HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues

Plant Physiology

Volumn 170, Issue 4, 2016, Pages 2461-2477

  Fragkostefanakis, Sotirios ^a   Mesihovic, Anida ^a   Simm, Stefan ^a   Paupière, Marine Josephine ^b   Hu, Yangjie ^a   Paul, Puneet ^a   Mishra, Shravan Kumar ^a,e   Tschiersch, Bettina ^c,f   Theres, Klaus ^d   Bovy, Arnaud ^b   Schleiff, Enrico ^a   Scharf, Klaus Dieter ^a,c  

^a GOETHE UNIVERSITY   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^e INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH MOHALI   (India)

^f BASF SE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; HEAT STRESS TRANSCRIPTION FACTORS; PLANT PROTEIN; TRANSCRIPTION FACTOR;

ANTIBODY SPECIFICITY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; HEAT SHOCK RESPONSE; HEAT TOLERANCE; METABOLISM; PHYSIOLOGY; PLANT GAMETOGENESIS; PLANT LEAF; POLLEN; SEEDLING; TOMATO; TRANSGENIC PLANT;

DNA-BINDING PROTEINS; FLOWERS; GAMETOGENESIS, PLANT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; LYCOPERSICON ESCULENTUM; ORGAN SPECIFICITY; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POLLEN; SEEDLINGS; THERMOTOLERANCE; TRANSCRIPTION FACTORS;

EID: 84962091341     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01913     Document Type: Article

References (62)

