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Journal of Virology, December 2001, p. 12153-12160, Vol. 75, No. 24
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.24.12153-12160.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Functional Specialization and Evolution of Leader
Proteinases in the Family Closteroviridae
Chih-Wen
Peng,1
Valera V.
Peremyslov,1
Arcady R.
Mushegian,2
William O.
Dawson,3 and
Valerian V.
Dolja1,*
Department of Botany and Plant Pathology and
Center for Gene Research and Biotechnology, Oregon State
University, Corvallis, Oregon 973311;
Akkadix Corporation, La Jolla, California
920372; and Department of Plant
Pathology, University of Florida, Lake Alfred, Florida
338503
Received 23 April 2001/Accepted 18 September 2001
Members of the Closteroviridae and
Potyviridae families of the plant positive-strand RNA
viruses encode one or two papain-like leader proteinases. In addition
to a C-terminal proteolytic domain, each of these proteinases possesses
a nonproteolytic N-terminal domain. We compared functions of the
several leader proteinases using a gene swapping approach. The leader
proteinase (L-Pro) of Beet yellows virus (BYV; a
closterovirus) was replaced with L1 or L2 proteinases of Citrus
tristeza virus (CTV; another closterovirus), P-Pro proteinase
of Lettuce infectious yellows virus (LIYV; a crinivirus), and HC-Pro proteinase of Tobacco etch virus
(a potyvirus). Each foreign proteinase efficiently processed the
chimeric BYV polyprotein in vitro. However, only L1 and P-Pro, not L2
and HC-Pro, were able to rescue the amplification of the chimeric BYV
variants. The combined expression of L1 and L2 resulted in an increased RNA accumulation compared to that of the parental BYV. Remarkably, this
L1-L2 chimera exhibited reduced invasiveness and inability to move from
cell to cell. Similar analyses of the BYV hybrids, in which only the
papain-like domain of L-Pro was replaced with those derived from L1,
L2, P-Pro, and HC-Pro, also revealed functional specialization of these
domains. In subcellular-localization experiments, distinct patterns
were observed for the leader proteinases of BYV, CTV, and LIYV. Taken
together, these results demonstrated that, in addition to a common
proteolytic activity, the leader proteinases of closteroviruses possess
specialized functions in virus RNA amplification, virus invasion, and
cell-to-cell movement. The phylogenetic analysis suggested that
functionally distinct L1 and L2 of CTV originated by a gene duplication event.
*
Corresponding author. Mailing address: Department of
Botany and Plant Pathology, Oregon State University, Cordley Hall 2082, Corvallis, OR 97331. Phone: (541) 737-5472. Fax: (541) 737-3573. E-mail: doljav{at}bcc.orst.edu.
Journal of Virology, December 2001, p. 12153-12160, Vol. 75, No. 24
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.24.12153-12160.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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