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Integration of rhythmic metabolome and transcriptome provides insights into the transmission of rhythmic fluctuations and temporal diversity of metabolism in rice

Abstract

Various aspects of the organisms adapt to cyclically changing environmental conditions via transcriptional regulation. However, the role of rhythmicity in altering the global aspects of metabolism is poorly characterized. Here, we subjected four rice (Oryza sativa) varieties to a range of metabolic profiles and RNA-seq to investigate the temporal relationships of rhythm between transcription and metabolism. More than 40% of the rhythmic genes and a quarter of metabolites conservatively oscillated across four rice accessions. Compared with the metabolome, the transcriptome was more strongly regulated by rhythm; however, the rhythm of metabolites had an obvious opposite trend between day and night. Through association analysis, the time delay of rhythmic transmission from the transcript to the metabolite level was ∼4 h under long-day conditions, although the transmission was nearly synchronous for carbohydrate and nucleotide metabolism. The rhythmic accumulation of metabolites maintained highly coordinated temporal relationships in the metabolic network, whereas the correlation of some rhythmic metabolites, such as branched-chain amino acids (BCAAs), was significantly different intervariety. We further demonstrated that the cumulative diversity of BCAAs was due to the differential expression of branched-chain aminotransferase 2 at dawn. Our research reveals the flexible pattern of rice metabolic rhythm existing with conservation and diversity.

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Acknowledgements

This work was supported by the Hainan Major Science and Technology Project (ZDKJ202002), the State Key Program of National Natural Science Foundation of China (31530052), the Key Research and Development Program of Hainan (ZDYF2020066), the Hainan Academician Innovation Platform (HD-YSZX-202003 and HD-YSZX-202004), and the Hainan University Startup Fund (KYQD(ZR)1866).

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Correspondence to Jie Luo.

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11427_2021_2064_MOESM1_ESM.pdf

Integration of rhythmic metabolome and transcriptome provides insight into the transmission of rhythm fluctuations and temporal diversity of metabolism in rice

Table S1. The scheduled MRM transitions for widely targeted metabolite analysis in leaf of rice (Oryza sativa L.) varieties.

Table S2. The rhythm of metabolites and log2-transformed relative content in four rice accessions.

Table S3. The KEGG enrichment of CRMs in four rice accessions.

Table S4. The rhythm of genes and FPKM of RNA-seq of four rice accessions.

Table S5. KEGG enrichment of CRGs in four rice accessions.

Table S6. KEGG enrichment of rhythmic genes in the rhythm module.

Table S7. Positive correlated rhythmic metabolites corresponding to gene modules

Table S8. Temporal correlation of CRMs among different rice accessions

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Zhou, J., Liu, C., Chen, Q. et al. Integration of rhythmic metabolome and transcriptome provides insights into the transmission of rhythmic fluctuations and temporal diversity of metabolism in rice. Sci. China Life Sci. 65, 1794–1810 (2022). https://doi.org/10.1007/s11427-021-2064-7

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  • DOI: https://doi.org/10.1007/s11427-021-2064-7

Keywords

  • Oryza sativa
  • diurnal cycle
  • metabolome
  • time delay
  • rhythmic diversity