Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy

References

• Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ 2013; 20:21-30; PMID:22722335; http://dx.doi.org/10.1038/cdd.2012.72
   PubMed Web of Science ®Google Scholar
• Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011; 475:324-32; PMID:21776078; http://dx.doi.org/10.1038/nature10317
   PubMed Web of Science ®Google Scholar
• Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147:728-41; PMID:22078875; http://dx.doi.org/10.1016/j.cell.2011.10.026
   PubMed Web of Science ®Google Scholar
• Ausubel FM. Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 2005; 6:973-9; PMID:16177805; http://dx.doi.org/10.1038/ni1253
   PubMed Web of Science ®Google Scholar
• Suzuki N, Koussevitzky S, Mittler R, Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012; 35:259-70; PMID:21486305; http://dx.doi.org/10.1111/j.1365-3040.2011.02336.x
   PubMed Web of Science ®Google Scholar
• Peleg Z, Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 2011; 14:290-5; PMID:21377404; http://dx.doi.org/10.1016/j.pbi.2011.02.001
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21; PMID:11099404; http://dx.doi.org/10.1126/science.290.5497.1717
   PubMed Web of Science ®Google Scholar
• Il Kwon S, Park OK. Autophagy in Plants. J Plant Biol 2008; 51:313-20; http://dx.doi.org/10.1007/BF03036132
   Web of Science ®Google Scholar
• Kim SH, Kwon C, Lee JH, Chung T. Genes for plant autophagy: Functions and interactions. Mol Cells 2012; 34:413-23; PMID:22772908; http://dx.doi.org/10.1007/s10059-012-0098-y
   PubMed Web of Science ®Google Scholar
• Diaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 2008; 4:851-65; PMID:18670193; http://dx.doi.org/10.4161/auto.6555
   PubMed Web of Science ®Google Scholar
• Liu YM, Bassham DC. TOR is a negative regulator of autophagy in Arabidopsis thaliana. Plos One 2010; 5(7): e11883; http://dx.doi.org/10.1371/journal.pone.0011883
   Web of Science ®Google Scholar
• Liu YM, Xiong Y, Bassham DC. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 2009; 5:954-63; PMID:19587533; http://dx.doi.org/10.4161/auto.5.7.9290
   PubMed Web of Science ®Google Scholar
• Zhou J, Wang J, Yu JQ, Chen Z. Role and regulation of autophagy in heat stress responses of tomato plants. Front Plant Sci 2014; 5:174; PMID:24817875
   PubMed Web of Science ®Google Scholar
• Akerfelt M, Morimoto RI, Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Bio 2010; 11:545-55; http://dx.doi.org/10.1038/nrm2938
   PubMed Web of Science ®Google Scholar
• von Koskull-Doring P, Scharf KD, Nover L. The diversity of plant heat stress transcription factors. Trends Plant Sci 2007; 12:452-7; PMID:17826296; http://dx.doi.org/10.1016/j.tplants.2007.08.014
   PubMed Web of Science ®Google Scholar
• Scharf KD, Berberich T, Ebersberger I, Nover L. The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Bba-Gene Regul Mech 2012; 1819:104-19.
