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A Stress-Associated Protein Containing A20/AN1 Zing-Finger Domains

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A Stress-Associated Protein Containing A20/AN1 Zing-Finger Domains Plant Physiology and Biochemistry 49 (2011) 303e310 Contents lists available at ScienceDirect Plant Physiology and Biochemistry journal homepage: www.elsevier.com/locate/plaphy Research article A stress-associated protein containing A20/AN1 zing-finger domains expressed in Medicago truncatula seeds Christine Gimeno-Gilles 1, Marie-Laure Gervais 1, Elisabeth Planchet*, Pascale Satour, Anis M. Limami, Eric Lelievre University of Angers, UMR-1191 Physiologie Moléculaire des Semences, IFR 149 Quasav, 2 Boulevard Lavoisier, 49045 Angers Cedex 01, France article info abstract Article history: MtSAP1 (Medicago truncatula stress-associated protein 1) was revealed as a down-regulated gene by Received 15 July 2010 suppressive subtractive hybridization between two mRNA populations of embryo axes harvested before Accepted 2 January 2011 and after radicle emergence. MtSAP1 is the first gene encoding a SAP with A20 and AN1 zinc-finger Available online 13 January 2011 domains characterized in M. truncatula. MtSAP1 protein shares 54% and 62% homology with AtSAP7 (Arabidopsis thaliana) and OsiSAP8 (Oryza sativa) respectively, with in particular a strong homology in the Keywords: A20 and AN1 conserved domains. MtSAP1 gene expression increased in the embryos during the acqui- A20/AN1 zinc-finger domain sition of tolerance to desiccation, reached its maximum in dry seed and decreased dramatically during Abiotic stress fi Desiccation the rst hours of imbibition. Abiotic stresses (cold and hypoxia), abscisic acid and desiccation treatments Medicago truncatula induced MtSAP1 gene expression and protein accumulation in embryo axis, while mild drought stress did SAP not affect significantly its expression. This profile of expression along with the presence of anaerobic Seed response elements and ABRE sequences in the upstream region of the gene is consistent with a role of MtSAP1 in the tolerance of low oxygen availability and desiccation during late stages of seed maturation. Silencing of MtSAP1 by RNA interference (RNAi) showed that the function of the encoded protein is required for adequate accumulation of storage globulin proteins, vicilin and legumin, and for the development of embryos able to achieve successful germination. Ó 2011 Elsevier Masson SAS. All rights reserved. 1. Introduction environmental challenges such as drought, salt, hypoxia, cold stress and pathogen attacks [2,3]. The tolerance to low oxygen availability Seed maturation is an important phase of seed development. in plants includes the induction of the so called ‘anaerobic’ poly- According to several plant models, this process can be divided into peptides [4], which the best characterized are enzymes involved in two stages, morphogenesis and maturation [1]. Seed maturation metabolic pathways related to oxidative catabolism of sugars begins when developing embryos cease their cell division, and start (glycolysis, ethanol and lactic fermentation) and carbon skeleton growing by cell enlargement and accumulating storage reserves. storage as amino acids (alanine fermentation). Maturation ends with a desiccation phase after which the embryo Stress-associated protein (SAP) families were characterized by enters into a quiescent state, thereby permitting its maintenance the presence of A20/AN1 domains. The A20 zinc-finger (ZnF) and survival under a range of environmental conditions. In domain was first identified in a TNF-a inducible protein in human maturing seeds, the embryo is challenged by two adverse condi- cells and is characterized by multiple Cys2/Cys2 finger motifs. The tions that are the low oxygen availability and the desiccation of the AN1 ZnF domain was first identified in the C-terminus of the tissues. Several genes regulated by the phytohormone abscisic acid ubiquitin-like protein coded by the Xenopus laevis animal hemi- (ABA) are induced in the embryo, besides to those required for the sphere 1 (AN1) maternal RNA [5] and is usually found associated synthesis of storage reserves they include those involved in the with the A20 ZnF domain. The AN1-type ZnF contains six conserved acquisition of desiccation tolerance. Actually, in most vegetative cysteines and two histidines that could potentially coordinate two tissues, ABA mediates several aspects of physiological responses to zinc atoms [5]. The role of the A20/AN1 proteins has been well studied in animal immune systems [6,7]. In plants, very few information is known about A20/AN1 proteins. Vij and Tyagi [8],by screening public databases, have conducted a survey of A20/AN1 * Corresponding author. Tel.: þ33 2 41 73 53 83; fax: þ33241735456. E-mail address: [email protected] (E. Planchet). ZnF protein across diverse organisms with a special emphasis 1 These authors contributed equally to this work. on plants (Arabidopsis thaliana, Oryza sativa, Populus trichocarpa, 0981-9428/$ e see front matter Ó 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.plaphy.2011.01.004 304 C. Gimeno-Gilles et al. / Plant Physiology and Biochemistry 49 (2011) 