Uridylation and the SKI complex orchestrate the Calvin cycle of photosynthesis through RNA surveillance of TKL1 in Arabidopsis
RNA uridylation, catalyzed by terminal uridylyl transferases (TUTases), represents a conserved and widespread posttranscriptional RNA modification in eukaryotes that affects RNA metabolism. In plants, several TUTases, including HEN1 SUPPRESSOR 1 (HESO1) and UTP: RNA URIDYLYLTRANSFERASE (URT1), have been characterized through genetic and biochemical approaches. However, little is known about their physiological significance during plant development. Here, we show that HESO1 and URT1 act cooperatively with the cytoplasmic 3'-5' exoribonucleolytic machinery component SUPERKILLER 2 (SKI2) to regulate photosynthesis through RNA surveillance of the Calvin cycle gene TRANSKETOLASE 1 (TKL1) in Arabidopsis. Simultaneous dysfunction of HESO1, URT1, and SKI2 resulted in leaf etiolation and reduced photosynthetic efficiency. In addition, we detected massive illegitimate short interfering RNAs (siRNAs) from the TKL1 locus in heso1 urt1 ski2, accompanied by reduced TKL1/2 expression and attenuated TKL activities. Consequently, the metabolic analysis revealed that the abundance of many Calvin cycle intermediates is dramatically disturbed in heso1 urt1 ski2. Importantly, all these molecular and physiological defects were largely rescued by the loss-of-function mutation in RNA-DEPENDENT RNA POLYMERASE 6 (RDR6), demonstrating illegitimate siRNA-mediated TKL silencing. Taken together, our results suggest that HESO1- and URT1-mediated RNA uridylation connects to the cytoplasmic RNA degradation pathway for RNA surveillance, which is crucial for TKL expression and photosynthesis in Arabidopsis.
| Medienart: |
E-Artikel |
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| Erscheinungsjahr: |
2022 |
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| Erschienen: |
2022 |
| Enthalten in: |
Zur Gesamtaufnahme - volume:119 |
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| Enthalten in: |
Proceedings of the National Academy of Sciences of the United States of America - 119(2022), 38 vom: 20. Sept., Seite e2205842119 |
| Sprache: |
Englisch |
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| Beteiligte Personen: |
Wang, Xiaoyan [VerfasserIn] |
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| Links: |
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| Anmerkungen: |
Date Completed 14.09.2022 Date Revised 13.03.2023 published: Print-Electronic Citation Status MEDLINE |
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| doi: |
10.1073/pnas.2205842119 |
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| funding: |
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| Förderinstitution / Projekttitel: |
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| PPN (Katalog-ID): |
NLM346121345 |
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| 100 | 1 | |a Wang, Xiaoyan |e verfasserin |4 aut | |
| 245 | 1 | 0 | |a Uridylation and the SKI complex orchestrate the Calvin cycle of photosynthesis through RNA surveillance of TKL1 in Arabidopsis |
| 264 | 1 | |c 2022 | |
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| 500 | |a Date Completed 14.09.2022 | ||
| 500 | |a Date Revised 13.03.2023 | ||
| 500 | |a published: Print-Electronic | ||
| 500 | |a Citation Status MEDLINE | ||
| 520 | |a RNA uridylation, catalyzed by terminal uridylyl transferases (TUTases), represents a conserved and widespread posttranscriptional RNA modification in eukaryotes that affects RNA metabolism. In plants, several TUTases, including HEN1 SUPPRESSOR 1 (HESO1) and UTP: RNA URIDYLYLTRANSFERASE (URT1), have been characterized through genetic and biochemical approaches. However, little is known about their physiological significance during plant development. Here, we show that HESO1 and URT1 act cooperatively with the cytoplasmic 3'-5' exoribonucleolytic machinery component SUPERKILLER 2 (SKI2) to regulate photosynthesis through RNA surveillance of the Calvin cycle gene TRANSKETOLASE 1 (TKL1) in Arabidopsis. Simultaneous dysfunction of HESO1, URT1, and SKI2 resulted in leaf etiolation and reduced photosynthetic efficiency. In addition, we detected massive illegitimate short interfering RNAs (siRNAs) from the TKL1 locus in heso1 urt1 ski2, accompanied by reduced TKL1/2 expression and attenuated TKL activities. Consequently, the metabolic analysis revealed that the abundance of many Calvin cycle intermediates is dramatically disturbed in heso1 urt1 ski2. Importantly, all these molecular and physiological defects were largely rescued by the loss-of-function mutation in RNA-DEPENDENT RNA POLYMERASE 6 (RDR6), demonstrating illegitimate siRNA-mediated TKL silencing. Taken together, our results suggest that HESO1- and URT1-mediated RNA uridylation connects to the cytoplasmic RNA degradation pathway for RNA surveillance, which is crucial for TKL expression and photosynthesis in Arabidopsis | ||
| 650 | 4 | |a Journal Article | |
| 650 | 4 | |a Research Support, Non-U.S. Gov't | |
| 650 | 4 | |a Calvin cycle | |
| 650 | 4 | |a Photosynthesis | |
| 650 | 4 | |a Post-transcriptional gene silencing | |
| 650 | 4 | |a RNA degradation | |
| 650 | 4 | |a RNA uridylation | |
| 650 | 7 | |a Arabidopsis Proteins |2 NLM | |
| 650 | 7 | |a RNA, Small Interfering |2 NLM | |
| 650 | 7 | |a Transketolase |2 NLM | |
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| 650 | 7 | |a RAX3 protein, Arabidopsis |2 NLM | |
| 650 | 7 | |a EC 3.6.4.13 |2 NLM | |
| 650 | 7 | |a RNA Helicases |2 NLM | |
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| 700 | 1 | |a Kong, Wenwen |e verfasserin |4 aut | |
| 700 | 1 | |a Wang, Yuan |e verfasserin |4 aut | |
| 700 | 1 | |a Wang, Jinhui |e verfasserin |4 aut | |
| 700 | 1 | |a Zhong, Luyao |e verfasserin |4 aut | |
| 700 | 1 | |a Lao, Kangwen |e verfasserin |4 aut | |
| 700 | 1 | |a Dong, Xianxin |e verfasserin |4 aut | |
| 700 | 1 | |a Zhang, Dingyu |e verfasserin |4 aut | |
| 700 | 1 | |a Huang, He |e verfasserin |4 aut | |
| 700 | 1 | |a Mo, Beixin |e verfasserin |4 aut | |
| 700 | 1 | |a Yu, Yu |e verfasserin |4 aut | |
| 700 | 1 | |a Ren, Guodong |e verfasserin |4 aut | |
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