–386.
| Regulation and critical role of potassium homeostasis in apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVGnurg%3D&md5=7e069765a0d4180b319ba7fb7a188b72CAS |
Zepeda-Jazo I, Shabala S, Chen Z, Pottosin II (2008) Na-K transport in roots under salt stress. Plant Signaling & Behavior 3, 401–403.
| Na-K transport in roots under salt stress.Crossref | GoogleScholarGoogle Scholar |
Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, Pottosin II (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiology 157, 2167–2180.
| Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ektL3E&md5=89603e86f9e7131c4b8c9f1a6e542b19CAS |
Zhai Y, Guo M, Wang H, Lu J, Liu J, Zhang C, Gong Z, Lu M (2016) Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L. Frontiers in Plant Science 7, 131
| Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L.Crossref | GoogleScholarGoogle Scholar |
Zhao J, Gao Y, Zhang Z, Chen T, Guo W, Zhang T (2013) A receptor-like kinase gene (GbRLK) from Gossypium barbadense enhances salinity and drought-stress tolerance in Arabidopsis. BMC Plant Biology 13, 110
| A receptor-like kinase gene (GbRLK) from Gossypium barbadense enhances salinity and drought-stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Zhong Y, Yan W, Chen J, Shangguan Z (2014) Net ammonium and nitrate fluxes in wheat roots under different environmental conditions as assessed by scanning ion-selective electrode technique. Scientific Reports 4, 7223
| Net ammonium and nitrate fluxes in wheat roots under different environmental conditions as assessed by scanning ion-selective electrode technique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXktlOiu7w%3D&md5=9c087c4f32823f9634c0f90b26447538CAS |
Zhou XM, Zhao P, Wang W, Zou J, Cheng TH, Peng XB, Sun MX (2015) A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues. DNA Research 22, 245–257.
| A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1CisLnP&md5=db6380cc4dd3f340d0e44c6ebc12f0e0CAS |
