Resistance-Gene-Mediated Defense Responses against Biotic Stresses in the Crop Model Plant Tomato
Chaudhary R1*and Atamian HS2
1National Cancer Institute, National Institutes of Health, Bethesda, USA
2Department of Plant Biology, University of California, California, USA
- *Corresponding Author:
- Chaudhary R
National Cancer Institute, National
Institutes of Health
9000 Rockville Pike, Bethesda, MD, USA
Tel: +1 9518233384
E-mail: [email protected]
Received Date: March 15, 2017; Accepted Date: April 13, 2017; Published Date: April 17, 2017
Citation: Chaudhary R, Atamian HS (2017) Resistance-Gene-Mediated Defense
Responses against Biotic Stresses in the Crop Model Plant Tomato. J Plant Pathol
Microbiol 8:404. doi: 10.4172/2157-7471.1000404
Copyright: © 2017 Chaudhary R, et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original
author and source are credited.
Visit for more related articles at Journal of Plant Pathology & Microbiology
Complex series of defense response activation, consistent with the studies conducted in the model plant Arabidopsis thaliana, has been demonstrated in tomato during incompatible pathogen/pest interactions. During the past two decades, numerous tomato genes have been identified conferring resistance to diverse pathogens/ pests in a gene-foR-gene manner. A few of these cloned resistance (R)-genes (Cf and Pto) have been extensively studied and excellent existing reviews describe R-gene function, interacting proteins and the mechanism of Avirulence effector perception. Recent comprehensive gene expression analysis of tomato responses to biotic stresses resulted in identification of genes and potential molecular processes that are associated with several of the tomato R-gene-mediated resistance responses. The purpose of this review is to provide an overview of tomato R-gene-mediated defense responses to different pathogens/pests together with the components involved in the organization of this highly complex network of plant defenses.
Resistance-gene; Biotic stresses; Arabidopsis thaliana;
Plants are subjected to various biotic stresses throughout their
sedentary life cycle. These continuous stressful conditions have
prompted development of a range of defense responses including
physical barriers [1-4], chemical weapons [5,6], and resistance (R)-
gene acquisition [7-10]. Tomato (Solanum lycopersicum) is the second
most important vegetable crop next to potato. About 170 million tons
of tomatoes were produced worldwide in 2014 . Due to the high
nutritional value of its fruit, high yield, short life cycle, and diverse
varieties and cultivars, tomato is widely grown all year round under both
outdoor and indoor conditions. However, this worldwide cultivation is
challenged by an abundance of diseases caused by microbial pathogens
composed of fungi, bacteria, and viruses, as well as insect and nematode
Two principal immune mechanisms operate against biotic stresses
in plants. The first line of defense is triggered by a class of immune
receptors upon recognition of pathogen associated molecular patterns
(PAMPs), chemical signatures that appear to be widely conserved
among certain pathogen clades [12,13]. This interaction is referred to
as PAMP-triggered immunity (PTI). As part of the continuous arms
race between plants and pathogens, the later have evolved to acquire
effector molecules to counteract the plant PTI mechanism and ensure
pathogenicity. This weakened plant immune response is known as
compatible interaction. This prompted plants in turn to develop specific
R-proteins that recognize the pathogen/pest effector(s) and initiate
the second principle immune mechanism termed effectoR-triggered
immunity (ETI) . This interaction is also referred to as incompatible
interaction and is generally characterized by a vast transcriptional
reprogramming after recognition of the pathogen/pest effector
molecule(s) . The recognized effector is termed as Avirulent (Avr)
and the recognition could be indirect or directly by an R-gene. R-Avr
interaction typically results in a hypersensitive cell death response (HR)
at the site of infection.
