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Plant Cell Advance Online Publication
Published on August 1, 2008; 10.1105/tpc.108.058339

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Received January 25, 2008
Returned for revision May 19, 2008
Accepted July 16, 2008

Arabidopsis Protein Disulfide Isomerase-5 Inhibits Cysteine Proteases during Trafficking to Vacuoles before Programmed Cell Death of the Endothelium in Developing Seeds

Christine Andème Ondzighi 1*, David A. Christopher 2*, Eun Ju Cho 2, Shu-Choeng Chang 3, and L. Andrew Staehelin 3

1 Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347; Department of Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, Hawaii 96822
2 Department of Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, Hawaii 96822
3 Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347

* To whom correspondence should be addressed. E-mail: ondzighi{at}colorado.edu; dchr@hawaii.edu.

* To whom correspondence should be addressed. E-mail: ondzighi{at}colorado.edu; dchr@hawaii.edu.

Protein disulfide isomerase (PDI) oxidizes, reduces, and isomerizes disulfide bonds, modulates redox responses, and chaperones proteins. The Arabidopsis thaliana genome contains 12 PDI genes, but little is known about their subcellular locations and functions. We demonstrate that PDI5 is expressed in endothelial cells about to undergo programmed cell death (PCD) in developing seeds. PDI5 interacts with three different Cys proteases in yeast two-hybrid screens. One of these traffics together with PDI5 from the endoplasmic reticulum through the Golgi to vacuoles, and its recombinant form is functionally inhibited by recombinant PDI5 in vitro. Peak PDI5 expression in endothelial cells precedes PCD, whereas decreasing PDI5 levels coincide with the onset of PCD-related cellular changes, such as enlargement and subsequent collapse of protein storage vacuoles, lytic vacuole shrinkage and degradation, and nuclear condensation and fragmentation. Loss of PDI5 function leads to premature initiation of PCD during embryogenesis and to fewer, often nonviable, seeds. We propose that PDI5 is required for proper seed development and regulates the timing of PCD by chaperoning and inhibiting Cys proteases during their trafficking to vacuoles before PCD of the endothelial cells. During this transitional phase of endothelial cell development, the protein storage vacuoles become the de facto lytic vacuoles that mediate PCD.




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