Uridylation and the SKI complex orchestrate the Calvin cycle of photosynthesis through RNA surveillance of TKL1 in Arabidopsis.
Uridylation and the SKI complex orchestrate the Calvin cycle of photosynthesis through RNA surveillance of TKL1 in Arabidopsis.
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拟南芥中尿苷化和 SKI 复合物通过 TKL1 的 RNA 监视协调光合作用的卡尔文循环
DOI:
10.1073/pnas.2205842119
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发表时间:
2022-09-20
影响因子:
11.1
通讯作者:
中科院分区:
文献类型:
--
作者:
RNA uridylation is a conserved and widespread posttranscriptional modification that impacts a multitude of RNA metabolic processes. In Arabidopsis, HEN1 SUPPRESSOR 1 (HESO1) and UTP: RNA URIDYLYLTRANSFERASE (URT1) catalyze uridylation of both small RNA and cytoplasmic RNA. Here we report that HESO1 and URT1 cooperate with the 3′–5′ RNA degradation component SUPERKILLER 2 (SKI2) to prevent spurious short interfering RNA biogenesis from a subset of messenger RNAs, including the TRANSKETOLASE 1 (TKL1) locus, thus ensuring proper Calvin cycle function and normal plant development. This study integrates RNA uridylation into the RNA surveillance pathway and sheds light on the role of RNA surveillance in photosynthesis. 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.
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影响因子:
14.9
作者:
Łabno A;Warkocki Z;Kuliński T;Krawczyk PS;Bijata K;Tomecki R;Dziembowski A
通讯作者:
Dziembowski A
影响因子:
5
作者:
Menezes MR;Balzeau J;Hagan JP
通讯作者:
Hagan JP
影响因子:
11.8
作者:
Gregory, Brian D.;O'Malley, Ronan C.;Ecker, Joseph R.
通讯作者:
Ecker, Joseph R.
影响因子:
7.2
作者:
Bowler, C;Benvenuto, G;Paszkowski, J
通讯作者:
Paszkowski, J
影响因子:
27.5
作者:
Liu L;Chen X
通讯作者:
Chen X