   Google Scholar
• Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperon 2001; 6:177-89; http://dx.doi.org/10.1379/1466-1268(2001)006%3c0177:AATHST%3e2.0.CO;2
   PubMed Web of Science ®Google Scholar
• Kotak S, Port M, Ganguli A, Bicker F, von Koskull-Doring P. Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J 2004; 39:98-112; PMID:15200645; http://dx.doi.org/10.1111/j.1365-313X.2004.02111.x
   PubMed Web of Science ®Google Scholar
• Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim JM, Seki M, Todaka D, et al. Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 2011; 286:321-32; PMID:21931939; http://dx.doi.org/10.1007/s00438-011-0647-7
   PubMed Web of Science ®Google Scholar
• Nishizawa-Yokoi A, Nosaka R, Hayashi H, Tainaka H, Maruta T, Tamoi M, Ikeda M, Ohme-Takagi M, Yoshimura K, Yabuta Y, et al. HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol 2011; 52:933-45; PMID:21471117; http://dx.doi.org/10.1093/pcp/pcr045
   PubMed Web of Science ®Google Scholar
• Liu HC, Liao HT, Charng YY. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 2011; 34:738-51; PMID:21241330; http://dx.doi.org/10.1111/j.1365-3040.2011.02278.x
   PubMed Web of Science ®Google Scholar
• Scharf KD, Heider H, Hohfeld I, Lyck R, Schmidt E, Nover L. The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol Cell Biol 1998; 18:2240-51; PMID:9528795
   PubMed Web of Science ®Google Scholar
• Liu Y, Zhang C, Chen J, Guo L, Li X, Li W, Yu Z, Deng J, Zhang P, Zhang K, et al. Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol Biochem 2013; 64:92-8; PMID:23399534; http://dx.doi.org/10.1016/j.plaphy.2012.12.013
   PubMed Web of Science ®Google Scholar
• Hahn A, Bublak D, Schleiff E, Scharf KD. Crosstalk between Hsp90 and Hsp70 Chaperones and Heat Stress Transcription Factors in Tomato. Plant Cell 2011; 23:741-55; PMID:21307284; http://dx.doi.org/10.1105/tpc.110.076018
   PubMed Web of Science ®Google Scholar
• Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD. In the complex family of heat stress transcription factors, HSfA1 has a unique role as master regulator of thermotolerance in tomato. Gene Dev 2002; 16:1555-67; PMID:12080093; http://dx.doi.org/10.1101/gad.228802
   PubMed Web of Science ®Google Scholar
• Lee JH, Hubel A, Schoffl F. Derepression of the Activity of Genetically-Engineered Heat-Shock Factor Causes Constitutive Synthesis of Heat-Shock Proteins and Increased Thermotolerance in Transgenic Arabidopsis. Plant J 1995; 8:603-12; PMID:7496404; http://dx.doi.org/10.1046/j.1365-313X.1995.8040603.x
   PubMed Web of Science ®Google Scholar
• Turnage MA, Muangsan N, Peele CG, Robertson D. Geminivirus-based vectors for gene silencing in Arabidopsis. Plant J 2002; 30:107-14; PMID:11967097; http://dx.doi.org/10.1046/j.1365-313X.2002.01261.x
   PubMed Web of Science ®Google Scholar
• Brigneti G, Martin-Hernandez AM, Jin HL, Chen J, Baulcombe DC, Baker B, Jones JD. Virus-induced gene silencing in Solanum species. Plant J 2004; 39:264-72; PMID:15225290; http://dx.doi.org/10.1111/j.1365-313X.2004.02122.x
   PubMed Web of Science ®Google Scholar
• Liu YL, Schiff M, Dinesh-Kumar SP. Virus-induced gene silencing in tomato. Plant J 2002; 31:777-86; PMID:12220268; http://dx.doi.org/10.1046/j.1365-313X.2002.01394.x
   PubMed Web of Science ®Google Scholar
• Zhou J, Wang J, Cheng Y, Chi YJ, Fan B, Yu JQ, Chen Z. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet 2013; 9:e1003196; PMID:23341779; http://dx.doi.org/10.1371/journal.pgen.1003196
   PubMed Web of Science ®Google Scholar
