N 6-methyladenosine modifications stabilize phosphate starvation response–related mRNAs in plant adaptation to nutrient-deficient stress

N<sup>6</sup>-methyladenosine (m<sup>6</sup>A), an abundant internal mRNA modification, is induced by various stress conditions and post-transcriptionally regulates gene expression. However, how m<sup>6</sup>A modifications help plants respond to nutrient-deficiency stress remains unclear. Here, we profile high-confidence m<sup>6</sup>A modifications in Arabidopsis transcriptome-wide under normal and inorganic orthophosphate (Pi)-deficient conditions (-P). High-confidence m<sup>6</sup>A modifications are identified using synthetic modification-free RNA libraries for systematic calibration. Pi starvation induces widespread m<sup>6</sup>A modifications, mediated by the Pi starvation response (PSR) master regulator PHOSPHATE STARVATION RESPONSE1 (PHR1) and its family members. Many Pi starvation-induced (PSI) m<sup>6</sup>A modifications occur on PSR-related mRNAs, including PHR1. In addition, PHR1 proteins interact with the m<sup>6</sup>A writers MRNA ADENOSINE METHYLASE (MTA) and METHYLTRANSFERASE B (MTB) in nuclei under -P conditions. m<sup>6</sup>A modifications facilitate systemic PSR signaling, as reflected by the reduced Pi content and PSR signaling in a knockdown artificial miRNA line targeting MTA, which shows a global decrease in m<sup>6</sup>A. Transcriptome-wide mRNA decay analysis reveals that PSI-m<sup>6</sup>A increases the stability of PSR-related mRNAs, but not through alternative polyadenylation site shifts. Analysis of transgenic plants with mutations in m<sup>6</sup>A loci demonstrates that m<sup>6</sup>A stabilizes PHR1 transcripts via a positive feedback loop. Our findings indicate that PSI-m<sup>6</sup>A modifications facilitate PSR signaling by enhancing the stability of certain mRNAs, shedding light on the role of m<sup>6</sup>A modifications in nutrient stress responses in plants.

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Journal
Nature Communications
Published
2025-05-01
DOI
https://doi.org/10.1038/s41467-025-59331-y
Citations
6
Primary Topic
RNA modifications and cancer
Type
article
Field-Weighted Citation Impact
4.84

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article

N 6-methyladenosine modifications stabilize phosphate starvation response–related mRNAs in plant adaptation to nutrient-deficient stress

Qiongli Jin, Haiyan Bai, Shuman Wang, Lulu Qiao et al.
6 citations
Nature Communications
RNA modifications and cancer
4.84
article

N 6-methyladenosine modifications stabilize phosphate starvation response–related mRNAs in plant adaptation to nutrient-deficient stress

Qiongli Jin, Haiyan Bai, Shuman Wang, Lulu Qiao, Zhonghui Zhang, Wen‐Fei Dong, Guan‐Zheng Luo, Zhiye Wang, Jingyi Wang, Kai Liu, Xiaojia Wang
article en
6 citations

Abstract

N<sup>6</sup>-methyladenosine (m<sup>6</sup>A), an abundant internal mRNA modification, is induced by various stress conditions and post-transcriptionally regulates gene expression. However, how m<sup>6</sup>A modifications help plants respond to nutrient-deficiency stress remains unclear. Here, we profile high-confidence m<sup>6</sup>A modifications in Arabidopsis transcriptome-wide under normal and inorganic orthophosphate (Pi)-deficient conditions (-P). High-confidence m<sup>6</sup>A modifications are identified using synthetic modification-free RNA libraries for systematic calibration. Pi starvation induces widespread m<sup>6</sup>A modifications, mediated by the Pi starvation response (PSR) master regulator PHOSPHATE STARVATION RESPONSE1 (PHR1) and its family members. Many Pi starvation-induced (PSI) m<sup>6</sup>A modifications occur on PSR-related mRNAs, including PHR1. In addition, PHR1 proteins interact with the m<sup>6</sup>A writers MRNA ADENOSINE METHYLASE (MTA) and METHYLTRANSFERASE B (MTB) in nuclei under -P conditions. m<sup>6</sup>A modifications facilitate systemic PSR signaling, as reflected by the reduced Pi content and PSR signaling in a knockdown artificial miRNA line targeting MTA, which shows a global decrease in m<sup>6</sup>A. Transcriptome-wide mRNA decay analysis reveals that PSI-m<sup>6</sup>A increases the stability of PSR-related mRNAs, but not through alternative polyadenylation site shifts. Analysis of transgenic plants with mutations in m<sup>6</sup>A loci demonstrates that m<sup>6</sup>A stabilizes PHR1 transcripts via a positive feedback loop. Our findings indicate that PSI-m<sup>6</sup>A modifications facilitate PSR signaling by enhancing the stability of certain mRNAs, shedding light on the role of m<sup>6</sup>A modifications in nutrient stress responses in plants.

Nature CommunicationsVol. 16(1)
Sun Yat-sen University (CN), South China Normal University (CN), First Affiliated Hospital Zhejiang University (CN), Zhejiang University (CN)
National Natural Science Foundation of China, Chinese Academy of Sciences, Zhejiang University, National Key Research and Development Program of China, Institute of Botany, Chinese Academy of Sciences, Natural Science Foundation of Zhejiang Province
Zero hunger
Openalex Percentile: Top 5%
RNA modifications and cancer
4.84
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