Planta

, Volume 242, Issue 2, pp 461–475 | Cite as

Heat shock transcription factors involved in seed desiccation tolerance and longevity retard vegetative senescence in transgenic tobacco

  • Concepción Almoguera
  • José-María Personat
  • Pilar Prieto-Dapena
  • Juan Jordano
Original Article
First Online:
Received:
Accepted:
Part of the following topical collections:
  1. Desiccation Biology

Abstract

Main conclusion

Transcription factors normally expressed in sunflower seeds delayed vegetative senescence induced by severe stress in transgenic tobacco. This revealed a novel connection between seed heat shock factors, desiccation tolerance and vegetative longevity.

HaHSFA9 and HaHSFA4a coactivate a genetic program that, in sunflower (Helianthus annuus L.), contributes to seed longevity and desiccation tolerance. We have shown that overexpression of HaHSFA9 in transgenic tobacco seedlings resulted in tolerance to drastic dehydration and oxidative stress. Overexpression of HaHSFA9 alone was linked to a remarkable protection of the photosynthetic apparatus. In addition, the combined overexpression of HaHSFA9 and HaHSFA4a enhanced all these stress-resistance phenotypes. Here, we find that HaHSFA9 confers protection against damage induced by different stress conditions that accelerate vegetative senescence during different stages of development. Seedlings and plants that overexpress HaHSFA9 survived lethal treatments of dark-induced senescence. HaHSFA9 overexpression induced resistance to effects of culture under darkness for several weeks. Only some homoiochlorophyllous resurrection plants are able to withstand this experimental severe stress condition. The combined overexpression of HaHSFA9 and HaHSFA4a did not result in further slowing of dark-induced seedling senescence. However, combined expression of the two transcription factors caused improved recovery of the photosynthetic organs of seedlings after lethal dark treatments. At later stages of vegetative development, HaHSFA9 delayed the appearance of senescence symptoms in leaves of plants grown under normal illumination. This delay was observed under either control or stress treatments. Thus, HaHSFA9 delayed both natural and stress-induced leaf senesce. These novel observations connect transcription factors involved in desiccation tolerance with leaf longevity.

Keywords

Drastic stress tolerance Heat shock factors Leaf senescence Seed longevity Transgenic tobacco 

Abbreviations

HSF

Heat shock factor

HSP

Heat shock proteins

sHSP

Small heat shock proteins

sHSP-P

Small heat shock protein (plastidial)

sHSP-CI

Small heat shock protein (cytosolic, Class I)

NT

Non-transgenic

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Notes

Acknowledgments

This work was supported by the European Regional Development Fund (FEDER) and the Spanish Secretary of Research, Development, and Innovation (Grants BIO2011-23440). Some additional funds came from the Andalusian Regional Government (Grant BIO148).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2015_2336_MOESM1_ESM.pdf (4.6 mb)
Supplementary material 1 (PDF 4686 kb)

