Nicolas Antoine, Papadopoulos Panagiotis, Caroulle Mattéo, Adroher Bernard, Chelysheva Liudmila, Goussot Magali, Sarthou Anne-Sophie, Arnaud Nicolas, Maugarny Aude, Laufs Patrick
Université Paris-Saclay, INRAE, AgroParisTech, Institute Jean-Pierre Bourgin for Plant Sciences (IJPB), Versailles, 78000, France.
Université Paris-Saclay, Orsay, 91405, France.
Plant J. 2025 Jul;123(1):e70321. doi: 10.1111/tpj.70321.
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.
基因调控网络（GRNs）在调节发育过程中发挥着重要作用，其在不同物种间的调控是进化创新的主要来源。然而，对于单个物种内不同器官之间基因调控网络是如何重新布线的，我们仍知之甚少。这个问题对于多效性基因尤为重要，多效性基因可能表现出器官特异性的基因调控网络调节，这可能反映了它们多样的功能。为了解决这个问题，我们研究了类NGATHA（NGAL）基因，将其作为多效性基因的一个模型，该基因通过涉及杯状子叶（CUC）和KLUH（KLU）基因的两条不同途径来调节拟南芥多个器官的生长或模式形成。通过将遗传分析与基因表达特征相结合，我们发现了NGAL/CUC/KLU调控模块存在显著的器官特异性重新布线。例如，NGAL基因对花瓣生长的调控是通过KLU途径实现的，而在茎生叶生长的调控中，KLU和CUC途径均在NGAL下游发挥作用。我们的研究结果表明，可能由发育限制引起的基因表达模式变化，在基因调控模块的器官特异性调节中起着关键作用。此外，分子和功能水平上的基因调控模块并不总是完美对齐，这可能是由于其他调控机制的影响。总之，我们的研究结果揭示了与多效性基因相关的基因调控网络存在显著调节。我们认为基因调控网络中的这种灵活性促进了基因多效性。
