Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality

Rocket (Eruca vesicaria subsp. sativa) is a source of sulfur-containing glucosinolates (GSLs). GSLs and their breakdown hydrolysis products (GHPs) are responsible for health-related benefits, such as anti-cancer and anti-neurodegenerative properties. Understanding how phytochemical composition chang...

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Main Authors: Luke Bell, Martin Chadwick, Manik Puranik, Jake Jasper, Richard Tudor, Lisa Methven, Carol Wagstaff
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1218984/full
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author Luke Bell
Martin Chadwick
Manik Puranik
Jake Jasper
Richard Tudor
Lisa Methven
Carol Wagstaff
author_facet Luke Bell
Martin Chadwick
Manik Puranik
Jake Jasper
Richard Tudor
Lisa Methven
Carol Wagstaff
author_sort Luke Bell
collection DOAJ
description Rocket (Eruca vesicaria subsp. sativa) is a source of sulfur-containing glucosinolates (GSLs). GSLs and their breakdown hydrolysis products (GHPs) are responsible for health-related benefits, such as anti-cancer and anti-neurodegenerative properties. Understanding how phytochemical composition changes between cultivation environments is key to developing cultivars with improved nutritional quality. Two consecutive harvests (first and second regrowth) of crops, grown in both Italy and the UK, were used to determine the phytochemical and transcriptomic differences between six lines of Eruca. Samples were taken upon delivery from field sites (D0) and after five days of cold storage (D5) for each location. Leaves were analysed for sulfur content, volatile organic compounds (VOCs), GSLs, GHPs, and sugars. Transcriptome data were associated with metabolite profiles to identify differentially expressed genes between plants grown in the two environments. VOC compounds (carbon disulfide, methyl thiocyanate) were associated with growth environment and with differences in sulfur metabolism gene expression (APR2, LSU2, LSU3, SDI1, SiR), GSL biosynthesis (MYB28, FMOGS-OX2) and GHP formation (ESM1, TGG1, TGG2). The concentrations of sugars were an order of magnitude greater in UK grown samples (up to 29.9 mg g-1 dry weight; dw). Sulfur content was significantly higher in the Italy plant samples (11.4 – 20.1 mg g-1 dw), which was in turn associated with higher concentrations of GSLs (pentyl GSL, up to 15.8 μmol g-1 dw; sinigrin, up to 0.005 μmol g-1 dw; glucoraphanin, up to 5.1 μmol g-1 dw; glucorucolamine, up to 23.6 μmol g-1 dw; neoglucobrassicin, up to 5.3 μmol g-1 dw) and hydrolysis products (sativin, up to 13.5 μmol g-1 dw; erucin, up to 1 μmol g-1 dw; sulforaphane, up to 34.7 μmol g-1 dw). VOC profiles of plants cultivated in the UK were distinct from Italy grown plants, with higher relative abundances of alkanes and esters in second cut and shelf-life (D5) samples. The data indicate a significant interaction of cultivar response with environment, highlighting the difficulty of producing Eruca crops with consistent phytochemical and postharvest traits. Genes with differential expression between plants grown in Italy and the UK could be used as markers of phytochemical quality and composition.
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spelling doaj.art-aa91e909888342968e799055ec8918682023-11-02T12:57:09ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-11-011410.3389/fpls.2023.12189841218984Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional qualityLuke Bell0Martin Chadwick1Manik Puranik2Jake Jasper3Richard Tudor4Lisa Methven5Carol Wagstaff6School of Agriculture, Policy & Development, Crop Sciences, University of Reading, Reading, United KingdomSchool of Chemistry, Food & Pharmacy, Food & Nutritional Sciences, University of Reading, Reading, United KingdomSchool of Chemistry, Food & Pharmacy, Food & Nutritional Sciences, University of Reading, Reading, United KingdomSchool of Chemistry, Food & Pharmacy, Food & Nutritional Sciences, University of Reading, Reading, United KingdomVegetable Plant Breeding, Elsoms Seeds Ltd., Spalding, United KingdomSchool of Chemistry, Food & Pharmacy, Food & Nutritional Sciences, University of Reading, Reading, United KingdomSchool of Chemistry, Food & Pharmacy, Food & Nutritional Sciences, University of Reading, Reading, United KingdomRocket (Eruca vesicaria subsp. sativa) is a source of sulfur-containing glucosinolates (GSLs). GSLs and their breakdown hydrolysis products (GHPs) are responsible for health-related benefits, such as anti-cancer and anti-neurodegenerative properties. Understanding how phytochemical composition changes between cultivation environments is key to developing cultivars with improved nutritional quality. Two consecutive harvests (first and second regrowth) of crops, grown in both Italy and the UK, were used to determine the phytochemical and transcriptomic differences between six lines of Eruca. Samples were taken upon delivery from field sites (D0) and after five days of cold storage (D5) for each location. Leaves were analysed for sulfur content, volatile organic compounds (VOCs), GSLs, GHPs, and sugars. Transcriptome data were associated with metabolite profiles to identify differentially expressed genes between plants grown in the two environments. VOC compounds (carbon disulfide, methyl thiocyanate) were associated with growth environment and with differences in sulfur metabolism gene expression (APR2, LSU2, LSU3, SDI1, SiR), GSL biosynthesis (MYB28, FMOGS-OX2) and GHP formation (ESM1, TGG1, TGG2). The concentrations of sugars were an order of magnitude greater in UK grown samples (up to 29.9 mg g-1 dry weight; dw). Sulfur content was significantly higher in the Italy plant samples (11.4 – 20.1 mg g-1 dw), which was in turn associated with higher concentrations of GSLs (pentyl GSL, up to 15.8 μmol g-1 dw; sinigrin, up to 0.005 μmol g-1 dw; glucoraphanin, up to 5.1 μmol g-1 dw; glucorucolamine, up to 23.6 μmol g-1 dw; neoglucobrassicin, up to 5.3 μmol g-1 dw) and hydrolysis products (sativin, up to 13.5 μmol g-1 dw; erucin, up to 1 μmol g-1 dw; sulforaphane, up to 34.7 μmol g-1 dw). VOC profiles of plants cultivated in the UK were distinct from Italy grown plants, with higher relative abundances of alkanes and esters in second cut and shelf-life (D5) samples. The data indicate a significant interaction of cultivar response with environment, highlighting the difficulty of producing Eruca crops with consistent phytochemical and postharvest traits. Genes with differential expression between plants grown in Italy and the UK could be used as markers of phytochemical quality and composition.https://www.frontiersin.org/articles/10.3389/fpls.2023.1218984/fullglucosinolatesisothiocyanatesbrassicaceaetranscriptome sequencingvolatile organic compoundsarugula
spellingShingle Luke Bell
Martin Chadwick
Manik Puranik
Jake Jasper
Richard Tudor
Lisa Methven
Carol Wagstaff
Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality
Frontiers in Plant Science
glucosinolates
isothiocyanates
brassicaceae
transcriptome sequencing
volatile organic compounds
arugula
title Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality
title_full Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality
title_fullStr Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality
title_full_unstemmed Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality
title_short Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality
title_sort genotypes of eruca vesicaria subsp sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels significantly impacting nutritional quality
topic glucosinolates
isothiocyanates
brassicaceae
transcriptome sequencing
volatile organic compounds
arugula
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1218984/full
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