Evolution of a Novel Phenolic Pathway for Pollen Development

• Published in: Science (American Association for the Advancement of Science) Vol. 325; no. 5948; pp. 1688 - 1692
• Main Authors: Matsuno,, Michiyo, Compagnon, Vincent, Schoch, Guillaume A, Schmitt, Martine, Debayle, Delphine, Bassard, Jean-Etienne, Pollet, Brigitte, Hehn, Alain, Heintz, Dimitri, Ullmann, Pascaline, Lapierre, Catherine, Bernier, François, Ehlting, Jürgen, Werck-Reichhart, Danièle
• Format: Journal Article
• Language: English
• Published: Washington, DC American Association for the Advancement of Science 25.09.2009; The American Association for the Advancement of Science; American Association for the Advancement of Science (AAAS)
• Subjects: Amino acids; Anthers; Arabidopsis - genetics; Arabidopsis - metabolism; Base Sequence; Biological and medical sciences; Brassica napus - genetics; Brassica napus - growth & development; Brassica napus - metabolism; Brassicaceae; Brassicaceae - genetics; Brassicaceae - growth & development; Brassicaceae - metabolism; Cellular Biology; Classical genetics, quantitative genetics, hybrids; cytochrome P-450; Cytochrome P-450 Enzyme System - chemistry; Cytochrome P-450 Enzyme System - genetics; Cytochrome P-450 Enzyme System - metabolism; Darwinism; Enzymes; Evolution; Evolution, Molecular; Evolutionary biology; Flower buds; Fundamental and applied biological sciences. Psychology; Gene Duplication; Genes; Genetics of eukaryotes. Biological and molecular evolution; Hydroxylation; Life Sciences; Metabolic Networks and Pathways; metabolism; Methylation; Models, Molecular; Molecular Sequence Data; Phenols; plant adaptation; Plant biology; Plant Proteins - chemistry; Plant Proteins - genetics; Plant Proteins - metabolism; Plants; Pollen; Pollen - growth & development; Pollen - metabolism; Positive selection; Pteridophyta, spermatophyta; Retroelements; RNA Interference; Selection, Genetic; Speciation; Spermidine - analogs & derivatives; Spermidine - metabolism; Vegetals; Duplication; Hydroxylation; Enzyme; Cytochrome P450; Molecular evolution; Gene; Cruciferae; Dicotyledones; Angiospermae; Development; Multigene family; Spermatophyta; Pollen; Speciation; Adaptation
• ISSN: 0036-8075; 1095-9203; 1095-9203
• DOI: 10.1126/science.1174095

Metabolic plasticity, which largely relies on the creation of new genes, is an essential feature of plant adaptation and speciation and has led to the evolution of large gene families. A typical example is provided by the diversification of the cytochrome P450 enzymes in plants. We describe here a retroposition, neofunctionalization, and duplication sequence that, via selective and local amino acid replacement, led to the evolution of a novel phenolic pathway in Brassicaceae. This pathway involves a cascade of six successive hydroxylations by two partially redundant cytochromes P450, leading to the formation of N¹,N⁵-di(hydroxyferuloyl)-N¹⁰-sinapoylspermidine, a major pollen constituent and so-far-overlooked player in phenylpropanoid metabolism. This example shows how positive Darwinian selection can favor structured clusters of nonsynonymous substitutions that are needed for the transition of enzymes to new functions.