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Journal ArticleDOI

Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid.

TL;DR: It is found that PR-1(P4) was a hallmark for the cultivar resistance conferred by Hero A against PCN and that nematode parasitism resulted in the inhibition of the SA signaling pathway in the susceptible cultivars.
Abstract: To understand the machinery underlying a tomato cultivar harboring the Hero A gene against cyst nematode using microarrays, we fi rst analyzed tomato gene expression in response to potato cyst nematode (PCN; Globodera rostochiensis ) during the early incompatible and compatible interactions at 3 and 7 days post-inoculation (dpi). Transcript levels of the phenylalanine ammonia lyase ( PAL ) and Myb related genes were up-regulated at 3 dpi in the incompatible interaction. Transcription of the genes encoding pyruvate decarboxylase ( PDC ) and alcohol dehydrogenase ( ADH ) was also up-regulated at 3 dpi in the incompatible interaction. On the other hand, the four genes ( PAL , Myb , PDC and ADH ) were down-regulated in the compatible interaction at 3 dpi. When the expression levels of several pathogenesis-related (PR) protein genes in tomato roots were compared between the incompatible and compatible interactions, the salicylic acid (SA)-dependent PR genes were found to be induced in the incompatible interaction at 3 dpi. The PR-1 ( P4 ) transcript increased to an exceptionally high level at 3 dpi in the cyst nematode-infected resistant plants compared with the uninoculated controls. The free SA levels were elevated to similar levels in both incompatible and compatible interactions. We then confi rmed that PR-1 ( P4 ) was not signifi cantly induced in the NahG tomato harboring the Hero A gene, compared with the resistant cultivar. We thus found that PR-1 ( P4 ) was a hallmark for the cultivar resistance conferred by Hero A against PCN and that nematode parasitism resulted in the inhibition of the SA signaling pathway in the susceptible cultivars.

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Citations
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Journal ArticleDOI
TL;DR: Genetic analysis of backcrosses indicated the successful inheritance of the mutations in BC1F2 populations, confirming the reproducibility in the morphological phenotyping of the M2 plants and developed the in silico database TOMATOMA, a relational system interfacing modules between mutant line names and phenotypic categories.
Abstract: The tomato is an excellent model for studies of plants bearing berry-type fruits and for experimental studies of the Solanaceae family of plants due to its conserved genetic organization. In this study, a comprehensive mutant tomato population was generated in the background of Micro-Tom, a dwarf, rapid-growth variety. In this and previous studies, a family including 8,598 and 6,422 M2 mutagenized lines was produced by ethylmethane sulfonate (EMS) mutagenesis and γ-ray irradiation, and this study developed and investigated these M2 plants for alteration of visible phenotypes. A total of 9,183 independent M2 families comprising 91,830 M2 plants were inspected for phenotypic alteration, and 1,048 individual mutants were isolated. Subsequently, the observed mutant phenotypes were classified into 15 major categories and 48 subcategories. Overall, 1,819 phenotypic categories were found in 1,048 mutants. Of these mutants, 549 were pleiotropic, whereas 499 were non-pleiotropic. Multiple different mutant alleles per locus were found in the mutant libraries, suggesting that the mutagenized populations were nearly saturated. Additionally, genetic analysis of backcrosses indicated the successful inheritance of the mutations in BC1F2 populations, confirming the reproducibility in the morphological phenotyping of the M2 plants. To integrate and manage the visible phenotypes of mutants and other associated data, we developed the in silico database TOMATOMA, a relational system interfacing modules between mutant line names and phenotypic categories. TOMATOMA is a freely accessible database, and these mutant recourses are available through the TOMATOMA (http://tomatoma.nbrp.jp/index.jsp).

