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J. Biol. Chem., Vol. 283, Issue 6, 3200-3210, February 8, 2008

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BAX Inhibitor-1 Modulates Endoplasmic Reticulum Stress-mediated Programmed Cell Death in Arabidopsis^*

From the Biotechnology Center for Agriculture and the Environment, Rutgers University, New Brunswick, New Jersey 08901-8550

The components and pathways that regulate programmed cell death (PCD) in plants remain poorly understood. Here we describe the impact of drug-induced endoplasmic reticulum (ER) stress on Arabidopsis seedlings and present evidence for the role of Arabidopsis BAX inhibitor-1 (AtBI1) as a modulator of ER stress-mediated PCD. We found that treatment of Arabidopsis seedlings with tunicamycin (TM), an inhibitor of N-linked glycosylation and an inducer of ER stress by triggering accumulation of unfolded proteins in the ER, results in strong inhibition of root growth and loss of survival accompanied by typical hallmarks of PCD such as accumulation of H₂O₂, chromatin condensation, and oligonucleosomal fragmentation of nuclear DNA. These phenotypes are alleviated by co-treatment with either of two different chemical chaperones, sodium 4-phenylbutyrate and tauroursodeoxycholic acid, both with chaperone properties that can reduce the load of misfolded protein in the ER. Expression of AtBI1 mRNA and its promoter activity are increased dramatically prior to initiation of TM-induced PCD. Compared with wild-type plants, two AtBI1 mutants (atbi1-1 and atbi1-2) exhibit hypersensitivity to TM with accelerated PCD progression. Conversely, overexpressing AtBI1 markedly reduces the sensitivity of Arabidopsis seedlings to TM. However, alterations in AtBI1 gene expression levels do not cause a significant effect on the expression patterns of typical ER stress-inducible genes (AtBip2, AtPDI, AtCRT1, and AtCNX1). We propose that AtBI1 plays a pivotal role as a highly conserved survival factor during ER stress that acts in parallel to the unfolded protein response pathway.

Received for publication, August 10, 2007 , and in revised form, October 29, 2007.

^* This work was supported by the Biotechnology Center for Agriculture and Environment, Rutgers University (to E. L.). 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.

¹ To whom correspondence should be addressed: Biotechnology Center for Agriculture and the Environment, Rutgers University, 59 Dudley Rd., New Brunswick, NJ 08901-8520. Tel.: 732-932-8165 (ext. 220); Fax: 732-932-6535; E-mail: lam{at}aesop.rutgers.edu.

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