| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
Plant Physiology 132:1901-1912 (2003) © 2003 American Society of Plant Biologists Overexpression of the Disease Resistance Gene Pto in Tomato Induces Gene Expression Changes Similar to Immune Responses in Human and Fruitfly1,[w]Plant Biology Division, Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73402 (K.S.M.); Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (K.S.M., M.D.D., X.H., G.B.M.); and Department of Plant Pathology, Cornell University, Ithaca, New York 14853 (G.B.M.)
The Pto gene encodes a serine/threonine protein kinase that confers resistance in tomato (Lycopersicon esculentum) to Pseudomonas syringae pv tomato strains that express the type III effector protein AvrPto. Constitutive overexpression of Pto in tomato, in the absence of AvrPto, activates defense responses and confers resistance to several diverse bacterial and fungal plant pathogens. We have used a series of gene discovery and expression profiling methods to examine the effect of Pto overexpression in tomato leaves. Analysis of the tomato expressed sequence tag database and suppression subtractive hybridization identified 600 genes that were potentially differentially expressed in Pto-overexpressing tomato plants compared with a sibling line lacking Pto. By using cDNA microarrays, we verified changes in expression of many of these genes at various time points after inoculation with P. syringae pv tomato (avrPto) of the resistant Pto-overexpressing line and the susceptible sibling line. The combination of these three approaches led to the identification of 223 POR (Pto overexpression responsive) genes. Strikingly, 40% of the genes induced in the Pto-overexpressing plants previously have been shown to be differentially expressed during the human (Homo sapiens) and/or fruitfly (Drosophila melanogaster) immune responses.
Both plants and animals are continually exposed to pathogens, and, as a result, they have evolved intricate defense mechanisms to recognize and defend themselves against a wide array of these disease-causing agents. Recent studies have revealed common mechanisms of pathogen virulence and host resistance underlying plant and animal diseases (Cohn et al., 2001  ;
Staskawicz et al., 2001;
Nurnberger and Brunner, 2002).
For example, bacterial pathogens of both plants and animals deliver virulence
proteins into the host cytoplasm via the type III secretion system
(He, 1998;
Galan and Collmer, 1999).
Pathogen-associated molecular patterns that are similar to those activating
immune responses in animals have been shown to mediate activation of plant
defenses (Nurnberger and Brunner,
2002). Some plant disease resistance (R) proteins share motifs
with signaling components of immune response pathways in mammals and
invertebrates (Staskawicz et al.,
2001). A striking similarity underlying the molecular mechanisms
of pathogen recognition in plants and animals is suggested by the recent
isolation of the intracellular receptors NOD1 and NOD2 involved in human
(Homo sapiens) Crohn's disease
(Ogura et al., 2001a). In
common with a large family of plant R proteins, the NOD1/2 proteins contain a
putative nucleotide-binding site and a region of Leu-rich repeats
(Ogura et al., 2001b).
In tomato (Lycopersicon esculentum), the R gene
Pto encodes a Ser/Thr kinase and confers resistance against strains
of Pseudomonas syringae pv tomato that express the effector
proteins AvrPto or AvrPtoB (Martin et al.,
1993
We have now used suppression subtractive hybridization (SSH;
Diatchenko et al., 1996
Use of in Silico EST Subtraction to Identify Genes That Are Differentially Expressed upon P. syringae pv tomato Inoculation in Tomato Leaves Overexpressing Pto As one method of identifying genes that might be differentially expressed in response to inoculation with P. syringae pv tomato(avrPto), we analyzed the tomato EST database for sequences derived from line R11-12 that expresses the Pto gene from the CaMV 35S promoter and a sibling line R11-13 that has segregated away this transgene. As described in "Materials and Methods," both lines were inoculated with the avirulent P. syringae pv tomato(avrPto), and leaves were harvested at various time points afterward. We analyzed 10,872 EST sequences from the R11-12 (R) and R11-13 (S) libraries (5,316 for R library and 5,556 for S library). A total of 6,921 of these EST sequences assembled into 1,414 contigs that contained either ESTs all derived from one of the libraries (116 contigs with at least three ESTs; 42 contained ESTs only from the R library, whereas 74 contigs contained ESTs only from the S library; Fig. 1) or a mix of ESTs from both libraries (1,298 contigs). The 3,953 singleton ESTs were excluded from further analysis. Of the 1,298 contigs with mixed R and S sequences, we identified 132 cases where the EST counts within a contig differed by more than 3-fold between R and S libraries (Fig. 1). An additional 51 contigs were identified that encoded known defense genes and that had counts between the libraries differing by more than 2-fold. To test if the genes corresponding to these ESTs were differentially expressed in P. syringae pv tomato-inoculated R11-12 and R11-13 leaves, we selected a representative cDNA clone from each of the 299 contigs (116 cases with at least three ESTs coming only from either R or S library, 132 cases with >3-fold differences, and the 51 cases with >2-fold differences) for microarray analysis (see below).
