Natural and Engineered Resistance to Plant Viruses, Volume 75

232 Pages·2009·9.01 MB·English

by  Gad Loebenstein, John Carr

SERIES EDITORS
KARL MARAMOROSCH
Rutgers University, New Jersey, USA
AARON J. SHATKIN
Center for Advanced Biotechnology
and Medicine, New Jersey, USA
FREDERICK A. MURPHY
University of Texas Medical Branch, Texas, USA
ADVISORY BOARD
DAVID BALTIMORE
ROBERT M. CHANOCK
PETER C. DOHERTY
H. J. GROSS
B. D. HARRISON
BERNARD MOSS
ERLING NORRBY
J. J. SKEHEL
M. H. V. VAN REGENMORTEL
Advances in
VIRUS RESEARCH
75
VOLUME
Natural and Engineered Resistance to
Plant Viruses
Edited by
GAD LOEBENSTEIN
Agricultural Research Organization
Bet Dagan, Israel
JOHN P. CARR
Department of Plant Sciences
University of Cambridge, U.K.
AMSTERDAM(cid:1)BOSTON(cid:1)HEIDELBERG(cid:1)LONDON
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PREFACE
Since the very earliest developments in agriculture, and probably even
before then, diseases affecting crop plants have posed an ever-present,
yet ever changing, threat to human survival. The Bible, for example,
explicitly mentions blights, blasts, and mildew diseases of wheat. Not
surprisingly, people sought to understand and mitigate the effects of
disease on crop productivity, and many earlier cultures have sought
divine aid in the fight against crop disease. The Romans, according to
somehistorians,celebratedthefestivalofRobigalia:anattempttomollify
Robigus, the god thought to protect crops from disease, and his less
benign sister Robiga (or Robigo), a primary goddess of Roman farmers,
known as the spirit of mildews and rusts. However, even during this
period there were attempts to understand plant diseases through the
application of reason: an approach exemplified in the writings of
Theophrastus (372–287 BC), who theorized about the nature of the
diseases of cereals and other plants. Meanwhile, over many centuries
farmers all over the world practiced domestication of plants from wild
populations and selected the best and hardiest plants grown under
agricultural conditions, thereby incidentally breeding plants resistant to
disease.
In the modern world the deployment of crops possessing genetically
based resistance is generally considered the best and most economical
approachfordiseasecontrol.Thisisespeciallytrueforprotectionagainst
viruses because, so far at least, no chemicals are available that could
provide the same degree of protection in the field against these
pathogens, as fungicides do against fungi and oomycetes. The transfer
by breeding of naturally occurring resistance genes from wild plants or
land races to cultivated lines is still an ongoing process, and has been
supplemented with other methods such as mutation, polyploidy
breeding, and the generation of haploids. Genetic resistance against
virus diseases can be surprisingly durable. A good example is that of
cucumbers bred for resistance to Cucumber mosaic virus. This resistance,
which depends on several genes, was found to be stable for many
decades against different strains of this virus.
Even though the majority of plants are resistant to most viruses (the
phenomenon of non-host or basal resistance), when viruses are able to
infect a crop plant, obtaining durable resistance by breeding is not
always possible. In certain cases, new virus strains overcome the
ix
x Preface
resistance and once again may cause severe crop losses. In addition, for
some crops and viruses, no suitable sources of resistance can be
identified among the wild relatives of a crop plant. Hence the need for
greaterunderstandingofnaturalresistance,andfortheinsightsitsstudy
can provide for the development of novel crop protection approaches.
In the last few years, much has been learned concerning the
mechanismsunderlyingseveralnaturalresistancemechanismsincluding
inter alia RNA silencing, induced resistance, and resistance conferred by
recessive and dominant genes, which will be discussed in this and the
followingvolumeoftheAdvances.Inaddition,researchoverthelasttwo
decades has made it possible to move resistance–conferring gene
sequences between plants from different botanical genera, or into plants
from other organisms, and even from the viruses themselves (pathogen-
derived resistance). This work opened a new vista for plant virus control,
and if combined with engineering for insect resistance could potentially
provide protection not only against the viruses themselves, but also
against their vectors. The work on pathogen-derived resistance also led
directly to the discovery of a natural resistance and gene regulation
mechanism,RNAsilencing,thathasramificationsthroughout thewhole
of biomedicine. Nevertheless, these technologies face technical and
sociological challenges, which are also addressed in these volumes.
Inallpartsoftheworld,butespeciallyamongthedevelopingnations,
agriculture faces the looming problems of emerging virus diseases,
population growth, and ecological change. We hope that the articles in
this volume and the following one will inform and stimulate research
on natural and engineered resistance, and thereby contribute to the
development of new approaches to disease control and the creation of
new resistant varieties that are desperately needed.
