Comparative genome-wide transcriptome analysis of Vitis vinifera responses to adapted and non-adapted strains of two-spotted spider mite, Tetranyhus urticae
- Jose Díaz-Riquelme†1, 2,
- Vladimir Zhurov†1,
- Cristina Rioja1, 2,
- Ignacio Pérez-Moreno3,
- Rafael Torres-Pérez2,
- Jérôme Grimplet2,
- Pablo Carbonell-Bejerano2,
- Sabina Bajda4, 5,
- Thomas Van Leeuwen4, 5,
- José Miguel Martínez-Zapater2,
- Miodrag Grbic1, 2Email author and
- Vojislava Grbic1, 2Email author
© Díaz-Riquelme et al. 2016
Received: 20 August 2015
Accepted: 18 January 2016
Published: 22 January 2016
The two-spotted spider mite, Tetranychus urticae, is an extreme generalist plant pest. Even though mites can feed on many plant species, local mite populations form host races that do not perform equally well on all potential hosts. An acquisition of the ability to evade plant defenses is fundamental for mite’s ability to use a particular plant as a host. Thus, understanding the interactions between the plant and mites with different host adaptation status allows the identification of functional plant defenses and ways mites can evolve to avoid them.
The grapevine genome-wide transcriptional responses to spider mite strains that are non-adapted and adapted to grapevine as a host were examined. Comparative transcriptome analysis of grapevine responses to these mite strains identified the existence of weak responses induced by the feeding of the non-adapted strain. In contrast, strong but ineffective induced defenses were triggered upon feeding of the adapted strain. A comparative meta-analysis of Arabidopsis, tomato and grapevine responses to mite feeding identified a core of 36 highly conserved genes involved in the perception, regulation and metabolism that were commonly induced in all three species by mite herbivory.
This study describes the genome-wide grapevine transcriptional responses to herbivory of mite strains that differ in their ability to use grapevine as a host. It raises hypotheses whose testing will lead to our understanding of grapevine defenses and mite adaptations to them.
KeywordsVitis vinifera Tetranychus urticae Constitutive defense responses Induced defense responses Adaptation Pest Herbivory
Plants have evolved both constitutive and induced defenses to deter herbivory. Constitutive defenses include various physical and chemical barriers that exist even in the absence of herbivore challenge, while induced defenses occur upon herbivore attack and result in the biosynthesis of defense compounds (metabolites and defense proteins) that reduce the performance of the herbivore through toxicity, anti-feeding effects and attraction of natural predators. Induced defenses also lead to changes in physical properties of plant tissues, of particular importance in defenses against pathogens .
The two-spotted spider mite (TSSM), Tetranychus urticae, is a polyphagous pest that feeds on more than 1,100 plant species [2, 3]. The ability of TSSM to feed on such a wide range of plant species implies that it is capable of evading diverse plant defenses. So far, we have characterized responses of Arabidopsis and tomato plants to TSSM feeding [4, 5]. In both cases, TSSM induced a conserved set of genes associated with the biosynthesis of plant hormone jasmonic acid (JA) and its signaling, but a highly divergent set of JA-regulated defense genes. For example, in Arabidopsis, indole glucosinolates were the most prominent defense compounds, while in tomato TSSM induced the expression of genes encoding enzymes predicted to interfere with mite’s ability to effectively digest plant nutrients [4, 5]. The ability of TSSM to avoid diverse plant defense compounds is associated with the expansion of gene families encoding detoxification enzymes and transporters, as well as acquisition of genes from various (micro)organisms through the horizontal gene transfers [6–8]. Even though TSSMs can feed on a wide array of plants, individual TSSM populations do not perform equally well on all potential hosts. Intraspecific variation leading to locally adapted populations has been demonstrated to be one of the mechanisms underlying the evolution of TSSM’s host range [9–12]. Conceptually, spider mite adaptation to a new host can be based on mite’s ability to evade physical/anatomical barriers to its feeding, or in the case of defenses that rely on plant defense compounds, to detoxify them or to attenuate their synthesis. Even though mite adaptation to a particular plant host is important for the understanding of its polyphagous nature, mechanisms of adaptation and molecular patterns of herbivore and/or host associated with mite adaptation have been described in only few instances. For example, T. lintearius, a specialist on gorse (Ulex europaeus) evades host constitutive defenses by adapting its feeding behavior. Gorse has a thick cuticle that hinders mite stylet penetration, however, T. linearius bypasses this barrier by inserting its stylet into the leaf mesophyll through the stomatal aperture . In addition, it has been shown that TSSMs can adapt to beans that constitutively synthesize cyanogenic glucosides by acquiring an ability to detoxify them through the overexpression of a member of the cysteine synthase family . Furthermore, plant and mite responses indicating involvement of both detoxification and attenuation of induced plant defenses have been described for mite adaptation to cultivated tomato, a plant host that relies on induced defenses to deter mite herbivory [4, 10, 12, 14]. The extent of chemical versus physical constitutive defenses across mite potential hosts is not known, nor is it clear if detoxification, rather than attenuation of metabolite biosynthesis, is a prevailing pattern of mite adaptation to hosts that rely on induced accumulation of defense metabolites to deter herbivory, and if the reverse is true in cases of mite adaptations to host proteaceous defense compounds (e.g., protease inhibitors). Therefore, description of multitude of plant interactions with adapted and non-adapted mite strains is required to gain insights into functional plant defenses and the ways mites can evolve to evade them.
Grapevine is a model plant for fruit-bearing perennial crops with established genomic resources . Several genome-wide studies of transcriptional changes over developmental and fruit maturation stages, as well as responses to abiotic stresses and fungal pathogens have been reported recently [16–21]. Grapevine responses to the specialist gall-forming aphid-like parasite phylloxera, Daktulosphaira vitifoliae, have been recently described , however, studies of grapevine responses to generalist herbivores are so far lacking. Here, we describe genome-wide grapevine transcriptional responses to herbivory of adapted and non-adapted spider mite strains in order to begin an understanding of the mechanism of TSSM adaptation to grapevine.
