Comparative Transcriptomics of Wild and Commercial Citrus During Early Ripening Reveals How Domestication Shaped Fruit Gene Expression

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.