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J. Biol. Chem., Vol. 283, Issue 29, 20209-20219, July 18, 2008

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A New Branch of Endoplasmic Reticulum Stress Signaling and the Osmotic Signal Converge on Plant-specific Asparagine-rich Proteins to Promote Cell Death^*

Maximiller D. L. Costa¹, Pedro A. B. Reis¹, Maria Anete S. Valente¹, André S. T. Irsigler¹², Claudine M. Carvalho³, Marcelo E. Loureiro, Francisco J. L. Aragão^¶, Rebecca S. Boston^||, Luciano G. Fietto, and Elizabeth P. B. Fontes⁴

From the Departamento de Bioquímica e Biologia Molecular, BIOAGRO and the Departamento de Biologia Vegetal, Universidade Federal de Viçosa, 36571.000, Viçosa, MG, Brazil, ^¶Embrapa Recursos Genéticos e Biotecnologia, PqEB W5 Norte, 70770-900, Brasília, DF, Brazil, and the ^||Department of Plant Biology, North Carolina State University, Raleigh, North Carolina 27695

NRPs (N-rich proteins) were identified as targets of a novel adaptive pathway that integrates endoplasmic reticulum (ER) and osmotic stress signals based on coordinate regulation and synergistic up-regulation by tunicamycin and polyethylene glycol treatments. This integrated pathway diverges from the molecular chaperone-inducing branch of the unfolded protein response (UPR) in several ways. While UPR-specific targets were inversely regulated by ER and osmotic stresses, NRPs required both signals for full activation. Furthermore, BiP (binding protein) overexpression in soybean prevented activation of the UPR by ER stress inducers, but did not affect activation of NRPs. We also found that this integrated pathway transduces a PCD signal generated by ER and osmotic stresses that result in the appearance of markers associated with leaf senescence. Overexpression of NRPs in soybean protoplasts induced caspase-3-like activity and promoted extensive DNA fragmentation. Furthermore, transient expression of NRPs in planta caused leaf yellowing, chlorophyll loss, malondialdehyde production, ethylene evolution, and induction of the senescence marker gene CP1. This phenotype was alleviated by the cytokinin zeatin, a potent senescence inhibitor. Collectively, these results indicate that ER stress induces leaf senescence through activation of plant-specific NRPs via a novel branch of the ER stress response.

Received for publication, April 4, 2008 , and in revised form, May 2, 2008.

^* This work was supported in part by the Brazilian Government Agency CNPq Grants 50.6119/2004-1 and 470878/2006-1 (to E. P. B. F.), FAPEMIG Grant EDT 523/07, and FINEP Grant 01.07.610.0 [EC] 0 (to E. P. B. F.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1–S6 and Table S1.

¹ Supported by a graduate fellowship from CNPq.

² Present address: Molecular Core Facility, Dept. of Biology, Florida State University, Tallahassee, FL 32306-4370.

³ A FAPEMIG (CBB 00112/07) postdoctoral fellow.

⁴ To whom correspondence should be addressed: Departamento de Bioquímica e Biologia Molecular/BIOAGRO, Universidade Federal de Viçosa, 36571.000 Viçosa, MG, Brazil. Tel.: 55-31-3899-2949; Fax: 55-31-3899-2864; E-mail: bbfontes{at}ufv.br.

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