Protoplasma (2002) 219: 184–196
Summary. Viral invasion of the root system of Nicotiana benthami-
ana was studied noninvasively with a tobacco mosaic virus (TMV)
vector expressing the green-fluorescent protein (GFP). Lateral root
primordia, which developed from the pericycle of primary roots,
became heavily infected as they emerged from the root cortex.
However, following emergence, a progressive wave of viral inhibi-
tion occurred that originated in the lateral-root meristem and
progressed towards its base. Excision of source and sink tissues sug-
gested that the inhibition of virus replication was brought about by
the basipetal movement of a root meristem signal. When infected
plants were inoculated with tobacco rattle virus (TRV) expressing
the red-fluorescent protein, DsRed, TRV entered the lateral roots
and suppressed the host response, leading to a reestablishment of
TMV infection in lateral roots. By infecting GFP-expressing trans-
genic plants with TMV carrying the complementary GFP sequence
it was possible to silence the host GFP, leading to the complete loss
of fluorescence in lateral roots.The data suggest that viral inhibition
in lateral roots occurs by a gene-silencing-like mechanism that is
dependent on the activation of a lateral-root meristem.
Keywords: Tobacco mosaic virus; Nicotiana benthamiana; Root;
Meristem; Viral suppression; Green-fluorescent protein.
Abbreviations: GFP green-fluorescent protein; PTGS posttran-
scriptional gene silencing; TMV tobacco mosaic virus; TRV tobacco
rattle virus.
Introduction
The cell-to-cell and long-distance movement of plant
viruses has been the subject of intense recent investi-
gation (for reviews, see Carrington et al. 1996, Lucas
and Wolf 1999, Oparka et al. 1996). In the case of
phloem-mobile viruses, the distribution patterns of
virus in developing sink tissues are strongly influenced
by source–sink relationships (A. Roberts et al. 1997).
It appears that once an infectious viral complex enters
the translocation stream, its final destination is largely
dependent on the flow of assimilates within the plant
(reviewed by Santa Cruz 2000). If systemic viruses
enter the phloem at a stage of development during
which the root system is a dominant sink, it might be
expected that such viruses would also be delivered to
developing roots. However, almost nothing is known
of the patterns of virus invasion in roots, despite the
fact that several viruses invade the root systems of
many commercially important crop species (Matthews
1991).
It appears that in both roots and shoots the apical
meristem is largely devoid of virus infection (Faccioli
and Colombarini 1996, Hsu et al. 2000, Matthews 1991,
Walkey et al. 1969). The inability of viruses to infect
apical meristems has been exploited commercially and
forms the basis of meristem tip culture, a method by
which virus-free clones can be obtained by growing
excised shoot tips in tissue culture (Matthews 1991,
Walkey et al. 1987). In general, a zone of variable
length (but usually within 100 mm of the root or shoot
tip) is free of replicating virus. At present, the reasons
why meristems fail to support virus replication are
unknown. It is possible that a barrier to meristem inva-
sion is enforced by cells some distance from the meri-
stem (see Matthews 1991), although such a putative
barrier has not been experimentally demonstrated.
While many viruses are thought to be unable to invade
meristems, virus particles from several unrelated
PROTOPLASMA
© Springer-Verlag 2002
Printed in Austria
Inhibition of tobacco mosaic virus replication in lateral roots is dependent on
an activated meristem-derived signal
T. A. Valentine, I. M. Roberts, and K. J. Oparka *
Unit of Cell Biology, Scottish Crop Research Institute, Dundee
Received July 23, 2001
Accepted October 11, 2001
* Correspondence and reprints: Unit of Cell Biology, Scottish
Crop Research Institute, Invergowrie, Dundee DD2 5DA, United
Kingdom.