In a second approach to identify differentially expressed genes, we
performed cDNA subtraction, an open-architecture gene expression profiling
technique. By using SSH (Diatchenko et
al., 1996
A total of 600 cDNA clones (some redundancy was observed) obtained from SSH and in silico EST subtraction were selected for microarray analysis. cDNA clones corresponding to known plant defense related genes were also included. Both R11-12 and R11-13 plants were inoculated with P. syringae pv tomato(avrPto), and RNA was isolated at different time points (0, 1, 2, 4, and 8 h) afterward. These RNA samples were used for microarray hybridization. From 299 genes identified by in silico EST subtraction, 159 (53%) of them were differentially expressed (>2-fold) in at least one of the five time points analyzed. Of the 301 clones that were identified by SSH, 158 clones (52%) were shown to be differentially expressed (>2-fold) in at least one of the five time points. Overall, by combining the approaches of in silico EST subtraction, SSH, and cDNA microarrays, we identified 223 nonredundant genes that were significantly differentially expressed at one or more time points between the R11-12 and R11-13 plants (see supplemental data Table S1 at http://www.plantphysiol.org). We designate these genes as POR (Pto overexpression responsive). Scatter plots were generated to display the differential expression of the POR genes at different time points after inoculation (Fig. 2). Interestingly, 106 genes were differentially expressed more than 2-fold at the 0-h time point (without any P. syringae pv tomato inoculation), and the transcripts of most of these genes were more abundant in Pto-overexpressing line R11-12 than in the susceptible line R11-13. Remarkably, the transcript abundance of some of the genes (osmotin like, class I chitinase, and basic 30-kD endochitinase precursor) at 0-h time point was greater than 100-fold in R11-12 as compared with R11-13. The number of genes with lower transcript abundance in R11-12 than in R11-13 increased markedly at 8 h after inoculation when compared with the 0-h time point (Fig. 2). The number of genes that were differentially expressed by more than 10-fold in R11-12 compared with R11-13 was reduced at 8 h after inoculation when compared with the 0-h time point. This is not unexpected because many defense-related genes are known to be expressed early in incompatible interactions and to then be very highly expressed later in the compatible interaction. Expression data of the 223 POR genes (those genes with >2-fold expression differences) were used for cluster analysis as described below.
The ratios of spot intensities of the 223 POR genes obtained at
different time points after inoculation of R11-12 and R11-13 with P.
syringae pv tomato(avrPto) were used to do a hierarchical
cluster analysis (Eisen et al.,
1998
Cluster E includes a set of genes whose expression in R11-12 is suppressed during the resistance response, in comparison with R11-13 plants, with the suppression starting at 4 h after inoculation and reaching a maximum at 8 h after inoculation. Cluster E contains mostly genes encoding chloroplast- and photosynthesis-related proteins (Fig. S2c). Cluster F contains genes whose expression was suppressed, without pathogen inoculation, in the R11-12 plants when compared with R11-13 plants. Cluster F comprises a variety of genes that encode proteins like translation initiation and elongation factors, ACC oxidase, prohibitin, proteasome alpha-subunit, and chromatin-associated proteins (Fig. S2c). Expression of genes in cluster G is very similar to Cluster E except that the suppression of these genes was observed only at 8 h after inoculation. Cluster G is also enriched with chloroplast- and photosynthesis-related genes (Fig. 3).
