GENERAL COMMENTARY
published: 03 February 2014
doi: 10.3389/fmicb.2014.00014
Closteroviridae: the beginning
Moshe Bar-Joseph* †
S. Tolkowsky Laboratory, Virology Department, Agricultural Research Organization, Plant Protection Institute, Bet Dagan, Israel
*Correspondence: mbjoseph@gmail.com
† Retired
Edited by:
Ricardo Flores, Instituto de Biología Molecular y Celular de Plantas (UPV-CSIC), Spain
Pedro Moreno, Instituto Valenciano de Investigaciones Agrarias, Spain
Bryce Falk, University of California, Davis, USA
Giovanni P. Martelli, University of Bari “Aldo Moro,” Italy
William O. Dawson, University of Florida, USA
Keywords: closteroviridae, virus taxonomy, history, characterization, viruses
A commentary on
Closteroviridae
by eds R. Flores, P. Moreno, B. Falk, G. P.
Martelli, and W. O. Dawson
Forty years ago, an unusual name—
closterovirus—was coined for an unusual
group of elongated plant viruses (BarJoseph and Hull, 1974). This essay reflects
my personal encounter with these viruses
between 1966 and 1986, a period that
could be considered the beginning of the
emergence of the Closteroviridae as an
exciting complex virus family.
The first two viruses assigned to this
group, Beet yellows virus (BYV) and
Citrus tristeza virus (CTV), have significant economic importance and, therefore,
attracted considerable biological and epidemiological attention long before their
molecular characterization. The seminal
paper by Kitajima et al. (1964) reporting
the association of long thread-like particles (TLP) with tristeza-expressing plants
triggered much interest on the possibility of using those particles for diagnostic purposes. In 1966, I embarked on a
Ph.D. project supervised by Prof. Gad
Loebenstein that aimed to purify the TLP
and develop a serological assay to be
eventually used for the rapid detection of
CTV-infected trees in case of an emerging epidemic. Isolating the long, thin,
fragile TLP from woody tissue in the
absence of a bioassay for quantitative estimation of the outcome of the numerous
clarification, concentration and purification steps was a difficult and frustrating
task. Indeed after almost three years, my
attempts were still mostly unsuccessful.
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In retrospect, allowing me to continue the
project at that stage was both remarkably
generous and far-sighted. Improvements
in TLP purification, including (i) the finding that young bark of only certain citrus species is the best source of TLP, (ii)
the use of a careful extraction procedure
and precipitation of TLP using polyethylene glycol, and (iii) the use of different
combinations of buffers for extraction and
resuspension allowed us to obtain sufficiently purified TLP particles to establish
their viral-like composition and biophysical nature (Bar-Joseph et al., 1972), the
infectivity of which was demonstrated by
Garnsey et al. (1977).
The capable assistance of Mr. J. Cohen
with electron microscopic analysis comparing the concentrations of TLP following the endless purification steps enabled
me to complete my Ph.D. thesis in
November 1972, almost six years after
starting. I then took a post-doc position
at the John Innes Institute (JII), Norwich.
Shortly after my arrival, I realized that,
3 years earlier, a JII Ph.D. candidate had
begun working on the characterization of
BYV, but that work had been discontinued
due to difficulties in obtaining purified
BYV preparations. I asked for permission to use the CTV purification procedure for the isolation of BYV and, to the
delight of the JII director, the late Prof. Roy
Markham, with a few minor modifications
this method was highly successful.
Working in cooperation with Roger
Hull, we obtained sufficient amounts of
BYV for the biophysical and molecular
characterization of the virions and determined the sizes of their major coat protein
subunits and RNA (Bar-Joseph and Hull,
1974). From these experiments we inferred
that CTV and BYV shared not only similar particle structures, as revealed earlier by
electron microscopy, but also closely similar RNA to coat protein mass ratios, thus
providing direct virological support for
their classification in a distinct taxonomic
group.
