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Distinct heat-shock element arrangements that mediate the heat shock, but not the late-embryogenesis induction of small heat-shock proteins, correlate with promoter activation in root-knot nematode feeding cells

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Abstract

Genes coding small heat-shock proteins (sHSPs) show distinct behaviours with respect to environmental and developmental signals. Their transcriptional regulation depends on particular combinations of heat stress cis-elements (heat-shock elements; HSEs) but many aspects regarding their regulation remain unclear. Cyst and root-knot nematodes induce, in the roots of infected plants, the differentiation of special feeding cells with high metabolic activity (syncytia and giant cells, respectively), a process accompanied by extensive gene expression changes. The Hahsp17.7G4 (G4) promoter was active in giant cells and its HSE arrangements were crucial for this activation. In the present work, we provide further basis to associate giant cell expression with the heat-shock response of this gene class, by analysing additional promoters. The Hahsp17.6G1 (G1) promoter, not induced by heat shock, was silent in giant cells, while Hahsp18.6G2 (G2), which responds to heat shock, was specifically induced in giant cells. In addition, a mutated Hahsp17.7G4 promoter version (G4MutP) with a strong heat-shock induction was also induced in giant cells. The responses of the different promoters correlated with distinct HSE configurations, which might have implications on differential trans-activation. Furthermore, the shortest giant cell and heat-shock-inducible sHSP promoter version analysed in tobacco (−83pb Hahsp17.7G4) fully maintained its expression profile in Arabidopsis. Cyst nematodes did not induce the Hahsp17.7G4 promoter, revealing additional specificity in the nematode response. These findings, together with the fact that the class I sHSP products of endogenous genes accumulated specifically in tobacco giant cells, support the idea that these nematode-induced giant cells represent a transcriptional state very similar to that produced by heat shock regarding this class of genes. The high metabolic rate of giant cells may result in unfolded proteins requiring class I sHSPs as chaperones, which might, somehow, mimic heat-shock and/or other stress responses.

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References

  • Almoguera C, Coca MA, Jordano J (1993) Tissue-specific expression of sunflower heat shock proteins in response to water stress. Plant J 4:947–958

    Article  CAS  Google Scholar 

  • Almoguera C, Prieto-Dapena P, Jordano J (1998) Dual regulation of a heat shock promoter during embryogenesis: stage-dependent role of heat shock elements. Plant J 13:437–446

    Article  PubMed  CAS  Google Scholar 

  • Almoguera C, Rojas A, Jordano J (2002a) Reversible heat-induced inactivation of chimeric beta-glucuronidase in transgenic plants. Plant Physiol 129:333–341

    Article  PubMed  CAS  Google Scholar 

  • Almoguera C, Rojas A, Diaz-Martin J, Prieto-Dapena P, Carranco R, Jordano J (2002b) A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. J Biol Chem 277:43866–43872

    Article  PubMed  CAS  Google Scholar 

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf K-D, Tripp J, Weber C, Zielinski D, von Koskull-Döring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487

    Article  PubMed  CAS  Google Scholar 

  • Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylides C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13:519–527

    Article  PubMed  CAS  Google Scholar 

  • Bar-Or C, Kapulnik Y, Koltai H (2005) A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. Eur J Plant Pathol 111:181–192

    Article  CAS  Google Scholar 

  • Basha E, Lee GJ, Breci LA, Hausrath AC, Buan NR, Giese KC, Vierling E (2004) The identity of proteins associated with a small heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J Biol Chem 279:7566–7575

    Article  PubMed  CAS  Google Scholar 

  • Bharti K (2003) Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with HAC1/CBP. Johann Wolfgang Goethe-Universität, Frankfurt am Main, 126

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bird AF (1961) The ultrastructure and histochemistry of a nematode-induced giant cell. J Biophys Biochem Cytol 11:701–715

    Article  PubMed  CAS  Google Scholar 

  • Bleve-Zacheo T, Melillo MT (1997) The biology of giant cells. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant–nematode interactions. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp 65–79

    Google Scholar 

  • Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510

    Article  PubMed  CAS  Google Scholar 

  • Busch W, Wunderlich M, Schöffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41:1–14

    Article  PubMed  CAS  Google Scholar 

  • Carranco R, Almoguera C, Jordano J (1997) A plant small heat shock protein gene expressed during zygotic embryogenesis but noninducible by heat stress. J Biol Chem 272:27470–27475

    Article  PubMed  CAS  Google Scholar 

  • Carranco R, Almoguera C, Jordano J (1999) An imperfect heat shock element and different upstream sequences are required for the seed-specific expression of a small heat shock protein gene. Plant Physiol 121:723–730

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Coca MA, Almoguera C, Jordano J (1994) Expression of sunflower low-molecular-weight heat-shock proteins during embryogenesis and persistence after germination: localization and possible functional implications. Plant Mol Biol 25:479–492

    Article  PubMed  CAS  Google Scholar 

  • Coca MA, Almoguera C, Thomas TL, Jordano J (1996) Differential regulation of small heat-shock genes in plants: analysis of a water-stress-inducible and developmentally activated sunflower promoter. Plant Mol Biol 31:863–876