POR genes were classified based on their potential cellular functions into 21 different groups (Table I). Of the 21 classes, the majority of the genes in 16 of the classes were "up-regulated" in R11-12 plants. Viewed broadly, they include genes involved in cell protection (from oxidative stress), cell wall fortification, hormone responses, HR, general metabolism, known plant defense functions, transport, signaling, ubiquitination, and water transport, and genes encoding pathogenesis-related proteins, ribosomal proteins, stress-related proteins, transcription factors, proteins with no homology to an annotated gene in the database, and genes encoding proteins of unknown function. Three classes of genes had both up- and down-regulated genes, and these include genes required for various other miscellaneous functions, phenylpropanoid metabolism, and senescence-associated proteins. It is interesting to note that almost 19% of the POR genes were photosynthesis- and chloroplast-related genes (see supplemental data Table S1 at http://www.plantphysiol.org). Without any exceptions, all the photosynthesis- and chloroplast-related genes were "down-regulated" during the resistance response. All photosynthesis- and chloroplast-related genes were suppressed only after pathogen inoculation and had maximum suppression at 8 h after inoculation.
We compared the POR genes with a recently identified set of genes
that is differentially expressed 4 h after inoculation with avirulent P.
syringae pv tomato(avrPto) in a tomato line expressing
Pto from its native promoter (RG-PtoR;
Mysore et al., 2002
Because striking similarities exist among both R proteins and downstream
signaling components of plants and certain animal and fruitfly proteins with
roles in immunity (Cohn et al.,
2001
Signaling pathways leading to activation of defense response genes in mammals, insects, and plants share many similar components (Cohn et al., 2001 ;
Staskawicz et al., 2001). For
example, the resistance protein Pto shares sequence similarity with the IRAK
proteins in human and Pelle in fruitfly, both of which play central roles in
controlling the innate immune response
(Cohn et al., 2001). To
investigate whether "downstream" defense responses are similar
among mammals, insects, and plants, we compared the POR genes with
previously published human and fruitfly immune response genes
(Gregorio et al., 2001;
Huang et al., 2001;
Irving et al., 2001).
Strikingly, 40% of the POR genes that were abundantly expressed in
Pto-overexpressing plants are functionally similar to genes
previously shown to be induced during human and/or fruitfly immune responses
(Table II). Some of these could
be general stress-responsive genes and may not be specific to pathogen-induced
immune response. However, they may also still play a role in conferring
immunity against pathogens. These results suggest that defense responses in
these diverse organisms are either conserved or may have arisen by convergent
evolution. For example, genes encoding metallothionein (MT), GST, thioredoxin
(TRX), cytochrome P450 (P450), heat shock proteins (HSPs), ribosomal proteins,
and ubiquitin-conjugating enzymes are all induced during defense responses in
Pto-overexpressing plants, humans, and fruitfly
(Table II). Although these
genes are reasonably well characterized in mammalian systems, their actual
role in immunity is not clear. Because of the availability of high-throughput
techniques like virus-induced gene silencing and reverse genetics in plants,
it might be easier to investigate the function of these in immunity by using a
plant model system.
The oxidative burst that precedes HR, a common phenomenon triggered by an
incompatible plant pathogen interaction, has been suggested to be a primary
event responsible for triggering the cascade of defense responses in various
plant species against infection with avirulent pathogens or pathogen-derived
elicitors. The oxidative burst may be followed by activation of genes encoding
antioxidant enzymes in tissue surrounding the initial infection site
(Lamb and Dixon, 1997
MTs and GSTs are a group of stress and immune response proteins that
contribute to cellular survival due to oxidative damage
(Borghesi and Lynes, 1996
Protein translation plays an important role during innate immunity in
plants, animals, and insects. For example, the fruitfly Thor gene has
been shown to be required for innate immunity in fruitfly by preferential
translation of immune transcripts (Bernal
and Kimbrell, 2000
Protein ubiquitination is not only essential for the normal physiological
turnover of proteins but appears to have been adapted as part of an
intracellular surveillance system that can be activated by altered, damaged,
or foreign proteins and organelles and has evolved to be an
"intracellular immune system"
(Ben-Neriah, 2002
Pto-overexpressing plants (R11-12) are slightly stunted, and they
develop small white veins in the leaves as they age
(Li et al., 2002
Requirement of Prf for the constitutive plant defense response
mediated by Pto overexpression
(Xiao et al., 2003
A recent report from Xiao et al.
(2001 We identified 21 different classes of genes that were differentially expressed in R11-12 after inoculation with P. syringae pv tomato expressing avrPto (Table I). Interestingly, genes belonging to these classes, with the exception of chloroplast- or photosynthesis-related genes, water transport-related genes, and ubiquitination pathway genes, were constitutively expressed in the R11-12 plants in the absence of P. syringae pv tomato expressing avrPto. Figure 4 depicts a model for constitutive plant defense responses due to Pto overexpression.
