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Plant Cell, Vol. 11, 2233-2248, November 1999, Copyright © 1999, American Society of Plant Physiologists

Saturation of the Endoplasmic Reticulum Retention Machinery Reveals Anterograde Bulk Flow

Andrew J. Croftsa,b, Nathalie Leborgne-Castela, Stefan Hillmerc, David G. Robinsonc, Belinda Phillipsona, Lena E. Carlssona, David A. Ashfordb, and Jürgen Deneckea,b
a Leeds Institute for Plant Biotechnology and Agriculture, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom
b Plant Laboratory, Department of Biology, University of York, P.O. Box 373, York YO10 5YW, United Kingdom
c Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Universität Göttingen, D-37073 Göttingen, Germany

Correspondence to: Jürgen Denecke, j.denecke{at}leeds.ac.uk (E-mail), 44-113-2332835 (fax)

We have studied the possible mechanisms of endoplasmic reticulum (ER) export and retention by using natural residents of the plant ER. Under normal physiological conditions, calreticulin and the lumenal binding protein (BiP) are efficiently retained in the ER. When the ER retention signal is removed, truncated calreticulin is much more rapidly secreted than truncated BiP. Calreticulin carries two glycans of the typical ER high-mannose form. Both glycans are competent for Golgi-based modifications, as determined from treatment with brefeldin A or based on the deletion of the ER retention motif. In contrast to BiP, calreticulin accumulation is strongly dependent on its retention signal, thereby allowing us to test whether saturation of the retention mechanism is possible. Overexpression of calreticulin led to 100-fold higher levels in dilated globular ER cisternae as well as dilated nuclear envelopes and partial secretion of both BiP and calreticulin. This result shows that both molecules are competent for ER export and supports the concept that proteins are secreted by default. This result also supports previous data suggesting that truncated BiP devoid of its retention motif can be retained in the ER by association with calreticulin. Moreover, even under these saturating conditions, cellular calreticulin did not carry significant amounts of complex glycans, in contrast to secreted calreticulin. This result shows that calreticulin is rapidly secreted once complex glycans have been synthesized in the medial/trans Golgi apparatus and that the modified protein does not appear to recycle back to the ER.




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