Dispersal behavior and leaf damage analysis of London and Murcia TSSM strains on grapevine
In this study we used two strains of TSSM: a) the reference London strain that was originally collected from apple trees; it has been propagated on bean plants for the last ten years ; and b) the Murcia strain that was collected from a heavily infested vineyard in the region of Murcia, Spain; this strain was subsequently maintained on grapevine plants for more than two years. We developed and used inbred lines of both strains to minimize genetic variability of field-collected Murcia strain. In addition, to eliminate the physiological effects of plant hosts (bean versus grapevine), both strains were reared for two generations on a common host prior to their experimental application. As London strain was not able to survive on grapevine, we used beans to rear London and Murcia mites for two generations. To establish the relationship between these mite strains and grapevine as a host, we determined their dispersal patterns and leaf damage they caused upon feeding.
The most common symptom of TSSM feeding is the formation of chlorotic spots on the host plant leaves [4, 5]. However, mite herbivory on grapevine does not result in the formation of macroscopic chlorotic spots. Rather, mite feeding induces an accumulation of red/brown spots that is referred to as leaf bronzing . Short-term symptoms of mite feeding (24 h) can be seen as individual brown spots, but longer-term, leaves turn red, desiccate and finally abscise, Fig. 1b, c. Thus, to measure the intensity of mite feeding we determined the area of brown spots that formed on leaves infested with 50 female mites of London or Murcia strains upon 24 h of herbivory. Leaves inoculated with Murcia mites developed significantly greater area of brown spots relative to London mites (220 vs. 29 mm2 respectively, Fig. 1d). Individual spots induced by London or Murcia mites were similar in appearance (data not shown), indicating that Murcia mites feed more than London strain. Ability of the Murcia mite strain to successfully develop on grapevine, to display significantly higher retention and to feed intensively even when maintained on beans for two generation, indicates that this strain has intrinsic ability to reduce/eliminate restrictions imposed by the grapevine as a host. We consider this strain adapted to grapevine. In contrast, London strain is non-adapted to grapevine, as it cannot establish its population, tends to disperse and has limited feeding on grapevine.
Induced grapevine responses to feeding of London and Murcia spider mite strains
Grapevine responses to feeding of non-adapted London mite strain
London mites induced marginal grapevine responses and clustered with untreated control state. However, the PCA analysis identified these responses as distinct. Thus, we further analyzed grapevine responses to non-adapted mites in search for induced responses that could explain plant resistance. We first looked at a set of 50 genes that were differentially expressed only upon feeding of London non-adapted mites, Fig. 2 and Additional file 4. Eighteen of these genes were down-regulated, including genes homologous to Arabidopsis NINE-CIS-EPOXYCAROTENOID DIOXYGENASE 3 (NCED3) and ABA INSENSITIVE 1 (ABI1) that are involved in ABA biosynthesis and signal transduction, as well as two genes encoding disease resistance proteins that may be involved in innate immune responses. Of thirty-two up-regulated genes, two are associated with thiamine biosynthesis process and additional two with UDP-glucose transport. Several other transcripts encoding signaling proteins (Ca2+ binding, tetratricopeptide repeat (TPR)-containing) were also differentially expressed. Some of these transcripts were also detected in response to abiotic stresses . However, differential expression of this set of 50 genes did not affect global changes in the expression of defense-related genes, thus, they unlikely impacted the grapevine defenses against the herbivory of the non-adapted London mites.
Grapevine responses to feeding of adapted Murcia mite strain
Despite the induction of the robust grapevine defense responses, successful establishment of Murcia mite population on grapevine indicates that these responses are ineffective to substantially limit their fitness. To gain further insights into Murcia-induced responses, we compared them with grapevine responses to methyl-jasmonate (MeJA) and cyclodextrins (CD) . Application of MeJA mimics naturally occurring increase in JA concentrations induced by TSSM herbivory  and CD triggers signal transduction cascade that results in the induction of genes involved in the stilbene synthesis and downregulation of programs associated with cell growth and division, also observed in response to TSSM feeding, Fig. 3. A total of 1,292 genes, clustered in 5 groups, demonstrated a high degree of variability across treatments, Fig. 5c and Additional file 8. Genes in cluster 1 were down-regulated only in response to mite treatments. These genes are associated with photosynthesis, a process that is altered in cultured cells used for the application of MeJA and CD, thus, the difference in the expression of these genes likely results from the nature of samples used. Clusters 2, 3 and 4 contain genes that are associated with various defense-related processes: genes in cluster 2 have a tendency toward down-regulation in response to MeJA and CD, but up-regulation in response to mites, while genes in clusters 3 and 4 are up-regulated by either spider mite feeding (cluster 3) or more prominently by MeJA and CD (cluster 4), indicating that while MeJA/CD and mites trigger similar differential expression of many common genes, there are also gene sets that are differentially regulated by these treatments. Finally, cell division and growth are commonly down-regulated across treatments, but MeJA and CD seem to affect greater number of these genes that are grouped in cluster 5. Thus, meta-analysis identified differences in the gene expression triggered by MeJA/CD and mite herbivory. However, none of the clusters displayed the expression pattern expected for the suppression of grapevine defenses by adapted mites. Responses induced by the London- and the Murcia-mites had similar trends and clustered together, indicating that differences between treatments resulted either from differences in samples used or were reflection of differential contribution of MeJA/CD and mite herbivory to the commonly affected processes.