Phenylpropanoids have been proposed to serve as flower pigments (anthocyanin), UV protectants, defense chemicals (phytoalexins and insect repellents), allelopathic agents, and signal molecules in plant-microbe interactions. We identified 10 different genes (POR97-105) involved in the phenylpropanoid pathway that are differentially expressed in the Pto-overexpressing plants, R11-12. Five of these 10 genes were constitutively differentially expressed in R11-12 plants. Cell wall reinforcement and thickening are associated with plant defense during resistance response. In this study, we have shown that majority of the cell wall-associated genes (POR20-21, POR23-24, and POR26-27) were constitutively up-regulated in R11-12 plants.
Overlap between the leaf senescence and pathogen defense programs has been
reported earlier (Quirino et al.,
1999
Water is essential for pathogen multiplication in the plant tissue. One of
the P. syringae pv tomato disease symptoms is water-soaked
lesions on tomato leaves. In this study, we have shown that four
aquaporin/tonoplast intrinsic proteins (POR220-223) were induced
during the resistance response. Interestingly, aquaporin genes were suppressed
during a previously studied Pto (native promoter driven)-mediated
disease resistance response (Mysore et
al., 2002
Several genes encoding known components of the Pto signal transduction
pathway were deliberately included in the microarray experiments to study
their expression in Pto-overexpressing plants (see supplemental data
Table S1 at
http://www.plantphysiol.org).
As expected, the Pto gene (POR161) was abundantly expressed
in the R11-12 plants when compared with the azygous plants at the 0-h time
point. Pto was slightly induced due to P. syringae pv
tomato expressing avrPto inoculation. This was probably due
to the CaMV 35S promoter used to overexpress the Pto gene. Tomato
plants infected by the avirulent P. syringae pv tomato have
been shown to accumulate SA (Oldroyd and
Staskawicz, 1998
Api1 and Api2 encode tomato proteins that interact with
AvrPto in a yeast two-hybrid system
(Bogdanove and Martin, 2000
The possible role of Pto in a basal defense response is suggested
by our recent report that the RG-PtoR plants constitutively induce several
defense-related genes, including PR genes without any pathogen infection
(Mysore et al., 2002
Plant Materials, Bacterial Strains, Plant Inoculation, and RNA Isolation
Tomato (Lycopersicon esculentum) Pto-transgenic line
R11-12 (35S::Pto/35S::Pto) and a sibling line R11-13 that has
segregated away the Pto transgene were described previously
(Tang et al., 1999
To create cDNA libraries, 4-week-old plants of tomato lines R11-12 and R11-13 were vacuum infiltrated with Pseudomonas syringae pv tomato strain T1 expressing avrPto at concentrations of either 105 or 108 cfu mL–1. At the 108 cfu mL–1 (high titer) inoculation level, leaves were harvested at 0, 2, 4, 6, and 8 h after inoculation. Effectiveness of the high-titer inoculations was verified by assessing defense-related gene expression (in R11-13) or by observation of the HR (in R11-12). At the 105 cfu mL–1 (low titer) inoculation level, leaves were harvested at 0, 12, 24, 36, and 48 h after inoculation. Effectiveness of the low-titer inoculations was verified by assessing defense-related gene expression (in both R11-12 and R11-13). Equal amounts of leaf tissues from the R11-12 and R11-13 plants from the different time points of high- and low-titer inoculations for each line were pooled and used to extract total RNA. Poly(A+) RNA was purified using the poly(A+) tract mRNA isolation system (Promega, Madison, WI). An oriented Uni-ZAP XR library was prepared using a ZAP-cDNA synthesis kit (Stratagene, La Jolla, CA) according to the manufacturer's instructions. The cDNA (0.4 µg) was ligated into Uni-ZAP XR digested with XhoI and EcoRI. This yielded 1.4 x 106 and 1.2 x 106 primary plaques for the R11-12 (R) library and the R11-13 (S) library. Mass excision was performed on 1 x 107 plaque-forming units from each library. Escherichia coli strain XL1-Blue MRF was used for propagating the library. The bacterial cultures were subsequently arrayed into 384-well plates and used for sequencing. Additional information about the libraries can be found online (http://sgn.cornell.edu or http://www.tigr.org/tdb/tgi/lgi). Approximately 5,500 clones from each of the R and S libraries were sequenced by The Institute for Genomics Research (TIGR; http://www.tigr.org/tdb/tgi/lgi).
