6,359
Views
115
CrossRef citations to date
0
Altmetric
Basic Research Paper

Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana

, , , , , , , , , , , & show all
Pages 2233-2246 | Received 12 Feb 2015, Accepted 20 Oct 2015, Published online: 06 Jan 2016

References

  • Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT. Making sense of low oxygen sensing. Trends Plant Sci 2012; 17:129-38; PMID:22280796; http://dx.doi.org/10.1016/j.tplants.2011.12.004
  • Bailey-Serres J, Voesenek LACJ. Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 2008; 59:313-39; PMID:18444902; http://dx.doi.org/10.1146/annurev.arplant.59.032607.092752
  • Voesenek LACJ, Sasidharan R. Ethylene– and oxygen signaling– drive plant survival during flooding. Plant Biol 2013; 15:426-35; PMID:23574304; http://dx.doi.org/10.1111/plb.12014
  • Geigenberger P. Response of plant metabolism to too little oxygen. Curr. Opin. Plant Biol 2003; 6:247-56; PMID:12753974; http://dx.doi.org/10.1016/S1369-5266(03)00038-4
  • Perata P, Voesenek LACJ. Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci 2007; 12:43-6; PMID:17208508; http://dx.doi.org/10.1016/j.tplants.2006.12.005
  • Sauter M. Root responses to flooding. Curr Opin Plant Biol 2013; 16:282-6; PMID:23608517; http://dx.doi.org/10.1016/j.pbi.2013.03.013
  • Bailey-Serres J, Voesenek LACJ. Life in the balance: a signaling network controlling survival of flooding. Curr Opin Plant Biol 2010; 13:489-94; PMID:20813578; http://dx.doi.org/10.1016/j.pbi.2010.08.002
  • Licausi F, Pucciariello C, Perata P. New role for an old rule: N-end rule-mediated degradation of ethylene responsive factor proteins governs low oxygen response in plants. J Integr Plant Biol 2013; 55:31-9; PMID:23164408; http://dx.doi.org/10.1111/jipb.12011
  • Métraux JP, Kende H. The role of ethylene in the growth response of submerged deep water rice. Plant Physiol 1983; 72:441-6; PMID:16663022
  • Peng HP, Lin TY, Wang NN, Shih MC. Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 2005; 58:15-25; PMID:16028113; http://dx.doi.org/10.1007/s11103-005-3573-4
  • Fukao T, Xu K, Ronald PC, Bailey-Serres J. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 2006; 18:2021-34; PMID:16816135
  • Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 2006; 442:705-8; PMID:6900200; http://dx.doi.org/10.1038/nature04920
  • Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P. HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 2010; 62:302-15; PMID:20113439; http://dx.doi.org/10.1111/j.1365-313X.2010.04149.x
  • Voesenek LACJ, Rijnders JHGM, Peeters AJM, van de Steeg HM, de Kroon H. Plant hormones regulate fast shoot elongation under water: from genes to communities. Ecology 2004; 85:16-27; http://dx.doi.org/10.1890/02-740
  • Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 2009; 460:1026-30; PMID:19693083; http://dx.doi.org/10.1038/nature08258
  • Nakano T, Suzuki K, Fujimura T, Shinshi H. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 2006; 140:411-32; PMID:16407444
  • Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R. Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 2010; 153:757-72; PMID:20357136; http://dx.doi.org/10.1104/pp.110.155077
  • Gibbs DJ, Lee SC, Isa NM, Gramuglia S, Fukao T, Bassel GW, Correia CS, Corbineau F, Theodoulou FL, Bailey-Serres J, et al. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 2011; 479:415-8; PMID:22020279; http://dx.doi.org/10.1038/nature10534
  • Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, van Dongen JT. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 2011; 479:419-22; PMID:22020282; http://dx.doi.org/10.1038/nature10536
  • Voesenek LACJ, Bailey-Serres J. Flooding tolerance: O2 sensing and survival strategies. Curr Opin Plant Biol 2013; 16:647-53; PMID:23830867; http://dx.doi.org/10.1016/j.pbi.2013.06.008
  • Giuntoli B, Lee SC, Licausi F, Kosmacz M, Oosumi T, van Dongen JT, Bailey-Serres J, Perata P. A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis. PLoS Biol 2014; 12:e1001950. PMID:25226037; http://dx.doi.org/10.1371/journal.pbio.1001950
