Transcriptional profiling of methyl jasmonate-induced defense responses in bilberry (Vaccinium myrtillus L.)

Benevenuto, Rafael Fonseca; Seldal, Tarald; Hegland, Stein Joar; Rodriguez‐Saona, Cesar; Kawash, Joseph; Polashock, James J.

doi:10.1186/s12870-019-1650-0

Cited by 46 publications

(36 citation statements)

References 123 publications

(123 reference statements)

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“…The downregulation of PHOTO gene, as well as substantial decreases in seasonal growth found in our study, suggests that the inhibitory effect of MeJA on photosynthesis is effective due to the reduction in the light‐harvesting complexes, consequently decreasing carbon fixation. Our findings corroborate with previous transcriptomic studies, where PHOTO and other important chlorophyll‐related genes from the photosystem II complex were downregulated in response to MeJA treatment in wild bilberries (Benevenuto et al, ; Bilgin et al, ). At the very last, high‐elevation genotypes showed to not immediately downregulate growth‐related genes in response to MeJA treatment as we have seen for low‐elevation genotypes.…”

Section: Discussionsupporting

confidence: 92%

“…Our findings indicate an effective trade‐off between growth/reproduction and defense in bilberry plants under herbivory pressure from warmer low‐elevation environments in the year of treatment, suggesting an investment strategy of protecting against future or persistent herbivore attacks. In a previous study exploring the transcriptional profiling of MeJA‐induced defense responses in bilberry, we found evidences for “gene regulation trade‐off”: the upregulation of genes involved in important defense‐related pathways and the corresponding downregulation of genes related to growth and nitrogen metabolism pathways (Benevenuto et al, ). Trade‐offs persisted one year after MeJA induction only at the lowest elevation site.…”

Section: Discussionmentioning

confidence: 97%

“…A list of target genes for real‐time PCR and the primers used in the analysis are provided in Table . The selection of these eight genes involved in defense and growth‐related pathways was based on our previous RNA‐seq study of MeJA‐treated wild bilberry plants (Benevenuto et al, ). Defense target genes, involved in circadian rhythm, phenylpropanoid, tyrosine, flavonoid, and anthocyanin biosynthesis pathways, are shikimate O‐hydroxycinnamoyltransferase ( SHIKIMATE ), tyrosine aminotransferase ( TYR ), leucoanthocyanidin dioxygenase ( LDOX ), UDP‐glycosyltransferase ( UDP ), MYB‐related transcription factor LHY ( LHY ), and flavonoid 3′,5′‐hydroxylase ( FLAV ).…”

Section: Methodsmentioning

confidence: 99%

“…Ubc28 was also found to be stable and was used as the interplate calibrator. The gene sequences used for primer design were selected from the RNA‐seq de novo assembly of the bilberry transcriptome (Benevenuto et al, ), because the complete genome sequence of this species is not available. The primers were designed based on the predicted coding sequence of each target gene by using the online tool PrimerQuest (Integrated DNA Technologies Inc., Skokie, IL, USA).…”

Section: Methodsmentioning

confidence: 99%

“…A list of target genes for real-time PCR and the primers used in the analysis are provided in Table S1. The selection of these eight genes involved in defense and growth-related pathways was based on our previous RNA-seq study of MeJA-treated wild bilberry plants (Benevenuto et al, 2019). Defense target genes, involved in circadian rhythm, phenylpropanoid, tyrosine, flavonoid, and anthocyanin bio- Several genes were tested to be used for normalization, based on those commonly used in publications and our own transcriptome data (i.e., those not differentially expressed).…”

Section: Gene Expression Analysismentioning

confidence: 99%

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Molecular and ecological plant defense responses along an elevational gradient in a boreal ecosystem

Benevenuto

Seldal

Polashock

et al. 2020

Ecology and Evolution

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Plants have the capacity to alter their phenotype in response to environmental factors, such as herbivory, a phenomenon called phenotypic plasticity. However, little is known on how plant responses to herbivory are modulated by environmental variation along ecological gradients. To investigate this question, we used bilberry (Vaccinium myrtillus L.) plants and an experimental treatment to induce plant defenses (i.e., application of methyl jasmonate; MeJA), to observe ecological responses and gene expression changes along an elevational gradient in a boreal system in western Norway. The gradient included optimal growing conditions for bilberry in this region (ca. 500 m a.s.l.), and the plant's range limits at high (ca. 900 m a.s.l.) and low (100 m a.s.l.) elevations. Across all altitudinal sites, MeJA‐treated plants allocated more resources to herbivory resistance while reducing growth and reproduction than control plants, but this response was more pronounced at the lowest elevation. High‐elevation plants growing under less herbivory pressure but more resource‐limiting conditions exhibited consistently high expression levels of defense genes in both MeJA‐treated and untreated plants at all times, suggesting a constant state of “alert.” These results suggest that plant defense responses at both the molecular and ecological levels are modulated by the combination of climate and herbivory pressure, such that plants under different environmental conditions differentially direct the resources available to specific antiherbivore strategies. Our findings are important for understanding the complex impact of future climate changes on plant–herbivore interactions, as this is a major driver of ecosystem functioning and biodiversity.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Gene Expression Analysismentioning

confidence: 99%

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Molecular and ecological plant defense responses along an elevational gradient in a boreal ecosystem