    Article  PubMed  CAS  Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281

    Article  PubMed  CAS  Google Scholar 

  • de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38:12–26

    Article  PubMed  Google Scholar 

  • de Meutter J, Robertson L, Parcy F, Mena M, Fenoll C, Gheysen G (2005) Differential activation of ABI3 and LEA genes upon plant parasitic nematode infection. Mol Plant Pathol 6:321–325

    Article  Google Scholar 

  • Diaz-Martin J, Almoguera C, Prieto-Dapena P, Espinosa JM, Jordano J (2005) Functional interaction between two transcription factors involved in the developmental regulation of a small heat stress protein gene promoter. Plant Physiol 139:1483–1494

    Article  PubMed  CAS  Google Scholar 

  • Dure L 3rd (1993) The LEA proteins of higher plants. In: Verma DPS (ed) Control of plant gene expression. CRC Press, Boca Raton, Florida, pp 325–335

    Google Scholar 

  • Escobar C, De Meutter J, Aristizábal FA, Sanz-Alférez S, del Campo FF, Barthels N, Van der Eycken W, Seurinck J, van Montagu M, Gheysen G, Fenoll C (1999) Isolation of the LEMMI9 gene and promoter analysis during a compatible plant-nematode interaction. Mol Plant Microbe Interact 12:440–449

    Article  PubMed  CAS  Google Scholar 

  • Escobar C, Barcala M, Portillo M, Almoguera C, Jordano J, Fenoll C (2003) Induction of the Hahsp17.7G4 promoter by root-knot nematodes: involvement of heat-shock elements in promoter activity in giant cells. Mol Plant Microbe Interact 16:1062–1068

    Article  PubMed  CAS  Google Scholar 

  • Fray RG, Lycett GW, Grierson D (1990) Nucleotide sequence of a heat-shock and ripening-related cDNA from tomato. Nucleic Acids Res 18:7148

    Article  PubMed  CAS  Google Scholar 

  • Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219

    Article  PubMed  CAS  Google Scholar 

  • Grundler FMW, Böckenhoff A (1997) Physiology of nematode feeding and feeding sites. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant-nematode interactions. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp 107–119

    Google Scholar 

  • Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846

    Article  PubMed  CAS  Google Scholar 

  • Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444

    Article  PubMed  CAS  Google Scholar 

  • Heungens K, Mugniéry D, Van Montagu M, Gheysen G, Niebel A (1996) A method to obtain disinfected Globodera infective juveniles directly from cysts. Fundam Appl Nematol 19:91–93

    Google Scholar 

  • Hong S-W, 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

    Article  PubMed  CAS  Google Scholar 

  • Hussey RS, Mims CW (1991) Ultrastructure of feeding tubes formed in giant-cells induced in plants by the root-knot nematode Meloidogyne incognita. Protoplasma 162:99–107

    Article  Google Scholar 

  • Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447–458

    Article  PubMed  CAS  Google Scholar 

  • Laskowska E, Wawrzynów A, Taylor A (1996) IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78:117–122

    Article  PubMed  CAS  Google Scholar 

  • Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16:659–671

    Article  PubMed  CAS  Google Scholar 

  • Lewi DM, Hopp HE, Escandón AS (2006) Sunflower (Helianthus annuus L.). Methods Mol Biol 343:291–297

    PubMed  CAS  Google Scholar 

  • Lohmann C, Eggers-Schumacher G, Wunderlich M, Schöffl F (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol Genet Genomics 271:11–21

    Article  PubMed  CAS  Google Scholar 

  • Löw D, Brändle 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

    Article  PubMed  Google Scholar 

  • Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot (Lond) 98:279–288

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mitchum MG, Sukno S, Wang X, Shani Z, Tsabary G, Shoseyov O, Davis EL (2004) The promoter of the Arabidopsis thaliana Cel1 endo-1,4-beta glucanase gene is differentially expressed in plant feeding cells induced by root-knot and cyst nematodes. Mol Plant Pathol 5:175–181

    Article  CAS  Google Scholar 

  • Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796

    PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nover L, Scharf K-D, Gagliardi D, Vergne P, Czarnecka-Verner E, Gurley WB (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones 1:215–223

    Article  PubMed  CAS  Google Scholar 

  • Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf K-D (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6:177–189

    Article  PubMed  CAS  Google Scholar 

  • Paulson RE, Webster JM (1970) Giant cell formation in tomato roots caused by Meloidogyne incognita and Meloidogyne hapla (Nematoda) infection. A light and electron microscope study. Can J Bot 48:271–276

    Article  Google Scholar 

  • Prändl R, Kloske E, Schöffl F (1995) Developmental regulation and tissue-specific differences of heat shock gene expression in transgenic tobacco and Arabidopsis plants. Plant Mol Biol 28:73–82