  • Turcotte S, Desrosiers RR, Béliveau R. HIF-1alpha mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J Cell Sci 2003; 116:2247-60; PMID:12697836
  • Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 2002; 296:2026-8; PMID:12065837; http://dx.doi.org/10.1126/science.1071505
  • Fukao T, Bailey-Serres J. Plant responses to hypoxia–is survival a balancing act? Trends Plant Sci 2004; 9:449-56; PMID:15337495; http://dx.doi.org/10.1016/j.tplants.2004.07.005
  • He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi.org/10.1146/annurev-genet-102808-114910
  • Liu Y, Bassham DC. Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 2012; 63:215-37; PMID:22242963; http://dx.doi.org/10.1146/annurev-arplant-042811-105441
  • Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K. Autophagy in development and stress responses of plants. Autophagy 2006; 2:2-11; PMID: 16874030; http://dx.doi.org/10.4161/auto.2092
  • Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40:280-93; PMID:20965422; http://dx.doi.org/10.1016/j.molcel.2010.09.023
  • Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouysségur J, Mazure NM. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 2009; 29:2570-81; PMID:19273585; http://dx.doi.org/10.1128/MCB.00166-09
  • Schaaf MBE, Cojocari D, Keulers TG, Jutten B, Starmans MH, de Jong MC, Begg AC, Savelkouls KGM, Bussink J, Vooijs M, et al. The autophagy associated gene, ULK1, promotes tolerance to chronic and acute hypoxia. Radiother Oncol 2013; 108:529-34; PMID:23849170; http://dx.doi.org/10.1016/j.radonc.2013.06.015
  • Li F, Vierstra RD. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 2012; 17:526-37; PMID:22694835; http://dx.doi.org/10.1016/j.tplants.2012.05.006
  • Bassham DC. Plant autophagy–more than a starvation response. Curr Opin Plant Biol 2007; 10:587-93; PMID:17702643; http://dx.doi.org/10.1016/j.pbi.2007.06.006
  • Han S, Yu B, Wang Y, Liu Y. Role of plant autophagy in stress response. Protein Cell 2011; 2:784-91; PMID:22058033; http://dx.doi.org/10.1007/s13238-011-1104-4
  • Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 2005; 138:2097-110; PMID:16040659
  • Xiao S, Gao W, Chen QF, Chan SW, Zheng SX, Ma J, Wang M, Welti R, Chye ML. Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell 2010; 22:1463-82; PMID:20442372; http://dx.doi.org/10.1105/tpc.110.075333
  • Zhuang X, Wang H, Lam SK, Gao C, Wang X, Cai Y, Jiang L. A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 2013; 25:4596-615; PMID:24249832; http://dx.doi.org/10.1105/tpc.113.118307
  • Sláviková S, Shy G, Yao Y, Glozman R, Levanony H, Pietrokovski S, Elazar Z, Galili G. The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. J Exp Bot 2005; 56:2839-49; PMID:16157655; http://dx.doi.org/10.1093/jxb/eri276
  • Li F, Chung T, Vierstra RD. AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell 2014; 26:788-807; PMID:24563201; http://dx.doi.org/10.1105/tpc.113.120014
  • Phillips AR, Suttangkakul A, Vierstra RD. The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 2008; 178:1339-53; PMID:18245858; http://dx.doi.org/10.1534/genetics.107.086199
  • Chung T, Phillips AR, Vierstra RD. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A and ATG12B loci. Plant J 2010; 62:483-93; PMID:20136727; http://dx.doi.org/10.1111/j.1365-313X.2010.04166.x
  • Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 2002; 14:2481-94; PMID:12368499
  • Torres MA, Dangl JL, Jones JDG. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 2002; 99:517-22; PMID:11756663; http://dx.doi.org/10.1073/pnas.012452499
  • Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 2003; 91:179-94; PMID:12509339; http://dx.doi.org/10.1093/aob/mcf118
  • Pucciariello C, Perata P. Flooding tolerance in plants. In: Shabala S (ed) Plant stress physiology. CAB International, Oxford, 2012; pp 148-171.
  • Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 2009; 21:2914-27; PMID:19773385; http://dx.doi.org/10.1105/tpc.109.068635
  • Xiao S, Chye ML. Overexpression of Arabidopsis ACBP3 enhances NPR1-dependent plant resistance to Pseudomonas syringe pv tomato DC3000. Plant Physiol 2011; 156:2069-81; PMID:21670223; http://dx.doi.org/10.1104/pp.111.176933
  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 2001; 414:562-5; PMID:11734859; http://dx.doi.org/10.1038/35107108
  • Shah J, Kachroo P, Klessig DF. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell 1999; 11:191-206; PMID:9927638
  • Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373-99; PMID:15377225; http://dx.doi.org/10.1146/annurev.arplant.55.031903.141701
  • Laloi C, Apel K, Danon A. Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 2004; 7:323-8; PMID:15134754; http://dx.doi.org/10.1016/j.pbi.2004.03.005
  • Pérez-Pérez ME, Lemaire SD, Crespo JL. Reactive oxygen species and autophagy in plants and algae. Plant Physiol 2012; 160:156-64; PMID:22744983; http://dx.doi.org/10.1104/pp.112.199992
  • Xiong Y, Contento AL, Nguyen PQ, Bassham DC. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 2007; 143:291-9; PMID:17098847
  • Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 2002; 99:6422-7; PMID:11983923; http://dx.doi.org/10.1073/pnas.092141899
  • Baena-González E, Rolland F, Thevelein JM, Sheen J. A central integrator of transcription networks in plant stress and energy signalling. Nature 2007; 448:938-42; PMID:17671505; http://dx.doi.org/10.1038/nature06069
  • Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13:132-41; PMID:21258367; http://dx.doi.org/10.1038/ncb2152
  • Liu Y, Bassham DC. TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One 2010; 5:e11883; PMID:20686696; http://dx.doi.org/10.1371/journal.pone.0011883
  • Cho YH, Hong JW, Kim EC, Yoo SD. Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 2012; 158:1955-64; PMID:22232383; http://dx.doi.org/10.1104/pp.111.189829
  • Perata P, Alpi A. Ethanol-induced injuries to carrot cells: the role of acetaldehyde. Plant Physiol 1991; 95:748-52; PMID:16668049
  • Hong-Brown LQ, Brown CR, Kazi AA, Huber DS, Pruznak AM, Lang CH. Alcohol and PRAS40 knockdown decrease mTOR activity and protein synthesis via AMPK signaling and changes in mTORC1 interaction. J Cell Biochem 2010; 109:1172-84; PMID:20127721; http://dx.doi.org/10.1002/jcb.22496
  • Chen G, Ke Z, Xu M, Liao M, Wang X, Qi Y, Zhang T, Frank JA, Bower KA, Shi X, et al. Autophagy is a protective response to ethanol neurotoxicity. Autophagy 2012; 8:1577-89; PMID:22874567; http://dx.doi.org/10.4161/auto.21376
  • Thapaliya S, Runkana A, McMullen MR, Nagy LE, McDonald C, Prasad SVN, Dasarathy S. Alcohol-induced autophagy contributes to loss in skeletal muscle mass. Autophagy 2014; 10:677-90; PMID:24492484; http://dx.doi.org/10.4161/auto.27918
  • Yang CY. Hydrogen peroxide controls transcriptional responses of ERF73/HRE1 and ADH1 via modulation of ethylene signaling during hypoxic stress. Planta 2014; 239:877-85; PMID:24395201; http://dx.doi.org/10.1007/s00425-013-2020-z
  • Prasad TK, Anderson MD, Martin BA, Stewart CR. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 1994; 6:65-74; PMID:12244221
  • Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H. A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 1999; 11:1195-206; PMID:10402422
  • Lai Z, Wang F, Zheng Z, Fan B, Chen Z. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 2011; 66:953-68; PMID:21395886; http://dx.doi.org/10.1111/j.1365-313X.2011.04553.x
  • Yang S, Hua J. A haplotype-specific resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 2004; 16: 1060-71; PMID: 15031411; http://dx.doi.org/10.1105/tpc.020479
  • Chae HS, Faure F, Kieber JJ. The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 2003; 15:545-59; PMID:12566591; http://dx.doi.org/10.1105/tpc.006882
  • Pan X, Welti R, Wang X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 2010; 5:986-92; PMID:20448544; http://dx.doi.org/10.1038/nprot.2010.37