Core plant responses induced by spider mites
Grapevine shows a host-resistance toward the non-adapted London strain. Efficient grapevine defenses are reflected in mite dispersal and limited feeding that is associated with the induction of weak host transcriptional responses. On the opposite end of the adaptation spectrum, Murcia mites are retained on grapevine leaves, they feed intensively and trigger prominent plant responses. Grapevine responses induced by these strains are similar in identity, but differ in levels that are proportional to damage inflicted, Figs. 1, 2, 3 and 4. Induced grapevine responses are characterized by the down-regulation of photosynthesis, cell division and growth, and an up-regulation of genes involved in biosynthesis, signaling and responses to JA, ET and SA, that were also observed in Arabidopsis and tomato responses to mite feeding [4, 5, 12]. Despite the conservation of these programs across three species, the majority of DEGs and defense compounds synthesized are species specific and reflect differences in secondary metabolism between these plants. While Arabidopsis defenses against spider mite herbivory rely on indole glucosinolates , tomato defenses are mostly based on the anti-digestive proteins such as proteinase inhibitors (PI), leucine amino peptidase (LAP), threonine deaminase (TD), and polyphenol oxidases (PPO) . The grapevine transcriptional responses to mite herbivory capture both anti-digestive proteins and defensive metabolites. For example, induced expression of PIs and PPOs in response to mite feeding is common between tomato and grapevine, but not in Arabidopsis where they are either lacking in the genome (PPOs)  or were not recruited for defense (PIs) . PIs were shown to be effective in restricting mite herbivory [45, 46], however, PPOs are likely ineffective in the mite’s acidic gut . In addition, the major metabolic output of grapevine-induced defenses is the production of stilbenes, phenylpropanoid metabolites derived from phenylalanine . Even though genes encoding phenylpropanoid biosynthetic enzymes are induced upon mite herbivory in all three species, stilbene synthase (STS) that allows the synthesis of stilbenes is only present in the grapevine genome, being absent in both tomato and Arabidopsis . Antifungal and antimicrobial activities of stilbenes are well characterized [49–51], however, their role in defense against herbivores is not clear. A spruce bark beetle, Ips typographus, associates with fungus Ceratocystis polonica in order to feed on Norway spruce, a plant species that also accumulates defensive stilbenes. The fungus is capable of degrading stilbenes , making it plausible that its detoxification may also benefit bark beetles. Stilbenes may be part of the functional output of grapevine defenses against spider mites, a hypothesis that should be tested by using the Arabidopsis or tomato transgenic plants that constitutively express heterologous STS genes and synthesize stilbenes [53, 54].
The prominence of grapevine induced transcriptional responses correlated with the feeding intensity, Figs. 1 and 2. This is an opposite pattern to one observed for tomato responses to feeding of tomato-adapted and non-adapted TSSMs . In this particular case, the non-adapted mites triggered robust responses expected to be efficient in restricting mite feeding, and tomato-adapted mites induced similar but attenuated transcriptional changes. Suppression of plant defenses by herbivores has been described in several cases and is mediated through secretion of salivary effectors at the feeding site where they interfere with plant responses [14, 55–60]. Reprograming of grapevine development, defenses and metabolism has been documented in the case of phylloxera (Daktulosphaira vitifoliae), a grapevine specialist and leaf-galling herbivore that induces ectopic formation of stomata and alters source-sink metabolism at the feeding site . We examined a possibility that Murcia-adapted mites manipulate grapevine responses by performing a meta-analysis that compared responses triggered by MeJA/CD and mite herbivory, but did not identify expression patterns expected for the suppression of grapevine responses by adapted mites, Fig. 5. In the absence of characterized effective grapevine defenses against spider mites, the functionality of Murcia-induced responses remains elusive. If Murcia-induced responses are effective to restrict herbivory of non-adapted mites, as suggested by its similarity to the effective Arabidopsis and tomato defenses, then Murcia strain evolved the ability to overcome them. It has been shown that mites can evolve resistance to pesticides or new hosts through reprograming of their xenobiotic metabolism within 10–30 generations [12, 61, 62], making it plausible that detoxification of grapevine defense compounds underlies adaptation of Murcia mites to grapevine. In this case, it is unclear if dampened grapevine responses triggered by London strain (Figs. 2, 3 and 4) are able to restrict its herbivory, or grapevine-resistance to London mites relies on potent constitutive defenses. The nature and the identity of potential constitutive defenses in grapevine are unknown, however, cuticle, trichomes and metabolites such as acylsugars, methyl ketones, terpenoids and cyanogenic glucosides cause mite mortality or deter mites from feeding on gorse, wild tomato relatives and beans [8, 13, 63–70].
Comparison of spider mite-induced responses between grapevine, tomato and Arabidopsis identified a core of 36 one-to-one orthologous genes, Fig. 6. Consistent with the conserved role of JA in regulating defenses against mite herbivory [4, 5], JA biosynthetic and signaling genes are included in this data set. In addition, orthologs of SOBIR1 and LYK4 receptors, previously identified in Arabidopsis and tomato responses to mite feeding  are also present in the grapevine data set. In Arabidopsis, LYK4 facilitates the recognition of chitin-related ligands by LYK5 . LYK5 is induced by mite feeding in Arabidopsis, however, its tomato and grapevine orthologs were not [4, 5]. In rice, chitin perception is mediated by the chitin-elicitor binding protein (CEBiP) [71–73], which contains an extracellular LysM motif and a transmembrane domain, but lacks an intracellular kinase domain. Thus, there is a possibility that some other plasma membrane-associated LysM motif-containing proteins contribute to chitin perception in tomato and grapevine. Chitin is the main component of the exoskeleton and gut lining in arthropods . A conceivable elicitation of plant responses by mite-originating chitin is potentiated by the induction of chitinases upon mite feeding in all three plant species. Chitinases are glycosyl hydrolases required for the chitin breakdown and the production of chitin oligomers that act as ligands. Chitinases are used by arthropod pathogens to hydrolyze exoskeletal chitin, to aid in penetration of their hosts (e.g. Beauveria bassiana that is also a pathogen of T. urticae [75, 76]). In addition, chitinases administered through an artificial diet that target chitin in the arthropode gut, were shown to affect growth and development of a wide range of pests [77, 78]. Significantly, plant chitinases require an acidic environment for their activity . In contrast to the alkaline pH of Lepidopteran guts, the mite gut is acidic . Therefore, plants may be able to generate and recognize mite-associated chitin oligomers, a possibility that should be challenged in the future.