References

  1. Abbasi AR, Saur A, Hennig P, Tschiersch H, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2009) Tocopherol deficiency in transgenic tobacco (Nicotiana tabacum L.) plants leads to accelerated senescence. Plant Cell Environ 32:144–157PubMedCrossRefGoogle Scholar
  2. Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674PubMedCrossRefGoogle Scholar
  3. Alamillo J, Almoguera C, Bartels D, Jordano J (1995) Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol Biol 29:1093–1099PubMedCrossRefGoogle Scholar
  4. Almoguera C, Rojas A, Diaz-Martin J, Prieto-Dapena P, Carranco R, Jordano J (2002) A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. J Biol Chem 277:43866–43872PubMedCrossRefGoogle Scholar
  5. Almoguera C, Prieto-Dapena P, Personat JM, Tejedor-Cano J, Lindahl M, Diaz-Espejo A, Jordano J (2012) Protection of the photosynthetic apparatus from extreme dehydration and oxidative stress in seedlings of transgenic tobacco. PLoS One. doi: 10.1371/journal.pone.0051443 PubMedCentralPubMedGoogle Scholar
  6. Arteca RN, Arteca JM (2000) A novel method for growing Arabidopsis thaliana plants hydroponically. Physiol Plant 108:188–193CrossRefGoogle Scholar
  7. Blomstedt CK, Griffiths CA, Fredericks DP, Hamill JD, Gaff DF, Neale AD (2010) The resurrection plant Sporobolus stapfianus: an unlikely model for engineering enhanced plant biomass? Plant Growth Regul 62:217–232CrossRefGoogle Scholar
  8. Borrell AK, Mullet JE, George-Jaeggli B, van Oosterom EJ, Hammer GL, Klein PE, Jordan DR (2014) Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. J Exp Bot 65:6251–6263PubMedCentralPubMedCrossRefGoogle Scholar
  9. Boudet J, Buitink J, Hoekstra FA, Rogniaux H, Larre C, Satour P, Leprince O (2006) Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140:1418–1436PubMedCentralPubMedCrossRefGoogle Scholar
  10. Breeze E, Harrison E, Page T, Warner N, Shen C, Zhang C, Buchanan-Wollaston V (2008) Transcriptional regulation of plant senescence: from functional genomics to systems biology. Plant Biol 10(Suppl. 1):99–109PubMedCrossRefGoogle Scholar
  11. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence-a genomics approach. Plant Biotechnol J 1:3–22PubMedCrossRefGoogle Scholar
  12. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585PubMedCrossRefGoogle Scholar
  13. Carranco R, Espinosa JM, Prieto-Dapena P, Almoguera C, Jordano J (2010) Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proc Natl Acad Sci USA 107:21908–21913PubMedCentralPubMedCrossRefGoogle Scholar
  14. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osorio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field? Photosynthesis and growth. Ann Bot 89:907–916PubMedCentralPubMedCrossRefGoogle Scholar
  15. Cushman JC, Oliver MJ (2011) Understanding vegetative desiccation tolerance using integrated functional genomics approaches within a comparative evolutionary framework. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Ecological studies, vol 215. Springer, Berlin, Heidelberg, pp 307–338CrossRefGoogle Scholar
  16. Denev I, Stefanov D, Terashima I (2012) Preservation of integrity and activity of Haberlea rhodopensis photosynthetic apparatus during prolonged light deprivation. Physiol Plant 146:121–128PubMedCrossRefGoogle Scholar
  17. Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci 182:29–41PubMedCrossRefGoogle Scholar
  18. Farrant JM, Moore JP (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14:340–345PubMedCrossRefGoogle Scholar
  19. Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant 127:343–352CrossRefGoogle Scholar
  20. Gaff DF, Oliver M (2013) The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct Plant Biol 40:315–328CrossRefGoogle Scholar
  21. Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D (2012) Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol Life Sci 69:3175–3186PubMedCrossRefGoogle Scholar
  22. Gregersen PL, Culetic A, Boschian L, Krupinska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622PubMedCrossRefGoogle Scholar
  23. Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci. doi: 10.3389/fpls.2014.00036 PubMedCentralPubMedGoogle Scholar
  24. Guo Y, Gan SS (2012) Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ 35:644–655PubMedCrossRefGoogle Scholar
  25. Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162PubMedCrossRefGoogle Scholar
  26. 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 157:1243–1254PubMedCentralPubMedCrossRefGoogle Scholar
  27. Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45:771–787PubMedCrossRefGoogle Scholar
  28. Islam S, Griffiths CA, Blomstedt CK, Le TN, Gaff DF, Hamill JD, Neale AD (2013) Increased biomass, seed yield and stress tolerance is conferred in Arabidopsis by a novel enzyme from the resurrection grass Sporobolus stapfianus that glycosylates the strigolactone analogue GR24. PLoS One. doi: 10.1371/journal.pone.0080035 Google Scholar