WewanttothankProfessorKarl Maramoroschfor invitingustoedit
these thematic volumes; all of our contributors who have prepared
comprehensive, stimulating, and thought-provoking reviews; the tech-
nicalstaffoftheAdvances,andspecificallyMr.EzhilvijayanBalakrishnan
and Ms. Narmada Thangavelu from Chennai, India.
October 2009 Gad Loebenstein
John P. Carr
Editors
1
CHAPTER
Mechanisms of Recognition in
R
Dominant Gene Mediated
Resistance
P. Moffett(cid:1),w
Contents I. Dominant GeneticResistance toPathogens 2
A. Plantinnate immunity 2
B. Diseaseresistance genes 3
II. NB-LRR ProteinStructure 6
A. The domainsofNB-LRR proteins 6
B. Interactionsbetween domains 8
III. Models ofNB-LRR Recognition 9
A. The guardhypothesis 9
B. The decoymodel 10
C. Recognition ofviral Avrsby NB-LRRproteins 10
D. The baitand switch model 17
IV. Perspectives 21
Acknowledgments 22
References 23
Abstract One branchofplant innateimmunity is mediated throughwhatis
traditionally known as race-specific or gene-for-gene resistance
wherein the outcome of an attempted infection is determined by
thegenotypesofboththehostandthepathogen.Dominantplant
disease resistance (R) genes confer resistance to a variety of
biotrophic pathogens, including viruses, encoding corresponding
dominantavirulence(Avr)genes.Rgenesareamongthemosthighly
variableplantgenesknown,bothwithinandbetweenpopulations.
Plantgenomesencode hundredsofRgenesthatcodeforNB-LRR
(cid:1)
BoyceThompsonInstituteforPlantResearch,TowerRoad,IthacaNY14853,USA
w De´partementdeBiologie,Universite´ deSherbrooke,2500Boulevarddel’Universite´,Sherbrooke,
Que´bec,CanadaJ1K2R1
AdvancesinVirusResearch,Volume75 r2009ElsevierInc.
ISSN:0065-3527, DOI:10.1016/S0065-3527(09)07501-0 AllRightsReserved.
1
2 P.Moffett
proteins, so named because they posses nucleotide-binding (NB)
andleucine-richrepeat(LRR)domains.ManymatchingpairsofNB-
LRR and Avr proteins have been identified as well as cellular
proteins that mediate R/Avr interactions, and the molecular
analysis of these interactions have led to the formulation of
modelsofhowproductsofRgenesrecognizepathogens.Datafrom
multipleNB-LRRsystemsindicatethattheLRRdomainsofNB-LRR
proteins determine recognition specificity. However, recent evi-
dence suggests that NB-LRR proteins have co-opted cellular
recognition co-factors that mediate interactions between Avr
proteinsandtheN-terminaldomainsofNB-LRRproteins.
I. DOMINANT GENETIC RESISTANCE TO PATHOGENS
A. Plant innate immunity
Pathogens exert significant constraints on host fitness. These pressures
have consequently applied strong selection on the evolution of host
genomessuchthatmosthostsdevotesignificantportionsoftheirgenomes
toencodingdefensesagainstpathogens.Likeallmulti-cellularorganisms,
plants possess an innate immune system: a system of defense against
pathogens based on germline-encoded components. In many cases, the
innate immune system functions to recognize pathogen-associated
molecularpatterns(PAMPs)viareceptor-likeproteinsknownaspathogen
recognitionreceptors(PRRs).PRRs areoftenwell conserved instructure
and function and recognize PAMPs that are also well conserved and
associated with broad classes of pathogens, such as bacterial flagellin,
fungalchitinandvariouscomponentsofbacterialcellwalls(Nicaiseetal.,
2009). Responses induced by PRRs, often referred to as PAMP-induced
immunity (PTI), are generally “low-impact” and are sufficient to confer
resistance to most pathogens (Chisholm et al., 2006). However, host-
adapted pathogens are able to overcome PTI mechanisms through the
deploymentofso-called“effector”proteins.Theseproteinsaredelivered
tothehostcytoplasmviathevarioussecretionmechanismsofbacteriaand
eukaryotic pathogens and for the most part it appears that the main
functionoftheseproteinsistointerferewithPTIsignaling(Chisholmetal.,
2006;Guoetal.,2009).Inturn,plantshavealsoevolvedseveralclassesof
receptor-like proteins that are more specific in their recognition spectra.
Theseplantproteinsrecognizespecificpathogen-associatedproteinsand
induceamuchmoredrasticsuiteof“highimpact”defenseresponses,often
culminatingintheinductionofatypeofprogrammedcelldeathknownat
the hypersensitive response (HR). Since many of the pathogen proteins
thatinducetheseresponsesareeffectorproteins,thisisoftenreferredtoas
effector-triggered immunity (ETI) (Chisholm et al., 2006). The plant
MechanismsofRecognitioninDominantRGeneMediatedResistance 3
proteins that induce ETI are highly expanded in number, and highly
variablebothwithinandbetweenspecies.Theinherentvariabilityofthese
proteins manifests as differences in resistance or susceptibility to
pathogenswithinaplantspeciesandhasledtothegeneticidentification
ofthelociresponsibleforthisvariability.
