protein-protein associations; see at Toc159 control), high-molecular-weight ubiquitin smears
were apparent in at Toc33 immunoprecipitates
(Fig. 3G). Abundance of polyubiquitinated at Toc33
was controlled by proteasomal activity, as revealed by MG132 treatment. Thus, TOC components are indeed ubiquitinated in vivo, which
controls their turnover. Genetic suppression by
sp1 is likely due to the stabilization of TOC components (such as at Toc75-III and at Toc34).
Our data imply a role for SP1 in the reor-
ganization of the TOC machinery (fig. S11) and
a mechanism for the regulation of plastid bio-
genesis. This might be important during devel-
opmental phases in which plastids convert from
one form to another through organellar proteome
changes (1–3). For example, during fruit ripen-
ing in crops such as tomato and citrus, chloroplasts
differentiate into chromoplasts, which accumu-
late carotenoid pigments of dietary importance
(3). In Arabidopsis, when etiolated seedlings are
exposed to light, heterotrophic etioplasts rapidly
differentiate into chloroplasts (29). This is es-
sential for initiation of photoautotrophic growth
after seed germination beneath the soil. In accord-
ance with the hypothesis, sp1 single mutants
de-etiolated inefficiently, displaying reduced sur-
vival rates linked to delayed organellar differen-
tiation (Fig. 4, A to E), reduced accumulation
of photosynthetic proteins, and imbalances in
TOC receptor levels (fig. S12). At the other end
of the life cycle, chloroplasts transform into
gerontoplasts as catabolic enzymes accumulate
to recover resources from the organelles of se-
nescent leaves for use elsewhere in the plant.
This response is characterized by declining pho-
tosynthetic performance and can be induced
prematurely by dark treatment (30). The sp1 mu-
tation also attenuated this transition (Fig. 4, F
and G), whereas SP1 overexpression enhanced
both senescence and de-etiolation (Fig. 4), pre-
sumably because of the hastening of organellar
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Acknowledgments: We thank M. Rashbrooke for assistance
with initial phenotype analyses and rough mapping of sp1;
U. Ranganathan for her contribution to the analysis of SPL1;
R. Patel and R. Berkeley for excellent technical assistance;
N. Allcock and S. Hyman for electron microscopy (EM) carried
out within the EM Laboratory, University of Leicester; C. Dean
and R. Trösch for helpful comments on the manuscript;
U. Flores-Perez for antigen preparation (at Toc132 and
at Toc34); M. Boutry (PMA2), N.E. Hoffman (LHCP), K. Inoue
(OEP80), F. Kessler (at Toc159), and G. Thorlby (SFR2) for
antibodies; C.E. Stebbins for the AtUBC8 clone; and the
Salk Institute Genomic Analysis Laboratory (SIGnAL) and the
Nottingham Arabidopsis Stock Centre (NASC) for the sp1-2
and sp1-3 alleles. This study was supported by grants from
the Biotechnology and Biological Sciences Research Council
(BBSRC; BB/D016541/1 and BB/H008039/1) to P.J., by the
Royal Society Rosenheim Research Fellowship to P.J., and by
a Royal Society International Incoming Fellowship to W.H. This
work is the subject of patent application number GB 1216090.9,
which covers the role of the ubiquitin-proteasome system in
the control of plastid development. The data are presented in
the manuscript and in the supplementary materials.
Materials and Methods
Figs. S1 to S12
22 May 2012; accepted 14 September 2012
Tricking the Guard: Exploiting Plant
Defense for Disease Susceptibility
J. Lorang,1 T. Kidarsa,1* C. S. Bradford,1† B. Gilbert,1 M. Curtis,1 S.-C. Tzeng,2
C. S. Maier,2 T. J. Wolpert1‡
Typically, pathogens deploy virulence effectors to disable defense. Plants defeat effectors with
resistance proteins that guard effector targets. We found that a pathogen exploits a resistance
protein by activating it to confer susceptibility in Arabidopsis. The guard mechanism of plant
defense is recapitulated by interactions among victorin (an effector produced by the necrotrophic
fungus Cochliobolus victoriae), TRX-h5 (a defense-associated thioredoxin), and LOV1 (an
Arabidopsis susceptibility protein). In LOV1’s absence, victorin inhibits TRX-h5, resulting in
compromised defense but not disease by C. victoriae. In LOV1’s presence, victorin binding to
TRX-h5 activates LOV1 and elicits a resistance-like response that confers disease susceptibility. We
propose that victorin is, or mimics, a conventional pathogen virulence effector that was defeated
by LOV1 and confers virulence to C. victoriae solely because it incites defense.
class of R proteins consists of nucleotide-binding
leucine-rich repeat (NB-LRR) proteins related to
innate immune response proteins in animals (2, 3).
The Arabidopsis thaliana gene LOV1 encodes a
typical NB-LRR but is unique because it confers
sensitivity to the fungal toxin victorin, and thus susceptibility (S) rather than resistance to C. victoriae
(1). Although LOV1 conditions disease susceptibility, it initiates a defense-like response and requires
structural features identical to those of resistance-associated NB-LRRs (1, 4). Additionally, LOV1
is widespread and conserved in Arabidopsis, implying that it is maintained for resistance to an
unidentified pathogen (4). In support of this presumption is the original description of C. victoriae
Disease susceptibility and resistance are normally considered opposite plant re- sponsesto pathogen challenge. However,
for disease caused by the fungus Cochliobolus
victoriae, susceptibility and the host resistance
response appear to be one and the same (1). Most
pathogens gain virulence by expressing effectors
that target proteins integral to host defense. The
guard model posits that plants defeat pathogen
virulence by guarding effector targets with resistance
(R) proteins in a process called effector-triggered
immunity or R-gene resistance (2, 3). The largest
1Department of Botany and Plant Pathology and Center for
Genome Research and Biocomputing, Oregon State University,
Corvallis, OR 97331, USA. 2Department of Chemistry, Oregon
State University, Corvallis, OR 97331, USA.
*Present address: Horticultural Crops Research Lab, USDA-ARS,
Corvallis, OR 97331, USA.
†Present address: Department of Environmental and Molecular
Toxicology, Oregon State University, Corvallis, OR 97331, USA.
‡To whom correspondence should be addressed. E-mail: