Local adaptation of a species involves the selection of adaptive alleles that confer a fitness advantage in their local environment. Inversions prevent recombination between the standard and inverted heterozygous hybrids. Inversions can play a crucial role in local adaptation by locking together a set of co-adapted alleles, acting as supergenes. Inv4m is a 13 Mb inversion in maize prevalent in highland maize and highland wild relatives from Mexico. Maize from the highlands of the Trans-Mexican volcanic belt has been shown to be well-adapted to volcanic, acidic soils with low phosphorus availability. Inv4m carries several genes involved in P acquisition and utilization. We therefore tested the hypothesis that Inv4m contributes to maize adaptation to these environments through enhanced phosphorus acquisition or utilization. Alternatively, Inv4m possible adaptive value may operate through constitutive developmental effects independent of nutrient stress responses. To test this hypothesis, we introgressed a highland maize variety from the highlands of Michoacan, Mexico, carrying Inv4m into the temperate line B73 and developed Near-Introgression Lines (NILs) carrying Inv4m. We then grew NILs carrying the inversion and controls without it in soils with different phosphorus levels and evaluated the fitness effects of the inversion, as well as changes in gene expression using RNA-Seq. Our results show that P starvation elicits highly conserved transcriptomic, lipidomic, and ionomic responses, independently of the Inv4m inversion genotype. Therefore, phosphorus deficiency does not seem to be driving the adaptive value of Inv4m. Additionally, we observed a phosphorus modulated transcriptional gradient from the collar leaf downward, characterized by a decrease in the expression of photosynthesis genes and an increase in the expression of senescence-associated genes, corresponding to the positional onset and initial stages of sequential leaf senescence. Although the magnitude of the phosphorus response increased with leaf age, we did not observe significant interactions with Inv4m. Nonetheless, a small number of genotype-by-phosphorus interactions (three genes, all outside inversion boundaries) exceed statistical thresholds, likely reflecting residual flanking introgression rather than Inv4m effects per se. These exceptions may be linked to phenotypic variation in height and flowering, which is dependent on the Inv4m karyotype. Our results highlight the robustness of P starvation responses across inverted and non-inverted Inv4m genotypes and provide an entry point for dissecting outlier interactions of potential adaptive significance.
Rodriguez-Zapata, F., Locklear, R., Barnes, A. C., Tandukar, N., Perez-Limon, S., Perryman, M. G., Pineros, M. A., Ojeda-Rivera, J. O., Runcie, D., Sawers, R., Rellan-Alvarez, R.
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