182 citations

Journal ArticleDOI
TL;DR: Two allelic mutants of SlETR1 (Sletr 1-1 and Sletr1-2) that resulted in reduced ethylene responses were identified, indicating that the Micro-Tom TILLING platform provides a powerful tool for the rapid detection of mutations in an EMS mutant library.
Abstract: To accelerate functional genomic research in tomato, we developed a Micro-Tom TILLING (Targeting Induced Local Lesions In Genomes) platform. DNA pools were constructed from 3,052 ethyl methanesulfonate (EMS) mutant lines treated with 0.5 or 1.0% EMS. The mutation frequency was calculated by screening 10 genes. The 0.5% EMS population had a mild mutation frequency of one mutation per 1,710kb, whereas the 1.0% EMS population had a frequency of one mutation per 737kb, a frequency suitable for producing an allelic series of mutations in the target genes. The overall mutation frequency was one mutation per 1,237kb, which affected an average of three alleles per kilobase screened. To assess whether a Micro-Tom TILLING platform could be used for efficient mutant isolation, six ethylene receptor genes in tomato (SlETR1–SlETR6) were screened. Two allelic mutants of SlETR1 (Sletr1-1 and Sletr1-2) that resulted in reduced ethylene responses were identified, indicating that our Micro-Tom TILLING platform provides a powerful tool for the rapid detection of mutations in an EMS mutant library. This work provides a practical and publicly accessible tool for the study of fruit biology and for obtaining novel genetic material that can be used to improve important agronomic traits in tomato.

160 citations


Cites methods from "Resistant and susceptible responses..."

  • ...Tomato has been widely used for studies of the biotic and abiotic response, such as salinity and wounding stress (Yin et al. 2010a, Sun et al. 2010, Sato et al. 2011) and infection by plant-parasitic nematodes (Bhattarai et al. 2008, Uehara et al. 2010)....

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Journal ArticleDOI
TL;DR: It is demonstrated that priming of tomato defense responses is one of the mechanisms of action of Fo47, which induces a reduced colonization of the root of the tomato plant preinoculated with Fo47.
Abstract: The protective Fusarium oxysporum strain Fo47 is effective in controlling Fusarium wilt in tomato. Previous studies have demonstrated the role of direct antagonism and involvement of induced resistance. The aim of the present study was to investigate whether priming of plant defense responses is a mechanism by which Fo47 controls Fusarium wilt. An in vitro design enabled inoculation of the tap root with Fo47 and the pathogenic strain (Fol8) at different locations and different times. The expression levels of six genes known to be involved in tomato defense responses were quantified using reverse-transcription quantitative polymerase chain reaction (qPCR). Three genes-CHI3, GLUA, and PR-1a-were overexpressed in the root preinoculated with Fo47, and then challenged with Fol8. The genes GLUA and PR-1a were upregulated in cotyledons after inoculation of Fo47. Fungal growth in the root was assessed by qPCR, using specific markers for Fo47 and Fol8. Results showed a reduction of the pathogen growth in the root of the tomato plant preinoculated with Fo47. This study demonstrated that priming of tomato defense responses is one of the mechanisms of action of Fo47, which induces a reduced colonization of the root by the pathogen.

130 citations

Journal ArticleDOI
TL;DR: The data presented in this study show that the repression of host defence SA signalling is associated with the successful development of R KNs, and that SA exogenously added as a soil drench is able to trigger a SAR-like response to RKNs in tomato.
Abstract: Summary The expression pattern of pathogenesis-related genes PR-1, PR-2 and PR-5, considered as markers for salicylic acid (SA)-dependent systemic acquired resistance (SAR), was examined in the roots and shoots of tomato plants pre-treated with SA and subsequently infected with root-knot nematodes (RKNs) (Meloidogyne incognita). PR-1 was up-regulated in both roots and shoots of SA-treated plants, whereas the expression of PR-5 was enhanced only in roots. The over-expression of PR-1 in the whole plant occurred as soon as 1 day after SA treatment. Up-regulation of the PR-1 gene was considered to be the main marker of SAR elicitation. One day after treatment, plants were inoculated with active juveniles (J2s) of M. incognita. The number of J2s that entered the roots and started to develop was significantly lower in SA-treated than in untreated plants at 5 and 15 days after inoculation. The expression pattern of PR-1, PR-2 and PR-5 was also examined in the roots and shoots of susceptible and Mi-1-carrying resistant tomato plants infected by RKNs. Nematode infection produced a down-regulation of PR genes in both roots and shoots of SA-treated and untreated plants, and in roots of Mi-carrying resistant plants. Moreover, in resistant infected plants, PR gene expression, in particular PR-1 gene expression, was highly induced in shoots. Thus, nematode infection was demonstrated to elicit SAR in shoots of resistant plants. The data presented in this study show that the repression of host defence SA signalling is associated with the successful development of RKNs, and that SA exogenously added as a soil drench is able to trigger a SAR-like response to RKNs in tomato.