Starting early nineties, extensive research led to the cloning of a
number of tomato R-genes (Table 1). These R-genes together with
those identified from additional plant species were assigned to different
classes based on the presence of various structural motifs that can be extracellular, cytoplasmic or transmembrane [16,17]. Majority of
the plant cloned R-genes encode for nucleotide-binding domain and
leucine-rich repeats (NLR) proteins with variable amino- and carboxyterminal
domains that may contain Toll/interleukin-1 receptor (TIR)-
or coiled-coil (CC)-domain (Table 1). Many R-genes belong to gene
families and are organized in tandem arrays, clusters, and supeR-clusters
[18,19]. Interestingly, these R-genes with low structural diversity were
shown to confer resistance to diverse pathogens and pests via recognition of
arsenal of effectors . This means that, besides the common mechanisms
underlying disease resistance signal transduction throughout the plant
kingdom, individual resistance gene products can act in unique signaling
pathways . In many plant species, it has been shown that during the
course of evolution, R-genes have undergone gene duplication and selection
pressures leading to divergent evolution. Genome-wide identification and
classification of Solanaceae NLRs have identified 267, 443, and 755 NLRencoding
genes in tomato, potato, and pepper genomes, respectively .
Heinz1706 tomato encodes 478 NLRs .
||Alternaria alternataf. sp. lycopersici
||Alfalfa mosaic virus
||Cucumber mosaic virus
||Fusarium oxysporumf.sp. radicis-lycopersici
||Fusarium oxysporum formaespecialeslycopersici
||Meloidogyne spp., Macrosiphum euphorbiae,Bemisiatabaci,Bactericercacockerelli
||M.R. Foolad et al., unpublished data
||Pseudomonas syringaepv tomato
||Potato virus Y, Tobacco etch virus
||Tomato spotted wilt virus
||Tomato spotted wilt virus, tomato chlorotic spot virus, groundnut ringspot virus
||Tomato spotted wilt virus
||Tomato yellow leaf curl virus
||Tomato yellow leaf curl virus, Tomato mosaic virus
||Tomato yellow leaf curl virus
||Tomato chlorotic mottle begomovirus
||Tomato leaf curl virus
||Tomato mosaic virus
||Tobacco mild green mosaic virus, Pepper mild mottle virus
||Tomato mosaic virus
Table 1: Comprehensive list of tomato resistant genes cloned or characterized by virus-induced gene silencing.
Most of our knowledge about plant defense originated from
studies conducted in the model plant Arabidopsis thaliana .
Extensive genome-wide transcriptional profiling including cDNAAFLP
[24,25], suppression subtractive hybridization (SSH) [26,27],
microarrays and RNA-sequencing technologies [28-30] provided
valuable insights into plant-pathogen interactions at the cellular and
molecular level. The identification of genes repressed or activated in
plants assisted in making novel hypotheses concerning the biology
of a given interaction (both compatible and incompatible). Further
analysis of the differentially regulated genes, using gene inactivation,
overexpression , and biochemical approaches, confirmed the crucial
roles for some of these genes in the plant ETI responses.
Global transcriptome profiling is an important initial step for
dissecting biological systems particularly with systems where not
much is known about the molecular basis of the resistance response.
The enrichment of the tomato EST databases initiated several genomewide
profiling studies [32-35]. This facilitated significant progress in the
characterization of tomato incompatible responses to Avr pathogens,
contributing to future gene identification and to the understanding of
the potential molecular processes that are associated with the different
tomato R-gene-mediated resistances . With the advent of next
generation sequencing technologies, and the tomato genome sequence
, additional genome wide studies have been conducted. With a
genome sequence and a high-density linkage and molecular maps
, combined with being a host for numerous pathogens and pests,
tomato has emerged as a powerful model system for crop plant defense
response studies. Moreover, the introgression of R-genes from wild
species into cultivated tomato provides a unique opportunity to study
different resistance mechanisms against very diverse biotic agents in a
single plant. In this review, we summarize the current understanding
of R-genes in tomato and the downstream signaling components that
are critical for activating defense responses. In addition, we discuss
the current and future technologies that will significantly enhance
our knowledge about tomato-pathogen interactions and will provide
alternative strategies to develop a sustainable resistance.
Tomato Resistance Genes and their Modes of Action
Host resistance is an important component of a sustainable disease
management system . It is an environmentally benign method
that can be used as an alternative to chemicals, as their applicability
is becoming limited due to adverse environmental and human health
effects [39,40] and the emergence of resistant pathogen/pest strains .