For in silico EST subtraction (Stekel
et al., 2000 SSH was done by using the CLONTECH PCR-Select cDNA Subtraction Kit (CLONTECH Laboratories Inc., Palo Alto, CA). Equal amounts of RNA from leaves 4 and 8 h after inoculation with P. syringae pv tomato(avrPto) were pooled for each of the R11-12 and R11-13 plants and used for SSH. Both forward (R11-12 as tester and R11-13 as driver) and reverse (R11-13 as tester and R11-12 as driver) subtractions were performed according to the manufacturer's protocol. The final PCR products (enriched for cDNAs corresponding to differentially expressed transcripts) resulting from the SSH were either digested with NotI and directly cloned into pBluescript vector or labeled with radioactive P32 (DECAprime DNA labeling kit, Ambion Inc., Austin, TX) and used as a probe on colony blots containing a nonredundant EST collection from the R and S libraries. PCR products cloned into pBluescript vector were sequenced (65 each from forward and reverse subtractions), and the sequences were searched against the NCBI databases. EST sequences corresponding to colonies that hybridized to the radiolabeled PCR product were obtained from the TIGR databases and were subsequently used for searches of the NCBI databases.
Inserts from approximately 650 cDNA clones corresponding to ESTs
(http://www.tigr.org)
were PCR amplified using T3 and T7 primers. This number included about 600
ESTs that corresponded to genes obtained by SSH (301) and in silico EST
subtraction (299), 38 ESTs that corresponded to known defense response genes,
and 12 controls (e.g. alpha-tubulin, beta-tubulin, and genes encoding
ribosomal proteins). PCR products were purified using MagBeads (Bangs Lab.,
Fishers, IN). Purified PCR products were vacuum dried and resuspended in 30
µl of spotting buffer (3x SSC + 0.1% [w/v] Sarkosyl). DNA spotting,
labeling, hybridization, and data analyses were performed as described earlier
(Mysore et al., 2002
Several quality control measures were implemented in our analysis of the
microarray data to meet the Minimum Information About a Microarray Experiment
(Brazma et al., 2001
We thank Paul Debbie (Boyce Thompson Institute Center for Gene Expression Profiling) for technical help with microarray experiments and David Wendell for deriving nonredundant cDNAs. Received February 26, 2003; returned for revision March 26, 2003; accepted May 3, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.022731.
1 This work was partly supported by Boyce Thompson Institute (innovation
grant to K.S.M.), by the Noble Foundation (grants to K.S.M.), and by the
National Science Foundation (Plant Genomics grant nos. IBN–9872617 and
IBN–0109633 to G.B.M.).
[w] The online version of this article contains Web-only data. The supplemental
material is available at
http://www.plantphysiol.org.
2 Present Address: U.S. Department of Agriculture, Agricultural Research
Service, Western Regional Research Center, Albany, CA 94710. * Corresponding author; e-mail ksmysore{at}noble.org; fax 580–224–6692.
Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in Early R gene-mediated plant defenses. Science 295: 2077–2080 Axelrod AE (1981) Role of the B vitamins in the immune response. Adv Exp Med Biol 135: 93–106[Medline]
Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu
K, Schulze-Lefert P (2002) The RAR1 interactor SGT1,
an essential component of R gene-triggered disease resistance.
Science 295:
2073–2076
Beck MA (2001) Antioxidants and viral
infections: host immune response and viral pathogenicity. J Am Coll
Nutr 20:
384S–388S Ben-Neriah Y (2002) Regulatory functions of ubiquitination in the immune system. Nat Immunol 3: 20–26[CrossRef][ISI][Medline]
Bernal A, Kimbrell DA (2000) Drosophila
Thor participates in host immune defense and connects a translational
regulator with innate immunity. Proc Natl Acad Sci USA
97:
6019–6024
Bogdanove AJ, Martin GB (2000) AvrPto-dependent
Pto-interacting proteins and AvrPto-interacting proteins in tomato.
