Fruit Colour and Novel Mechanisms of Genetic Regulation of Pigment Production in Tomato Fruits

Silvia Gonzali,Pierdomenico Perata

doi:10.3390/horticulturae7080259

Abstract

Fruit colour represents a genetic trait with ecological and nutritional value. Plants mainly use colour to attract animals and favour seed dispersion. Thus, in many species, fruit colour coevolved with frugivories and their preferences. Environmental factors, however, represented other adaptive forces and further diversification was driven by domestication. All these factors cooperated in the evolution of tomato fruit, one of the most important in human nutrition. Tomato phylogenetic history showed two main steps in colour evolution: the change from green-chlorophyll to red-carotenoid pericarp, and the loss of the anthocyanic pigmentation. These events likely occurred with the onset of domestication. Then spontaneous mutations repeatedly occurred in carotenoid and phenylpropanoid pathways, leading to colour variants which often were propagated. Introgression breeding further enriched the panel of pigmentation patterns. In recent decades, the genetic determinants underneath tomato colours were identified. Novel evidence indicates that key regulatory and biosynthetic genes undergo mechanisms of gene expression regulation that are much more complex than what was imagined before: post-transcriptional mechanisms, with RNA splicing among the most common, indeed play crucial roles to fine-tune the expression of this trait in fruits and offer new substrate for the rise of genetic variables, thus providing further evolutionary flexibility to the character.

Highlights

Fruit colour represents a genetic trait with ecological and nutritional value
The genetic diversification of the flavonoid pathway is mainly found at the regulatory level [18], while the evolution of the structural genes, encoding the enzymatic proteins acting along the biosynthetic way, was strongly constrained, for those genes involved in the early reactions, common to multiple pathways
The fruit colour is a complex phenotypic trait that can be modelled by different factors: environmental elements, phylogenetic constraints and, more than others, coevolution with seeds dispersers’ preferences

Summary

Function and Evolution of Fruit Colour

Colour is one of the main qualitative attributes of fleshy fruits. Its importance is strictly dependent on its primary ecological function, which is attracting seed dispersers. The genetic diversification of the flavonoid pathway is mainly found at the regulatory level [18], while the evolution of the structural genes, encoding the enzymatic proteins acting along the biosynthetic way, was strongly constrained, for those genes involved in the early reactions, common to multiple pathways In this case, differences in fruit colour often rely on the presence or absence of specific classes of pigments, in turn depending on the specific activation or repression exerted by different transcription factors (TFs) on the pathway, or part of it. Anthocyanins are generally not present in tomato fruits, but when synthesized belong to the delphinidin-type (Figure 1B), and are accumulated in the epidermis and in the sub-epidermal layer

Phylogenetic Reconstruction and Human Selection of Fruit Colour in Tomato

Findings

Conclusions