Cultivated tomato, S. lycopersicum, has a narrow genetic base and is
consequently vulnerable to many diseases and pests. On the other hand,
a repertoire of genetically diverse wild tomato species represents a rich
source of R-genes. Over the past 50 years, several race-specific disease resistant genes have been identified in wild tomato species (Table 1), and
extensive tomato breeding programs have been based on the transfer of
R-genes from wild accessions into cultivated tomato. So far, majority of
the identified tomato R-genes conferring resistance to diverse pathogens
and pests belongs the NLR class. An array of mechanisms in tomato
R-gene-mediated resistances has been documented depending on the
particular R-gene and pathogen/pest combination [42,43].
Cladosporium fulvum–tomato pathosystem is a well-established
model system that complies with the gene-foR-gene concept first
described by . Elegant experiments demonstrated the involvement heatof
pathogen effectors or Avrs in the induction of ETI post recognition
by the Cf genes, resulting in incompatible interaction [45-48]. The Cf
genes belong to family of LRR-RLP (ReceptoR-Like Protein) encoding
R-genes and mediate resistance against the apoplast-colonizing foliar
fungal pathogen C. fulvum. The Cf-mediated resistance involves
formation of cell wall appositions, callose deposition and phytoalexin
accumulation. Moreover, the tomato resistance phenotype against C. fulvum is accompanied by HR, typically described as necrotic brown
spots near the site of infection that limits further growth and spread
of the pathogens . About five Avr genes (Avr2, Avr4, Avr4E,
Avr5, and Avr9) have been cloned and characterized from C. fulvum,
and are recognized by the corresponding Cf-2, Cf-4, Cf-4E, Cf-5,
and Cf-9 genes (Table 1). Thus, Cf-mediated resistance phenotype
is the combined result of HR and other defense responses. Another
well-known tomato fungal pathosystem is the xylem colonizing Fusarium oxysporum formae speciales lycopersici (Fol). Resistance to
Fol is mediated by I (Immunity)-genes that mainly involves callose
deposition, accumulation of phenolics and formation of tyloses
(outgrowths of xylem contact cells) and gels in the infected vessels .
Of the three cloned I-genes, only I-2 encodes for CC-NLR (CNL) while
the remaining two encode membrane associated receptoR-like kinase
(RLK), such as I-3 which encodes a S-RLK, or RLP, and I-7 encodes
a LRR-RLP [51-53]. Three Fol effectors, Avr1 (Six4), Avr2 (Six3) and
Avr3 (Six1) are recognized by I (and the non-allelic I-1), I-2 and I-3
genes respectively [54-56]. I-7 confers resistance to Fol races 1, 2 and
3 and I-7-mediated resistance is not suppressed by Avr1 . The Avr
effector that recognizes I-7 is yet to be identified. Unlike Cf-mediated
resistance, I-gene-mediated resistance lacks the classical HR described
above. In the vicinity of the I-2 locus another resistance locus Ty-1,
against Tomato yellow leaf curl geminivirus (TYLCV), is also mapped
. The I-2 locus on chromosome 6 is one of the most divergent R-gene
loci in tomato, partly due to gene duplications among the homologs.
This diversity is also attributed to micro RNAs (miRNAs), specifically
miR6024 that triggers phasiRNAs from I-2 homologs in tomato .
Ouyang et al., 2014 performed deep sequencing from resistant and
susceptible tomato cultivar to identify miRNAs that correlate with Fol
resistance. Interestingly, they found that two miRNAs (slmiR482f and
slmiR5300) were repressed in the resistant plants and these miRNAs
targeted four genes with full or partial NB domains, however, I-2 was
not among these targets . This suggests that there could be more
R-genes involved in the immune signaling against Fol.
In tomato, Ve is a single dominant locus that confers resistance
against Verticillium. The Ve locus contains two closely linked and
inversely oriented genes, Ve1 and Ve2, both encoding a RLP-type cell
surface receptor. Ve1 R-gene provides resistance against race 1 isolates
of Verticillium , by recognition of the Ave1 effector from race 1
strains of V. dahliae . The detailed mechanism of tomato resistance
against Verticillium wilt mediated by Ve1 recognition of Ave1 is not
well understood. However, domain-swapping analysis of Ve1 and Ve2
identified the domains essential for Ve1 functionality in tomato . It
has been suggested that HR is not absolutely required for Verticillium wilt resistance, and may occur as a consequence of escalated signaling
upon Ave1 recognition in both tomato and tobacco . Transgenic
tomato expressing Ave1 induced various defense genes including
PR-1, PR-2 and peroxidases, independently of Ve1 . Homologs of
tomato Ve1 have also been reported from other plant species including
tobacco, potato, wild eggplant, hop and cotton suggesting a conserved
recognition mechanism [65,66]. Host-induced gene silencing (HIGS)
has been successfully used in tomato, Arabidopsis and cotton plants
to suppress Verticillium wilt disease by targeting various virulence
effectors of V. dahliae [67,68].
Distinct resistant mechanisms associated with the Ol-genes
against the powdery mildew species Oidium neolycopersici have been
demonstrated using neaR-isogenic lines (NIL) . The dominant
resistance genes (Ol-1, Ol-3, Ol-4, Ol-5, and Ol-6) hamper the
fungal growth via classical HR of the host epidermal cells, while the
recessive gene ol-2 confers resistance via papilla formation [70,71]. By
performing complementation experiments using transgenic tomato
lines as well as virus-induced gene silencing (VIGS) assays it was
demonstrated that the ol-2–mediated powdery mildew resistance is
due to loss of SlMlo1 (mildew resistance locus O) function . Ol-1-
mediated resistance to powdery mildew in tomato requires enzymes
glutathione S-Transferase  and acetolactate synthase . More
recently, 15 other SlMlo homologs were identified and characterized
for their structural organization, phylogenetic analysis and expression
profiles . In the future, it would be interesting to investigate the
possible roles of these homologs in tomato defense against other
powdery mildew species including Erysiphe orontii and Leveillula
As opposed to the specific response to pathogen-encoded effectors in
gene-foR-gene host-pathogen interactions, the mode of action of Asc-1-
mediated resistance to the late blight disease caused by the fungus Alternaria
alternaria formae speciales lycopersici is based on insensitivity to
sphinganine-analog mycotoxins (SAMs) . Consequently, Asc-1
has no homology to any published plant disease resistance gene but
is homologous to the Saccharomyces cerevisiae LAG1 that has been
associated with life span in yeast. Thus, the mechanism of Asc-1-
mediated resistance is by preventing apoptosis in resistant plants by
the restoration of EGGAP transport . Overexpression of Asc-1 gene
also confers resistance to Alternaria in Nicotiana umbratical .
Nematodes and Insects
In nematodes two R-genes have been cloned so far including
Mi and Hero. Differences in resistance mechanisms or incompatible
responses to nematodes are also evident in tomato. Hero-mediated
resistance against potato cyst nematodes (PCNs) (Globodera spp.) is
often described as a “hypersensitive-like” or “delayed hypersensitive”
response that appears after syncytium (feeding structure) induction,
leading to slow deterioration or abnormal development of the feeding
site . Although PCNs and similar cyst-forming nematodes are able
to invade and develop on resistant plants, however, their reproduction
is severely compromised . Hero encodes a NLR protein and confers
resistance to all pathotypes of G. rostochiensis and partial resistance to
G. pallidaMacrosiphum euphorbiae . Hero gene is not only expressed in roots but also in
aerial parts including, stems, leaves, and flower buds, its expression
is upregulated in roots in response to PCN infection and correlates
with the timing of syncytium death . Interestingly, inoculation of
tomato leaves with PCN also leads to HR indicating that Hero-mediated
resistance response is not tissue-specific .
