Inherited proliferation states organize plant transcriptomes

A central question in plant biology is whether natural transcriptome variation primarily reflects environmental adaptation or intrinsic genetic programs. Using transcriptomes from 665 natural Arabidopsis thaliana accessions, we show that inherited population structure, not environmental gradients, is the primary organizer of global transcriptome architecture. Genomic population structure uniquely explains 30.0% of transcriptome wide variation, while environmental variables account for only 2.5%. This architecture is dominated by a single co-expression program (proliferation Module Eigengene: prolifME), enriched for cell cycle regulation and ribosome biogenesis, regulated by a bipartite transcription factor architecture, and genetically encoded at discrete loci with broad trans regulatory effects. This proliferation program is associated with reduced plant size, biomass, growth rate and water use efficiency, and these relationships persist under common garden conditions. Gene contributions to this proliferation program are non randomly conserved in rice and maize across 150~200 million years of divergence. These findings identify an intrinsic transcriptional proliferation program as a primary state of plant population transcriptomes, conserved across plant species.