Transcription Factors Evolve Faster Than Their Structural Gene Targets in the Flavonoid Pigment Pathway

Author:

Wheeler Lucas C1ORCID,Walker Joseph F23,Ng Julienne1,Deanna Rocío14,Dunbar-Wallis Amy1,Backes Alice5,Pezzi Pedro H5,Palchetti M Virginia4,Robertson Holly M2,Monaghan Andrew6,de Freitas Loreta Brandão5,Barboza Gloria E47,Moyroud Edwige2ORCID,Smith Stacey D1ORCID

Affiliation:

1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA

2. Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom

3. Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL, USA

4. Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET and Universidad Nacional de Córdoba, Córdoba, Argentina

5. Laboratory of Molecular Evolution, Department of Genetics, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

6. Research Computing, University of Colorado, Boulder, CO, USA

7. Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Haya de la Torre y Medina Allende, Córdoba, Argentina

Abstract

Abstract Dissecting the relationship between gene function and substitution rates is key to understanding genome-wide patterns of molecular evolution. Biochemical pathways provide powerful systems for investigating this relationship because the functional role of each gene is often well characterized. Here, we investigate the evolution of the flavonoid pigment pathway in the colorful Petunieae clade of the tomato family (Solanaceae). This pathway is broadly conserved in plants, both in terms of its structural elements and its MYB, basic helix–loop–helix, and WD40 transcriptional regulators, and its function has been extensively studied, particularly in model species of petunia. We built a phylotranscriptomic data set for 69 species of Petunieae to infer patterns of molecular evolution across pathway genes and across lineages. We found that transcription factors exhibit faster rates of molecular evolution (dN/dS) than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative data set to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions, although expression levels do predict molecular evolutionary rates. Although shifts in floral pigmentation were only weakly related to changes affecting coding regions, we found a strong relationship with the presence/absence patterns of MYB transcripts. Intensely pigmented species express all three main MYB anthocyanin activators in petals, whereas pale or white species express few or none. Our findings reinforce the notion that pathway regulators have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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