In contrast to Hero, Mi-1.2-mediated resistance against root-knot
nematodes (RKN) (Meloidogyne spp.) is early and involves HR. As a
result, the invading juvenile is not able to induce a feeding site and
becomes surrounded and embedded among necrotized cells . The
Mi-1.2 gene also confers resistance to certain potato aphid isolates
(Macrosiphum euphorbiae), whitefly (Bemisia tabaci) and to some
extend to psyllids (Bactericerca cockerelli) [84-88] via yet unidentified
mechanism(s) that does not involve HR. Although Mi-1 is an effective
source of RKN resistance, Mi-1-mediated resistance is inactive above
28°C soil temperature . More recently, another nematode resistant
gene Mi-9, from the wild species Solanum arcanum, was genetically
characterized and identified as a homolog of Mi-1 that conferred heatof stable resistance to RNK . Interestingly, silencing Mi-1 homologs
in tomato lines carrying Ol-4 and Ol-6 compromised the resistance to O. neolycopersici in those lines, suggesting that Ol-4 and Ol-6 are Mi-1
homologs . About 59 Mi-1 homologs have been identified in the
genome of the cultivated potato species S. tuberosum and S. phureja . The evolutionary history of Mi-1 and another R-gene family
member Sw5 (CNL protein that provides resistance to tomato spotted
wilt virus (TSWV) [93,94]) is analyzed in closely related Solanaceae family members S. tuberosum and S. lycopersicum . In this study,
the authors reported that the potato genome carries larger R-gene
families than tomato and this could due to sequential duplications in
the potato genome or recurrent gene losses in tomato. Further, they
observed that Sw5 and Mi-1 gene families had dissimilar evolutionary
histories. Overall, this work suggests that gene clusters are more prone
to duplication and translocation, which may occur through unequal
crossing overs or errors in the replication or recombination processes.
Interestingly, a recent study reported that Mi-1.2 has direct negative
effects on a zoophytophagous biocontrol agent Orius insidiosus .
Taken together, these findings suggests that a single dominant R-gene
mediated resistance can impact organisms belonging to very diverse
Besides conferring resistance against C. fulvum, the Cf-2 also
mediates resistance to the root parasitic nematode G. rostochiensis and
this resistance requires Rcr3pim protein of S. pimpinellifolium . A
tomato root cDNA library was screened in a yeast two-hybrid assay,
by using G. rostochiensis effector GR-VAP1 as bait. In this screen, it
was found that GR-VAP1interacts with apoplastic papain-like cysteine
proteases Rcr3pim. Tomato plants that lack the Cf-2 gene but has the
functional Rcr3pim allele have higher number of nematodes than the
Cf-0/Rcr3lycand Cf-0/rcr3-3 plants suggesting that Rcr3pim is the
virulence target of G. rostochiensis. Transient expression of GR-
VAP1 in tomato plants harboring Cf-2 and Rcr3pim triggers an HR
Plant viruses cause disease and severe losses in tomato. Similar
to other classes of pathogens, tomato plants have acquired a series of
R-genes against these viruses. Tomato virus can spread by different
ways such as transmission via contaminated seeds or insect borne
transmission. Tomato mosaic virus (ToMV) is a seed borne virus that
can be spread by human activities for instance agricultural workers
with contaminated hands, tools, and clothing, however transmission
by insects is rare. Tomato Tm-1-mediated resistance against ToMV
involves direct or indirect binding of the Tm-1 gene to replication
proteins of ToMV, thus, inhibiting RNA replication even before
formation of the active replication complexes on the membranes,
however there is no HR . The Tm-1 protein is predicted to have
the TIM barrel structure but there are no clues about their cellular
functions. Interestingly, the product of the Tm-1 (allelic to Tm-1)
gene found in the ToMV susceptible tomatoes can neither bind to
ToMV replication proteins nor inhibit ToMV multiplication but have
been shown to bind to the replication proteins of non-host viruses
tobacco mild green mosaic virus (TMGMV) and pepper mild mottle
virus (PMMoV) and inhibit their RNA replication in vitro resulting
in non-host resistance [98-100]. Another tomato R-gene, Tm-22,
confers resistance to ToMV by the recognition of the carboxy terminus
of the ToMV movement protein and interfering with viral cell-tocell
movement in plants . Tm-22 belongs to the CNL class of
resistance proteins . Transgenic tobacco plants expressing Tm-22
gene become resistant against infection with ToMV . Similarly,
transgenic potato plants over expressing Tm-22 gene confers resistance to multiple viruses like tobacco mosaic virus, ToMV, potato virus X
(PVX) and PVY .
An example of virus transmitted by insects mainly thrips is TSWV.
