Loss of CmMAIL2 compromises chloroplast function but permits developmental progression in melon

Plant mobile domain-containing (PMD-C) proteins have emerged as chromatin-associated regulators that stabilize gene expression during plant development. In Arabidopsis thaliana, disruption of PMD-C family members, including MAIN, MAIL1 and MAIL2, causes severe developmental defects, leading to the view that these proteins are broadly indispensable. However, the developmental consequences of complete MAIL2 loss in crop species remain unclear. Here, we identify and characterize a melon (Cucumis melo) mutant carrying a 6.6-kb genomic deletion that completely removes the CmMAIL2 locus. Despite severe and systemic chloroplast dysfunction, manifested as impaired photosynthetic performance and disrupted thylakoid organization, mutant plants retained substantial post-embryonic developmental progression and produced fertile fruits and viable seeds under field conditions. Transcriptome profiling revealed extensive transcriptional reprogramming, characterized by upregulation of plastid- and thylakoid-associated genes and coordinated repression of extracellular, cell wall-related, iron-dependent, and cytoskeleton-associated pathways. Subcellular localization analyses revealed that melon CmMAIL2 localizes predominantly to the nucleus, supporting an indirect role in regulating chloroplast function through nuclear gene expression. Together, our findings demonstrate that loss of CmMAIL2 compromises chloroplast function but does not abolish developmental progression in melon. This study reveals a previously unrecognized degree of developmental robustness in a crop species lacking MAIL2 and highlights the species-dependent consequences of disrupting PMD-C-mediated chromatin regulation.