Transcriptome Reveals Allele Contribution to Heterosis in Maize

Abstract

Heterosis, which has greatly increased maize yields, is associated with gene expression patterns during key developmental stages that enhance hybrid phenotypes relative to parental phenotypes. Before heterosis can be more effectively used for crop improvement, hybrid maize developmental gene expression patterns must be better understood. Here, six maize hybrids, including the popular hybrid Zhengdan958 (ZC) from China, were studied. Maize hybrids created in-house were generated using an incomplete diallel cross (NCII)-based strategy from four elite inbred parental lines. Differential gene expression (DEG) profiles corresponding to three developmental stages revealed that hybrid partial expression patterns exhibited complementarity of expression of certain parental genes, with parental allelic expression patterns varying both qualitatively and quantitatively in hybrids. Single-parent expression (SPE) and parent-specific expression (PSE) types of qualitative variation were most prevalent, 43.73 and 41.07% of variation, respectively. Meanwhile, negative super-dominance (NSD) and positive super-dominance (PSD) types of quantitative variation were most prevalent, 31.06 and 24.30% of variation, respectively. During the early reproductive growth stage, the gene expression pattern differed markedly from other developmental stage patterns, with allelic expression patterns during seed development skewed toward low-value parental alleles in hybrid seeds exhibiting significant quantitative variation-associated superiority. Comparisons of qualitative gene expression variation rates between ZC and other hybrids revealed proportions of SPE-DEGs (41.36%) in ZC seed DEGs that significantly exceeded the average proportion of SPE-DEGs found in seeds of other hybrids (28.36%). Importantly, quantitative gene expression variation rate comparisons between ZC and hybrids, except for transgressive expression, revealed that the ZC rate exceeded the average rate for other hybrids, highlighting the importance of partial gene expression in heterosis. Moreover, enriched ZC DEGs exhibiting distinct tissue-specific expression patterns belonged to four biological pathways, including photosynthesis, plant hormone signal transduction, biology metabolism and biosynthesis. These results provide valuable technical insights for creating hybrids exhibiting strong heterosis.

Allele‐specific expression and chromatin accessibility contribute to heterosis in tea plants (Camellia sinensis)

“…ASE caused by sequence variation in the parental genomes greatly enhances the plasticity of hybrids, and can also better explain different genetic hypotheses (Botet & Keurentjes, 2020). For instance, the complementarity of the superior allele relative to the silent allele in maize hybrids could explain the dominant effect of heterosis (Paschold et al., 2012; Wu, et al., 2021a). Biallelic expression in hybrids that exceed two parents is a typical example to explain overdominance.…”

“…Therefore, the differential regulation of parental biallelic genes improves the plasticity of gene expression in hybrids, and enables them to exhibit a broader range of phenotypes and resistance capabilities (Botet & Keurentjes, 2020). However, high‐precision ASE is only systematically analyzed in a few plant species, such as Arabidopsis (Klosinska et al., 2016; Zhang & Borevitz, 2009), maize (Baldauf et al., 2020; Paschold et al., 2014; Waters et al., 2017; Wu, et al., 2021a; Zhu et al., 2022) and rice (Ma et al., 2021; Shao et al., 2019), due to the need for well‐assembled parental genomes. The contribution of ASE to heterosis in woody plants is currently unclear.…”

Natural variations of heterosis-related allele-specific expression genes in promoter regions lead to allele-specific expression in maize

“…ASEGs, varying in number and function among different organisms and conditions, play a crucial role in adapting to growth stages [ 17 , 45 , 46 ]. Maize, a typical C4 crop, is sensitive to light.…”