Genetic Contribution of Paleopolyploidy to Adaptive Evolution in Angiosperms

Ancient whole-genome duplications (WGDs or polyploidy) are prevalent in plants, and some WGDs occurred during the timing of severe global environmental changes. It has been suggested that WGDs may have contributed to plant adaptation. However, this still lacks empirical evidence at the genetic level to support the hypothesis. Here, we investigated the survivors of gene duplicates from multiple ancient WGD events on the major branches of angiosperm phylogeny, and aimed to explore genetic evidence supporting the significance of polyploidy. Duplicated genes co-retained from three waves of independent WGDs (～120 million years ago [Ma], ～66, and <20 Ma) were investigated in 25 selected species. Gene families functioning in low temperature and darkness were commonly retained gene duplicates after the eight independently occurring WGDs in many lineages around the Cretaceous-Paleocene boundary, when the global cooling and darkness were the two main stresses. Moreover, the commonly retained duplicates could be key factors which may have contributed to the robustness of the critical stress-related pathways. In addition, genome-wide transcription factors (TFs) functioning in stresses tend to retain duplicates after waves of WGDs, and the coselected gene duplicates in many lineages may play critical roles during severe environmental stresses. Collectively, these results shed new light on the significant contribution of paleopolyploidy to plant adaptation during global environmental changes in the evolutionary history of angiosperms.

A Transcriptional Network Promotes Anthocyanin Biosynthesis in Tomato Flesh

Dietary anthocyanins are important health-promoting antioxidants that make a major contribution to the quality of fruits. It is intriguing that most tomato cultivars do not produce anthocyanins in fruit. However, the purple tomato variety Indigo Rose, which has the dominant Aft locus combined with the recessive atv locus from wild tomato species, exhibits light-dependent anthocyanin accumulation in the fruit skin. Here, we report that Aft encodes a functional anthocyanin activator named SlAN2-like, while atv encodes a nonfunctional version of the anthocyanin repressor SlMYBATV. The expression of SlAN2-like is responsive to light, and the functional SlAN2-like can activate the expression of both anthocyanin biosynthetic genes and their regulatory genes, suggesting that SlAN2-like acts as a master regulator in the activation of anthocyanin biosynthesis. We further showed that cultivated tomatoes contain nonfunctional alleles of SlAN2-like and therefore fail to produce anthocyanins. Consistently, expression of a functional SlAN2-like gene driven by the fruit-specific promoter in a tomato cultivar led to the activation of the entire anthocyanin biosynthesis pathway and high-level accumulation of anthocyanins in both the peel and flesh. Taken together, our study exemplifies that efficient engineering of complex metabolic pathways could be achieved through tissue-specific expression of master transcriptional regulators.