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DNA methylome analysis provides insights into gene regulatory mechanism for better performance of rice under fluctuating environmental conditions: epigenomics of adaptive plasticity

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Abstract

Main conclusion

Roots play an important role in adaptive plasticity of rice under dry/direct-sown conditions. However, hypomethylation of genes in leaves (resulting in up-regulated expression) complements the adaptive plasticity of Nagina-22 under DSR conditions.

Abstract

Rice is generally cultivated by transplanting which requires plenty of water for irrigation. Such a practice makes rice cultivation a challenging task under global climate change and reducing water availability. However, dry-seeded/direct-sown rice (DSR) has emerged as a resource-saving alternative to transplanted rice (TPR). Though some of the well-adapted local cultivars are used for DSR, only limited success has been achieved in developing DSR varieties mainly because of a limited knowledge of adaptability of rice under fluctuating environmental conditions. Based on better morpho-physiological and agronomic performance of Nagina-22 (N-22) under DSR conditions, N-22 and IR-64 were grown by transplanting and direct-sowing and used for whole genome methylome analysis to unravel the epigenetic basis of adaptive plasticity of rice. Comparative methylome and transcriptome analyses indicated a large number (4078) of genes regulated through DNA methylation/demethylation in N-22 under DSR conditions. Gene × environment interactions play important roles in adaptive plasticity of rice under direct-sown conditions. While genes for pectinesterase, LRK10, C2H2 zinc-finger protein, splicing factor, transposable elements, and some of the unannotated proteins were hypermethylated, the genes for regulation of transcription, protein phosphorylation, etc. were hypomethylated in CG context in the root of N-22, which played important roles in providing adaptive plasticity to N-22 under DSR conditions. Hypomethylation leading to up-regulation of gene expression in the leaf complements the adaptive plasticity of N-22 under DSR conditions. Moreover, differential post-translational modification of proteins and chromatin assembly/disassembly through DNA methylation in CHG context modulate adaptive plasticity of N-22. These findings would help developing DSR cultivars for increased water-productivity and ecological efficiency.

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Data availability

The raw data for WGBS (submission ID: SUB11780954) and transcriptome (BioProject ID PRJNA805549) have been submitted to NCBI Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/sra), which can also be made available on request.

Abbreviations

DEG:

Differentially expressed gene

DMR:

Differentially methylated region

DSR:

Dry/direct-sown rice

GO:

Gene ontology

TE:

Transposable element

TF:

Transcription factor

TPR:

Transplanted rice

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Funding

The research was carried out with financial support from the National Agricultural Science Fund (NASF/ABP-70161/2018–19) from the Indian Council of Agricultural Research, Govt. of India, New Delhi, India.

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Authors and Affiliations

  1. Division of Biochemistry, ICAR-Indian Agricultural Research Institute, New Delhi, India

    Suresh Kumar, Karishma Seem & Archana Singh

  2. Decode Genomics Private Limited, New Delhi, India

    Santosh Kumar

  3. Division of Genetics, ICAR-Indian Agricultural Research Institute, New Delhi, India

    S. Gopala Krishnan

  4. Indian Council of Agricultural Research, New Delhi, India

    Trilochan Mohapatra

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Contributions

SuK and TM conceived the experiments. GKS provided genetically pure rice cultivars and helped grow them through different methods of planting over the generations. KS, SuK and AS carried out the experiments. SaK performed bioinformatic analyses. SuK and AS prepared the initial draft. TM revised the manuscript. All the authors approved the finalized draft for publication.

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Correspondence to Suresh Kumar or Trilochan Mohapatra.

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The authors declare that they have no competing interests. Santosh Kumar is employed at the Decode Genomics Private Limited, New Delhi, and the work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Kumar, S., Seem, K., Kumar, S. et al. DNA methylome analysis provides insights into gene regulatory mechanism for better performance of rice under fluctuating environmental conditions: epigenomics of adaptive plasticity. Planta 259, 4 (2024). https://doi.org/10.1007/s00425-023-04272-3

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