Tomato Sw5 gene confers resistance against TSWV [93,94]. The Avr
determinant of tomato Sw-5 protein is the NSm movement protein of
TSWV . Transient expression of the NSm protein in tomato and
generation of transgenic N. benthamiana harboring the Sw5-b gene
triggers an HR . Eight TSWV R-genes (Sw1a, Sw1b, Sw2, Sw3,
Sw4, Sw-5, Sw-6 and Sw-7) have been reported to date .
TYLCV belongs to the class of DNA viruses that are transmitted
via whiteflies and affects tomato production worldwide. There are total
six TYLCV resistance genes Ty-1 to Ty-6. Ty-1 and Ty-3, both derived
from Solanum chilense and are allelic. The Ty-1/Ty-3-mediated defense
against TYLCV is somehow different from tomato defense against
other viruses as TYLCV shows low levels of viral replication and
systemic spread but with moderate (as with Ty-3) or no (as with Ty-
1) visual symptoms . Ty-1 and Ty-3 are allelic and represents a
unique category of R-genes that encode for RNA-dependent RNA
polymerases (RdRp) unlike most of the R-genes discussed so far that
belongs to NLR family. Ty-1 and Ty-3 are proposed to confer resistance
to TYLCV by amplifying the RNAi signal . The catalytic domain
of the Ty-1/Ty-3 allele is characterized by a five-amino acid motif,
DFDGD . As compared to susceptible tomato plants, Ty-1/Ty-3
plants have higher levels of siRNA amplifications and Ty-1 plants also
show higher levels of TYLCV DNA methylation . Interestingly,
Ty-1-mediated resistance is also effective against the bipartite tomato
severe rugose begomo virus, suggesting enhanced transcriptional gene
silencing, however, a mixed infection of TYLCV with a RNA virus
such as cucumber mosaic virus (CMV) compromised the resistance
leading to a decrease in Ty-1–mounted anti-geminiviral RNAi response
. Under natural field conditions with the occurrences of mixed
viral infection Ty-1-mediated resistance might not be very effective.
Unlike Rx-mediated resistance that results in extreme resistance (ER)
against potato virus X , TYLCV mediated resistance results in
virus tolerance rather than immunity. Functional Ty-1/Ty-3-like
alleles are also present in several other S. chilense wild type tomato
accessions, shown by fine mapping and VIGS . Additionally,
the DFDGD catalytic domain of the Ty-1and Ty-3 genes is conserved
among Solanum species . In a recent study, Ty-2 and Ty-3 genes
were used to develop a series of R-gene pyramided tomato lines and the
linked markers were evaluated for their diagnostic value and utility in
pyramiding Ty genes .
Pseudomonas syringae pv. tomato (Pst) causes bacterial speck
of tomato and the major sources of Pst infection can be seed and
infected crop debris. In tomato a serine-threonine protein kinase Pto
gene confers resistance to Pst strains carry the avirulence gene AvrPto
. Prf that encodes an NLR resides in the middle of the Pto gene
cluster . In tomato, Prf-mediated resistance against Pst involves
recognition of secreted effectors (AvrPto or AvrPtoB) by two highly
homologous tomato protein kinases Pto and Fen [114-117]. Changes
in these kinases upon binding to the effectors are detected by Prf,
resulting in HR at the sites of attempted infection.
Signaling Components Acting Downstream of Tomato
Early understanding of host-pathogen interaction came from
studies conducted in Arabidopsis. Identification and characterization
of host components underlying ETI revealed both common and specific signaling components in R-gene mediated resistances against different
biotic stresses [118-120]. Some of the important components of R-gene
mediated downstream signaling from Arabidopsis include Non-Race-
Specific Disease Resistance1 (NDR1), Enhanced Disease Susceptibility1
(EDS1), Phytoalexin Deficient 4 (PAD4), Nonexpresser of PR genes
1 (NPR1), Suppressor of the G2 allele of SKP1 (SGT1), Required for
Mla 12 Resistance (RAR1), RAR2, AvrPphB susceptible 3 (PBS3), Heat
Shock Protein (HSP90) [42,121]. Additional signaling components
include, the mitogen-activated protein (MAP) kinases, one of the
largest group of plant kinases that function in the regulation of complex
plant defense reactions by altering the activity of the different signal
transduction pathways through phosphorylation/dephosphorylation of
proteins . Defense associated phytohormones including jasmonic
acid (JA), ethylene (ET) and salicylic acid (SA) regulate plant responses
to a wide range of pests and pathogens. There are excellent reviews
focusing on the complex network of defense signaling pathways that
involve these three phytohormones .