B. Disease resistance genes
Thecontributionofsinglemajorgenetoresistancetopathogensinplants
was initially noted by Biffen upon the popularization of Mendel’s laws,
whoreportedonthepresenceofrecessivesourcesofpathogenresistance
in wheat (Biffen, 1905). Recessive resistance is common in plants and its
molecular basis has been reviewed elsewhere (Iyer-Pascuzzi and
McCouch, 2007; Robaglia and Caranta, 2006). In many cases, recessive
resistanceresultsfromtheinabilityofthepathogentoinfectthehostdue
toalackofcompatibilitybetweenpathogen-encodedfactorsandthehost
proteins they need to interact with to establish an infection. This is
particularly well-defined for recessive plant resistance to viruses
(Robaglia and Caranta, 2006) and can be viewed in essence, not as a
recognition of the pathogen by the plant, but as a lack of recognition of
the plant by the pathogen.
In a series of studies, Flor documented the existence of dominant
diseaseresistance(R)genesindifferentcultivarsofflaxwhichconferred
resistance to specific strains of flax rust (Flor, 1971). Resistance was also
dependent on the presence of genes in the pathogen that rendered the
pathogen avirulent, but only on those host genotypes possessing a
correspondingRgene(Fig.1).LikeRgenes,theseavirulence(Avr)genes
werealsodominant,suggestinganactiverecognitionprocessonthepart
of the plant that responds to specific pathogen-associated molecules.
Thus, the result of an attempted infection is dependent on both the
genotype of the host and that of the pathogen and as such, this form of
resistance is known as gene-for-gene resistance. Gene-for-gene relation-
ships have since been shown to exist between hosts and many other
pathogens and pests, including insects, nematodes, fungi, oomycetes,
bacteria and viruses (Martin et al., 2003). A large numberof dominant R
genes have been cloned (Sacco and Moffett, 2009) which encode for a
relatively small number of receptor-like protein classes (Fig. 2).
A number of R genes encode proteins with transmembrane and
extracellular leucine-rich repeat (LRR) domains. To date, these proteins,
knownasLRRreceptor-likeproteins(LRR-RLPs),haveonlybeenshown
to confer resistance to fungal pathogens, recognizing proteins secreted
from the pathogen into the host apoplast. In addition, two rice R genes
conferring resistance to a bacterial pathogen (Xa21 and Xa3/Xa26)
4 P.Moffett
Plant Genotype
rr R_
e
p avr(avr) Disease* Disease*
y
ot
n
e
G
n
e
g
o
h
at Avr_ Disease Resistance
P
FIGURE1 Gene-for-gene resistance. Dominant resistance (R)genesconfer resistance
tospecific pathogens.This resistance isdependent on whether thepathogen
possessesamatching avirulence (Avr) geneor not(avr).Asterisks andlighter gray
shading indicate thatinmanycases, mutation ordeletion of theAvrgene results in
afitnesscost forthepathogen such that although itgainsvirulence on resistant
hosts,itsuffersa fitnesspenalty onsusceptible hosts.
encode proteins of similar structure, but with the addition of an intra-
cellular receptor-like kinase domain (LRR-RLKs; Fig. 2). However, since
AvrAx21 is thought to be a sulfated peptide rather than a protein, it has
beenproposedthatXa21maybemoreappropriatelyconsideredasaPRR
similar to several PRRs which also encode LRR-RLKs (Lee et al., 2006;
Nicaise et al., 2009).
The majority of cloned R genes encode for NB-LRR proteins; so
named for the presence of a conserved nucleotide-binding (NB) and a
C-terminal LRR domain (Fig. 2). NB-LRR-encoding genes are rapidly
diversifying and make up one of the largest and most variable gene
families found in plants (Clark et al., 2007), with 149 members in
Arabidopsis,317inpoplar,54inpapaya,400–500inMedicago,233ingrape
and 480 identified in rice (Ameline-Torregrosa et al., 2008; Kohler et al.,
2008;Meyersetal.,2003;Porteretal.,2009;Velascoetal.,2007;Zhouetal.,
2004). To date, over seventy R genes encoding NB-LRR proteins with
known resistance specificities have been cloned, which confer resistance
to the gamut of plant pathogens, including insects, nematodes,
oomycetes, fungi, bacteria and viruses (Sacco and Moffett, 2009).
Importantly, there do not appear to be any characteristics that define
the NB-LRR proteins that recognize different pathogens. That is, the
NB-LRR proteins that recognize bacteria, for example, cannot be
distinguished from those that recognize viruses. Indeed, very similar