This study describes genome-wide grapevine transcriptional changes triggered by the grapevine-adapted and the non-adapted spider mite strains. The adapted mites induced robust plant responses that captured biological processes previously associated with effective defenses against mite feeding in Arabidopsis and tomato. However, it remained elusive if pronounced grapevine transcriptional reprograming in response to the adaptive strain merely associates with the greater tissue damage or it establishes defense that adapted mites can detoxify. In contrast, the non-adapted mites induced similar grapevine responses but of lower magnitude that clustered with untreated control. Association of host-resistance that efficiently restricts the performance of non-adapted mites with responses that are limited both in numbers of DEGs and the amplitude of their induction, raises a possibility that constitutive responses may present a barrier to feeding of the non-adapted spider mites. Resolution of the effectiveness of grapevine responses to mite feeding and the corresponding adaptation mechanism(s) evolved by Murcia mites to override feeding restrictions necessitates the identification of additional independent patterns of grapevine responses to both adapted and non-adapted mite strains in future.
Comparison of the spider mite responses induced in grapevine, Arabidopsis and tomato identified the conserved core of 36 orthologous genes that were differentially expressed in all three species. Consistent with the established conserved role of JA in regulation of plant responses to herbivory, the core group includes genes involved in JA biosynthesis and signaling. In addition, core also included orthologous receptors associated with chitin perception, raising a possibility that plants recognize mite-associated chitin oligomers.
Tetranychus urticae strain selection
Murcia strain was collected from heavily infested vineyard of Vitis vinifera L. cv. ‘Crimson Seedless’ in Alhama de Murcia (Región de Murcia, Spain). The taxonomic status of the Murcia TSSM strain has been confirmed through the shape of male aedeagus . Inbred lines were developed for both London and Murcia strains from isofemale lines that underwent eight and seven consecutive generations of mother-son matings respectively. Murcia mites were mass reared in the laboratory on potted Vitis vinifera L. cv. ‘Tempranillo’, while London mites were reared on bean plants (Phaseolus vulgaris ‘California Red Kidney’; Stokes) in growth chambers at 25 °C ± 1 °C with a 16:8 h (light/dark) photoperiod. To eliminate the effect of rearing plant hosts on physiological state of mites, both Murcia and London mites were kept for two generations on bean leaves prior to transferring them to the experimental grapevine plants.
Preparation of grapevine plantlets
A protocol for production of healthy and physiologically uniform grapevine plantlets has been developed and is described in Additional file 1 [81, 82]. Dormant grapevine cuttings (cv. Tempranillo) have been collected from the field-grown vines in Logrono, La Rioja, in December of 2013 and were kept at 4 °C until the propagation.
A single leaf on a plant with 1–2 leaves was isolated with wet cotton and lanolin barrier 24 h ahead of the experiment and was inoculated with 50 female mites of either Murcia (reared for two generations on bean) or London TSSM strain. Untreated plants were used as a control. After feeding for 24 h, leaves were cut and scanned with transmitted light using an Epson Scan V370 Photo with film adapter (Epson, Suwa, Japan) using following settings: document type—film; type of film—positive color; resolution—1200 dpi. Leaf images were processed using the Gimp software v2.6 (http://www.gimp.org/) that allowed selection and quantification of all the brownish spots that were associated with mite feeding. Signal that was considered as damage was negligible on untreated leaves. Leaf damage data was analyzed using factorial ANOVA to assess significance of the mite strain and experimental block effects. ANOVA was followed by Tukey’s Honestly Significant Difference test.
A single leaf on a plant with 1–2 leaves was inoculated with 50 female mites of either Murcia (reared for two generations on bean) or London TSSM strain. Number of mites retained on the inoculated leaf after 24 h was determined. Proportion of mites retained was arcsine transformed and factorial ANOVA was used to assess significance of the mite strain and experimental block effects. ANOVA was followed by Tukey’s Honestly Significant Difference test.
Preparation of samples for transcriptome analysis
Plants with developed first two leaves were grown under 100 to 150 μmol m−2 s−1 cool-white fluorescent light at 26 °C with a 16 h/8 h (light/dark) photoperiod in controlled growth chambers. Petioles of experimental leaves were surrounded with wet cotton and lanolin to confine mites on the inoculated leaves. The barrier was placed 24 h ahead of mite inoculation and on all experimental plants in order to unify potential effects of this plant manipulation. 50 adult female spider mites of either Murcia or London strain were applied per plant and allowed to feed for 24 h. Untreated plants were used as control. Four biological replicates containing leaves from two plants were generated per treatment. Treated leaves were collected, frozen in liquid nitrogen and kept at −80 °C until they were used for RNA extraction. Total RNA was extracted from frozen tissues using the Spectrum Plant Total RNA Kit (Sigma-Aldrich) and performing on-column DNase I digestion according to manufacturer’s protocol to avoid DNA contamination.
RNA-Seq analysis of grapevine responses to spider mite feeding
RNA samples were processed to construct strand-specific cDNA libraries (one per biological sample) using Illumina TruSeq RNA Library Preparation Kit (Illumina, San Diego, CA). Sequencing of all 12 libraries was conducted on a single sequencing lane using Illumina HiSeq 2000 platform (Illumina, San Diego, CA) to produce 4.2–5.2 million strand-specific 100 bp paired-end reads per library. Reads were mapped to the reference (12X) grapevine genome using STAR aligner  allowing only for unique mapping and up to two mismatches per read mapped, using v.2.1 gene prediction provided by CRIBI Biotechnology Center, University of Padua. Read counts were generated using HTSeq at the level of gene locus . Analysis of differential gene expression was performed using voom/limma workflow for genes that demonstrated expression level of at least 1 count per million (CPM) in at least 4 samples .
