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Inheritance of Secondary Metabolites and Gene Expression Related to Tomato Fruit Quality.

ABSTRACT: Flavour and nutritional quality are important goals for tomato breeders. This study aimed to shed light upon transgressive behaviors for fruit metabolic content. We studied the metabolic contents of 44 volatile organic compounds (VOCs), 18 polyphenolics, together with transcriptome profiles in a factorial design comprising six parental lines and their 14 F1 hybrids (HF1) among which were five pairs of reciprocal HF1. After cluster analyses of the metabolome dataset and co-expression network construction of the transcriptome dataset, we characterized the mode of inheritance of each component. Both overall and per-cross mode of inheritance analyses revealed as many additive and non-additive modes of inheritance with few reciprocal effects. Up to 66% of metabolites displayed transgressions in a HF1 relative to parental values. Analysis of the modes of inheritance of metabolites revealed that: (i) transgressions were mostly of a single type whichever the cross and poorly correlated to the genetic distance between parental lines; (ii) modes of inheritance were scarcely consistent between the 14 crosses but metabolites belonging to the same cluster displayed similar modes of inheritance for a given cross. Integrating metabolome, transcriptome and modes of inheritance analyses suggested a few candidate genes that may drive important changes in fruit VOC contents.

SUBMITTER: Bineau E

PROVIDER: S-EPMC9181508 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Inheritance of Secondary Metabolites and Gene Expression Related to Tomato Fruit Quality.

Bineau Estelle E Rambla José Luis JL Duboscq Renaud R Corre Marie-Noëlle MN Bitton Frédérique F Lugan Raphaël R Granell Antonio A Plissonneau Clémence C Causse Mathilde M

International journal of molecular sciences 20220531 11

Flavour and nutritional quality are important goals for tomato breeders. This study aimed to shed light upon transgressive behaviors for fruit metabolic content. We studied the metabolic contents of 44 volatile organic compounds (VOCs), 18 polyphenolics, together with transcriptome profiles in a factorial design comprising six parental lines and their 14 F1 hybrids (HF1) among which were five pairs of reciprocal HF1. After cluster analyses of the metabolome dataset and co-expression network cons ...[more]

PMID: 35682842

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Project description:BackgroundThe destructive phytopathogen Colletotrichum gloeosporioides causes anthracnose disease in fruit. During host colonization, it secretes ammonia, which modulates environmental pH and regulates gene expression, contributing to pathogenicity. However, the effect of host pH environment on pathogen colonization has never been evaluated. Development of an isogenic tomato line with reduced expression of the gene for acidity, SlPH (Solyc10g074790.1.1), enabled this analysis. Total RNA from C. gloeosporioides colonizing wild-type (WT) and RNAi-SlPH tomato lines was sequenced and gene-expression patterns were compared.ResultsC. gloeosporioides inoculation of the RNAi-SlPH line with pH 5.96 compared to the WT line with pH 4.2 showed 30% higher colonization and reduced ammonia accumulation. Large-scale comparative transcriptome analysis of the colonized RNAi-SlPH and WT lines revealed their different mechanisms of colonization-pattern activation: whereas the WT tomato upregulated 13-LOX (lipoxygenase), jasmonic acid and glutamate biosynthesis pathways, it downregulated processes related to chlorogenic acid biosynthesis II, phenylpropanoid biosynthesis and hydroxycinnamic acid tyramine amide biosynthesis; the RNAi-SlPH line upregulated UDP-D-galacturonate biosynthesis I and free phenylpropanoid acid biosynthesis, but mainly downregulated pathways related to sugar metabolism, such as the glyoxylate cycle and L-arabinose degradation II. Comparison of C. gloeosporioides gene expression during colonization of the WT and RNAi-SlPH lines showed that the fungus upregulates ammonia and nitrogen transport and the gamma-aminobutyric acid metabolic process during colonization of the WT, while on the RNAi-SlPH tomato, it mainly upregulates the nitrate metabolic process.ConclusionsModulation of tomato acidity and pH had significant phenotypic effects on C. gloeosporioides development. The fungus showed increased colonization on the neutral RNAi-SlPH fruit, and limited colonization on the WT acidic fruit. The change in environmental pH resulted in different defense responses for the two tomato lines. Interestingly, the WT line showed upregulation of jasmonate pathways and glutamate accumulation, supporting the reduced symptom development and increased ammonia accumulation, as the fungus might utilize glutamate to accumulate ammonia and increase environmental pH for better expression of pathogenicity factors. This was not found in the RNAi-SlPH line which downregulated sugar metabolism and upregulated the phenylpropanoid pathway, leading to host susceptibility.

Project description:Genome Wide Association Studies (GWAS) have been recently used to dissect complex quantitative traits and identify candidate genes affecting phenotype variation of polygenic traits. In order to map loci controlling variation in tomato marketable and nutritional fruit traits, we used a collection of 96 cultivated genotypes, including Italian, Latin American, and other worldwide-spread landraces and varieties. Phenotyping was carried out by measuring ten quality traits and metabolites in red ripe fruits. In parallel, genotyping was carried out by using the Illumina Infinium SolCAP array, which allows data to be collected from 7,720 single nucleotide polymorphism (SNP) markers.The Mixed Linear Model used to detect associations between markers and traits allowed population structure and relatedness to be evidenced within our collection, which have been taken into consideration for association analysis. GWAS identified 20 SNPs that were significantly associated with seven out of ten traits considered. In particular, our analysis revealed two markers associated with phenolic compounds, three with ascorbic acid, β-carotene and trans-lycopene, six with titratable acidity, and only one with pH and fresh weight. Co-localization of a group of associated loci with candidate genes/QTLs previously reported in other studies validated the approach. Moreover, 19 putative genes in linkage disequilibrium with markers were found. These genes might be involved in the biosynthetic pathways of the traits analyzed or might be implied in their transcriptional regulation. Finally, favourable allelic combinations between associated loci were identified that could be pyramided to obtain new improved genotypes.Our results led to the identification of promising candidate loci controlling fruit quality that, in the future, might be transferred into tomato genotypes by Marker Assisted Selection or genetic engineering, and highlighted that intraspecific variability might be still exploited for enhancing tomato fruit quality.

Dataset Information

Inheritance of Secondary Metabolites and Gene Expression Related to Tomato Fruit Quality.

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Inheritance of Secondary Metabolites and Gene Expression Related to Tomato Fruit Quality.

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