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Combined population transcriptomic and genomic analysis reveals cis-regulatory differentiation of non-coding RNAs in maize

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Abstract

Key message

Long intergenic non-coding RNA (lincRNA), cis-acting expression quantitative trait locus (cis-eQTL), maize, regulatory evolution.

Abstract

The law of genetic variation during domestication explains the evolutionary mechanism and provides a theoretical basis for improving existing varieties of maize. Previous studies focused on exploiting regulatory variations controlling the expression of protein-coding genes rather than of non-protein-coding genes. Here, we examined the genetic and evolutionary features of long non-coding RNAs from intergenic regions (long intergenic non-coding RNAs, lincRNAs) using population-scale transcriptome data and identified 1168 lincRNAs with cis-acting expression quantitative trait loci (cis-eQTLs). We found that lincRNAs are more likely to be regulated by cis-eQTLs, which exert stronger effects than the protein-coding genes. During maize domestication and improvement, upregulated alleles of lincRNAs, which originated from both standing variation and new mutation, accumulate more frequently and show larger effect sizes than the coding genes. A stronger signature of genetic differentiation was observed in their regulatory regions compared to those of randomly sampled lincRNAs. In addition, we found that cis-regulatory differentiation of lincRNAs is related to the sequence conservation of lincRNA transcripts. Non-conserved lincRNAs more tend to gain upregulated alleles and show a stronger relationship with selected traits than conserved lincRNAs between maize and its wild relatives. Our findings in maize improve the understanding of cis-regulatory variation in lincRNA genes during domestication and improvement and provide an effective approach for prioritizing candidates for further investigation.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31571683), the Modern Agro-Industry Technology Research System of Maize (CARS-02-13), the Yazhou Bay Seed Lab (JBGS+B21HJ0221), and the Agricultural Science and Technology Innovation Program of CAAS. We would like to thank Lingjie Yin (ICS-CAAS bioinformatics group) for providing computing support. We thank Editage (www.editage.cn) for English language editing.

Funding

This work was supported by the National Natural Science Foundation of China (31571683), the Modern Agro-Industry Technology Research System of Maize (CARS-02–13), and the Agricultural Science and Technology Innovation Program of CAAS.

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Contributions

Conceptualization was done by JF, JL, and Y-XL; methodology was done by JF and XZ; formal analysis was done by J-WL, S-HZ, JZ, CH, and XW; validation was done by J-WL, YC, ZW, and SZ; investigation was done by J-WL, JF, XZ, and RG; resources were done by LL, GW, and JW; writing—original draft preparation were done by J-WL; writing—review and editing were done by JF, XZ, YX, and RG; visualization was done by J-WL and S-HZ; project administration was done by JF; funding acquisition was done by JF. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Riliang Gu, Xiaoming Zheng or Junjie Fu.

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The authors have no relevant financial or non-financial interests to disclose.

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Communicated by Thomas Lubberstedt.

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Lu, J., Zhen, S., Zhang, J. et al. Combined population transcriptomic and genomic analysis reveals cis-regulatory differentiation of non-coding RNAs in maize. Theor Appl Genet 136, 16 (2023). https://doi.org/10.1007/s00122-023-04293-2

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  • DOI: https://doi.org/10.1007/s00122-023-04293-2

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