title: Deeply diverged alleles in the Arabidopsis AREB1 transcription factor drive genome-wide differences in transcriptional response to the environment.
abstract: Gene regulatory variation is an important driver of the evolution of physiological and developmental responses to the environment. The abscisic acid (ABA) signaling pathway has long been studied as a key component of the cellular response to abiotic stresses in plants. We identify two haplotypes in an Arabidopsis thaliana transcription factor, AREB1, which plays a central role in ABA-mediated response to osmotic stress. These two haplotypes show the sequence signature of long-term maintenance of genetic diversity, suggesting a role for a diversifying selection process such as balancing selection. We find that the two haplotypes, distinguished by a large number of single nucleotide polymorphisms and the presence or absence of four small insertion/deletions in AREB1 intron 1 and exon 2, are at roughly equal frequencies in Arabidopsis, and show high linkage disequilibrium and deep sequence divergence. We use a transgenic approach, along with mRNA Sequencing-based assay of genome-wide expression levels, and find considerable functional divergence between alleles representing the two haplotype groups. Specifically, we find that, under benign soil-water conditions, transgenic lines containing different AREB1 alleles differ in the expression of a large number of genes associated with pathogen response. There are relatively modest gene expression differences between the two transgenic lines under restricted soil water content. Our finding of pathogen-related activity expands the known roles of AREB1 in A. thaliana and reveals the molecular basis of gene-by-environment interaction in a putatively adaptive plant regulatory protein.
authors.affiliation: Department of Integrative Biology and Institute for Cellular and Molecular Biology, The University of Texas at Austin desmarais@fas.harvard.edu tjuenger@austin.texas.edu.
authors.forename: David L
authors.initials: DL
authors.lastname: Des Marais
authors.affiliation: Department of Integrative Biology and Institute for Cellular and Molecular Biology, The University of Texas at Austin.
authors.forename: Wesley D
authors.initials: WD
authors.lastname: Skillern
authors.affiliation: Department of Integrative Biology and Institute for Cellular and Molecular Biology, The University of Texas at Austin desmarais@fas.harvard.edu tjuenger@austin.texas.edu.
authors.forename: Thomas E
authors.initials: TE
authors.lastname: Juenger
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000502:physiology; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000502:physiology; D050976:Basic-Leucine Zipper Transcription Factors / Q000235:genetics* / Q000502:physiology; D055864:Droughts; D018506:Gene Expression Regulation, Plant; D059647:Gene-Environment Interaction; D006239:Haplotypes; D011110:Polymorphism, Genetic; D013312:Stress, Physiological / Q000235:genetics*; D059467:Transcriptome
chemical_list: D029681:Arabidopsis Proteins; D050976:Basic-Leucine Zipper Transcription Factors; C508877:At1g45249 protein, Arabidopsis
keywords: abscisic acid; balancing selection; gene expression; gene-by-environment interaction; signaling network