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Transcriptome analysis reveals the key role of overdominant expression of photosynthetic and respiration-related genes in the formation of tobacco(Nicotiana tabacum L.) biomass heterosis

ABSTRACT: Heterosis, a phenomenon where hybrids exhibit superior performance in various traits such as yield, quality, and resistance compared to their parents, has long been a focus of agricultural research. Although tobacco biomass significantly affects tobacco yield and economic profitability, the underlying reasons for the dominance of tobacco biomass hybrids and their formation remain unclear. To address this, we selected 5 tobacco varieties (lines) with large differences in tobacco biomass as the parents and formulated F1 hybrids to analyze the expression of tobacco biomass heterosis. Our findings demonstrate that tobacco leaf biomass exhibits a clear heterosis advantage. In particular, the hybrid Va116×GDH94 showed strong heterosis, with 76.69% of differentially expressed genes (DEGs) displaying Overdominant expression pattern. Notably, these Overdominant DEGs were significantly enriched in biological processes such as photosynthesis and respiration. During photosynthesis, transgressive up-regulation of Lhc improved light-harvesting efficiency, while the up-regulation of Psa and Psb in the photosystem enhanced the defense of chloroplasts against strong light. Additionally, the up-regulation of rbcl promoted the increase of photosynthetic products in the hybrids. During respiration, the down-regulation of MDH, ACO, and OGDH suppressed the tricarboxylic acid cycle (TCA cycle) and weakened respiratory consumption in the hybrids. Furthermore, we observed that the net photosynthetic rate and intercellular CO2 concentration of the hybrids were significantly higher than those of the parents. Taken together, our results suggest that the overdominant expression effect of DEGs plays a crucial role in the formation of tobacco biomass hybrid advantage. The overdominant expression effect of photosynthesis and respiration-related genes enhanced the photosynthetic capacity of the hybrids, reduced respiration consumption, and promoted the increase of tobacco biomass, thus demonstrating the obvious hybrid advantage.

ORGANISM(S): Nicotiana tabacum

PROVIDER: GSE252097 | GEO | 2024/01/01

REPOSITORIES: GEO

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Project description:Hybrid plants and animals grow larger and more vigorously than the parents, a common phenomenon known as hybrid vigor or heterosis. Heterosis often correlates with the genetic distance between hybridizing parents, but the mechanism for this is largely unknown. We found that genetic distance was correlated with natural variation of stress responses under the control of the circadian clock. CIRCADIAN-CLOCK-ASSOCIATED1 (CCA1) and LATE-ELONGATED-HYPOCOTYL (LHY) or CCA1 alone mediate expression amplitudes and periods of these stress-responsive genes in stress and non-stress conditions. In Arabidopsis thaliana intraspecific hybrids, genome-wide expression of many biotic and abiotic stress-responsive genes was diurnally repressed to promote biomass heterosis, which is associated with several biomass quantitative trait loci (QTLs). Expression differences in four selected stress-responsive genes among ten ecotypes could be used to predict heterosis in their hybrids. Parent plants with larger expression differences between stress-responsive genes produced higher-vigor hybrids, while those with smaller differences produced lower-vigor hybrids. Stress-responsive genes were epigenetically repressed in the hybrids under normal conditions but induced during times of stress at certain times of the day, balancing the tradeoff between stress responses and growth. Consistently, repressing the stress genes in diploids increased growth vigor. We demonstrate how hybrids manipulate diurnal stress-responsive gene expression to enhance growth vigor. Both circadian and epigenetic regulation play key roles in the altered expression of stress-responsive genes in hybrids. Our findings provide a conceptual advance and mechanistic understanding of heterosis, as well as selection criteria for parents to be effectively used for producing high-yield hybrids. Examination of gene expression in Arabidopsis thaliana F1 hybrids between Col and C24 and 3 time points using mRNA-seq

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Transcriptome analysis reveals the key role of overdominant expression of photosynthetic and respiration-related genes in the formation of tobacco(Nicotiana tabacum L.) biomass heterosis

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