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:
综合性期刊1区
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RNA尿苷化是一种保守的、广泛存在的转录后修饰,影响着许多RNA代谢过程。在拟南芥中,HESO 1和URT 1催化小RNA和胞质RNA的尿苷化。在这里,我们报告HESO 1和URT 1与3′-5′ RNA降解组分SUPERKILLER 2(SKI 2)合作,以防止来自信使RNA子集(包括转SKETOLASE 1(TKL 1)位点)的假短干扰RNA生物合成,从而确保适当的卡尔文循环功能和正常的植物发育。这项研究将RNA尿苷化整合到RNA监视途径中,揭示了RNA监视在光合作用中的作用。由末端尿苷酰转移酶(TUTases)催化的RNA尿苷酸化代表了真核生物中影响RNA代谢的保守且广泛的转录后RNA修饰。在植物中,已经通过遗传和生物化学方法表征了几种TUTases,包括HEN 1 SUPPLYOR 1(HESO 1)和UTP:RNA尿苷酰转移酶(URT 1)。然而,对它们在植物发育过程中的生理意义知之甚少。在这里,我们发现HESO 1和URT 1与细胞质3′-5′核糖核酸外切机制组分SUPERKILLER 2(SKI 2)合作,通过拟南芥卡尔文循环基因转酮酶1(TKL 1)的RNA监视来调节光合作用。HESO 1、URT 1和SKI 2的同时功能障碍导致叶片黄化并降低光合效率。此外,我们检测到大量的非法短干扰RNA(siRNA)从TKL 1基因座heso 1 urt 1 ski 2,伴随着减少TKL 1/2的表达和衰减TKL活动。因此,代谢分析表明,许多卡尔文循环中间体的丰度显着干扰heso 1 urt 1 ski 2。重要的是,所有这些分子和生理缺陷在很大程度上被RNA依赖性RNA聚合酶6(RDR 6)中的功能缺失突变所挽救,证明了非法的siRNA介导的TKL沉默。总之,我们的研究结果表明,HESO 1和URT 1介导的RNA尿苷化连接到细胞质RNA降解途径的RNA监视,这是至关重要的TKL表达和光合作用在拟南芥。
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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发表时间: 2016-12-01
影响因子: 14.9
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