• Wang Y, Yu B, Zhao J, Guo J, Li Y, Han S, Huang L, Du Y, Hong Y, Tang D, et al. Autophagy contributes to leaf starch degradation. Plant Cell 2013; 25:1383-99; PMID:23564204; http://dx.doi.org/10.1105/tpc.112.108993
   PubMed Web of Science ®Google Scholar
• Kwon SI, Cho HJ, Kim SR, Park OK. The Rab GTPase RabG3b positively regulates autophagy and immunity-associated hypersensitive cell death in Arabidopsis. Plant Physiol 2013; 161:1722-36; PMID:23404918; http://dx.doi.org/10.1104/pp.112.208108
   PubMed Web of Science ®Google Scholar
• Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP, Naylor RL. Prioritizing climate change adaptation needs for food security in 2030. Science 2008; 319:607-10; PMID:18239122; http://dx.doi.org/10.1126/science.1152339
   PubMed Web of Science ®Google Scholar
• Zhu JK. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 2002; 53:247-73; PMID:12221975; http://dx.doi.org/10.1146/annurev.arplant.53.091401.143329
   PubMed Web of Science ®Google Scholar
• Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 2006; 57:781-803; PMID:16669782; http://dx.doi.org/10.1146/annurev.arplant.57.032905.105444
   PubMed Web of Science ®Google Scholar
• Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot 2007; 58:221-7; PMID:17075077; http://dx.doi.org/10.1093/jxb/erl164
   PubMed Web of Science ®Google Scholar
• Hoekstra FA, Golovina EA, Buitink J. Mechanisms of plant desiccation tolerance. Trends Plant Sci 2001; 6:431-8; PMID:11544133; http://dx.doi.org/10.1016/S1360-1385(01)02052-0
   PubMed Web of Science ®Google Scholar
• Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech 2005; 16:123-32; PMID:15831376; http://dx.doi.org/10.1016/j.copbio.2005.02.001
   PubMed Web of Science ®Google Scholar
• Goyal K, Walton LJ, Tunnacliffe A. LEA proteins prevent protein aggregation due to water stress. Biochem J 2005; 388:151-7; PMID:15631617; http://dx.doi.org/10.1042/BJ20041931
   PubMed Web of Science ®Google Scholar
• Wang WX, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004; 9:244-52; PMID:15130550; http://dx.doi.org/10.1016/j.tplants.2004.03.006
   PubMed Web of Science ®Google Scholar
• Liu LJ, Cui F, Li QL, Yin BJ, Zhang HW, Lin BY, Wu Y, Xia R, Tang S, Xie Q. The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res 2011; 21:957-69; PMID:21187857; http://dx.doi.org/10.1038/cr.2010.181
   PubMed Web of Science ®Google Scholar
• Zhou J, Zhang Y, Qi JX, Chi YJ, Fan BF, Yu JQ, et al. E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses. PLoS Genet 2014; 10(1): e1004116; http://dx.doi.org/10.1371/journal.pgen.1004116
   Web of Science ®Google Scholar
• Kraft E, Stone SL, Ma LG, Su N, Gao Y, Lau OS, Deng XW, Callis J. Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 2005; 139:1597-611; PMID:16339806; http://dx.doi.org/10.1104/pp.105.067983
   PubMed Web of Science ®Google Scholar
• Walsh CK, Sadanandom A. Ubiquitin chain topology in plant cell signaling: a new facet to an evergreen story. Front Plant Sci 2014; 5:122; http://dx.doi.org/10.3389/fpls.2014.00122
   Web of Science ®Google Scholar
• Gamerdinger M, Carra S, Behl C. Emerging roles of molecular chaperones and co-chaperones in selective autophagy: focus on BAG proteins. J Mol Med 2011; 89:1175-82; PMID:21818581; http://dx.doi.org/10.1007/s00109-011-0795-6
   PubMed Web of Science ®Google Scholar
• Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU. Molecular Chaperone Functions in Protein Folding and Proteostasis. Annu Rev Biochem 2013; 82:323-55; PMID:23746257; http://dx.doi.org/10.1146/annurev-biochem-060208-092442
   PubMed Web of Science ®Google Scholar