  29. Kotak S, Vierling E, Baumlein H, Koskull-Doring P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19:182–195PubMedCentralPubMedCrossRefGoogle Scholar
  30. Lichtenthaler HK, Buschmann C (2001) Chlorophyll and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem F4(3):1–8Google Scholar
  31. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  32. Lobell DB, Gourdji SM (2012) The influence of climate change on global crop productivity. Plant Physiol 160:1686–1697PubMedCentralPubMedCrossRefGoogle Scholar
  33. Luo PG, Deng KJ, Hu XY, Li LQ, Li X, Chen JB, Zhang HY, Tang ZX, Zhang Y, Sun QX, Tan FQ, Ren ZL (2013) Chloroplast ultrastructure regeneration with protection of photosystem II is responsible for the functional ‘stay-green’ trait in wheat. Plant Cell Environ 36:683–696PubMedCrossRefGoogle Scholar
  34. Munné-Bosch S, Alegre L (2002) Plant aging increases oxidative stress in chloroplasts. Planta 214:608–615PubMedCrossRefGoogle Scholar
  35. Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100CrossRefGoogle Scholar
  36. Oliver MJ, Jain R, Balbuena TS, Agrawal G, Gasulla F, Thelen JJ (2011) Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochemistry 72:1273–1284PubMedCrossRefGoogle Scholar
  37. Personat JM, Tejedor-Cano J, Prieto-Dapena P, Almoguera C, Jordano J (2014) Co-overexpression of two Heat Shock Factors results in enhanced seed longevity and in synergistic effects on seedling tolerance to severe dehydration and oxidative stress. BMC Plant Biol 14:56. doi: 10.1186/1471-2229-14-56 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Prieto-Dapena P, Castaño R, Almoguera C, Jordano J (2006) Improved resistance to controlled deterioration in transgenic seeds. Plant Physiol 142:1102–1112PubMedCentralPubMedCrossRefGoogle Scholar
  39. 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 54:1004–1014PubMedCrossRefGoogle Scholar
  40. Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636PubMedCentralPubMedCrossRefGoogle Scholar
  41. Roberts IN, Caputo C, Criado MV, Funk C (2012) Senescence-associated proteases in plants. Physiol Plant 145:130–139PubMedCrossRefGoogle Scholar
  42. Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119PubMedCrossRefGoogle Scholar
  43. Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60PubMedCrossRefGoogle Scholar
  44. Tejedor-Cano J, Prieto-Dapena P, Almoguera C, Carranco R, Hiratsu K, Ohme-Takagi M, Jordano J (2010) Loss of function of the HSFA9 seed longevity program. Plant Cell Environ 33:1408–1417PubMedGoogle Scholar
  45. Tejedor-Cano J, Carranco R, Personat JM, Prieto-Dapena P, Almoguera C, Espinosa JM, Jordano J (2014) A passive repression mechanism that hinders synergic transcriptional activation by heat shock factors involved in sunflower seed longevity. Mol Plant 7:256–259PubMedCrossRefGoogle Scholar
  46. Thomas H, De Villiers L (1996) Gene expression in leaves of Arabidopsis thaliana induced to senesce by nutrient deprivation. J Exp Bot 47:1845–1852CrossRefGoogle Scholar
  47. Tsong AE, Tuch BB, Li H, Johnson AD (2006) Evolution of alternative transcriptional circuits with identical logic. Nature 443:415–420PubMedCrossRefGoogle Scholar
  48. Verdier J, Lalanne D, Pelletier S, Torres-Jerez I, Righetti K, Bandyopadhyay K, Leprince O, Chatelain E, Vu BL, Gouzy J, Gamas P, Udvardi MK, Buitink J (2013) A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiol 163:757–774PubMedCentralPubMedCrossRefGoogle Scholar
  49. 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 112:747–757PubMedCentralPubMedCrossRefGoogle Scholar
  50. Wingler A, Brownhill E, Pourtau N (2005) Mechanisms of the light-dependent induction of cell death in tobacco plants with delayed senescence. J Exp Bot 56:2897–2905PubMedCrossRefGoogle Scholar
  51. Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munne-Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue GP, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24:482–506PubMedCentralPubMedCrossRefGoogle Scholar
  52. Yamatani H, Sato Y, Masuda Y, Kato Y, Morita R, Fukunaga K, Nagamura Y, Nishimura M, Sakamoto W, Tanaka A, Kusaba M (2013) NYC4, the rice ortholog of Arabidopsis THF1, is involved in the degradation of chlorophyll - protein complexes during leaf senescence. Plant J 74:652–662PubMedCrossRefGoogle Scholar
  53. Zavaleta-Mancera HA, Franklin KA, Ougham HJ, Thomas H, Scott IM (1999) Regreening of senescent Nicotiana leaves. I. Reappearance of NADPH-protochlorophyllide oxidoreductase and light-harvesting chlorophyll a/b-binding protein. J Exp Bot 50:1677–1682Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Concepción Almoguera
    • 1
  • José-María Personat
    • 1
  • Pilar Prieto-Dapena
    • 1
  • Juan Jordano
    • 1
  1. 1.Departamento de Biotecnología Vegetal, Instituto de Recursos Naturales y Agrobiología de SevillaConsejo Superior de Investigaciones Científicas (CSIC)SevilleSpain

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