Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus

*Brain Korea-21, Division of Applied Life Science and Environmental Biotechnology National Core Research Center, Graduate School of Gyeongsang National University, Jinju 660-701, Korea;
^†Molekulare Physiologie der Pflanzen, Institut für Botanik, Westfälische Wilhelms-Universität Münster, Schlossgarten 3, 48149 Münster, Germany;
^‡Vegetable and Fruit Improvement Center, Department of Horticultural Sciences, and Molecular and Environmental Plant Science Program, Texas A&M University, College Station, TX 77843-2133;
^§International Center for Biotechnology, Osaka University, 2-1 Yamada-oka, Suita, Osaka 565-0871, Japan; and
^¶Cotton Fiber Bioscience Research Unit, Southern Regional Research Center, Agricultural Research Service, United States Department of Agriculture, 1100 Robert E. Lee Boulevard, New Orleans, LA 70124

Edited by Maarten J. Chrispeels, University of California at San Diego, La Jolla, CA, and approved February 26, 2008 (received for review January 9, 2008)

Abstract

Protein N-glycosylation in the endoplasmic reticulum (ER) and in the Golgi apparatus is an essential process in eukaryotic cells. Although the N-glycosylation pathway in the ER has been shown to regulate protein quality control, salt tolerance, and cellulose biosynthesis in plants, no biological roles have been linked functionally to N-glycan modifications that occur in the Golgi apparatus. Herein, we provide evidence that mutants defective in N-glycan maturation, such as complex glycan 1 (cgl1), are more salt-sensitive than wild type. Salt stress caused growth inhibition, aberrant root-tip morphology, and callose accumulation in cgl1, which were also observed in an ER oligosaccharyltransferase mutant, staurosporin and temperature sensitive 3a (stt3a). Unlike stt3a, cgl1 did not cause constitutive activation of the unfolded protein response. Instead, aberrant modification of the plasma membrane glycoprotein KORRIGAN 1/RADIALLY SWOLLEN 2 (KOR1/RSW2) that is necessary for cellulose biosynthesis occurred in cgl1 and stt3a. Genetic analyses identified specific interactions among rsw2, stt3a, and cgl1 mutations, indicating that the function of KOR1/RSW2 protein depends on complex N-glycans. Furthermore, cellulose deficient rsw1-1 and rsw2-1 plants were also salt-sensitive. These results establish that plant protein N-glycosylation functions beyond protein folding in the ER and is necessary for sufficient cell-wall formation under salt stress.

Footnotes

^‖To whom correspondence may be addressed. E-mail: koiwa{at}neo.tamu.edu, sylee{at}nongae.ac.kr, or schaewen{at}uni-muenster.de
Author contributions: J.S.K., J.F., and C.H.K. contributed equally to this work; J.D.B., A.v.S., and H. Koiwa designed research; J.S.K., J.F., C.H.K., H. Kajiura, M.V., A.U., S.K., B.T., K.F., S.Y.L., A.v.S., and H. Koiwa performed research; B.T., K.F., and S.Y.L. contributed new reagents/analytic tools; H. Kajiura, J.D.B., B.T., S.Y.L., A.v.S., and H. Koiwa analyzed data; and A.v.S. and H. Koiwa wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0800237105/DCSupplemental.