Proc Natl Acad Sci USA 97:
8836–8840 Borghesi LA, Lynes MA (1996) Stress proteins as agents of immunological change: some lessons from metallothionein. Cell Stress Chaperones 1: 99–108[CrossRef][ISI][Medline] Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC et al. (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29: 365–371[CrossRef][ISI][Medline]
Brocksted E, Rickers A, Kostka S, Laubersheimer A, Dorken B,
Wittmann-Liebold B, Bommert K, Otto A (1998) Identification
of apoptosis-associated proteins in a human Burkitt lymphoma cell line:
cleavage of heterogeneous nuclear ribonucleoprotein A1 by caspase 3. J
Biol Chem 273:
28057–28064 Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48: 181–199[ISI] Cohn J, Sessa G, Martin GB (2001) Innate immunity in plants. Curr Opin Immunol 13: 55–62[CrossRef][ISI][Medline] Di Leo A, Messa C, Russo F, Linsalata M, Amati L, Caradonna L, Pece S, Pellegrino NM, Caccavo D, Antonaci S et al. (1999) Helicobacter pylori infection and host cell responses. Immunopharmacol Immunotoxicol 21: 803–846[Medline]
Diatchenko L, Lau Y-FC, Campbell AP, Chenchik A, Moqadam F,
Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED et al.
(1996) Suppression subtractive hybridization: a method for
generating differentially regulated or tissue-specific cDNA probes and
libraries. Proc Natl Acad Sci USA
93:
6025–6030 Efron DT, Barbul A (1999) Arginine and nutrition in renal disease. J Ren Nutr 9: 142–144[Medline]
Eisen MB, Spellman PT, Brown PO, Botstein D
(1998) Cluster analysis and display of genome-wide expression
patterns. Proc Natl Acad Sci USA
95:
14863–14868
Galan JE, Collmer A (1999) Type III secretion
machines: bacterial devices for protein delivery into host cells.
Science 284:
1322–1328
Gregorio ED, Spellman PT, Rubin GM, Lemaitre B
(2001) Genome-wide analysis of the Drosophila immune
response by using oligonucleotide microarrays. Proc Natl Acad Sci
USA 98:
12590–12595
Gu YQ, Yang C, Venkatappa TK, Zhou J, Martin GB
(2000) Pti4 is induced by ethylene and salicylic acid,
and its product is phosphorylated by the Pto kinase. Plant Cell
12:
771–785 He SY (1998) Type III protein secretion systems in plant and animal pathogenic bacteria. Annu Rev Phytopathol 36: 363–392[CrossRef][ISI][Medline]
Hirota K, Nakamura H, Masutani H, Yodoi J
(2002) Thioredoxin superfamily and thioredoxin-inducing agents.
Ann N Y Acad Sci 957:
189–199
Huang Q, Liu D, Majewski P, Schulte LC, Korn JM, Young RA,
Lander ES, Hacohen N (2001) The plasticity of
dendritic cell responses to pathogens and their components.
Science 294:
870–875
Irving P, Troxler L, Heuer TS, Belvin M, Kopczynski C, Reichhart
JM, Hoffman JA, Hetru C (2001) A genome-wide analysis
of immune responses in Drosophila. Proc Natl Acad Sci
USA 98:
15119–15124 Ishii T, Itoh K, Sato H, Bannai S (1999) Oxidative stress-inducible proteins in macrophages. Free Radic Res 31: 351–355[CrossRef][ISI][Medline]
Jo SH, Son MK, Koh HJ, Lee SM, Song IH, Kim YO, Lee YS, Jeong
KS, Kim WB, Park JW et al. (2001) Control of
mitochondrial redox balance and cellular defense against oxidative damage by
mitochondrial NADP+-dependent isocitrate dehydrogenase. J Biol
Chem 276:
16168–16176
Karinch AM, Pan M, Lin CM, Strange R, Souba WW
(2001) Glutamine metabolism in sepsis and infection. J
Nutr 131:
2535S–2538S Kim YJ, Lin N-C, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109: 589–598[CrossRef][ISI][Medline] Komissarenko SV, Gulaia NM, Gaivoronskaia GG, Karlova NP, Tarusova NB (1986) Inorganic pyrophosphatase activity of the mouse spleen in the immune response and after treatment with bis-phosphonates. Ukr Biokhim Zh 58: 22–27[Medline] Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275[CrossRef][ISI][Medline] Li J, Shan L, Zhou J-M, Tang X (2002) Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol Plant-Microbe Interact 15: 654–661[Medline] Liu Y, Schiff M, Dinesh-Kumar SP (2002a) Virus-induced gene silencing in tomato. Plant J 31: 777–786[CrossRef][ISI][Medline]
