Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression

Abstract

Background Interspecific hybridizations and admixtures were key in Citrus domestication, but very little is known about their impact at the transcriptomic level. To determine the effects of genome introgressions on gene expression, the transcriptomes of the pulp and flavedo of three pure species (citron, pure mandarin and pummelo) and four derived domesticated genetic admixtures (sour orange, sweet orange, lemon and domesticated mandarin) have been analyzed at color break. Results Many genes involved in relevant physiological processes for domestication, such sugar/acid metabolism and carotenoid/flavonoid synthesis, were differentially expressed among samples. In the low-sugar, highly acidic species lemon and citron, many genes involved in sugar metabolism, the TCA cycle and GABA shunt displayed a reduced expression, while the P-type ATPase CitPH5 and most subunits of the vacuolar ATPase were overexpressed. The red-colored species and admixtures were generally characterized by the overexpression in the flavedo of specific pivotal genes involved in the carotenoid biosynthesis, including phytoene synthase, ζ-carotene desaturase, β-lycopene cyclase and CCD4b, a carotenoid cleavage dioxygenase. The expression patterns of many genes involved in flavonoid modifications, especially the flavonoid and phenylpropanoid O-methyltransferases showed extreme diversity. However, the most noticeable differential expression was shown by a chalcone synthase gene, which catalyzes a key step in the biosynthesis of flavonoids. This chalcone synthase was exclusively expressed in mandarins and their admixed species, which only expressed the mandarin allele. In addition, comparisons between wild and domesticated mandarins revealed that the major differences between their transcriptomes concentrate in the admixed regions. Conclusion In this work we present a first study providing broad evidence that the genome introgressions that took place during citrus domestication largely shaped gene expression in their fruits.

Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability

“…Thus, the KEGG data show that gene expression of practically all genes encoding enzymatic activities involved in glycolysis (Supplementary Figure 4 4.002), and several subunits of the major regulatory complex of the oxidative phosphorylation process (Supplementary Figure 4.014) were upregulated in the papeda. As in SCM, in the highly acidic species lemon and citron, several genes involved in the TCA cycle and GABA shunt also displayed reduced expression during ripening (Borredá et al, 2022). Based on these observations, we propose that in the papeda, the generation of energy in the ATP form, is stimulated through the increase of the carbon flux via both glycolysis and fatty acid degradation, generating pyruvate and acetyl CoA, respectively, to fuel the Krebs cycle (Figure 6).…”

“…During the last years, most attention has been paid to the identification of genes or gene families impacting palatability traits, fruit characteristics and reproductive behavior. Among the palatability traits, wide evidence indicates that domestication has modulated pivotal genes regulating major components of citrus flavor, such as acidity (Butelli et al, 2019;Strazzer et al, 2019;Feng et al, 2021;Borredá et al, 2022), bitterness (Chen et al, 2021) or sweetness (Li et al, 2019;Feng et al, 2021). Domestication also appears to have reduced certain chemical defenses in citrus (Gonzalez-Ibeas et al, 2021a,b;Rao et al, 2021), as reported in many crops (Köllner et al, 2008;Yactayo-Chang et al, 2020).…”

“…During the last centuries, a myriad of crosses between ancestral hybrids and admixtures, gave rise to the current basic types of edible citrus that were progressively improved through somatic mutations and recurrent selection (Talon et al, 2020). We have also used genomic and transcriptomic analyses on wild and domesticated citrus to discriminate major determinants of evolution and domestication (Gonzalez-Ibeas et al, 2021a,b) and to identify genes involved in relevant physiological processes for domestication (Borredá et al, 2022).…”

Review of phytochemical and nutritional characteristics and food applications of Citrus L. fruits

“…Carotenoids have special relevance to human nutrition and health-related aspects of immunity enhancement, eyes protection, and cancer and cardiovascular disease prevention ( Figure 3 ) ( 10 ). As an important source of natural carotenoids, citrus carotenoids not only contribute nutritional value to citrus fruits, but also are responsible for the attractive color of yellow, orange, and red ( 10 , 70 ). Carotenoids are naturally occurring fat-soluble pigments with antioxidant functions and some of them (provitamin A carotenoids, including α-carotene, β-carotene, and β-cryptoxanthin) can be converted into vitamin A (retinol) ( 71 ), thus make citrus become a valuable source to fulfill the recommended daily ingestion specifications.…”

FveARF2 negatively regulates fruit ripening and quality in strawberry

“…Overexpression of FaSUT1 in strawberry fruit may increase both sucrose and ABA content and accelerate fruit ripening (Jia et al, 2013). OMT (O-methyltransferase) is a flavonoid-modifying enzyme that determines the diversity of flavonoids (Borredáet al, 2022). The expression of MdoOMT1 increases strongly with ethylene and is correlated with increased estragole production in ripened apples (Yauk et al, 2015).…”