ABA is required for plant acclimation to a combination of salt and heat stress

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Suzuki, Nobuhiro ^a   Bassil, Elias ^b   Hamilton, Jason S ^c   Inupakutika, Madhuri A ^c   Zandalinas, Sara Izquierdo ^d   Tripathy, Deesha ^c   Luo, Yuting ^c   Dion, Erin ^c   Fukui, Ginga ^a   Kumazaki, Ayana ^a   Nakano, Ruka ^a   Rivero, Rosa M ^e   Verbeck, Guido F ^c   Azad, Rajeev K ^c   Blumwald, Eduardo ^b   Mittler, Ron ^c  

^a SOPHIA UNIVERSITY   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF NORTH TEXAS   (United States)

^d UNIVERSITAT JAUME I   (Spain)

^e RESEARCH GROUP ON QUALITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; CHLOROPHYLL; ETHYLENE; JASMONIC ACID; POTASSIUM ION; SALICYLIC ACID; SODIUM ION; TRANSCRIPTOME; ARABIDOPSIS PROTEIN; SODIUM CHLORIDE;

ABIOTIC STRESS; ACCLIMATIZATION; ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENETIC ANALYSIS; HEAT STRESS; MUTANT; NONHUMAN; PLANT GROWTH; PLANT LEAF; SALT STRESS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION; WILD TYPE; ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; HEAT; METABOLISM; PHYSIOLOGICAL STRESS; SALINITY;

ABSCISIC ACID; ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; HOT TEMPERATURE; SALINITY; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL;

EID: 84958206453     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147625     Document Type: Article

References (63)

