Large-scale plant genomic identification and analysis uncover ASMT/COMT copy number variation driving melatonin dosage balance

Abstract

ASMT/COMT, as a key rate-limiting enzyme regulating melatonin biosynthesis, has garnered significant attention. This study investigates the evolutionary mechanisms of the ASMT/COMT gene family in melatonin biosynthesis. A total of 28 010 ASMT/COMT genes from 1052 species were identified through an integrated approach combining large-scale identifications and analyses. At the pan-genome level, we identified 5186, 336, 2137, and 1814 ASMT/COMT genes respectively in Triticum aestivum, Aegilops tauschii, diploid and tetraploid Solanum tuberosum haplotype genomes (247, 86, 670, and 96 orthologous gene groups). Expansion patterns of the ASMT/COMT gene family were explored through synteny networks in 104 Poaceae and 88 Solanaceae plants. Further investigation of copy number variation (CNV) in the 1052 species, along with a focused analysis of hexaploid wheat and its diploid progenitor Ae. tauschii, indicated a functional divergence linked to gene dosage. The catalytically efficient COMT is maintained at low-copy conditions, whereas the less active ASMT is amplified under high-copy conditions. Intriguingly, in polyploid potatoes, the total ASMT/COMT copy number was lower in tetraploids than in diploids, suggesting a distinct dosage balance mechanism operating in polyploids. In contrast, the melatonin receptor CAND2 consistently remained in a low-copy state, with no significant correlation to ASMT/COMT copy number. Expression analysis revealed that COMT is generally expressed at higher levels than ASMT, highlighting a compensatory relationship between gene dosage and transcriptional regulation. Collectively, our findings uncover a dosage balance mechanism that fine-tunes melatonin biosynthetic homeostasis through coordinated CNV and expression regulation, offering a new perspective on the evolution of metabolic enzymes.

Acknowledgements

We sincerely thank Y. Zhou and Z. Zhang (State Key Laboratory of Crop Stress Adaptation and Improvement, Henan University) for their guidance and feedback. We thank graduate students S. Ding, F. Yuan, and Y. Ke at the same institution. Appreciation is extended to: Y. Wang (Radiation Biology Center, Kyoto University); Z. Xu (Marine Environmental Science, The Hong Kong University of Science and Technology); H. Zhu (Division of Life Science, The Hong Kong University of Science and Technology); S. Kan and W. Zhang (Marine College, Shandong University). The computational infrastructure of the State Key Laboratory of Crop Stress Adaptation and Improvement (Henan University) and Shandong University’s Marine College facilitated data processing in this study. The authors declare no competing interests. This study was supported by National Natural Science Foundation of China (no. 32501846), Shandong Provincial Natural Science Foundation (no. ZR2023QC278), the Undergraduate Scientific Research Innovation Projects at Shandong University (no. 202510422024) and the Youth Student Fundamental Research Funds of Shandong University (no. SDUQM2523).

Data availability statement

All data supporting the findings of this study is available in the article and the Supplementary information files. All source codes and raw data can be obtained on figshare (https://doi.org/10.6084/m9.figshare.30315934.v2 or https://figshare.com/articles/dataset/Large-Scale_Plant_Genomic_Identification_and_Analysis_Uncover_i_ASMT_COMT_i_Copy_Number_Variation_Driving_Melatonin_Dosage_Balance/30315934).

Conflicts of interest statement

The authors declare no conflicts of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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