Gene set analysis
Gene set analysis (GSA) was performed using a custom version of Bioconductor package piano . Log2 FC, p- and t-values obtained using limma/voom were used as the input gene level statistics for analysis utilizing the PAGE algorithm . Biological Process Gene Ontology annotation was used to classify genes into sets. We used a combination of automated Blast2GO annotation provided by CRIBI Biotechnology Center, University of Padua and V1 curated annotation  to identify biological processes enriched in DEGs, see Additional file 10 for final GO annotation file.
Gene ontology analysis
GO analysis was performed using topGO with Fisher’s test statistic and “weight01” algorithm  to generate a list of top 50 Biological Process GO annotations and annotate lists of genes that were detected as differentially expressed. The lists were further filtered by applying a cut-off of 0.05 to Fisher’s weighted p-values.
Comparison of grapevine responses to spider mite feeding and those induced by the application of JA and/or elicitors
CEL files for grapevine induced JA response  were retrieved from PLEXdb (accession vv44) . Expression measures were computed using RMA  and Log2 fold changes for all genes and for all relevant contrasts were calculated using limma . Correspondence between Affymetrix probe ID and current grapevine genome annotation was established according to Grimplet et al., 2012 . To retain genes that were informative for the inference of relatedness between effects of JA and elicitors and spider mite herbivory we have selected a sample standard deviation cut-off of Log2 fold change across compared experiments and contrasts equal to 1. We retained a data matrix of 1,292 genes (Additional file 8) and their respective Log2 fold changes across experiments for subsequent study comparison.
Establishment of bidirectional best hit orthologs between grapevine, tomato and Arabidopsis
To determine one-to-one orthologs using the bidirectional best hit (BBH) approach , reciprocal blastp  searches were conducted using v.2.1 release of grapevine provided by CRIBI Biotechnology Center, ITAG v.2.3 release of tomato and TAIR10 release of Arabidopsis protein sequences with cut-off of E < 10−4. Output files were further processed to retain BBH trios, listed in Additional file 9.
Availability of supporting data
The transcriptome data set supporting the results of this article is available through the Sequence Read Archive (SRA) accession SRP067967. In addition, the data sets supporting the results of this article, as well as Additional Method, are included as additional files.
We would like to thank Dr. Richard Clark for critical reading of the manuscript. This Project was funded by the Government of Canada through Genome Canada and the Ontario Genomics Institute (OGI-046, to MG and VG) and Ontario Research Fund–Global Leadership in Genomics and Life Sciences (GL2-01-035, to MG and VG), the Spanish Ministry of Science and Innovation (AGL2011-24584, to IPM), the Spanish MINECO grant BIO2011-026229 to JMZ. JG was a recipient of a Contract Ramon y Cajal from Spanish MINECO (RYC-2011-07791). SB was partially supported by the Fund for Scientific Research Flanders, grant G.0093.12 N to TVL.
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- Kessler A, Baldwin IT. Plant responses to insect herbivory: The emerging molecular analysis. Annu Rev Plant Biol. 2002;53:299–328.View ArticlePubMedGoogle Scholar
- Jeppson LR, Keifer HH, Baker EW. Mites injurious to economic plants. Berkeley: London: University of California Press; 1975.Google Scholar
- Spider Mites Web: a comprehensive database for the Tetranychidae. [http://www.montpellier.inra.fr/CBGP/spmweb]
- Martel C, Zhurov V, Navarro M, Martinez M, Cazaux M, Auger P, et al. Tomato Whole Genome Transcriptional Response to Tetranychus urticae Identifies Divergence of Spider Mite-Induced Responses Between Tomato and Arabidopsis. Mol Plant Microbe Interact. 2015;28(3):343–61.View ArticlePubMedGoogle Scholar
- Zhurov V, Navarro M, Bruinsma KA, Arbona V, Santamaria ME, Cazaux M, et al. Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite. Plant Physiol. 2014;164(1):384–99.PubMed CentralView ArticlePubMedGoogle Scholar
- Grbic M, Van Leeuwen T, Clark RM, Rombauts S, Rouze P, Grbic V, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479(7374):487–92.View ArticlePubMedGoogle Scholar
- Dermauw W, Osborne EJ, Clark RM, Grbic M, Tirry L, Van Leeuwen T. A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics. 2013;14:317.PubMed CentralView ArticlePubMedGoogle Scholar
- Wybouw N, Dermauw W, Tirry L, Stevens C, Grbic M, Feyereisen R, et al. A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. eLife. 2014;3:e02365.PubMed CentralView ArticlePubMedGoogle Scholar
- Agrawal AA, Vala F, Sabelis MW. Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: adaptive plasticity? Am Nat. 2002;159(5):553–65.View ArticlePubMedGoogle Scholar
- Kant MR, Sabelis MW, Haring MA, Schuurink RC. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. P R Soc B. 2008;275(1633):443–52.View ArticleGoogle Scholar
- Barrett LG, Heil M. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 2012;17(5):282–92.View ArticlePubMedGoogle Scholar
- Wybouw N, Zhurov V, Martel C, Bruinsma KA, Hendrickx F, Grbić V, et al. Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host. Mol Ecol. 2015.Google Scholar
