Have Ancient Genome Duplications Contributed to Novel Trait Evolution in the Brassicales?

Ancient whole genome duplication (WGD), or paleopolyploidy, and subsequent gene and pathway divergence have likely played profound roles in generating the complexity of life on earth. However, we have limited examples of how particular ecological relevant traits have evolved as a consequence of paleopolyploidy. We illustrate the link between WGDs and key-trait evolution by investigating the glucosinolate defense pathway in the plant order Brassicales. The analysis of the Arabidopsis genome revealed evidence of three WGDs in the evolution of the Brassicaceae. The most recent event is called the At-α (alpha) and is unique to the Brassicaceae. The intermediate event is referred to as the At-ß (beta), which is shared with at least the Cleomaceae but is absent from Papaya within the Brassicales. The oldest is the At-γ (gamma) and is shared with all Rosid and potentially Asterid species. The major chemical defenses in the Brassicales are the sulfur- containing glucosinolates. Large differences in glucosinolate profiles exist with much of the variation due to four classes of amino acid precursors. Glucosinolates derived from Val, Ile, Leu, or Ala are aliphatic, those from Phe or Tyr are aromatic, and those from Trp are indole glucosinolates. The fourth class, the Met-derived glucosinolates, is unique sub-set of aliphatic glucosinolates to the most speciose family, the Brassicaceae. We provide chemical and molecular data supporting the hypothesis that the creation of the divergence of the glucosinolates is coupled to WGDs. Using the wealth of new and emerging Brassicales genomics data we are identifying homologs of key regulatory and enzymatic genes from the glucosinolate pathway. Ongoing molecular evolutionary and gene expression analysis support that retained duplicate copies of key genes has contributed to glucosinolate diversification, specifically that the appearance of the indole pathway coincides with the At-β event and that Met-derived compounds coincide with the At-α event of the Brassicaceae. Glucosinolates are known not only to have affects on insect herbivores, but also fungi, other plants and human health. Hence, our research should benefit ongoing and future efforts to alter glucosinolate profiles in Brassicales crop species.