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Plant Physiol, December 2001, Vol. 127, pp. 1656-1666
Colocalization of Plastid Division Proteins in the Chloroplast
Stromal Compartment Establishes a New Functional Relationship between
FtsZ1 and FtsZ2 in Higher Plants1
Rosemary S.
McAndrew,
John E.
Froehlich,
Stanislav
Vitha,
Kevin D.
Stokes, and
Katherine W.
Osteryoung*
Department of Plant Biology (R.S.M., S.V., K.D.S., K.W.O.) and
Department of Energy-Plant Research Laboratory (J.E.F.), Michigan State
University, East Lansing, Michigan 48824
Chloroplast division is driven by a macromolecular complex
containing components that are positioned on the cytosolic surface of
the outer envelope, the stromal surface of the inner envelope, and in
the intermembrane space. The only constituents of the division apparatus identified thus far are the tubulin-like proteins FtsZ1 and
FtsZ2, which colocalize to rings at the plastid division site. However,
the precise positioning of these rings relative to the envelope
membranes and to each other has not been previously defined. Using
newly isolated cDNAs with open reading frames longer than those
reported previously, we demonstrate here that both FtsZ2 proteins in
Arabidopsis, like FtsZ1 proteins, contain cleavable transit peptides
that target them across the outer envelope membrane. To determine their
topological arrangement, protease protection experiments designed to
distinguish between stromal and intermembrane space localization were
performed on both in vitro imported and endogenous forms of FtsZ1 and
FtsZ2. Both proteins were shown to reside in the stromal compartment of
the chloroplast, indicating that the FtsZ1- and FtsZ2-containing rings
have similar topologies and may physically interact. Consistent with
this hypothesis, double immunofluorescence labeling of various plastid
division mutants revealed precise colocalization of FtsZ1 and FtsZ2,
even when their levels and assembly patterns were perturbed.
Overexpression of FtsZ2 in transgenic Arabidopsis inhibited plastid
division in a dose-dependent manner, suggesting that the stoichiometry between FtsZ1 and FtsZ2 is an important aspect of their function. These
studies raise new questions concerning the functional and evolutionary
significance of two distinct but colocalized forms of FtsZ in plants
and establish a revised framework within which to understand the
molecular architecture of the plastid division apparatus in higher plants.
1
This work was supported, in part, by the
National Science Foundation (grants MCB-9604412 and MCB-9904524) and
the Division of Energy Biosciences at the U.S. Department of Energy.
*
Corresponding author; e-mail osteryou{at}msu.edu; fax
517-353-1926.
© 2001 American Society of Plant Physiologists
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