- Marriott J, Florentine S, Raman A. Effects of Tetranychus lintearius (Acari: Tetranychidae) on the structure and water potential in the foliage of the invasive Ulex europaeus (Fabaceae) in Australia. Int J Acarol. 2013;39(4):275–84.View ArticleGoogle Scholar
- Alba JM, Schimmel BC, Glas JJ, Ataide LM, Pappas ML, Villarroel CA, et al. Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol. 2014;205(2):828–40.PubMed CentralView ArticlePubMedGoogle Scholar
- Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449(7161):463–7.View ArticlePubMedGoogle Scholar
- Almagro L, Carbonell-Bejerano P, Belchi-Navarro S, Bru R, Martinez-Zapater JM, Lijavetzky D, et al. Dissecting the Transcriptional Response to Elicitors in Vitis vinifera Cells. PloS one. 2014;9(10):e109777.Google Scholar
- Lijavetzky D, Carbonell-Bejerano P, Grimplet J, Bravo G, Flores P, Fenoll J, et al. Berry Flesh and Skin Ripening Features in Vitis vinifera as Assessed by Transcriptional Profiling. PloS one. 2012;7(6):e39547.Google Scholar
- Albertazzi G, Milc J, Caffagni A, Francia E, Roncaglia E, Ferrari F, et al. Gene expression in grapevine cultivars in response to Bois Noir phytoplasma infection. Plant Sci. 2009;176(6):792–804.View ArticleGoogle Scholar
- Fung RW, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, et al. Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol. 2008;146(1):236–49.PubMed CentralView ArticlePubMedGoogle Scholar
- Rocheta M, Becker JD, Coito JL, Carvalho L, Amancio S. Heat and water stress induce unique transcriptional signatures of heat-shock proteins and transcription factors in grapevine. Funct Integr Genomic. 2014;14(1):135–48.View ArticleGoogle Scholar
- Agudelo-Romero P, Erban A, Rego C, Carbonell-Bejerano P, Nascimento T, Sousa L, et al. Transcriptome and metabolome reprogramming in Vitis vinifera cv. Trincadeira berries upon infection with Botrytis cinerea. J Exp Bot. 2015;66(7):1769–85.View ArticlePubMedGoogle Scholar
- Nabity PD, Haus MJ, Berenbaum MR, DeLucia EH. Leaf-galling phylloxera on grapes reprograms host metabolism and morphology. Proc Natl Acad Sci U S A. 2013;110(41):16663–8.PubMed CentralView ArticlePubMedGoogle Scholar
- Hussey NW, Parr WJ. Dispersal of the glasshouse red spider mitetetranychus urticaekoch (acarina, tetranychidae). Entomol Exp Appl. 1963;6(3):207–14.View ArticleGoogle Scholar
- Margolies DC, Kennedy GG. Movement of the 2-Spotted Spider-Mite, Tetranychus-Urticae, among Hosts in a Corn-Peanut Agroecosystem. Entomol Exp Appl. 1985;37(1):55–61.View ArticleGoogle Scholar
- van den Boom CEM, van Beek TA, Dicke M. Differences among plant species in acceptance by the spider mite Tetranychus urticae Koch. J Appl Entomol. 2003;127(3):177–83.View ArticleGoogle Scholar
- Helle W, Sabelis MW. Spider mites: Their biology, natural enemies and control. Amsterdam: New York: Elsevier Science Publishers; 1985Google Scholar
- Carbonell-Bejerano P, Santa Maria E, Torres-Perez R, Royo C, Lijavetzky D, Bravo G, et al. Thermotolerance responses in ripening berries of Vitis vinifera L. cv Muscat Hamburg. Plant Cell Physiol. 2013;54(7):1200–16.View ArticlePubMedGoogle Scholar
- Rudus I, Terai H, Shimizu T, Kojima H, Hattori K, Nishimori Y, et al. Wound-induced expression of DEFECTIVE IN ANTHER DEHISCENCE1 and DAD1-like lipase genes is mediated by both CORONATINE INSENSITIVE1-dependent and independent pathways in Arabidopsis thaliana. Plant Cell Rep. 2014;33(6):849–60.View ArticlePubMedGoogle Scholar
- Pauwels L, Goossens A. Fine-tuning of early events in the jasmonate response. Plant Signal Behav. 2008;3(10):846–7.PubMed CentralView ArticlePubMedGoogle Scholar
- Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W, et al. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci U S A. 2008;105(4):1380–5.PubMed CentralView ArticlePubMedGoogle Scholar
- Herde M, Gartner K, Kollner TG, Fode B, Boland W, Gershenzon J, et al. Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell. 2008;20(4):1152–68.PubMed CentralView ArticlePubMedGoogle Scholar
- Piofczyk T, Jeena G, Pecinka A. Arabidopsis thaliana natural variation reveals connections between UV radiation stress and plant pathogen-like defense responses. Plant Physiol Bioch. 2015;93:34–43.View ArticleGoogle Scholar
- Wan JR, Tanaka K, Zhang XC, Son GH, Brechenmacher L, Tran HNN, et al. LYK4, a Lysin Motif Receptor-Like Kinase, Is Important for Chitin Signaling and Plant Innate Immunity in Arabidopsis. Plant Physiol. 2012;160(1):396–406.PubMed CentralView ArticlePubMedGoogle Scholar
- Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JH, America AH, et al. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci U S A. 2013;110(24):10010–5.PubMed CentralView ArticlePubMedGoogle Scholar
- Liebrand TWH, van den Burg HA, Joosten MHAJ. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 2014;19(2):123–32.View ArticlePubMedGoogle Scholar
- Joshi V, Jander G. Arabidopsis Methionine gamma-Lyase Is Regulated According to Isoleucine Biosynthesis Needs But Plays a Subordinate Role to Threonine Deaminase. Plant Physiol. 2009;151(1):367–78.PubMed CentralView ArticlePubMedGoogle Scholar
- Rébeillé F, Jabrin S, Bligny R, Loizeau K, Gambonnet B, Van Wilder V, et al. Methionine catabolism in Arabidopsis cells is initiated by a γ-cleavage process and leads to S-methylcysteine and isoleucine syntheses. Proc Natl Acad Sci. 2006;103(42):15687–92.PubMed CentralView ArticlePubMedGoogle Scholar
- Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ. The phenylpropanoid pathway and plant defence - a genomics perspective. Mol Plant Pathol. 2002;3(5):371–90.View ArticlePubMedGoogle Scholar
- Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH. Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ. 2010;33(10):1597–613.View ArticlePubMedGoogle Scholar
- Pajerowska-Mukhtar KM, Wang W, Tada Y, Oka N, Tucker CL, Fonseca JP, et al. The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition. Curr Biol. 2012;22(2):103–12.PubMed CentralView ArticlePubMedGoogle Scholar
- Gross W, Lenze D, Nowitzki U, Weiske J, Schnarrenberger C. Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. Gene. 1999;230(1):7–14.View ArticlePubMedGoogle Scholar
- Roxrud I, Lid SE, Fletcher JC, Schmidt ED, Opsahl-Sorteberg HG. GASA4, one of the 14-member Arabidopsis GASA family of small polypeptides, regulates flowering and seed development. Plant Cell Physiol. 2007;48(3):471–83.View ArticlePubMedGoogle Scholar
- Lin PC, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, et al. The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J. 2011;65(2):253–68.View ArticlePubMedGoogle Scholar
- Tran LT, Taylor JS, Constabel CP. The polyphenol oxidase gene family in land plants: Lineage-specific duplication and expansion. BMC Genomics. 2012;13:395.PubMed CentralView ArticlePubMedGoogle Scholar
- Santamaria ME, Martinez ICM, Pozancos C, Gonzalez-Melendi P, Grbic V, Castanera P, et al. Gene Pyramiding of Peptidase Inhibitors Enhances Plant Resistance to the Spider Mite Tetranychus urticae. PloS one 2012, 7(8):e43011.Google Scholar
- Santamaria ME, Arnaiz A, Diaz-Mendoza M, Martinez M, Diaz I. Inhibitory properties of cysteine protease pro-peptides from barley confer resistance to spider mite feeding. PLoS One. 2015;10(6):e0128323.PubMed CentralView ArticlePubMedGoogle Scholar
- Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA. Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol. 2007;143(4):1954–67.PubMed CentralView ArticlePubMedGoogle Scholar
- Vannozzi A, Dry IB, Fasoli M, Zenoni S, Lucchin M. Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biol. 2012;12:130.Google Scholar
- Pezet R, Gindro K, Viret O, Richter H. Effects of resveratrol, viniferins and pterostilbene on Plasmopara viticola zoospore mobility and disease development. Vitis. 2004;43(3):145–8.Google Scholar
- Bru R, Selles S, Casado-Vela J, Belchi-Navarro S, Pedreno MA. Modified cyclodextrins are chemically defined glucan inducers of defense responses in grapevine cell cultures. J Agric Food Chem. 2006;54(1):65–71.View ArticlePubMedGoogle Scholar
- Adrian M, Jeandet P. Effects of resveratrol on the ultrastructure of Botrytis cinerea conidia and biological significance in plant/pathogen interactions. Fitoterapia. 2012;83(8):1345–50.View ArticlePubMedGoogle Scholar
- Hammerbacher A, Schmidt A, Wadke N, Wright LP, Schneider B, Bohlmann J, et al. A Common Fungal Associate of the Spruce Bark Beetle Metabolizes the Stilbene Defenses of Norway Spruce. Plant Physiol. 2013;162(3):1324–36.PubMed CentralView ArticlePubMedGoogle Scholar
- D'Introno A, Paradiso A, Scoditti E, D'Amico L, De Paolis A, Carluccio MA, et al. Antioxidant and anti-inflammatory properties of tomato fruits synthesizing different amounts of stilbenes. Plant Biotechnol J. 2009;7(5):422–9.View ArticlePubMedGoogle Scholar
- Rimando AM, Pan ZQ, Polashock JJ, Dayan FE, Mizuno CS, Snook ME, et al. In planta production of the highly potent resveratrol analogue pterostilbene via stilbene synthase and O-methyltransferase co-expression. Plant Biotechnol J. 2012;10(3):269–83.View ArticlePubMedGoogle Scholar
- Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet 2010, 6(21124944):e1001216.Google Scholar
- Hogenhout SA, Bos JI. Effector proteins that modulate plant--insect interactions. Curr Opin Plant Biol. 2011;14(4):422–8.View ArticlePubMedGoogle Scholar
- Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, et al. Herbivory: caterpillar saliva beats plant defences. Nature. 2002;416(6881):599–600.View ArticlePubMedGoogle Scholar
- Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen MS, et al. A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci U S A. 2008;105(29):9965–9.PubMed CentralView ArticlePubMedGoogle Scholar
- Elzinga DA, Jander G. The role of protein effectors in plant-aphid interactions. Curr Opin Plant Biol. 2013;16(4):451–6.View ArticlePubMedGoogle Scholar
- Zhao C, Escalante LN, Chen H, Benatti TR, Qu J, Chellapilla S, et al. A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Curr Biol. 2015;25(5):613–20.View ArticlePubMedGoogle Scholar
- Fry JD. Trade-Offs in Fitness on Different Hosts: Evidence from a Selection Experiment with a Phytophagous Mite. Am Nat. 1990;136(5):569–80.View ArticleGoogle Scholar
- Magalhaes S, Fayard J, Janssen A, Carbonell D, Olivieri I. Adaptation in a spider mite population after long-term evolution on a single host plant. J Evol Biol. 2007;20(5):2016–27.View ArticlePubMedGoogle Scholar
- Glas JJ, Schimmel BC, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci. 2012;13(12):17077–103.PubMed CentralView ArticlePubMedGoogle Scholar
- Blauth SL, Churchill GA, Mutschler MA. Identification of quantitative trait loci associated with acylsugar accumulation using intraspecific populations of the wild tomato, Lycopersicon pennellii. Theor Appl Genet. 1998;96(3–4):458–67.View ArticlePubMedGoogle Scholar
