Unraveling regulation of the small heat shock proteins by the heat shock factor HvHsfB2c in barley: Its implications in drought stress response and seed development

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Reddy, Palakolanu Sudhakar ^a,f   Kavi Kishor, Polavarapu B ^a,b   Seiler, Christiane ^a   Kuhlmann, Markus ^a,c   Eschen Lippold, Lennart ^d   Lee, Justin ^d   Reddy, Malireddy K ^e   Sreenivasulu, Nese ^a,c,g  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b OSMANIA UNIVERSITY   (India)

^c Interdisciplinary Center for Crop Plant Research (IZN)   (Germany)

^d LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^e INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^f INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI ARID TROPICS ICRISAT   (India)

^g INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ALPHA CRYSTALLIN; CHAPERONE; COMPLEMENTARY DNA; HEAT SHOCK TRANSCRIPTION FACTOR; POLYPEPTIDE; SMALL HEAT SHOCK PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; DNA BINDING PROTEIN;

ARTICLE; BARLEY; BINDING SITE; CELL NUCLEUS; CELL ORGANELLE; COMPUTER MODEL; CONTROLLED STUDY; CYTOPLASM; DESICCATION; DEVELOPMENTAL STAGE; DNA ISOLATION; DNA RESPONSIVE ELEMENT; DROUGHT; DROUGHT STRESS; ENVIRONMENTAL EXPOSURE; ENZYME SPECIFICITY; ESCHERICHIA COLI; EVOLUTIONARY ADAPTATION; GENE FUNCTION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HEAT STRESS; HVHSFB2C GENE; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PLANT GENE; PLASTID; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS REGULATION; REGULATOR GENE; REGULATORY MECHANISM; SEED DEVELOPMENT; STRUCTURE ANALYSIS; UPREGULATION; CHEMISTRY; COMPUTER SIMULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; HEAT SHOCK RESPONSE; HORDEUM; METABOLISM; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DEVELOPMENT; PLANT SEED; PROTEIN PROTEIN INTERACTION; RICE; STRUCTURAL HOMOLOGY;

COMPUTER SIMULATION; DNA-BINDING PROTEINS; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; HEAT-SHOCK PROTEINS, SMALL; HEAT-SHOCK RESPONSE; HORDEUM; HOT TEMPERATURE; MULTIGENE FAMILY; ORYZA SATIVA; PHYLOGENY; PLANT DEVELOPMENT; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION MAPS; SEEDS; STRESS, PHYSIOLOGICAL; STRUCTURAL HOMOLOGY, PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84897056716     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089125     Document Type: Article

References (64)

1. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9: 244-252. (Pubitemid 38617223)
2. van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8: 1025-1030. (Pubitemid 33101621)
3. Basha E, Jones C, Wysocki V, Vierling E (2010) Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J Biol Chem 285: 11489-11497.
4. Puigderrajols P, Jofre A, Mir G, Pla M, Verdaguer D, et al. (2002) Developmentally and stress- induced small heat shock proteins in cork oak somatic embryos. J Exp Bot 53: 1445-1452. (Pubitemid 34589559)
5. Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10: 393.
6. Wehmeyer N, Hernandez LD, Finkelstein RR, Vierling E (1996) Synthesis of small heat-shock proteins is part of the developmental program of late seed maturation. Plant Physiol 112: 747-757.
7. 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. (Pubitemid 30221389)
8. Scharf KD, 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.
9. Kotak S, Port M, Ganguli A, Bicker F, von Koskull-Doring P (2004) 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 39: 98-112. (Pubitemid 38893581)
10. Prandl R, Schoffl F (1996) Heat shock elements are involved in heat shock promoter activation during tobacco seed maturation. Plant Mol Biol 31: 157-162. (Pubitemid 26320406)
11. Rojas A, Almoguera C, Jordano J (1999) Transcriptional activation of a heat shock gene promoter in sunflower embryos: synergism between ABI3 and heat shock factors. Plant J 20: 601-610.
12. Long TA, Brady SM, Benfey PN (2008) Systems approaches to identifying gene regulatory networks in plants. Annu Rev Cell Dev Biol 24: 81-103.
13. Ma S, Bohnert HJ (2007) Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol 8: R49.
14. Hong SW, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27: 25-35.
15. Kotak S, Vierling E, Baumlein H, von Koskull-Doring P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19: 182-195. (Pubitemid 46852710)
16. Matsumoto T, Tanaka T, Sakai H, Amano N, Kanamori H, et al. (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 156: 20-28.
17. Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U, et al. (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146: 1738-1758. (Pubitemid 352844076)
18. Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, et al. (2004) A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol 134: 960-968. (Pubitemid 38398245)
19. Mutwil M, Klie S, Tohge T, Giorgi FM, Wilkins O, et al. (2011) PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23: 895-910.
20. De Bodt S, Hollunder J, Nelissen H, Meulemeester N, Inze D (2012) CORNET 2.0: integrating plant coexpression, protein-protein interactions, regulatory interactions, gene associations and functional annotations. New Phytol 195: 707-720.
21. Mayer KF, Martis M, Hedley PE, Simkova H, Liu H, et al. (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23: 1249-1263.
22. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297-300. (Pubitemid 29209466)
23. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, et al. (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30: 325-327. (Pubitemid 34685468)
24. Kuhlmann M, Horvay K, Strathmann A, Heinekamp T, Fischer U, et al. (2003) The alpha-helical D1 domain of the tobacco bZIP transcription factor BZI-1 interacts with the ankyrin-repeat protein ANK1 and is important for BZI-1 function, both in auxin signaling and pathogen response. J Biol Chem 278: 8786-8794. (Pubitemid 36800636)
25. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572.
26. Sun CW, Callis J (1997) Independent modulation of Arabidopsis thaliana polyubiquitin mRNAs in different organs and in response to environmental changes. Plant J 11: 1017-1027.
27. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41. (Pubitemid 47223816)
28. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage- associated molecular patterns. Plant J 68: 100-113.
29. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201. (Pubitemid 43205406)
30. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
31. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40.
32. Reddy PS, Reddy GM, Pandey P, Chandrasekhar K, Reddy MK (2012) Cloning and molecular characterization of a gene encoding late embryogenesis abundant protein from Pennisetum glaucum: protection against abiotic stresses. Mol Biol Rep 39: 7163-7174.
33. Reddy PS, Thirulogachandar V, Vaishnavi CS, Aakrati A, Sopory SK, et al. (2011) Molecular characterization and expression of a gene encoding cytosolic Hsp90 from Pennisetum glaucum and its role in abiotic stress adaptation. Gene 474: 29-38.
34. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
35. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36.
36. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4: 1581-1590. (Pubitemid 38738317)
37. Chauhan H, Khurana N, Agarwal P, Khurana P (2011) Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol Genet Genomics 286: 171-187.
38. Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, et al. (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12: 76.
39. Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem 47: 785-795.
40. Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64: 391-403.
41. Caspers GJ, Leunissen JA, de Jong WW (1995) The expanding small heat-shock protein family, and structure predictions of the conserved ©alpha-crystallin domain". J Mol Evol 40: 238-248.
42. Straub PF, Shen Q, Ho TD (1994) Structure and promoter analysis of an ABA-and stress- regulated barley gene, HVA1. Plant Mol Biol 26: 617-630. (Pubitemid 2158250)
43. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-587.
44. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37: D387-392.
45. Stamler R, Kappe G, Boelens W, Slingsby C (2005) Wrapping the alpha-crystallin domain fold in a chaperone assembly. J Mol Biol 353: 68-79. (Pubitemid 41338840)
46. Lee GJ, Pokala N, Vierling E (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270: 10432-10438.
47. Siddique M, Port M, Tripp J, Weber C, Zielinski D, et al. (2003) Tomato heat stress protein Hsp16.1-CIII represents a member of a new class of nucleocytoplasmic small heat stress proteins in plants. Cell Stress Chaperones 8: 381-394. (Pubitemid 38222884)
48. Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13: 127-142.
49. Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant Cell Environ 35: 1912-1931.
50. Sreenivasulu N, Radchuk V, Strickert M, Miersch O, Weschke W, et al. (2006) Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA- regulated maturation in developing barley seeds. Plant J 47: 310-327. (Pubitemid 43974636)
51. Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annual review of plant biology 64: 189-217.
52. Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506: 265-273.
53. Rana RM, Dong S, Tang H, Ahmad F, Zhang H (2012) Functional analysis of OsHSBP1 and OsHSBP2 revealed their involvement in the heat shock response in rice (Oryza sativa L.). J Exp Bot 63: 6003-6016.
54. Almoguera C, Rojas A, Diaz-Martin J, Prieto-Dapena P, Carranco R, et al. (2002) A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. J Biol Chem 277: 43866-43872. (Pubitemid 36157809)
55. Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, et al. (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6: 177-189. (Pubitemid 32912002)
56. von Koskull-Doring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12: 452-457. (Pubitemid 47465032)
57. Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor- dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41: 1-14.
58. Lohmann C, Eggers-Schumacher G, Wunderlich M, Schoffl F (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol Genet Genomics 271: 11-21. (Pubitemid 38299681)
59. 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.
60. Begum T, Reuter R, Schoffl F (2013) Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis. Mech Dev 130: 54-60.
61. Ren Y, Liu Y, Chen H, Li G, Zhang X, et al. (2012) Type 4 metallothionein genes are involved in regulating Zn ion accumulation in late embryo and in controlling early seedling growth in Arabidopsis. Plant Cell Environ 35: 770-789.
62. Morrow G, Inaguma Y, Kato K, Tanguay RM (2000) The small heat shock protein Hsp22 of Drosophila melanogaster is a mitochondrial protein displaying oligomeric organization. J Biol Chem 275: 31204-31210.
63. Low D, Brandle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211: 575-582.
64. Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27: 407-415. (Pubitemid 32943820)