Variations in regulatory sequences rewire gene networks that differentiate wild and cultivated rice for leaf development and photosynthesis

Abstract

A comprehensive understanding of gene regulatory networks and the key regulators underlying developmental and physiological progression along the leaf developmental gradient is crucial for optimizing photosynthetic competence. Comparisons of developmental and photosynthetic features across successive leaf developmental stages revealed pronounced differences between wild rice (Oryza australiensis) and three cultivated rice accessions. Global gene expression profiling identified three major transcriptional phases across leaf stages: a predominance of developmental genes at SAM+Pi (initiating primordia) and P3; genes for photosynthetic transition at P3 and P4; and enriched core photosynthetic genes at P4 and P5. O. australiensis showed a more prominent expression of developmental and photosynthetic genes than cultivated accessions across leaf stages. Multivariate analysis further supported a distinct transcriptional landscape in O. australiensis compared with cultivated accessions. Integration of gene expression with species-specific variations in regulatory sequences, derived from synteny-anchored orthology analysis, generated stage-resolved gene regulatory networks and identified key transcription factors (TFs) mediating the developmental and physiological progression. A cross-species comparison of TF-target regulatory networks revealed extensive stage- and accession-dependent rewiring of the regulatory networks of key TFs, with strong regulatory divergence in O. australiensis. Gene silencing of two candidate TFs, OsDOF8 and OsARID2, altered the rice photosynthetic competence with accession-specific effects. Taken together, the study highlights promoter-driven regulatory divergence as a potential mechanism underlying developmental and photosynthetic differences among the rice accessions. The resource is available through an interactive public database, Rice DEV-LEAF (https://nipgr.ac.in/DEV-LEAF/), enabling exploration of gene expression dynamics and regulatory networks across the rice leaf developmental gradient.