Benevenuto

Seldal

Polashock

et al. 2020

Ecology and Evolution

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Fruit ripening in Lycium barbarum and Lycium ruthenicum is associated with distinct gene expression patterns

Zhao

Yin

et al. 2020

FEBS Open Bio

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Goji berries have been used as food and medicine for millennia. Due to their high morphological similarity, fruits of two distinct species belonging to the family Solanaceae, Lycium barbarum (LB) and Lycium chinense (Chinese boxthorn), are usually marketed together as goji berries, but nearly 90% of all commercially available goji berries belong to the former species. A third closely related species, a wild perennial thorny shrub native to north‐western China, Lycium ruthenicum (LR; known as Russian box thorn, and its fruit as black wolfberry), has become a popular choice for combating soil desertification and for alleviating soil salinity/alkalinity due to its high resistance to the harsh environment of saline deserts. Despite the phylogenetic closeness of LB and LR, their fruits are very different. To identify the genes involved in these distinct phenotypes, here we studied expression patterns of 22 transcriptional regulators that may be crucial drivers of these differences during five developmental stages. BAM1 may contribute to higher sugar content in LB. High expression of BFRUCT in ripe LR is likely to be an evolutionary adaptation to fruit ripening in an arid environment. Two arogenate dehydratase paralogues, CHS and LDOX, are probably crucial elements of the mechanism by which LR accumulates much higher levels of anthocyanin. DXS2 (carotenoid accumulation in LB) and CCD4 (carotenoid degradation in ripe LR fruit) may be crucial drivers behind the much higher content of carotenoids in LB. EIL3 and ERF5 are two transcription factors that may contribute to the higher abiotic stress resilience of LR. GATA22‐like appears to have more important roles in growth than ripening in LB fruit and vice versa in LR. HAT5‐like exhibited opposite temporal patterns in two fruits: high in the 1st stage in LB and high in the 5th stage in LR. PED1 was expressed at a much lower level in LR. Finally, we hypothesise that the poorly functionally characterised SCL32 gene may play a part in the increased resistance to environmental stress of LR. We suggest that BAM1, BFRUCT, EIL3, ERF5, ADT paralogues (for functional redundancy), PED1, GATA22‐like, HAT5‐like and SCL32 warrant further functional studies.

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Ecometabolomics of plant–herbivore and plant–fungi interactions: a synthesis study

et al. 2021

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The functional adaptive responses of higher plants to biotic interactions with herbivores and fungi have long been topics of research. One constraint to obtaining a comprehensive understanding of the most general plant responses, however, has been the difficulty of studying all plant functional shifts simultaneously due to analytical limitations. Now this is possible with the advent of metabolomics. Using 151 records from the WEB of SCIENCE database, we have analyzed the development and application of metabolomic profiles to ecological studies in the last two decades. We have used meta-analysis and pathway enrichment analyses to assess the whole set of constitutive and inducible defenses. Constitutive defenses against herbivores were mainly based on a significant high level of the metabolism of several amino acids with parallel increases in the concentrations of flavones (phenolics) and saponins (glycosides). Inducible defenses, though, were mainly based on the increases in concentration of methyl-ketone, pantothenate, and Coenzyme A. Butyrate metabolism and the mitochondrial electron-transport chain were upregulated, in agreement with previous reports that herbivory-activated plant chemical defenses were mainly based on jasmonic acid, salicylic acid, and ethylene-associated pathways. The metabolic responses/acclimations to pathogenic fungi were mainly linked with increases in aspartate and pyruvate metabolism, the transfer of acetyl groups within mitochondria, and the upregulation of branched-chain amino acids degradation pathways. These responses/acclimations were accompanied by higher concentrations of the most important groups of secondary metabolites such as phenolics (anthocyanins, flavonoids), quinones, alkaloids, terpenoids, and polyamines and other compounds related to antistress mechanisms such as proline. The leaves of mycorrhized plants accumulated nucleotide sugars, sphingolipids, and methylhistidine. These responses were associated with maintaining the integrity of plant cell membranes under fungal hypha penetration. The responses were accompanied by increases in the concentrations of phenolics, blumenols, and alkaloids and decreases in the concentrations of polyamines, consistent with the mycorrhizal inhibition of polyamines. This summary provides a clear synthesis of the most successful plant strategies selected after millions of years of evolution and will be a very promising tool for the management of crops and ecosystems and for selecting the main lines in breeding studies for future research.

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Transcriptional profiling of methyl jasmonate-induced defense responses in bilberry (Vaccinium myrtillus L.)

Cited by 46 publications

References 123 publications

Molecular and ecological plant defense responses along an elevational gradient in a boreal ecosystem

Molecular and ecological plant defense responses along an elevational gradient in a boreal ecosystem

Fruit ripening in Lycium barbarum and Lycium ruthenicum is associated with distinct gene expression patterns

Ecometabolomics of plant–herbivore and plant–fungi interactions: a synthesis study

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