Allele‐specific expression and genetic determinants of transcriptomic variations in response to mild water deficit in tomato

Abstract

Characterizing the natural diversity of gene expression across environments is an important step in understanding how genotype-by-environment interactions shape phenotypes. Here, we analyzed the impact of water deficit onto gene expression levels in tomato at the genome-wide scale. We sequenced the transcriptome of growing leaves and fruit pericarps at cell expansion stage in a cherry and a large fruited accession and their F hybrid grown under two watering regimes. Gene expression levels were steadily affected by the genotype and the watering regime. Whereas phenotypes showed mostly additive inheritance, ~80% of the genes displayed non-additive inheritance. By comparing allele-specific expression (ASE) in the F hybrid to the allelic expression in both parental lines, respectively, 3005 genes in leaf and 2857 genes in fruit deviated from 1:1 ratio independently of the watering regime. Among these genes, ~55% were controlled by cis factors, ~25% by trans factors and ~20% by a combination of both types of factors. A total of 328 genes in leaf and 113 in fruit exhibited significant ASE-by-watering regime interaction, among which ~80% presented trans-by-watering regime interaction, suggesting a response to water deficit mediated through a majority of trans-acting loci in tomato. We cross-validated the expression levels of 274 transcripts in fruit and leaves of 124 recombinant inbred lines (RILs) and identified 163 expression quantitative trait loci (eQTLs) mostly confirming the divergences identified by ASE. Combining phenotypic and expression data, we observed a complex network of variation between genes encoding enzymes involved in the sugar metabolism.

Genetic basis of phenotypic plasticity and genotype x environment interaction in a multi-parental population

“…Studying plasticity as a trait per se is therefore of a major interest since breeding in both direction (considering the mean phenotype and its plasticity) is achievable. Through transcriptomic analyses, Albert et al (2018) observed that genotype x water deficit interaction was mostly associated to trans- acting genes which could be assimilated to the gene-regulatory model in agreement with our results.…”

“…control vs stress). Albert et al (2018) for example identified different WD-response quantitative trait loci (QTL) in a bi-parental population derived from a cross of large and cherry tomato accessions. Tomato heat-response QTLs were also identified in different experimental populations including interspecific and intraspecific populations (Grilli et al, 2007; Xu et al, 2017a; Driedonks et al, 2018).…”

Genetic basis of phenotypic plasticity and genotype × environment interactions in a multi-parental tomato population

“…control versus stress). For example, Albert et al (2018) identified different quantitative trait loci (QTL) for the WD response in a bi-parental population derived from a cross of large and cherry tomato accessions. Tomato heat-response QTLs have also been identified in different experimental populations, including both inter- and intraspecific ( Grilli et al , 2007 ; Xu et al , 2017 a ; Driedonks et al , 2018 ).…”

Trait discovery and editing in tomato

“…Increased analytical throughput and widening of the range of metabolites identified and of genetic diversity studied led to the detection of hundreds of metabolite QTLs (mQTLs) controlling fruit composition (primary and specialized metabolites, volatiles, cuticle components, etc.) (Alseekh et al ., , ; Ballester et al ., ; Ofner et al ., ; Tieman et al ., ; Albert et al ., ; Garbowicz et al ., ; Zhu et al ., ). This was the first step for identification by map‐based cloning of genes involved in metabolite variations such as a glycosyltransferase controlling smoky aroma (Tikunov et al ., ) and a MYB transcription factor responsible for pink fruit color (Ballester et al ., ).…”