128 citations


Cites background or methods from "Resistant and susceptible responses..."

  • ...The early necroses caused by CNs may trigger a rapid but MOLECULAR PLANT PATHOLOGY (2014) 15(3 ) , 255–264 © 2013 BSPP AND JOHN WILEY & SONS LTD transient increase in SA and an early activation of SA signalling (Van Kan et al., 1995), which should not occur in Meloidogyne– plant interactions....

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  • ..., 2005), whereas broad and general activation of defence signalling is observed during CN infection (Hamamouch et al., 2011; Uehara et al., 2010; Wubben et al., 2008)....

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  • ...CNs do not form discrete giant cells for their feeding; rather, they induce the breakdown of the cell walls between the initial feeding site and its neighbouring cells, resulting in the development of a multinucleate syncytium (Williamson and Gleason, 2003)....

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  • ...After penetrating the roots, CNs move to the vascular cylinder and pierce cell walls with their stylets, thus disrupting cells, whereas RKNs move intercellularly and do not cause any remarkable tissue damage....

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  • ...Comparably, in Arabidopsis thaliana, pretreatment of plants with SA significantly decreased their susceptibility to CNs, whilst simultaneously inducing PR-1 gene expression in both roots and shoots (Wubben et al., 2008)....

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Book ChapterDOI
16 Aug 2017
TL;DR: The importance of plant-parasitic nematodes in agriculture and the molecular events involved in plant-nematode interactions are highlighted.
Abstract: Plant-parasitic nematodes are costly burdens of crop production. Ubiquitous in nature, phytoparasitic nematodes are associated with nearly every important agricultural crop and represent a significant constraint on global food security. Root-knot nematodes (Meloidogyne spp.) cyst nematodes (Heterodera and Globodera spp.) and lesion nematodes (Pratylenchus spp.) rank at the top of list of the most economically and scientifically important species due to their intricate relationship with the host plants, wide host range, and the level of damage ensued by infection. Limitations on the use of chemical pesticides have brought increasing interest in studies on alternative methods of nematode control. Among these strategies of nonchemical nematode management is the identification and implementation of host resistance. In addition, nematode genes involved in parasitism represent key targets for the development of control through gene silencing methods such as RNA interference. Recently, transcriptome profiling analyses has been used to distinguish nematode resistant and susceptible genotypes and identify the specific molecular components and pathways triggered during the plant immune response to nematode invasion. This summary highlights the importance of plant-parasitic nematodes in agriculture and the molecular events involved in plant-nematode interactions.

105 citations


Cites background from "Resistant and susceptible responses..."

  • ...rostochiensis-infected resistant plants compared with the uninoculated controls [110]....

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References
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Journal ArticleDOI
TL;DR: A system of cluster analysis for genome-wide expression data from DNA microarray hybridization is described that uses standard statistical algorithms to arrange genes according to similarity in pattern of gene expression, finding in the budding yeast Saccharomyces cerevisiae that clustering gene expression data groups together efficiently genes of known similar function.
Abstract: A system of cluster analysis for genome-wide expression data from DNA microarray hybridization is de- scribed that uses standard statistical algorithms to arrange genes according to similarity in pattern of gene expression. The output is displayed graphically, conveying the clustering and the underlying expression data simultaneously in a form intuitive for biologists. We have found in the budding yeast Saccharomyces cerevisiae that clustering gene expression data groups together efficiently genes of known similar function, and we find a similar tendency in human data. Thus patterns seen in genome-wide expression experiments can be inter- preted as indications of the status of cellular processes. Also, coexpression of genes of known function with poorly charac- terized or novel genes may provide a simple means of gaining leads to the functions of many genes for which information is not available currently.

