MOLECULAR PLANT PATHOLOGY (2001) 2 (2), 109–115
© 2001 BLACKWELL SCIENCE LTD 109
Blackwell Science, Ltd
Review
Targeting the targets of Type III effector proteins secreted by
phytopathogenic bacteria
ROGER W. INNES
Department of Biology, Indiana University, Bloomington, IN 47405 -3700, USA
INTRODUCTION
Many Gram-negative bacterial pathogens of both plants and
animals depend on a type III secretion system to infect their host
organism (Hueck, 1998). Type III secretion systems have been most
intensively studied in species of Yersinia and Salmonella, where it
has been established that they function to inject multiple effector
proteins directly into host cells (Hueck, 1998). In mammalian cells,
these effector proteins interact physically with specific signal
transduction proteins, leading to multiple changes in host cell
physiology, including major alterations in the actin cytoskeleton,
suppression of immune responses, and activation of apoptosis
(programmed cell death) (Cornelis, 2000; Galan and Zhou, 2000).
By comparison, very little is known about the function of effector
proteins secreted by plant pathogens. However, several recent
papers are beginning to shed new light. I will discuss the implications
of these new papers and discuss some promising new directions
for elucidating the function of effector proteins secreted by plant
pathogens.
BACKGROUND
Although the function of the type III secretion system was first
elucidated in animal pathogens (Cornelis, 2000), genes encoding
the components of type III systems were first identified in the
plant pathogen Pseudomonas syringae pv. phaseolicola (Lindgren
et al., 1986). In this early work, several P. s. pv. phaseolicola mutants
were identified that failed to induce a hypersensitive resistance
response on tobacco, a non-host. Importantly, these mutants also
failed to cause disease on their normal host, bean. Mutations in
several different genes, which were clustered in a small interval
of DNA, gave rise to this phenotype. This cluster was designated
the hrp cluster for h ypersensitive r esistance and p athogenicity.
The mechanistic basis of this phenotype did not become clear
until 6 years later, when the first gene sequences from the Yersinia
type III secretion apparatus were published and recognized to
be homologous to hrp genes from P. syringae, Xanthomonas
campestris pv. vesicatoria and Pseudomonas solanacearum (now
known as Ralstonia solanacearum ) (Fenselau et al., 1992; Gough
et al., 1992). This observation indicated that protein secretion by
phytopathogenic bacteria is an essential aspect of both patho-
genesis and the induction of host defence responses.
Establishing the mechanistic links between type III effectors
(proteins secreted by the type III system), pathogenesis, and
induction of the HR in plants has been difficult. Most putative
type III effectors from phytopathogenic bacteria were first iden-
tified genetically as the products of classical avirulence ( avr )
genes. Avirulence genes in bacteria are defined as genes that can
convert a normally virulent strain to avirulence in a host-specific
manner. Avirulence is usually manifested as an induction of an HR
on resistant host plants. Because induction of the HR is depend-
ent on hrp genes, it was hypothesized that the products of avr
genes are secreted by the type III secretion system directly into
the cytoplasm of host cells. Compelling data supporting this
hypothesis have been provided by expressing avr genes directly
inside plant cells using transient delivery methods and/or expression
under an inducible promoter (Bonas and Van den Ackervaken,
1997). In all cases, the expression of an avr gene inside a plant
cell leads to induction of an HR-like response (i.e. cell death) that
is dependent on a cognate disease resistance ( R ) gene in the plant.
It is thus assumed that the hrp secretion system’s only role relative to
HR induction is the delivery of Avr proteins into plant cells; however,
direct proof of such protein translocation is yet to be obtained.
The existence of specific type III effectors in phytopathogenic
bacteria that induce strong defence responses in plants is para-
doxical, unless they also play a role in pathogenesis. Surprisingly,
the first avr genes identified, which were in the soybean patho-
gen P. syringae pv. glycinea, appeared to make no significant
contribution to pathogenesis; mutation of these genes did not
affect the virulence of these strains on normally susceptible hosts,
and many P. syringae strains completely lacked these avr genes
(Staskawicz et al., 1984; Staskawicz et al., 1987). Many other avr
genes have been identified subsequently, and several do indeed
Correspondence : Department of Biology, 1001 East Third Street, Jordan Hall 142, Indiana
University, Bloomington, IN 47405-3700, USA. E-mail: rinnes@bio.indiana.edu