Structured 3′ UTRs destabilize mRNAs in plants
Abstract Background RNA secondary structure (RSS) can influence the regulation of transcription, RNA processing, and protein synthesis, among other processes. 3′ untranslated regions (3′ UTRs) of mRNA also hold the key for many aspects of gene regulation. However, there are often contradictory resul...
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| Format: | Article |
| Language: | English |
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BMC
2024-02-01
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| Series: | Genome Biology |
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| Online Access: | https://doi.org/10.1186/s13059-024-03186-x |
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| author | Tianru Zhang Changhao Li Jiaying Zhu Yanjun Li Zhiye Wang Chun-Yip Tong Yu Xi Yi Han Hisashi Koiwa Xu Peng Xiuren Zhang |
| author_facet | Tianru Zhang Changhao Li Jiaying Zhu Yanjun Li Zhiye Wang Chun-Yip Tong Yu Xi Yi Han Hisashi Koiwa Xu Peng Xiuren Zhang |
| author_sort | Tianru Zhang |
| collection | DOAJ |
| description | Abstract Background RNA secondary structure (RSS) can influence the regulation of transcription, RNA processing, and protein synthesis, among other processes. 3′ untranslated regions (3′ UTRs) of mRNA also hold the key for many aspects of gene regulation. However, there are often contradictory results regarding the roles of RSS in 3′ UTRs in gene expression in different organisms and/or contexts. Results Here, we incidentally observe that the primary substrate of miR159a (pri-miR159a), when embedded in a 3′ UTR, could promote mRNA accumulation. The enhanced expression is attributed to the earlier polyadenylation of the transcript within the hybrid pri-miR159a-3′ UTR and, resultantly, a poorly structured 3′ UTR. RNA decay assays indicate that poorly structured 3′ UTRs could promote mRNA stability, whereas highly structured 3′ UTRs destabilize mRNA in vivo. Genome-wide DMS-MaPseq also reveals the prevailing inverse relationship between 3′ UTRs’ RSS and transcript accumulation in the transcriptomes of Arabidopsis, rice, and even human. Mechanistically, transcripts with highly structured 3′ UTRs are preferentially degraded by 3′–5′ exoribonuclease SOV and 5′–3′ exoribonuclease XRN4, leading to decreased expression in Arabidopsis. Finally, we engineer different structured 3′ UTRs to an endogenous FT gene and alter the FT-regulated flowering time in Arabidopsis. Conclusions We conclude that highly structured 3′ UTRs typically cause reduced accumulation of the harbored transcripts in Arabidopsis. This pattern extends to rice and even mammals. Furthermore, our study provides a new strategy of engineering the 3′ UTRs’ RSS to modify plant traits in agricultural production and mRNA stability in biotechnology. |
| first_indexed | 2024-03-07T14:58:49Z |
| format | Article |
| id | doaj.art-cce8238e71cf407d8e1a085baa61602d |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-03-07T14:58:49Z |
| publishDate | 2024-02-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-cce8238e71cf407d8e1a085baa61602d2024-03-05T19:17:14ZengBMCGenome Biology1474-760X2024-02-0125113110.1186/s13059-024-03186-xStructured 3′ UTRs destabilize mRNAs in plantsTianru Zhang0Changhao Li1Jiaying Zhu2Yanjun Li3Zhiye Wang4Chun-Yip Tong5Yu Xi6Yi Han7Hisashi Koiwa8Xu Peng9Xiuren Zhang10Department of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Medical Physiology, College of Medicine, Texas A&M UniversityNational Engineering Laboratory of Crop Stress Resistence Breeding, School of Life Sciences, Anhui Agricultural UniversityDepartment of Horticultural Sciences, Texas A&M UniversityDepartment of Medical Physiology, College of Medicine, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityAbstract Background RNA secondary structure (RSS) can influence the regulation of transcription, RNA processing, and protein synthesis, among other processes. 3′ untranslated regions (3′ UTRs) of mRNA also hold the key for many aspects of gene regulation. However, there are often contradictory results regarding the roles of RSS in 3′ UTRs in gene expression in different organisms and/or contexts. Results Here, we incidentally observe that the primary substrate of miR159a (pri-miR159a), when embedded in a 3′ UTR, could promote mRNA accumulation. The enhanced expression is attributed to the earlier polyadenylation of the transcript within the hybrid pri-miR159a-3′ UTR and, resultantly, a poorly structured 3′ UTR. RNA decay assays indicate that poorly structured 3′ UTRs could promote mRNA stability, whereas highly structured 3′ UTRs destabilize mRNA in vivo. Genome-wide DMS-MaPseq also reveals the prevailing inverse relationship between 3′ UTRs’ RSS and transcript accumulation in the transcriptomes of Arabidopsis, rice, and even human. Mechanistically, transcripts with highly structured 3′ UTRs are preferentially degraded by 3′–5′ exoribonuclease SOV and 5′–3′ exoribonuclease XRN4, leading to decreased expression in Arabidopsis. Finally, we engineer different structured 3′ UTRs to an endogenous FT gene and alter the FT-regulated flowering time in Arabidopsis. Conclusions We conclude that highly structured 3′ UTRs typically cause reduced accumulation of the harbored transcripts in Arabidopsis. This pattern extends to rice and even mammals. Furthermore, our study provides a new strategy of engineering the 3′ UTRs’ RSS to modify plant traits in agricultural production and mRNA stability in biotechnology.https://doi.org/10.1186/s13059-024-03186-x3′ UTRRNA secondary structure (RSS)3′ end target-specific DMS-MaPseqDIM-2P-seqmRNA stability |
| spellingShingle | Tianru Zhang Changhao Li Jiaying Zhu Yanjun Li Zhiye Wang Chun-Yip Tong Yu Xi Yi Han Hisashi Koiwa Xu Peng Xiuren Zhang Structured 3′ UTRs destabilize mRNAs in plants Genome Biology 3′ UTR RNA secondary structure (RSS) 3′ end target-specific DMS-MaPseq DIM-2P-seq mRNA stability |
| title | Structured 3′ UTRs destabilize mRNAs in plants |
| title_full | Structured 3′ UTRs destabilize mRNAs in plants |
| title_fullStr | Structured 3′ UTRs destabilize mRNAs in plants |
| title_full_unstemmed | Structured 3′ UTRs destabilize mRNAs in plants |
| title_short | Structured 3′ UTRs destabilize mRNAs in plants |
| title_sort | structured 3 utrs destabilize mrnas in plants |
| topic | 3′ UTR RNA secondary structure (RSS) 3′ end target-specific DMS-MaPseq DIM-2P-seq mRNA stability |
| url | https://doi.org/10.1186/s13059-024-03186-x |
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