16,371 citations


"Resistant and susceptible responses..." refers methods in this paper

  • ...The normalized microarray data were clustered and visualized with CLUSTER and TREE-VIEW software, respectively (Eisen et al. 1998)....

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Journal ArticleDOI
TL;DR: This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens.
Abstract: It has been suggested that effective defense against biotrophic pathogens is largely due to programmed cell death in the host, and to associated activation of defense responses regulated by the salicylic acid-dependent pathway. In contrast, necrotrophic pathogens benefit from host cell death, so they are not limited by cell death and salicylic acid-dependent defenses, but rather by a different set of defense responses activated by jasmonic acid and ethylene signaling. This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens. While the model above seems generally correct, there are exceptions and additional complexities.

3,721 citations


"Resistant and susceptible responses..." refers background in this paper

  • ...In contrast, JA-dependent resistance appears to be more effective against necrotrophic pathogens and insects (Keeler and Baldwin 2002, Glazebrook 2005)....

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  • ...Defense signaling pathways The SA- and JA-regulated defense pathways are known to be important for both basal and R-gene-mediated resistance to foliar pathogens and insects (Glazebrook, 2005)....

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  • ...6 SA-dependent signaling seems to be crucial for resistance against biotrophic pathogens (Glazebrook 2005, Loake and Grant 2007)....

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  • ...The SA- and JA-regulated defense pathways are known to be important for both basal and R-gene-mediated resistance to foliar pathogens and insects (Glazebrook, 2005)....

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Journal ArticleDOI
TL;DR: Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses.
Abstract: ▪ Abstract Plants respond to herbivore attack with a bewildering array of responses, broadly categorized as direct and indirect defenses, and tolerance. Plant-herbivore interactions are played out on spatial scales that include the cellular responses, well-studied in plant-pathogen interactions, as well as responses that function at whole-plant and community levels. The plant's wound response plays a central role but is frequently altered by insect-specific elicitors, giving plants the potential to optimize their defenses. In this review, we emphasize studies that advance the molecular understanding of elicited direct and indirect defenses and include verifications with insect bioassays. Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses. Such organizational elements could help elucidate the molecular control over the d...

1,423 citations

Journal ArticleDOI
TL;DR: Many disease resistance (R) proteins of plants detect the presence of disease-causing bacteria, viruses, or fungi by recognizing specific pathogen effector molecules that are produced during the infection process.
Abstract: ■ Abstract Many disease resistance (R) proteins of plants detect the presence of disease-causing bacteria, viruses, or fungi by recognizing specific pathogen effector molecules that are produced during the infection process. Effectors are often pathogen proteins that probably evolved to subvert various host processes for promotion of the pathogen life cycle. Five classes of effector-specific R proteins are known, and their sequences suggest roles in both effector recognition and signal transduction. Although some R proteins may act as primary receptors of pathogen effector proteins, most appear to play indirect roles in this process. The functions of various R proteins require phosphorylation, protein degradation, or specific localization within the host cell. Some signaling components are shared by many R gene pathways whereas others appear to be pathway specific. New technologies arising from the genomics and proteomics revolution will greatly expand our ability to investigate the role of R proteins in plant disease resistance.

926 citations


"Resistant and susceptible responses..." refers background in this paper

  • ...All genes, except Hs1, belong to the leucine zipper, nucleotide-binding site, leucine-rich repeat class of plant R genes (Martin et al. 2003)....

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  • ...All genes, except Hs1pro-1, belong to the leucine zipper, nucleotide-binding site, leucine-rich repeat class of plant R genes (Martin et al. 2003)....

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Journal ArticleDOI
TL;DR: It is now clear that gene-for-gene resistance can be mediated through at least three genetically distinguishable pathways.

763 citations


"Resistant and susceptible responses..." refers background in this paper

  • ...(Glazebrook 2001,Hammond-Kosack and Parker 2003, Glazabrook 2005, Kim et al. 2008)....

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