© Benaki Phytopathological Institute
1
Laboratory of Bacteriology, Department of Phytopa-
thology, Benaki Phytopathological Institute, 8 St. Del-
ta St., GR-145 61 Kifissia, Athens, Greece
2
The Sainsbury Laboratory, John Innes Centre, Nor-
wich Research Park, Norwich NR4 7UH, UK
3
Professor Emeritus, University of California, Berkeley,
CA, USA and University of Crete, P.O. Box 2208, Herak-
lion GR 71409, Greece.
Corresponding authors:
Introduction
Bacteria have evolved different strategies to
adapt and colonize specific niches, includ-
ing the plant phyllosphere and rhizosphere.
Dependence on the host for survival has
lead bacterial species to adapt to a symbiot-
ic or a pathogenic lifestyle, the latter includ-
ing strategies to proliferate, disperse and
overcome plant defenses in order to be suc-
cessful pathogens. For this purpose, patho-
gens deploy an arsenal of molecular weap-
ons, of which toxins, phytohormones, cell
wall degrading enzymes, lipo- and exopoly-
saccharides were identified and character-
ized during the 60s and 70s. In the same pe-
riod, scientists studied the various lines of
plant defense, focusing on preformed phys-
ical barriers, phytoalexins and other antimi-
crobial compounds that pre-existed or were
formed post-infection (reviewed in Hückel-
hoven, 2007). However, with few exceptions,
plant defense, pathogen virulence and host
range (especially race-cultivar specificity)
could not be adequately explained on such
bases (reviewed in Hückelhoven, 2007) but
instead was thought to rely largely upon in-
duction of a series of host immune respons-
es. Flor’s seminal analysis of the complemen-
Hellenic Plant Protection Journal
5:
31-47, 2012
REVIEW ARTICLE
Targeting injectisomes of virulence: Benefits of thirty years of
research on bacterial secretion systems, to crop protection
N. Skandalis
1
, P.F. Sarris
2
and N.J. Panopoulos
3
Summary
The discovery in the mid-80s of contiguous gene clusters that were later shown to code
for a novel protein secretion system has been a milestone in plant pathology and the study of plant-
bacterial interactions. This system, named type III secretion system (T3SS), is dedicated to the trans-
location of virulence-related proteins, called effectors, from the pathogen to the host and is common
among phytopathogenic, zoopathogenic and symbiotic bacteria. Bacterial pathogens overcome mul-
tiple layers of plant defense, both preformed barriers and inducible mechanisms. To accomplish this
they deploy sophisticated molecular devices to secrete selected sets of proteins either to the inter-
cellular spaces or directly inside the plant cell. Such proteins enable pathogens to avoid recognition,
block induction of immune responses and/or interfere with the defense signaling network. Recent de-
velopments in molecular biology facilitated research on these interactions and rendered the inter-
kingdom trafficking of proteins a key element of pathogenicity, virulence and host specificity of Gram-
negative bacterial pathogens. While basic research on phytobacterial pathogens has progressed, lit-
tle has changed on the crop protection schemes against bacterial infections. In this review, we sum-
marize the latest findings on the different levels at which contact-dependent protein secretion from
Gram-negative bacteria subverts and/or manipulates plant immunity. Additionally, we focus on the
biotechnological applications which have emerged from basic research on phytobacterial T3SS and its
cognate effectors, ranging from bacterial diagnostics, plant resistance and anti-virulence chemicals to
toolkits for gene targeting in plants.
Additional keywords:
Diagnostics, effector protein,
hrp
, resistance, type III secretion
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