Tomato became another ideal model for studying host-pathogen
interaction as it is natural host of many pests and pathogens as well as
possesses a repertoire of R-genes. The application of VIGS, transient
reverse genetics approach, has been successfully used to study the
function of certain tomato genes . To analyze the function of some
of tomato R-genes that produce HR and to identify their downstream
signaling components and mechanisms many groups have performed
experiments in tomato. However, given the moderate efficiency of
VIGS in tomato, large-scale random screens have been conducted in
the heterologous system N. benthamiana, where VIGS is more effective.
Many of the functional studies in N. benthamiana have been performed
by using an auto active tomato R-gene and by transient expression of
corresponding Avr, to consistently and uniformly activate the host
system and thus avoiding variations caused by the infecting organisms.
Tomato and C. fulvum interaction is a model to study the
receptoR-mediated resistance . Using VIGS in tomato and/
or N. bethamiana or N. tobaccum the different components of this interaction have been identified (Figure 1), including Cf-9-interacting
thioredoxin (CITRX) , Avr9/Cf-9 induced kinase 1 (ACIK1)
, the NLR protein required for HR-associated cell death 1 (NRC1)
, the U-box protein CMPG1 , the LeMPK1, LeMPK2, and
LeMPK3 , Avr9/Cf-9–Induced F-Box1 (ACIF) , members
of the phospholipase C family , Suppressor of BAK1-Interacting
RLK1 1 (SOBIR1) , Somatic Embryogenesis Receptor Kinase1
(SERK3)/BAK1 , endoplasmic reticulum residing chaperones
including HSP70 binding proteins (BiPs) and a lectin-type calreticulin
Figure 1: Downstream signaling components of tomato R-genes.
Likewise, using VIGS in tomato the signaling cascade downstream
of Ve1 is shown to require several components including EDS1, NDR1,
NRC1, ACIF, MEK2 and SERK3/BAK1 (Figure 1) . To identify
additional components involved in Ve1-mediated signaling, a GFPtagged
version of Ve1 protein was overexpressed in N. benthamiana leaves, followed by mass spectrometry. This resulted in the identification
of BiPs and CRT as Ve1 interacting proteins. VIGS mediated
knockdown of BiPs and CRTs in tomato resulted in compromised
Ve1-mediated resistance to V. dahliae in most cases, showing that
these chaperones play an important role in Ve1 functionality .
Furthermore, by using VIGS it has been demonstrated that SOBIR1
and SERK3/BAK1 are also required for I/Avr1-dependent necrosis
in N. benthamiana . In a genetic based screening F2 tomato
seedlings, those homozygous for the eds1 mutation (eds1/eds1) and
those that were heterozygous (EDS1/eds1), were chosen for a disease
assay and were inoculated with Fol race 3. Samples were screened for
the disease resistance and it was found that EDS1 is required for I-7
mediated resistance .
By applying VIGS in tomato plants it has been shown that Mi-1.2-
mediated resistance against nematodes and aphids requires Hsp90,
Sgt1, members of the MAP kinase cascade and WRKY transcription
factors (Figure 1) [138-141]. In addition, by utilizing transgenic tomato
plants expressing NahG (encodes for an enzyme that metabolizes SA) a
role for SA in Mi-1–mediated resistance to potato aphids was identified . In a VIGS screen performed in N. benthamiana to identify
the components of Mi-signaling that can suppress HR triggered by a
constitutively active form of Mi-1, Mi-DS4, SERK1 was identified as an
important player [142,143].
To identify the tomato proteins that interact with ToMV movement
protein or Tm-22-LRR yeast two-hybrid screens were performed
and tomato cDNA library was screened, by using ToMV movement
protein and Tm-22-LRR as respective baits . In these screens
Rubisco small subunit (RbCS) was identified as interacting with ToMV
movement protein and SGT1 as interacting with Tm-22, in addition
MP-Interacting Protein 1 (MIP1), a group of type I J-domain proteins
was found to interact with both ToMV movement protein and Tm-22.