However, because of the considerable
variation in length, we suggested that the
new group should be named Closter virus
(closter is Greek for thread) to reflect
the common morphological characteristic
of its members, in contrast to previous
groups of elongated plant viruses whose
names were derived from their type members. Later analysis of Carnation necrotic
fleck virus (CNFV), which shares several
common biological features with BYV,
further indicated the considerable degree
of molecular and cytopathological similarity among closteroviruses as reported
in the first review of this group (BarJoseph et al., 1979), which after a third
of a century remains the main source
of information on the biology of these
viruses.
In 1980, Dr. Allan Dodds found large
amounts of distinct dsRNA molecules in
CTV-infected citrus tissues. The extension of his analyses to plants infected
with BYV and CNFV revealed considerable similarities in the amounts
of dsRNA they contained, as well as
in their dsRNA profiles (Dodds and
Bar-Joseph, 1983). It is interesting to
note that years later the accumulation of large amounts of dsRNAs in
plants infected by other members of
the Closteroviridae was instrumental for
their molecular cloning and genome
February 2014 | Volume 5 | Article 14 | 1
Bar-Joseph
characterization, despite the absence of
purified virions.
The first phase of my Closteroviridae
work ended in 1986 with the realization
that, despite advances in serological and
molecular detection methods, the natural spread of CTV in Israel had developed
into an epidemic that could not be controlled by eradication. Fortunately, most
prevalent isolates induced only mild symptoms and even now, almost 30 years later,
CTV remains a minor disease problem
regardless of earlier projections that giving up on eradication would destroy the
local citrus industry (see Bar-Joseph et al.,
1989).
The other reasons for considering this
period as the beginning has to do with
considerable advances in Closteroviridae
research mostly by new groups of
molecular virologists whose excellent
work is summarized in the present
Frontiers series. Looking back, despite the
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Closteroviridae: the beginning
difficulties and disappointments, I feel a
great deal of satisfaction from friendships
shared through these years with numerous dear colleagues and students that,
unfortunately, space limits prevent listing.
REFERENCES
Bar-Joseph, M., Garnsey, S. M., and Gonsalves, D.
(1979). The closteroviruses: a distinct group of
elongated plant viruses. Adv. Virus Res. 25, 93–168.
doi: 10.1016/S0065-3527(08)60569-2
Bar-Joseph, M., and Hull, R. (1974). Purification
and partial characterization of sugar beet yellows
virus. Virology 62, 552–562. doi: 10.1016/00426822(74)90415-2
Bar-Joseph, M., Loebenstein, G., and Cohen, J.
(1972). Further purification and characterization
of threadlike particles associated with the citrus tristeza disease. Virology 50, 821–828. doi:
10.1016/0042-6822(72)90436-9
Bar-Joseph, M., Marcus, R., and Lee, R. F. (1989).
The continuous challenge of citrus tristeza virus
control. Ann. Rev. Phytopathol. 27, 291–316. doi:
10.1146/annurev.py.27.090189.001451
Dodds, J. A., and Bar-Joseph, M. (1983). Doublestranded RNA from plants infected with
closteroviruses. Phytopathology 73, 419–423.
doi: 10.1094/Phyto-73-419
Garnsey, S. M., Gonsalves, D., and Purcifull, D.
E. (1977). Mechanical transmission of citrus
tristeza virus. Phytopathology 67, 965–968. doi:
10.1094/Phyto-67-965
Kitajima, E. W., Silva, D. M., Oliviera, A. R., Muller,
G. W., and Costa, A. S. (1964). Thread-particles
associated with tristeza disease of citrus. Nature
201, 1011–1012. doi: 10.1038/2011011a0
Received: 10 January 2014; accepted: 10 January 2014;
published online: 03 February 2014.
Citation: Bar-Joseph M (2014) Closteroviridae: the
beginning. Front. Microbiol. 5:14. doi: 10.3389/fmicb.
2014.00014
This article was submitted to Virology, a section of the
journal Frontiers in Microbiology.
Copyright © 2014 Bar-Joseph. This is an open-access
article distributed under the terms of the Creative
Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted,
provided the original author(s) or licensor are credited
and that the original publication in this journal is cited,
in accordance with accepted academic practice. No use,
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