Liu Y, Schiff M, Serino G, Deng X-W, Dinesh-Kumar SP
(2002b) Role of SCF ubiquitin-ligase and the COP9 signalosome in
the N gene mediated resistance response to Tobacco mosaic
virus. Plant Cell 14:
1483–1496 Mabondzo A, Le Naour R, Raoul H, Clayette P, Lafuma C, Barre-Sinoussi FC, Cayre Y, Dormont D (1991) In vitro infection of macrophages by HIV: correlation with cellular activation, synthesis of tumour necrosis factor alpha and proteolytic activity. Res Virol 142: 205–212[CrossRef][Medline] Malaviya R, Abraham SN (2001) Mast cell modulation of immune responses to bacteria. Immunol Rev 179: 16–24[CrossRef][Medline]
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal
MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993)
Map-based cloning of a protein kinase gene conferring disease resistance in
tomato. Science 262:
1432–1436 Morfin R (2002) Involvement of steroids and cytochrome P(450) species in the triggering of immune defenses. J Steroid Biochem Mol Biol 80: 273–290[CrossRef][Medline] Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB (2002) Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J 32: 299–315[CrossRef][ISI][Medline] Nurnberger T, Brunner F (2002) Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 5: 318–324[CrossRef][ISI][Medline] Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH et al. (2001a) A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603–606[CrossRef][Medline]
Ogura Y, Inohara N, Benito A, Chen FF, Yamaoka S, Nunez G
(2001b) Nod2, a Nod1/Apaf-1 family member that is restricted to
monocytes and activates NF-kB. J Biol Chem
276:
4812–4818
Oldroyd GED, Staskawicz BJ (1998) Genetically
engineered broadspectrum disease resistance in tomato. Proc Natl Acad
Sci USA 95:
10300–10305 Pitarch A, Diez-Orejas R, Molero G, Pardo M, Sanchez M, Gil C, Nombela C (2001) Analysis of the serological response to systematic Candida albicans infection in a murine model. Proteomics 1: 550–559[CrossRef][Medline] Qin XF, Holuigue L, Horvath DM, Chua NH (1994) Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6: 863–874[Abstract] Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5: 278–282[CrossRef][ISI][Medline] Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40: 267–278[CrossRef][ISI][Medline] Ross D, Kepa JK, Winski SL, Beall HD, Anwar A, Siegel D (2000) NAD(P) H:quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem Biol Interact 129: 77–97[CrossRef][ISI][Medline] Shukla A, Berglund L, Nielsen LP, Nielsen S, Hoffman HJ, Dahl R (2000) Regulated exocytosis in immune functions: are SNARE-proteins involved? Respir Med 94: 10–17[CrossRef][Medline]
Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE
(2001) Common and contrasting themes of plant and animal
diseases. Science 292:
2285–2289
Stekel DJ, Git Y, Falciani F (2000) The
comparison of gene expression from multiple cDNA libraries. Genome
Res 10:
2055–2061
Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB
(1999) Overexpression of Pto activates defense responses
and confers broad resistance. Plant Cell
11:
15–30 Thara VK, Tang X, Gu YQ, Martin GB, Zhou JM (1999) Pseudomonas syringae pv tomato induces the expression of tomato EREBP-like genes Pti4 and Pti5 independent of ethylene, salicylate and jasmonate. Plant J 20: 475–483[CrossRef][ISI][Medline]
Xiao F, Lu M, Li J, Zhao T, Yi SH, Thara VK, Tang X, Zhou J
(2003) Pto mutants differentially activate
Prf-dependent, avrPto-independent resistance and
gene-for-gene resistance. Plant Physiol
131:
1239–1249
Xiao F, Tang X, Zhou J (2001) Expression of
35S::Pto globally activates defense-related genes in tomato plants.
Plant Physiol 126:
1637–1645
Zancope-Oliver RM, Reiss E, Lott TJ, Mayer LW, Deepe GS
(1999) Molecular cloning, characterization, and expression of the
M antigen of Histoplasma capsulatum. Infect Immunol
67:
1947–1953 Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16: 3207–3218[CrossRef][ISI] |
TOP
ABSTRACT
RESULTS
, Differential
expression; ^, mouse immune response.