1. Alexander MP (1980) A versatile stain for pollen fungi, yeast and bacteria. Stain Technol 55: 13-18
2. Almoguera C, Prieto-Dapena P, Díaz-Martín J, Espinosa JM, Carranco R, Jordano J (2009) The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biol 9: 75
3. Becker D, Kemper E, Schell J, Masterson R (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol Biol 20: 1195-1197
4. Bharti K, Von Koskull-Döring P, Bharti S, Kumar P, Tintschl-Körbitzer A, Treuter E, Nover L (2004) Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB binding protein ortholog HAC1. Plant Cell 16: 1521-1535
5. Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA (2011) The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Res 39: D1149-D1155
6. Carreno-Quintero N, Acharjee A, Maliepaard C, Bachem CW, Mumm R, Bouwmeester H, Visser RG, Keurentjes JJ (2012) Untargeted metabolic quantitative trait loci analyses reveal a relationship between primary metabolism and potato tuber quality. Plant Physiol 158: 1306-1318
7. Chan-Schaminet KY, Baniwal SK, Bublak D, Nover L, Scharf K-D (2009) Specific interaction between tomato HsfA1 and HsfA2 creates heterooligomeric superactivator complexes for synergistic activation of heat stress gene expression. J Biol Chem 284: 20848-20857
8. Charng YY, Liu HC, Liu NY, ChiWT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143: 251-262
9. Chaturvedi P, Ischebeck T, Egelhofer V, Lichtscheidl I, Weckwerth W (2013) Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. J Proteome Res 12: 4892-4903
10. Chauhan H, Khurana N, Agarwal P, Khurana JP, Khurana P (2013) A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment. PLoS One 8: e79577
11. Coberly LC, Rausher MD (2003) Analysis of a chalcone synthase mutant in Ipomoea purpurea reveals a novel function for flavonoids: amelioration of heat stress. Mol Ecol 12: 1113-1124
12. Duck NB, Folk WR (1994) Hsp70 heat shock protein cognate is expressed and stored in developing tomato pollen. Plant Mol Biol 26: 1031-1039
13. Finka A, Mattoo RU, Goloubinoff P (2011) Meta-analysis of heat-and chemically upregulated chaperone genes in plant and human cells. Cell Stress Chaperones 16: 15-31
14. Fragkostefanakis S, Röth S, Schleiff E, Scharf KD (2015a) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ 38: 1881-1895
15. Fragkostefanakis S, Simm S, Paul P, Bublak D, Scharf K-D, Schleiff E (2015b) Chaperone network composition in Solanum lycopersicum explored by transcriptome profiling and microarray meta-analysis. Plant Cell Environ 38: 693-709
16. Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142: 1004-1013
17. Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60: 3891-3908
18. Giorno F, Wolters-Arts M, Grillo S, Scharf K-D, VriezenWH, Mariani C (2010) Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. J Exp Bot 61: 453-462
19. Gou J-Y, Miller LM, Hou G, Yu X-H, Chen X-Y, Liu C-J (2012) Acetylesterasemediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell 24: 50-65
20. Hahn A, Bublak D, Schleiff E, Scharf K-D (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23: 741-755
21. Ikeda M, Mitsuda N, Ohme-Takagi M (2011) Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol 157: 1243-1254
22. Iwahori S (1966) High temperature injuries in tomato. V. Fertilization and development of embryo with special reference to the abnormalities caused by high temperature. J Jpn Soc Hortic Sci 35: 55-62
23. Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204: 383-396
24. James LR, Andrews S, Walker S, de Sousa PR, Ray A, Russell NA, Bellamy TC (2011) High-throughput analysis of calcium signalling kinetics in astrocytes stimulated with different neurotransmitters. PLoS One 6: e26889
25. Jung K-H, Ko H-J, Nguyen MX, Kim S-R, Ronald P, An G (2012) Genomewide identification and analysis of early heat stress responsive genes in rice. J Plant Biol 55: 458-468
26. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136: 4159-4168
27. Kent WJ (2002) BLAT-the BLAST-like alignment tool. Genome Res 12: 656-664
28. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19: 479-509
29. Knapp S, Larondelle Y, Rossberg M, Furtek D, Theres K (1994) Transgenic tomato lines containing Ds elements at defined genomic positions as tools for targeted transposon tagging. Mol Gen Genet 243: 666-673
30. Kotak S, Vierling E, Bäumlein H, von Koskull-Döring P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19: 182-195
31. Liu HC, Charng YY (2013) Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol 163: 276-290
32. Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 34: 738-751
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-D D C(T)) method. Methods 25: 402-408
34. Lommen A, Kools HJ (2012) MetAlign 3.0: performance enhancement by efficient use of advances in computer hardware. Metabolomics 8: 719-726
35. Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf K-D (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16: 1555-1567
36. Ning Z, Cox AJ, Mullikin JC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11: 1725-1729
37. Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48: 535-547
38. Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58: 3373-3383
39. Paupière MJ, van Heusden AW, Bovy AG (2014) The metabolic basis of pollen thermo-tolerance: perspectives for breeding. Metabolites 4: 889-920
40. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515
41. Port M, Tripp J, Zielinski D, Weber C, Heerklotz D, Winkelhaus S, Bublak D, Scharf K-D (2004) Role of Hsp17.4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2. Plant Physiol 135: 1457-1470
42. Prieto-Dapena P, Castaño R, Almoguera C, Jordano J (2006) Improved resistance to controlled deterioration in transgenic seeds. Plant Physiol 142: 1102-1112
43. Prieto-Dapena P, Castaño R, Almoguera C, Jordano J (2008) The ectopic overexpression of a seed-specific transcription factor, HaHSFA9, confers tolerance to severe dehydration in vegetative organs. Plant J 54: 1004-1014
44. Queitsch C, Hong S-W, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12: 479-492
45. Rivero RM, Ruiz JM, García PC, López-Lefebre LR, Sánchez E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci 160: 315-321
46. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696
47. Sarkar NK, Kim Y-K, Grover A (2014) Coexpression network analysis associated with call of rice seedlings for encountering heat stress. Plant Mol Biol 84: 125-143
48. Sato S, Peet M, Thomas J (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill) under chronic, mild heat stress. Plant Cell Environ 23: 719-726
49. Scharf K-D, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819: 104-119
50. Scharf K-D, Heider H, Höhfeld I, Lyck R, Schmidt E, Nover L (1998) 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 18: 2240-2251
51. Scharf K-D, Rose S, Zott W, Schöffl F, Nover L (1990) Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO J 9: 4495-4501
52. Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, von Koskull-Döring P (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol 60: 759-772
53. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504
54. Simm S, Fragkostefanakis S, Paul P, Keller M, Einloft J, Scharf K-D, Schleiff E (2015) Identification and expression analysis of ribosome biogenesis factor co-orthologs in Solanum lycopersicum. Bioinform Biol Insights 9: 1-17
55. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21: 2213-2223
56. Tikunov YM, Laptenok S, Hall RD, Bovy A, de Vos RC (2012) MSClust: a tool for unsupervised mass spectra extraction of chromatography-mass spectrometry ion-wise aligned data. Metabolomics 8: 714-718
57. Wehmeyer N, Vierling E (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol 122: 1099-1108
58. Yakovlev IA, Lee Y, Rotter B, Olsen JE, Skrøppa T, Johnsen Ø, Fossdal CG (2014) Temperature-dependent differential transcriptomes during formation of an epigenetic memory in Norway spruce embryogenesis. Tree Genet Genomes 10: 355-366
59. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227: 957-967
60. Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim JM, Seki M, Todaka D, et al (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 286: 321-332
61. Zawada AM, Rogacev KS, Müller S, Rotter B, Winter P, Fliser D, Heine GH (2014) Massive analysis of cDNA ends (MACE) and miRNA expression profiling identifies proatherogenic pathways in chronic kidney disease. Epigenetics 9: 161-172
62. Zheng X, Moriyama EN (2013) Comparative studies of differential gene calling using RNA-Seq data. BMC Bioinformatics (Suppl) 14: S7