    Article  PubMed  Google Scholar 

  • Ramsay K, Wang Z, Jones MGK (2004) Using laser capture microdissection to study gene expression in early stages of giant cells induced by root-knot nematodes. Mol Plant Pathol 5:587–592

    Article  CAS  Google Scholar 

  • Rieping M, Schöffl F (1992) Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco. Mol Gen Genet 231:226–232

    PubMed  CAS  Google Scholar 

  • Reindl A, Schöffl F (1998) Interaction between the Arabidopsis thaliana heat shock transcription factor HSF1 and the TATA binding protein TBP. FEBS Lett 436:318–322

    Article  PubMed  CAS  Google Scholar 

  • Reindl A, Schöffl F, Schell J, Koncz C, Bako L (1997) Phosphorylation by a cyclin-dependent kinase modulates DNA binding of the Arabidopsis heat-shock transcription factor HSF1 in vitro. Plant Physiol 115:93–100

    Article  PubMed  CAS  Google Scholar 

  • Rojas A, Almoguera C, Carranco R, Scharf K-D, Jordano J (2002) Selective activation of the developmentally regulated Ha hsp17.6 G1 promoter by heat stress transcription factors. Plant Physiol 129:1207–1215

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Scharf K-D, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones 6:225–237

    Article  PubMed  CAS  Google Scholar 

  • Shingles J, Lilley CJ, Atkinson HJ, Urwin PE (2007) Meloidogyne incognita: molecular and biochemical characterisation of a cathepsin L cysteine proteinase and the effect on parasitism following RNAi. Exp Parasitol 115:114–120

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    PubMed  CAS  Google Scholar 

  • Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125

    Article  PubMed  CAS  Google Scholar 

  • Van der Eycken W, de Almeida Engler J, Inzé D, Van Montagu M, Gheysen G (1996) A molecular study of root-knot nematode-induced feeding sites. Plant J 9:45–54

    Article  PubMed  Google Scholar 

  • Vanholme B, De Meutter J, Tytgat T, Van Montagu M, Coomans A, Gheysen G (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332:13–27

    Article  PubMed  CAS  Google Scholar 

  • Vercauteren I, Goeleven E, Barthels N, Van Montagu M, Gheysen G (1998) The rha1 gene, encoding a small GTP-binding protein, is induced in nematode infection sites. Arch Physiol Biochem 106:158

    Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Volkov RA, Panchuk II, Schöffl F (2005) Small heat shock proteins are differentially regulated during pollen development and following heat stress in tobacco. Plant Mol Biol 57:487–502

    Article  PubMed  CAS  Google Scholar 

  • Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325–338

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM, Cosgrove DJ, Kreil DP, Puzio PS, Bohlmann H, Grundler FMW (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J 48:98–112

    Article  PubMed  CAS  Google Scholar 

  • Wunderlich M, Werr W, Schöffl F (2003) Generation of dominant-negative effects on the heat shock response in Arabidopsis thaliana by transgenic expression of a chimaeric HSF1 protein fusion construct. Plant J 35:442–451

    Article  PubMed  CAS  Google Scholar 

  • Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99:7530–7535

    Article  PubMed  CAS  Google Scholar 

  • Yu JH, Kim KP, Park SM, Hong CB (2005) Biochemical analysis of a cytosolic small heat shock protein, NtHSP18.3, from Nicotiana tabacum. Mol Cells 19:328–333

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Mugnièry for kindly providing the Globodera tabacum population and Ana Belén Yuste for her technical help in the analysis of the Arabidopsis transformants. This work was supported by grants from the Fundación Ramón Areces and the Ministerio de Educación (AGL-2004-08103-C02-02) to CE, from a collaboration project from the National Science Foundation of the USA to Elizabeth Vierling and from the European Commission (QLK5-1999-01501) and the Junta de Comunidades de Castilla-La Mancha (JCCM, GC-02-011) to CF. MB was a recipient of an FPU fellowship from the Ministerio de Educación and AG from the “Junta de Comunidades de Castilla-La Mancha.”

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  1. Facultad de Ciencias del Medio Ambiente, Universidad de Castilla-La Mancha, Campus de la Real Fábrica de Armas, 45071, Toledo, Spain

    Marta Barcala, Alejandra García, Carmen Fenoll & Carolina Escobar

  2. Centro Nacional de Biotecnología, Departamento de Genética Molecular de Plantas, Campus Universidad Autónoma de Madrid, 28049, Cantoblanco, Madrid, Spain

    Pilar Cubas

  3. Instituto de Recursos Naturales y Agrobiología, Consejo Superior de Investigaciones Científicas, Apartado 1052, 41080, Seville, Spain

    Concepción Almoguera & Juan Jordano

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  1. Marta Barcala
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  2. Alejandra García
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Correspondence to Carolina Escobar.

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Barcala, M., García, A., Cubas, P. et al. Distinct heat-shock element arrangements that mediate the heat shock, but not the late-embryogenesis induction of small heat-shock proteins, correlate with promoter activation in root-knot nematode feeding cells. Plant Mol Biol 66, 151–164 (2008). https://doi.org/10.1007/s11103-007-9259-3

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