Protection of the photosynthetic apparatus from extreme dehydration and oxidative stress in seedlings of transgenic tobacco.

Concepción Almoguera,Javier Tejedor-Cano,Antonio Diaz-Espejo,Pilar Prieto-Dapena,Marika Lindahl,Juan Jordano,José-María Personat,Miguel A. Blazquez

doi:10.1371/journal.pone.0051443

Abstract

A genetic program that in sunflower seeds is activated by Heat Shock transcription Factor A9 (HaHSFA9) has been analyzed in transgenic tobacco seedlings. The ectopic overexpression of the HSFA9 program protected photosynthetic membranes, which resisted extreme dehydration and oxidative stress conditions. In contrast, heat acclimation of seedlings induced thermotolerance but not resistance to the harsh stress conditions employed. The HSFA9 program was found to include the expression of plastidial small Heat Shock Proteins that accumulate only at lower abundance in heat-stressed vegetative organs. Photosystem II (PSII) maximum quantum yield was higher for transgenic seedlings than for non-transgenic seedlings, after either stress treatment. Furthermore, protection of both PSII and Photosystem I (PSI) membrane protein complexes was observed in the transgenic seedlings, leading to their survival after the stress treatments. It was also shown that the plastidial D1 protein, a labile component of the PSII reaction center, and the PSI core protein PsaB were shielded from oxidative damage and degradation. We infer that natural expression of the HSFA9 program during embryogenesis may protect seed pro-plastids from developmental desiccation.

Highlights

In plant seeds the developing zygotic embryo survives desiccation
We showed partial association to thylakoid membranes, under unstressed growth conditions, of the plastidial small Heat Shock Proteins (sHSPs) overexpressed in the T lines
The HSFA9 program is seed-specific and our results suggest that such program is involved in the protection of seed non-photosynthetic plastids and proplastids, since these and other organelles must survive developmental desiccation

Summary

Introduction

In plant seeds the developing zygotic embryo survives desiccation. Mature seeds can germinate after prolonged storage leading to seed aging. The known target genes activated by HSFA9 (the HSFA9 program) encode different Heat Shock Proteins (HSPs), among them HSP101 and distinct subsets of small Heat Shock Proteins (sHSPs) that belong to the cytosol-localized CI and CII classes [1,2,3,6]. In sunflower these sHSPs include polypeptides that accumulate (or predominantly) in developing seeds at normal growth temperature, but they do not so (or do it to lesser extent) in response to heat stress in vegetative organs. We observed enhanced seed longevity [1] and achieved tolerance to drastic levels of dehydration in vegetative organs [2], respectively

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Conclusion