Developmental rewiring of the NGAL/CUC/KLU network associated with pleiotropic roles of NGAL genes

Abstract

Gene regulatory networks (GRNs) play prominent roles in regulating developmental processes, and their modulation across species is a major source for evolutionary innovation. However, it remains poorly understood how GRNs are rewired between different organs within a single species. This question is particularly relevant for pleiotropic genes, which may exhibit organ-specific GRN modulations potentially reflecting their diverse functions. To address this, we investigated the NGATHA-like (NGAL) genes as a model for pleiotropic genes that regulate growth or patterning in multiple Arabidopsis organs via two distinct pathways involving the CUP-SHAPED COTYLEDON (CUC) and KLUH (KLU) genes. By combining genetic analysis with gene expression characterization, we uncovered significant organ-specific rewiring of the NGAL/CUC/KLU regulatory module. For instance, the regulation of growth by NGAL genes occurs through the KLU pathway in petals, while both the KLU and CUC pathways function downstream of NGAL to regulate cauline leaf growth. Our findings highlight that changes in gene expression patterns, potentially arising from developmental constraints, play a pivotal role in the organ-specific modulation of gene regulatory modules. Furthermore, gene regulatory modules at the molecular and functional levels do not always align perfectly, potentially due to the influence of additional regulatory mechanisms. Altogether, our findings reveal significant modulation of the GRNs associated with pleiotropic genes. We propose that this flexibility in GRNs facilitates gene pleiotropy.