303e310 Sorghum bicolor and Vitis vinifera). All the species contain between (62%) and Arabidopsis AtSAP7 (54%) (Fig. 2B), but also with virtually one to nineteen A20/AN1 proteins. From A. thaliana and O. sativa translated ESTs of Lotus japonicus (TC14575, 87%) and soya bean genomes, fourteen and eighteen genes code for SAP respectively, (ACU14538, 77%), and presents identical ZnF domains (Fig. 2B). In and most of them encode proteins with A20/AN1 domains. comparison to some human proteins containing A20/AN1 domains, A member of SAP gene family from rice OsiSAP1 (O. sativa stress- MtSAP1 shares 46% and 47% homology with human ZnF216 and associated protein 1) was the first plant protein identified as a ZnF AWP1 proteins respectively, and shows identities in the ZnF protein and has been shown to be induced in rice seedlings domains (data not shown). in response to environmental challenges and abscisic acid (ABA) treatment, and to confer abiotic stress tolerance to transgenic 2.2. MtSAP1 gene expression in embryo axis during maturation, tobacco over-expressing the gene [9]. Recently, the over-expression germination and post-germination of M. truncatula of OsiSAP8 has been shown to confer tolerance to salt, drought and cold stress [10] suggesting that protein encoded by this gene is The expression of MtSAP1 in embryo axis was investigated by likely to intervene in the stress signaling pathway. The mechanism real RT-PCR during seed development, germination and post- by which the over-expression of OsiSAP8 conferred stress tolerance germination growth (Fig. 3). During seed development, gene is still unknown. The authors demonstrated that A20 and AN1-type transcription exhibited a low level during the first 20 days after ZnF domains from the protein OsiSAP8 interact with each other but pollination (DAP). A strong increase in MtSAP1 gene expression was only A20 interacts with itself in a yeast two-hybrid system. observed after 28 and 35 DAP when desiccation was complete in Our strategy for improving knowledge of crucial events of the dry seed. Five hours after imbibition, amounts of mRNA germination was based on a suppressive subtractive hybridization decreased and picked up a low background expression after 25 h fi (SSH) transcriptomic analysis of embryo axis for the identi cation and remained constant even after 96 h. These data show of genes involved in germination completion. The subtraction was that MtSAP1 gene expression kinetic is correlated with a progres- carried out between two mRNA populations extracted at two sive tissue dehydration occurring in the last 10 days of seed imbibition stages, at the end of the phase of passive and massive development. uptake of water and after germination completion characterized by radicle protrusion. In our previous studies, our attention was focused on up-regulated genes with the attempt to unravel their 2.3. Analysis of RNAi MtSAP1 lines involvement in the control and the completion of germination process [11,12]. At the opposite, in the present work we focused our Plants disrupted in the expression of MtSAP1 gene were attention on a down-regulated gene that encodes a SAP protein. obtained by RNAi technology. These MtSAP1 silencing plants dis- Only little work was dedicated to SAP proteins in plants, and to our played fewer leaves than the control plants, and furthermore, the best of knowledge this is the first study dedicated to a SAP protein leaves became chlorotic in comparison to the WT (data not shown). expressed in seed. We have shown that MtSAP1 gene expression From seven transgenic lines selected by PCR, three lines were increased in embryos during maturation reaching its maximum further analysed by immunoblotting with anti-MtSAP1 antibody on during tolerance of desiccation phase and declining after few hours the mature dry seeds. The MtSAP1 protein was highly abundant of seed imbibition. The expression of the gene and the quantity of in the mature WT seeds and faintly detectable in the mature seeds the protein were re-induced after germination in embryo axes by of the transgenic line (Fig. 4A). The disruption of the expression of ABA treatment and hypoxia and desiccation stresses. Seeds of RNAi MtSAP1 resulted in a severe seed phenotype. The transgenic seeds transgenic plants in which MtSAP1 gene expression was disrupted were smaller in terms of size and weight compared to the WT showed lower level of storage globulin proteins, vicilin and legu- (Fig. 4B and C). The analysis of the seed protein content showed that min, and deficient germination. the total protein content was not affected, while the accumulation of legumin and vicilin, storage globulin proteins, was specifically 2. Results reduced in RNAi seeds in comparison to the WT seeds, even if the reduction of vicilin content in RNAi lines appeared to less signifi- 2.1. Cloning of MtSAP1 and in silico analysis cant (Fig. 4D). A germination test run on seeds from WT and three RNAi lines An SSH library was constructed from embryo axis between two was carried out. The disruption of the expression of MtSAP1 early steps of Medicago truncatula seed germination (6 h and 23 h severely affected the germination capacity of the transgenic lines.
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