The teosinte mexicana chromosomal inversion Inv4m modulates maize flowering time, plant height, and growth regulation gene networks

Abstract

Chromosomal inversions facilitate local adaptation by maintaining co-adapted allele complexes as a single inherited unit, but the genes driving their phenotypic effects are rarely identified. Inv4m is an inversion from the highland teosinte Zea mays ssp. mexicana that is nearly fixed at 2500 masl in Mexican traditional varieties but absent in temperate maize. While association studies link Inv4m to flowering time, its key adaptive trait, the mechanisms connecting it to this phenotype remain unknown. Here, we generate near isogenic lines by introgressing the highland Michoacan 21 (Mi21) Inv4m haplotype into temperate B73 through eight backcross generations. We assemble the Inv4m-Mi21 NIL genome and, aligning to three Zea reference genomes, provide the first precise delimitation of Inv4m, a 15.2 Mb region with breakpoints overlapping knob repeat arrays. In field trials across Pennsylvania and North Carolina, Inv4m consistently accelerated flowering, whereas its plant height effect reversed sign between regions, a genotype by environment interaction consistent with environment-dependent fitness. Using RNA-seq, we identify 465 differentially expressed genes, the strongest from a cluster of JUMONJI histone demethylases (JMJ). Comparing five Zea genomes, the B73 reference carries a lineage-specific tandem expansion of five JMJ paralogs while highland genotypes carrying Inv4m retain a single ancestral copy, a difference that accounts for most of the clusters differential expression. We then show Inv4m disrupts growth related coexpression modules, with the JMJ cluster losing connectivity, and traced a trans regulatory network linking it to cell proliferation genes including pcna2 and sec6. In summary, we identify candidate genes and networks underlying Inv4ms effects and propose that part of this inversions adaptive value may reside in a dosage-sensitive regulator whose action propagates through a downstream network of genes that are involved in growth and flowering and are important for highland adaptation. Recombination suppression may thus protect a co-adapted regulatory architecture rather than independent alleles alone. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=194 HEIGHT=200 SRC="FIGDIR/small/732082v1_ufig1.gif" ALT="Figure 1"> View larger version (106K): org.highwire.dtl.DTLVardef@85400org.highwire.dtl.DTLVardef@c2f820org.highwire.dtl.DTLVardef@301c0aorg.highwire.dtl.DTLVardef@80e715_HPS_FORMAT_FIGEXP M_FIG C_FIG