J Integr Plant Biol. ›› 2020, Vol. 62 ›› Issue (7): 967-983.DOI: 10.1111/jipb.12867

Special Issue: Photosynthesis

• Molecular Physiology • Previous Articles     Next Articles

Arabidopsis DXO1 possesses deNADding and exonuclease activities and its mutation affects defense-related and photosynthetic gene expression

Shuying Pan1†, Kai-en Li1†, Wei Huang2, Huan Zhong1, Huihui Wu3, Yuan Wang4, He Zhang1, Zongwei Cai2, Hongwei Guo3, Xuemei Chen4 and Yiji Xia1,2,5*   

  1. 1Department of Biology, Hong Kong Baptist University, Hong Kong, China
    2State Key Laboratory of Environmental and Biological Analysis, Department of Chemistry, Hong Kong Baptist University, Hong Kong, China
    3Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China
    4Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California 92521, USA
    5State Key Laboratory of Agricultural Biotechnology, School of Life Sciences, Chinese University of Hong Kong, Hong Kong, China

    These authors made equal contribution
    Email: Yiji Xia (yxia@hkbu.edu.hk)
  • Received:2019-07-01 Accepted:2019-08-23 Online:2019-08-26 Published:2020-07-01


RNA capping and decapping tightly coordinate with transcription, translation, and RNA decay to regulate gene expression. Proteins in the DXO/Rai1 family have been implicated in mRNA decapping and decay, and mammalian DXO was recently found to also function as a decapping enzyme for NAD+‐capped RNAs (NAD‐RNA). The Arabidopsis genome contains a single gene encoding a DXO/Rai1 protein, AtDXO1. Here we show that AtDXO1 possesses both NAD‐RNA decapping activity and 5ʹ‐3ʹ exonuclease activity but does not hydrolyze the m7G cap. The atdxo1 mutation increased the stability of NAD‐RNAs and led to pleiotropic phenotypes, including severe growth retardation, pale color, and multiple developmental defects. Transcriptome profiling analysis showed that the atdxo1 mutation resulted in upregulation of defense‐related genes but downregulation of photosynthesis‐related genes. The autoimmunity phenotype of the mutant could be suppressed by either eds1 or npr1 mutation. However, the various phenotypes associated with the atdxo1 mutant could be complemented by an enzymatically inactive AtDXO1. The atdxo1 mutation apparently enhances post‐transcriptional gene silencing by elevating levels of siRNAs. Our study indicates that AtDXO1 regulates gene expression in various biological and physiological processes through its pleiotropic molecular functions in mediating RNA processing and decay.

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