By using VIGS and other in vitro and in vivo functional analysis in
N. benthamiana, it was shown that MIP1s are required for both virus
infection and plant immunity . Furthermore, transgenic N.
benthamiana plants expressing Tm-22, provides extreme resistance to
ToMV, and VIGS mediated silencing of NbRbCS compromised Tm-22-
dependent resistance, suggesting that RbCS of N. benthamiana plays an
important role in ToMV movement and plant antiviral defenses .
To identify the genes involved in TYLCV resistance a reverse genetic
approach was used where the susceptible and resistance tomato inbred
lines from the same breeding program were inoculated with TYLCV
. cDNA libraries from inoculated and non-inoculated plants
were compared and a trans membranal transporter protein Permease
I-like was found to be preferentially expressed in resistant plants and
VIGS mediated silencing of Permease gene in tomato led to decrease
in resistance . Furthermore, VIGS mediated silencing of hexose
transporter LeHT1, resulted in plant growth inhibition and enhanced
virus accumulation and spread and also resulted in a necrotic response
along the stem and petioles of infected LeHT1-silenced R plants .
Pto-mediated resistance involves several components including
kinases MEK1 andMEK2, wound-induced protein kinase (WIPK),
NTF6, two transcription factors TGA1a and TGA2.2 and NPR1
(Figure 1) . Furthermore, using stable RNAi/CaMV transient
overexpression/VIGS about 25 genes were identified to play a role in
Pto-mediated ETI as reviewed by .
Current and Future Perspective
Plants are continuously being challenged by new pathogen and pest
races/strains, some of which being able to overcome the plant R-gene
mediated defenses. One of the main goals of agricultural research is
to develop technologies to overcome resistance breaking to prevent
disease. In the past, few decades use of molecular markers has facilitated
identification, mapping, characterization and transfer of many
important traits in tomato including the traits for disease resistance
[149,150]. With the recent advances in molecular biology and genetic
approaches, several R-genes have been cloned (as discussed above).
A broad-spectrum application for crop improvement and managing
resistance that has gained great attention is non-host resistance .
Other alternatives include functional stacking of R-genes that has been
successfully used in potato and tomato [152-154] and targeting the
susceptible genes can result in a more broad-spectrum and durable type
of resistance . Furthermore, there has been increase resistance
against some pathogens in tomato by transferring the R-genes from
other plant species like pepper and potato [156,157].
Apart from the breeding technologies, a deeper understanding of
plant innate immune perception and signaling is equally important.
Here comes the role of model plants A. thaliana and easily amenable
plant species such as Nicotiana species [158,159]. RNAi based approaches including siRNAs, miRNAs and Agrobacterium-mediated
transient expression of dsRNA have been used against viruses, insects,
and fungal pathogens . Spray-induced gene silencing strategy
utilizing dsRNAs and small RNAs targeting pathogen genes has also
been successful against Botrytis cinerea . More recently genomeediting
technologies such as TALENs and CRISPR/Cas9 have been
used in plant crop improvement, plant-breeding and enhanced
pathogen resistance [162-164]. CRISPR/Cas9 has been successfully
used to target TYLCV genome. Guide RNAs specific for coding and
non-coding sequences of TYLCV were delivered via tobacco rattle
virus into N. benthamiana plants stably overexpressing the Cas9
endonuclease. Subsequent challenge of these plants with TYLCV lead to
a significant reduction in TYLCV accumulation and disease symptoms
. Recently, CRISPR-Cas9 system has been also used to inactivate
tomato SlDMR6-1 (downy mildew resistance 6) resulting in disease
resistance against different pathogens, including P. syringae, P. capsici
and Xanthomonas spp. with no significant effect on plant growth and
development . Overall suggesting that these new technologies can
be utilized for multiplex targeting of the pathogen virulence genes as
well as plant susceptibility genes. Thus, there is a potential to enhance
plant resistance by targeting newly evolved effectors and generating a
platform for dissecting natural resistance and immune functions. At
the same time, it will provide biotechnologists with a powerful tool for
producing crop plants resistant to multiple viral infections.
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