Maternal organellar inheritance and cytosine patterning shape salinity responses in rice hybrids: a multi‐omics perspective

SUMMARY Maternally inherited extranuclear genomes (ptDNA and mtDNA) and epigenetic mechanisms are known to affect offspring phenotypes; nevertheless, their integrated function in stress adaptation remains incompletely understood. Classical breeding strategies have mostly ignored these non‐Mendelian influences by focusing exclusively on nuclear genome inheritance. We developed reciprocal rice hybrids from selected salt‐tolerant and salt‐sensitive progenitors and utilized a multi‐omics strategy—comprising whole‐genome sequencing, WGS‐derived cytosine content profiling, transcriptomics, and phenotypic evaluations—to understand the maternal contribution to salinity tolerance of rice offspring. Despite sharing a broadly biparental nuclear genetic background, maternal‐tolerant rice hybrids demonstrated improved performance, including better growth, photosynthesis, ion homeostasis, and yield relative to maternal‐sensitive rice hybrids under salinity stress. Organellar genome sequencing revealed predominantly maternal inheritance. Cytosine profiling indicated CpG and CHG content similarity to the maternal genotype. Transcriptomic data revealed maternal‐aligned expression of stress‐responsive and organelle‐associated genes, consistent with enhanced performance in maternal‐tolerant hybrids. Our results from a multi‐omics approach support a strong association between maternal cytoplasmic inheritance and differential stress responses in rice hybrids. This non‐Mendelian model of stress tolerance, informed by multi‐omics integration, provides innovative insights into maternal regulation of stress resilience in rice and proposes an effective strategy for breeding salt‐tolerant crops in climate‐challenged areas.