- Mirnezhad M, Romero-Gonzalez RR, Leiss KA, Choi YH, Verpoorte R, Klinkhamer PG. Metabolomic analysis of host plant resistance to thrips in wild and cultivated tomatoes. Phytochem Anal. 2010;21(1):110–7.View ArticlePubMedGoogle Scholar
- Mutschler MA, Doerge RW, Liu SC, Kuai JP, Liedl BE, Shapiro JA. QTL analysis of pest resistance in the wild tomato Lycopersicon pennellii: QTLs controlling acylsugar level and composition. Theor Appl Genet. 1996;92(6):709–18.View ArticlePubMedGoogle Scholar
- Resende JT, Maluf WR, Cardoso M, Nelson DL, Faria MV. Inheritance of acylsugar contents in tomatoes derived from an interspecific cross with the wild tomato Lycopersicon pennellii and their effect on spider mite repellence. Genet Mol Res. 2002;1(2):106–16.PubMedGoogle Scholar
- Salinas M, Capel C, Alba JM, Mora B, Cuartero J, Fernandez-Munoz R, et al. Genetic mapping of two QTL from the wild tomato Solanum pimpinellifolium L. controlling resistance against two-spotted spider mite (Tetranychus urticae Koch). TAG Theoretical and Applied Genetics Theoretische und Angewandte Genetik. 2013;126(1):83–92.View ArticlePubMedGoogle Scholar
- Antonious GF, Kamminga K, Snyder JC. Wild tomato leaf extracts for spider mite and cowpea aphid control. J Environ Sci Heal B. 2014;49(7):527–31.View ArticleGoogle Scholar
- Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, et al. Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci U S A. 2012;109(49):20124–9.PubMed CentralView ArticlePubMedGoogle Scholar
- Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, et al. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A. 2006;103(29):11086–91.PubMed CentralView ArticlePubMedGoogle Scholar
- Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, et al. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci U S A. 2014;111(3):E404–413.PubMed CentralView ArticlePubMedGoogle Scholar
- Kouzai Y, Nakajima K, Hayafune M, Ozawa K, Kaku H, Shibuya N, et al. CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol Biol. 2014;84(4–5):519–28.View ArticlePubMedGoogle Scholar
- Merzendorfer H, Zimoch L. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol. 2003;206(Pt 24):4393–412.View ArticlePubMedGoogle Scholar
- Fan YH, Pei XQ, Guo SJ, Zhang YJ, Luo ZB, Liao XG, et al. Increased virulence using engineered protease-chitin binding domain hybrid expressed in the entomopathogenic fungus Beauveria bassiana. Microb Pathogenesis. 2010;49(6):376–80.View ArticleGoogle Scholar
- Gatarayiha MC, Laing MD, Miller RM. Field evaluation of Beauveria bassiana efficacy for the control of Tetranychus urticae Koch (Acari: Tetranychidae). J Appl Entomol. 2011;135(8):582–92.View ArticleGoogle Scholar
- Broadway RM, Gongora C, Kain WC, Sanderson JP, Monroy JA, Bennett KC, et al. Novel chitinolytic enzymes with biological activity against herbivorous insects. J Chem Ecol. 1998;24(6):985–98.View ArticleGoogle Scholar
- Carrillo L, Martinez M, Ramessar K, Cambra I, Castanera P, Ortego F, et al. Expression of a barley cystatin gene in maize enhances resistance against phytophagous mites by altering their cysteine-proteases. Plant Cell Rep. 2011;30(1):101–12.View ArticlePubMedGoogle Scholar
- Nagpure A, Choudhary B, Gupta RK. Chitinases: in agriculture and human healthcare. Crit Rev Biotechnol. 2014;34(3):215–32.View ArticlePubMedGoogle Scholar
- Erban T, Hubert J. Determination of pH in regions of the midguts of acaridid mites. J Insect Sci (Online). 2010;10:42.View ArticleGoogle Scholar
- Alley CJ. Grapevine Propagation.11. Rooting of Cuttings - Effects of Indolebutyric Acid (Iba) and Refrigeration on Rooting. Am J Enol Viticult. 1979;30(1):28–32.Google Scholar
- Wheatley MD, Tattersall EAR, Tillett RL, Cramer GR. An Expanded Clay Pebble, Continuous Recirculating Drip System for Viable Long-Term Hydroponic Grapevine Culture. Am J Enol Viticult. 2009;60(4):542–9.Google Scholar
- Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21.PubMed CentralView ArticlePubMedGoogle Scholar
- Anders S, Pyl PT, Huber W. HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166-9.Google Scholar
- Law CW, Chen Y, Shi W, Smyth GK. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 2014;15(2):R29.PubMed CentralView ArticlePubMedGoogle Scholar
- Varemo L, Nielsen J, Nookaew I. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res. 2013;41(8):4378–91.PubMed CentralView ArticlePubMedGoogle Scholar
- Kim SY, Volsky DJ. PAGE: Parametric analysis of gene set enrichment. Bmc Bioinformatics. 2005;6:144.Google Scholar
- Grimplet J, Van Hemert J, Carbonell-Bejerano P, Diaz-Riquelme J, Dickerson J, Fennell A, et al. Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences. BMC Research Notes. 2012;5(1):213.PubMed CentralView ArticlePubMedGoogle Scholar
- Alexa A, Rahnenfuhrer J, Lengauer T. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics. 2006;22(13):1600–7.View ArticlePubMedGoogle Scholar
- Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA. PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res. 2012;40(D1):D1194–201.PubMed CentralView ArticlePubMedGoogle Scholar
- Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249–64.View ArticlePubMedGoogle Scholar
- Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article3.PubMedGoogle Scholar
- Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N. The use of gene clusters to infer functional coupling. Proc Natl Acad Sci U S A. 1999;96(6):2896–901.PubMed CentralView ArticlePubMedGoogle Scholar
- Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402.PubMed CentralView ArticlePubMedGoogle Scholar