• Dokladny K, Myers OB, Moseley PL. Heat shock response and autophagy—cooperation and control. Autophagy 2015; 11:200-13; PMID:25714619; http://dx.doi.org/10.1080/15548627.2015.1009776
   PubMed Web of Science ®Google Scholar
• Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292:1552-5; PMID:11375494; http://dx.doi.org/10.1126/science.292.5521.1552
   PubMed Web of Science ®Google Scholar
• Peteranderl R, Rabenstein M, Shin YK, Liu CW, Wemmer DE, King DS, Nelson HC. Biochemical and biophysical characterization of the trimerization domain from the heat shock transcription factor. Biochem 1999; 38:3559-69; http://dx.doi.org/10.1021/bi981774j
   PubMed Web of Science ®Google Scholar
• Busch W, Wunderlich M, Schoffl F. Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 2005; 41:1-14; PMID:15610345; http://dx.doi.org/10.1111/j.1365-313X.2004.02272.x
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Xiong Y, Contento AL, Bassham DC. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 2005; 42:535-46; PMID:15860012; http://dx.doi.org/10.1111/j.1365-313X.2005.02397.x
   PubMed Web of Science ®Google Scholar
• Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 2004; 134:1683-96; PMID:15047901; http://dx.doi.org/10.1104/pp.103.033431
   PubMed Web of Science ®Google Scholar
• Desai S, Liu ZX, Yao J, Patel N, Chen JQ, Wu Y, Ahn EE, Fodstad O, Tan M. Heat shock factor 1 (HSF1) controls chemoresistance and autophagy through transcriptional regulation of autophagy-related protein 7 (ATG7). J Biol Chem 2013; 288:9165-76; PMID:23386620; http://dx.doi.org/10.1074/jbc.M112.422071
   PubMed Web of Science ®Google Scholar
• Chan-Schaminet KY, Baniwal SK, Bublak D, Nover L, Scharf KD. Specific interaction between tomato HsfA1 and HsfA2 creates hetero-oligomeric superactivator complexes for synergistic activation of heat stress gene expression. J Biol Chem 2009; 284:20848-57; PMID:19491106; http://dx.doi.org/10.1074/jbc.M109.007336
   PubMed Web of Science ®Google Scholar
• Li SX, Liu JX, Liu ZY, Li XR, Wu FJ, He YK. HEAT-INDUCED TAS1 TARGET1 mediates thermotolerance via HEAT STRESS TRANSCRIPTION FACTOR A1a-directed pathways in Arabidopsis. Plant Cell 2014; 26:1764-80; PMID:24728648; http://dx.doi.org/10.1105/tpc.114.124883
   PubMed Web of Science ®Google Scholar
• Fillatti JJ, Kiser J, Rose R, Comai L. Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Bio-Technol 1987; 5:726-30; http://dx.doi.org/10.1038/nbt0787-726
   Web of Science ®Google Scholar
• Ekengren SK, Liu YL, Schiff M, Dinesh-Kumar SP, Martin GB. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 2003; 36:905-17; PMID:14675454; http://dx.doi.org/10.1046/j.1365-313X.2003.01944.x
   PubMed Web of Science ®Google Scholar
• Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ. Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 2014; 37:2036-50; PMID:24428600; http://dx.doi.org/10.1111/pce.12275
   PubMed Web of Science ®Google Scholar
• Zhou YH, Lam HM, Zhang JH. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot 2011; 58:1207-17; http://dx.doi.org/10.1093/jxb/erl291
   Web of Science ®Google Scholar
• Welsch R, Wust F, Bar C, Al-Babili S, Beyer P. A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol 2008; 147:367-80; PMID:18326788; http://dx.doi.org/10.1104/pp.108.117028
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 2004; 16:2967-83; PMID:15494556; http://dx.doi.org/10.1105/tpc.104.025395
   PubMed Web of Science ®Google Scholar
• Lai ZB, Li Y, Wang F, Cheng Y, Fan BF, Yu JQ, Chen Z. Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 2011; 23:3824-41; PMID:21990940; http://dx.doi.org/10.1105/tpc.111.090571
   PubMed Web of Science ®Google Scholar