Production of viable progeny from interploid crosses requires precise regulation of gene expression from maternal and paternal chromosomes, yet the transcripts contributed to hybrid seeds from polyploid parent species have rarely been explored. To investigate the genome-wide maternal and paternal contributions to polyploid grain development, we analyzed the transcriptomes of developing embryos, from zygote to maturity, alongside endosperm in two stages of development, using reciprocal crosses between tetraploid and hexaploid wheats. Reciprocal crosses between species with varied levels of ploidy displayed broad impacts on gene expression, including shifts in alternative splicing events in select crosses, as illustrated by active splicing events, enhanced protein synthesis and chromatin remodeling. Homoeologous gene expression was repressed on the univalent D genome in pentaploids, but this suppression was attenuated in crosses with a higher ploidy maternal parent. Imprinted genes were identified in endosperm and early embryo tissues, supporting predominant maternal effects on early embryogenesis. By systematically investigating the complex transcriptional networks in reciprocal-cross hybrids, this study presents a framework for understanding the genomic incompatibility and transcriptome shock that results from interspecific hybridization and uncovers the transcriptional impacts on hybrid seeds created from agriculturally-relevant polyploid species.
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