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Transcriptomic analysis reveals overdominance playing a critical role in nicotine heterosis in Nicotiana tabacum L.

ABSTRACT: BACKGROUND:As a unique biological phenomenon, heterosis has been concerned with the superior performance of the heterosis than either parents. Despite several F1 hybrids, containing supernal nicotine content, had been discovered and applied to heterosis utilization in Nicotiana tabacum L., nevertheless, the potential molecular mechanism revealing nicotine heterosis has not been illustrated clearly. RESULT:Phenotypically, the F1 hybrids (Vall6?×?Basma) show prominent heterosis in nicotine content by 3 years of field experiments. Transcriptome analysis revealed that genes participating in nicotine anabolism (ADC, PMT, MPO, QPT, AO, QS, QPT, A622, BBLs) and nicotine transport (JAT2, MATE1 and 2, NUP1 and 2) showed an upregulated expression in the hybrid, a majority of which demonstrated an overdominant performance. RT-PCR confirmed that nicotine anabolism was induced in the hybrid. CONCLUSIONS:These findings strongly suggest that nicotine synthesis and transport efficiency improved in hybrid and overdominance at gene-expression level played a critical role in heterosis of nicotine metabolism.

SUBMITTER: Tian M

PROVIDER: S-EPMC5863848 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Transcriptomic analysis reveals overdominance playing a critical role in nicotine heterosis in Nicotiana tabacum L.

Tian Maozhu M Nie Qiong Q Li Zhenhua Z Zhang Jie J Liu Yiling Y Long Yao Y Wang Zhiwei Z Wang Guoqing G Liu Renxiang R

BMC plant biology 20180322 1

<h4>Background</h4>As a unique biological phenomenon, heterosis has been concerned with the superior performance of the heterosis than either parents. Despite several F1 hybrids, containing supernal nicotine content, had been discovered and applied to heterosis utilization in Nicotiana tabacum L., nevertheless, the potential molecular mechanism revealing nicotine heterosis has not been illustrated clearly.<h4>Result</h4>Phenotypically, the F1 hybrids (Vall6 × Basma) show prominent heterosis in n ...[more]

PMID: 29566653

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Project description: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.

Project description:BACKGROUND:Non-coding RNAs (ncRNAs), including microRNAs (miRNAs), long ncRNAs (lncRNAs) and circular RNAs (circRNAs), accomplish remarkable variety of biological functions. However, the composition of ncRNAs and their interactions with coding RNAs in modulating and controlling of cellular process in plants is largely unknown. Using a diverse group of high-throughput sequencing strategies, the mRNA, miRNA, lncRNA and circRNA compositions of tobacco (Nicotiana tabacum) roots determined and their alteration and potential biological functions in response to topping treatment analyzed. RESULTS:A total of 688 miRNAs, 7423 non-redundant lncRNAs and 12,414 circRNAs were identified, among which, some selected differentially expressed RNAs were verified by quantitative real-time PCR. Using the differentially expressed RNAs, a co-expression network was established that included all four types of RNAs. The number of circRNAs identified were higher than that of miRNAs and lncRNAs, but only two circRNAs were present in the co-expression network. LncRNAs appear to be the most active ncRNAs based on their numbers presented in the co-expression network, but none of them seems to be an eTM (endogenous Target Mimicry) of miRNAs. Integrated with analyses of sequence interaction, several mRNA-circRNA-miRNA interaction networks with a potential role in the regulation of nicotine biosynthesis were uncovered, including a QS-circQS-miR6024 interaction network. In this network miR6024 was significantly down-regulated, while the expression levels of its two targets, circQS and its host gene QS, were sharply increased following the topping treatment. CONCLUSIONS:These results illustrated the transcriptomic profiles of tobacco roots, the organ responsible for nicotine biosynthesis. mRNAs always play the most important roles, while ncRNAs are also expressed extensively for topping treatment response, especially circRNAs are the most activated in the ncRNA pool. These studies also provided insights on the coordinated regulation module of coding and non-coding RNAs in a single plant biological sample. The findings reported here indicate that ncRNAs appear to form interaction complex for the regulation of stress response forming regulation networks with transcripts involved in nicotine biosynthesis in tobacco.

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Transcriptomic analysis reveals overdominance playing a critical role in nicotine heterosis in Nicotiana tabacum L.

Publications

Transcriptomic analysis reveals overdominance playing a critical role in nicotine heterosis in Nicotiana tabacum L.

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