1. Cushman JC, Bohnert HJ. Genomic approaches to plant stress tolerance. Curr Opin Plant Biol. 2000; 3 (2):117-24. Epub 2000/03/14. PMID: 10712956.
2. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006; 11 (1):15-9. Epub 2005/12/20. doi: 10.1016/j.tplants.2005.11.002 PMID: 16359910.
3. Zhu Y, Qian W, Hua J. Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 2010; 6(4):e1000844. Epub 2010/04/07. doi: 10.1371/journal.ppat.1000844 PMID: 20368979; PubMed Central PMCID: PMCPmc2848567.
4. Mittler R, Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol. 2010; 61:443-62. Epub 2010/03/03. doi: 10.1146/annurev-arplant-042809-112116 PMID: 20192746.
5. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014; 203(1):32-43. Epub 2014/04/12. doi: 10.1111/nph.12797 PMID: 24720847.
6. Rizhsky L, Liang H, Mittler R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 2002; 130(3):1143-51. Epub 2002/11/13. doi: 10.1104/pp.006858 PMID: 12427981; PubMed Central PMCID: PMCPmc166635.
7. Rizhsky L, Liang H, 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 (4):1683-96. Epub 2004/03/30. doi: 10.1104/pp.103.033431 PMID: 15047901; PubMed Central PMCID: PMCPmc419842.
8. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, et al. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 2013; 161(4):1783-94. Epub 2013/03/01. doi: 10.1104/pp.112.210773 PMID: 23447525 PubMed Central PMCID: PMCPmc3613455.
9. De Boeck HJ, Bassin S, Verlinden M, Zeiter M, Hiltbrunner E. Simulated heat waves affected alpine grassland only in combination with drought. New Phytol. 2015. Epub 2015/08/13. doi: 10.1111/nph. 13601 PMID: 26267066.
10. Hu X, Wu L, Zhao F, Zhang D, Li N, Zhu G, et al. Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Front Plant Sci. 2015; 6:298. Epub 2015/05/23. doi: 10.3389/fpls.2015.00298 PMID: 25999967; PubMed Central PMCID: PMCPmc4419667.
11. Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, et al. Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol. 2015; 15:152. Epub 2015/06/21. doi: 10.1186/s12870-015-0511-8 PMID: 26092253; PubMed Central PMCID: PMCPmc4474349.
12. Sghaier DB, Duarte B, Bankaji I, Cacador I, Sleimi N. Growth, chlorophyll fluorescence and mineral nutrition in the halophyte Tamarix gallica cultivated in combined stress conditions: Arsenic and NaCl. J Photochem Photobiol B. 2015; 149:204-14. Epub 2015/06/21. doi: 10.1016/j.jphotobiol.2015.06.003 PMID: 26093232.
13. Shinde S, Behpouri A, McElwain JC, Ng CK. Genome-wide transcriptomic analysis of the effects of sub-ambient atmospheric oxygen and elevated atmospheric carbon dioxide levels on gametophytes of the moss, Physcomitrella patens. J Exp Bot. 2015; 66(13):4001-12. Epub 2015/05/08. doi: 10.1093/jxb/erv197 PMID: 25948702; PubMed Central PMCID: PMCPmc4473992.
14. Zhang YP, E ZG, Jiang H, Wang L, Zhou J, Zhu DF. A comparative study of stress-related gene expression under single stress and intercross stress in rice. Genet Mol Res. 2015; 14(2):3702-17. Epub 2015/05/13. doi: 10.4238/2015.April.17.20 PMID: 25966139.
15. Yamaguchi T, Blumwald E. Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci. 2005; 10(12):615-20. Epub 2005/11/11. doi: 10.1016/j.tplants.2005.10.002 PMID: 16280254.
16. Lobell DB, Schlenker W, Costa-Roberts J. Climate trends and global crop production since 1980. Science. 2011; 333(6042):616-20. Epub 2011/05/10. doi: 10.1126/science.1204531 PMID: 21551030.
17. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. PLANT CELLULAR AND MOLECULAR RESPONSES TO HIGH SALINITY. Annu Rev Plant Physiol Plant Mol Biol. 2000; 51:463-99. Epub 2004/03/12. doi: 10.1146/annurev.arplant.51.1.463 PMID: 15012199.
18. Conde A, Silva P, Agasse A, Conde C, Geros H. Mannitol transport and mannitol dehydrogenase activities are coordinated in Olea europaea under salt and osmotic stresses. Plant Cell Physiol. 2011; 52 (10):1766-75. Epub 2011/09/07. doi: 10.1093/pcp/pcr121 PMID: 21893515.
19. Zhang J-H, Liu Y-P, Pan Q-H, Zhan J-C, Wang X-Q, Huang W-D. Changes in membrane-associated H +-ATPase activities and amounts in young grape plants during the cross adaptation to temperature stresses. Plant Sci. 2006; 170(4):768-77.
20. Janicka-Russak M, Kabala K. Abscisic acid and hydrogen peroxide induce modification of plasma membrane H(+)-ATPase from Cucumis sativus L. roots under heat shock. J Plant Physiol. 2012; 169 (16):1607-14. Epub 2012/07/04. doi: 10.1016/j.jplph.2012.05.013 PMID: 22749287.
21. Yoon HS, Kim SY, Kim IS. Stress response of plant H+-PPase-expressing transgenic Escherichia coli and Saccharomyces cerevisiae: a potentially useful mechanism for the development of stress-tolerant organisms. J Appl Genet. 2013; 54(1):129-33. Epub 2012/10/12. doi: 10.1007/s13353-012-0117-x PMID: 23055406.
22. Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot. 2007; 58(2):221-7. Epub 2006/11/01. doi: 10.1093/jxb/erl164 PMID: 17075077.
23. Li H, Liu SS, Yi CY, Wang F, Zhou J, Xia XJ, et al. Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant Cell Environ. 2014; 37 (12):2768-80. Epub 2014/04/30. doi: 10.1111/pce.12360 PMID: 24773056.
24. Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, et al. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell. 2013; 25(9):3553-69. Epub 2013/09/17. doi: 10.1105/tpc.113.114595 PMID: 24038652; PubMed Central PMCID: PMCPmc3809549.
25. Mittler R, Blumwald E. The roles of ROS and ABA in systemic acquired acclimation. Plant Cell. 2015; 27(1):64-70. Epub 2015/01/22. doi: 10.1105/tpc.114.133090 PMID: 25604442; PubMed Central PMCID: PMCPmc4330577.
26. Wen X, Qiu N, Lu Q, Lu C. Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. Planta. 2005; 220(3):486-97. Epub 2004/12/08. doi: 10.1007/s00425- 004-1382-7 PMID: 15580526.
27. Keles Y, Oncel I. Response of antioxidative defence system to temperature and water stress combinations in wheat seedlings. Plant Sci. 2002; 163(4):783-90.WOS:000179310900014.
28. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V. The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ. 2014; 37(5):1059-73. Epub 2013/09/14. doi: 10.1111/pce.12199 PMID: 24028172.
29. Nawrath C, Metraux JP. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell. 1999; 11 (8):1393-404. Epub 1999/08/17. PMID: 10449575; PubMed Central PMCID: PMCPmc144293.
30. Caldelari D, Wang G, Farmer EE, Dong X. Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol Biol. 2011; 75(1-2):25-33. Epub 2010/11/06. doi: 10. 1007/s11103-010-9701-9 PMID: 21052784.
31. Van Der Straeten D, Djudzman A, Van Caeneghem W, Smalle J, Van Montagu M. Genetic and Physiological Analysis of a New Locus in Arabidopsis That Confers Resistance to 1-Aminocyclopropane-1- Carboxylic Acid and Ethylene and Specifically Affects the Ethylene Signal Transduction Pathway. Plant Physiol. 1993; 102(2):401-8.PMID: 12231830
32. Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem. 2008; 283(14):9269-75. Epub 2008/01/19. doi: 10.1074/jbc.M709187200 PMID: 18201973.
33. Suzuki N, Miller G, Sejima H, Harper J, Mittler R. Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2. J Exp Bot. 2013; 64(1):253-63. Epub 2012/11/28. doi: 10.1093/jxb/ers335 PMID: 23183257; PubMed Central PMCID: PMCPmc3528037.
34. Assmann SM, Snyder JA, Lee Y-RJ. ABA-deficient (aba1) and ABA-insensitive (abi1-1, abi2-1) mutants of Arabidopsis have a wild-type stomatal response to humidity. Plant Cell Environ. 2000; 23 (4):387-95. doi: 10.1046/j.1365-3040.2000.00551.x
35. Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lewis BD. Potassium uptake supporting plant growth in the absence of AKT1 channel activity: Inhibition by ammonium and stimulation by sodium. J Gen Physiol. 1999; 113(6):909-18. Epub 1999/06/03. PMID: 10352038; PubMed Central PMCID: PMCPmc2225604.
36. Yalovsky S, Ne'eman E, Schuster G, Paulsen H, Harel E, Nechushtai R. Accumulation of a light-harvesting chlorophyll a/b protein in the chloroplast grana lamellae. The lateral migration of the membrane protein precursor is independent of its processing. J Biol Chem. 1992; 267(29):20689-93. Epub 1992/10/15. PMID: 1400385.
37. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signal. 2009; 2(84): ra45. Epub 2009/08/20. doi: 10.1126/scisignal.2000448 PMID: 19690331.
38. Hamilton JS, Mach PM, Gorishek EL, Sturtevant D, Ladage ML, Suzuki N, et al. Evaluation of a custom single Peltier-cooled ablation cell for spatially resolved elemental imaging of biological samples in laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). J Anal At Spectrom. 2015.
39. Nemhauser JL, Hong F, Chory J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006; 126(3):467-75. Epub 2006/08/12. doi: 10.1016/j. cell.2006.05.050 PMID: 16901781.
40. Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, et al. Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol. 2009; 70(1-2):79-102. Epub 2009/02/10. doi: 10.1007/s11103-009-9458-1 PMID: 19199050.
41. Davletova S, Schlauch K, Coutu J, Mittler R. The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 2005; 139(2):847-56. Epub 2005/09/27. doi: 10.1104/pp.105.068254 PMID: 16183833; PubMed Central PMCID: PMCPmc1256000.
42. Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM. Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol. 2008; 66(4):361-78. Epub 2007/12/26. doi: 10.1007/s11103-007-9274-4 PMID: 18158584; PubMed Central PMCID: PMCPmc2758387.
43. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, et al. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 2006; 141 (2):436-45. Epub 2006/04/11. doi: 10.1104/pp.106.078717 PMID: 16603662; PubMed Central PMCID: PMCPmc1475436.
44. Huang D, Wu W, Abrams SR, Cutler AJ. The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot. 2008; 59(11):2991-3007. Epub 2008/06/17. doi: 10.1093/jxb/ern155 PMID: 18552355; PubMed Central PMCID: PMCPmc2504347.
45. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, et al. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol. 2008; 49(8):1135-49. Epub 2008/07/16. doi: 10.1093/pcp/pcn101 PMID: 18625610.
46. Larkindale J, Vierling E. Core genome responses involved in acclimation to high temperature. Plant Physiol. 2008; 146(2):748-61. Epub 2007/12/07. doi: 10.1104/pp.107.112060 PMID: 18055584; PubMed Central PMCID: PMCPmc2245833.
47. Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand A. Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol. 2007; 144(3):1391-406. Epub 2007/05/05. doi: 10.1104/pp.107.098293 PMID: 17478635; PubMed Central PMCID: PMCPmc1914119.
48. Ding F, Cui P, Wang Z, Zhang S, Ali S, Xiong L. Genome-wide analysis of alternative splicing of premRNA under salt stress in Arabidopsis. BMC genomics. 2014; 15:431. Epub 2014/06/06. doi: 10.1186/1471-2164-15-431 PMID: 24897929; PubMed Central PMCID: PMCPmc4079960.
49. Tosti N, Pasqualini S, Borgogni A, Ederli L, Falistocco E, Crispi S, et al. Gene expression profiles of O3- treated Arabidopsis plants. Plant Cell Environ. 2006; 29(9):1686-702. Epub 2006/08/18. doi: 10.1111/j. 1365-3040.2006.01542.x PMID: 16913859.
50. Consales F, Schweizer F, Erb M, Gouhier-Darimont C, Bodenhausen N, Bruessow F, et al. Insect oral secretions suppress wound-induced responses in Arabidopsis. J Exp Bot. 2012; 63(2):727-37. Epub 2011/10/14. doi: 10.1093/jxb/err308 PMID: 21994175; PubMed Central PMCID: PMCPmc3254683.
51. Truman W, de Zabala MT, Grant M. Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J. 2006; 46(1):14-33. Epub 2006/03/24. doi: 10.1111/j.1365-313X.2006.02672.x PMID: 16553893.
52. Atkinson NJ, Lilley CJ, Urwin PE. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 2013; 162(4):2028-41. Epub 2013/06/27. doi: 10.1104/pp.113.222372 PMID: 23800991; PubMed Central PMCID: PMCPmc3729780.
53. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25. Epub 2009/03/06. doi: 10.1186/gb- 2009-10-3-r25 PMID: 19261174; PubMed Central PMCID: PMCPmc2690996.
54. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics (Oxford, England). 2009; 25(9):1105-11. Epub 2009/03/18. doi: 10.1093/bioinformatics/btp120 PMID: 19289445; PubMed Central PMCID: PMCPmc2672628.
55. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010; 28(5):511-5. Epub 2010/05/04. doi: 10.1038/nbt.1621 PMID: 20436464; PubMed Central PMCID: PMCPmc3146043.
56. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, et al. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell. 2005; 17 (1):268-81. Epub 2004/12/21. doi: 10.1105/tpc.104.026971 PMID: 15608336; PubMed Central PMCID: PMCPmc544504.
57. Moeder W, Ung H, Mosher S, Yoshioka K. SA-ABA antagonism in defense responses. Plant Signal Behav. 2010; 5(10):1231-3. Epub 2010/09/24. doi: 10.4161/psb.5.10.12836 PMID: 20861686; PubMed Central PMCID: PMCPmc3115354.
58. Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, et al. Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol. 2012; 158 (4):1705-14. Epub 2012/02/01. doi: 10.1104/pp.111.192740 PMID: 22291200; PubMed Central PMCID: PMCPmc3320179.
59. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, et al. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem. 2008; 283 (49):34197-203. Epub 2008/10/15. doi: 10.1074/jbc.M806337200 PMID: 18852264; PubMed Central PMCID: PMCPmc2590703.
60. Shabala S, Cuin TA. Potassium transport and plant salt tolerance. Physiol Plant. 2008; 133(4):651-69. Epub 2008/08/30. PMID: 18724408.
61. Swindell WR, Huebner M, Weber AP. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC genomics. 2007; 8:125. Epub 2007/05/24. doi: 10.1186/1471-2164-8-125 PMID: 17519032; PubMed Central PMCID: PMCPmc1887538.
62. Kim DH, Xu ZY, Hwang I. AtHSP17.8 overexpression in transgenic lettuce gives rise to dehydration and salt stress resistance phenotypes through modulation of ABA-mediated signaling. Plant Cell Rep. 2013; 32(12):1953-63. Epub 2013/10/02. doi: 10.1007/s00299-013-1506-2 PMID: 24081610.
63. Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol. 2005; 139(3):1313-22. Epub 2005/10/26. doi: 10.1104/pp.105.070110 PMID: 16244138; PubMed Central PMCID: PMCPmc1283768.