Gene regulatory effects of a large chromosomal inversion in highland maize

Abstract

Chromosomal inversions play an important role in local adaptation. Inversions can capture multiple locally adaptive functional variants in a linked block by repressing recombination. However, this recombination suppression makes it difficult to identify the genetic mechanisms that underlie an inversion's role in adaption.In this study, we explore how large-scale transcriptomic data can be used to dissect the functional importance of a 13 Mb inversion locus (Inv4m) found almost exclusively in highland populations of maize (Zea mays ssp. mays). Inv4m introgressed into highland maize from the wild relative Zea mays ssp.mexicana, also present in the highlands of Mexico, and is thought to be important for the adaptation of these populations to cultivation in highland environments. First, using a large publicly available association mapping panel, we confirmed that Inv4m is associated with locally adaptive agronomic phenotypes, but only in highland fields. Second, we created two families segregating for standard and inverted haplotypess of Inv4m in a isogenic B73 background, and measured gene expression variation association with Inv4m across 9 tissues in two experimental conditions. With these data, we quantified both the global transcriptomic effects of the highland Inv4m haplotype, and the local cis-regulatory variation present within the locus. We 1/33 found diverse physiological effects of Inv4m, and speculate that the genetic basis of its effects on adaptive traits is distributed across many separate functional variants. Author SummaryChromosomal inversions are an important type of genomic structural variant. However, mapping causal alleles within their boundaries is difficult because inversions suppress recombination between homologous chromosomes. This means that inversions, regardless of their size, are inherited as a unit. We leveraged the high-dimensional phenotype of gene expression as a tool to study the genetics of a large chromosomal inversion found in highland maize populations in Mexico -Inv4m. We grew plants carrying multiple versions of Inv4m in a common genetic background, and quantified the transcriptional reprogramming induced by alternative alleles at the locus. Inv4m has been shown in previous studies to have a large effect on flowering, but we show that the functional variation within Inv4m affects many developmental and physiological processes.Chromosomal inversions are structural rearrangements that form when a portion of a chromosome breaks in 2 two places and reinserts in the opposite orientation. The reversed order of loci prevent recombination with 3 the non-inverted homologous chromosome, as crossover products are imbalanced and often non-viable [1]. 4This spontaneous, long-distance genetic linkage is important for speciation and local adaptation because it 5 can capture multiple adaptive and potentially interacting loci in a single haplotype [2][3][4]. Inversions are 6 common across taxa [1], often pre-date speciation events, and can spread through admixture [5,6]. They 7 have been link...

An adaptive teosintemexicanaintrogression modulates phosphatidylcholine levels and is associated with maize flowering time

“…The effects of genetic variation at HPC1 on flowering time in Mexican landraces indicated a strong GxE interaction, whereby the highland allele leads to an acceleration of flowering and ASI in highland environments (Figure 4), similar to the effects observed with the well-known teosinte mexicana introgression inv4m (18). Other flowering time loci analyzed did not show this clear G x E effect (20).…”

“…RNA-seq libraries were constructed, sequenced, and analyzed following (18). Briefly, randomly primed, strand specific, mRNA-seq libraries were constructed using the BRaD-seq (92) protocol.…”

Selective sorting of ancestral introgression in maize and teosinte along an elevational cline

“…Additionally, we identify outlier loci across the genome where mexicana ancestry forms steep clines across elevation (Fig 7). Our top candidate for strong associations between introgression and elevation in maize is Inv4m, a large 14 Mb inversion on chromosome 4 previously identified to have introgressed into high elevation maize landraces [15,34,42,105]. This inversion maintains steep elevational clines within teosintes [79], overlaps QTLs for leaf pigmentation [49] and macrohairs [49], and is associated with increased yield in maize at high elevations and decreased yield at low elevations [15], but has thus far eluded functional characterization of genes within the inversion [15].…”

A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)

“…Second, breakpoints may change the relative positions of genes and their transcription regulators, changing expression patterns [22, 23]. Third, the linked variation within an inversion can contain cis or trans acting regulatory elements that can evolve independently in the two arrangements due to suppressed recombination between them [16, 24–26]. As variants within inversions are highly linked, it is difficult to distinguish between cis regulation and trans -acting loci in linkage disequilibrium with their targets.…”

“…Additionally, the reduced recombination and effective population size within the inverted region facilitates the accumulation of neutral and deleterious variation [15], increasing divergence between the arrangements and increasing the likelihood of detecting phenotype or environment associations with non-causative loci. Finally, larger inversions, such as the lnv4m inversion in Zea mays, may contain hundreds of genes that affect a wide variety of phenotypes that vary in their selective pressures [16].…”