Hybrids reveal accessible chromatin trans genetic associations

Abstract

Crosses between genetically distant Zea mays (Maize) inbreds cause hybrid vigour (heterosis): an over-dominant increase in vegetative growth and grain yield. Although the contributing loci are unknown, heterosis strength varies polygenically, with crosses between stiff stalk and non-stiff stalk lineages often producing the highly heterotic F1 seed used for agriculture. As F1 genomes conserve the parental cis-regulatory state, F1 trans-interactions between haplotypes underpin F1 trait over-dominance and heterotic gene expression. Gene expression relies upon transcription factors binding cis-regulatory elements in accessible chromatin regions (ACRs) and recruiting RNA POLYMERASE II. Here, assay for transposase accessible chromatin sequencing (ATAC-seq) examined cis-regulatory element chromatin accessibility inheritance in three different F1 parent-offspring pairs, including a representative stiff stalk-by-non-stiff stalk (B73xOh43) cross. Using concatenated reference alignment, we categorized ACR modes of inheritance (additive, dominant, under/over-dominant), revealing that ACRs are largely inherited additively, and, concordantly, that chromatin accessibility has strong narrow-sense heritability. However, mirroring other heterotic phenotypes, the B73xOh43 cross exhibited the most dominant and over-dominant inheritance. Comparing allele-specific parent-to-offspring chromatin accessibility, we identified F1 differentially trans-regulated ACRs. Using a matched chromatin accessible diversity panel, we found B73xOh43 SNPs with more ACR trans-associations than expected due to chance. These trans-regulatory variants revealed how cell-division and anabolism are elevated in heterotic F1 seedlings. This multiple discovery filtering (MDF) approach to trans-regulatory variant detection is genomic modality agnostic and stands to empower trans-relationship dissection in diverse genetic models.