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Degradation of SERRATE via ubiquitin-independent 20S proteasome to survey RNA metabolism

Abstract

SERRATE (SE) is a key factor in RNA metabolism. Here, we report that SE binds 20S core proteasome α subunit G1 (PAG1) among other components and is accumulated in their mutants. Purified PAG1-containing 20S proteasome degrades recombinant SE via an ATP- and ubiquitin-independent manner in vitro. Nevertheless, PAG1 is a positive regulator for SE in vivo, as pag1 shows comparable molecular and/or developmental defects relative to se. Furthermore, SE is poorly assembled into macromolecular complexes, exemplified by the microprocessor in pag1 compared with Col-0. SE overexpression triggered the destruction of both transgenic and endogenous protein, leading to similar phenotypes of se and SE overexpression lines. We therefore propose that PAG1 degrades the intrinsically disordered portion of SE to secure the functionality of folded SE that is assembled and protected in macromolecular complexes. This study provides insight into how the 20S proteasome regulates RNA metabolism through controlling its key factor in eukaryotes.

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Fig. 1: Knockdown mutants of PAG1, a partner of SE, cause developmental defects in Arabidopsis.
Fig. 2: PAG1 impacts SE-mediated RNA metabolism.
Fig. 3: SE is degraded via PAG1-containing 20S proteasome, but not through the ubiquitin-proteasome pathway.
Fig. 4: In vitro degradation of SE by purified Arabidopsis 20S proteasome.
Fig. 5: Overaccumulation of disordered SE protein interferes with its normal function.
Fig. 6: Proposed model for the degradation of SE protein by PAG1.

Data availability

The RNA-seq and sRNA-seq data were deposited in the NCBI BioProject database with accession code PRJNA613247. All other data supporting the findings of the study are present in the main text and/or the Supplementary Information. Additional data related to this study are available from the corresponding authors upon request. Source data are provided with this paper.

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Acknowledgements

We thank Zhang lab members for careful proofreading of this manuscript. The work was supported by grants from the NIH (grant nos. GM132401 and GM127742), NSF (grant no. MCB-1716243) and Welch Foundation (grant no. A-1973-20180324) to X.Z. Y.L., D.S., L.W. and X.Y. were supported by China Scholar Council fellowships.

Author information

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Authors

Contributions

X.Z. conceived the project. Z.W. and X.Z. designed the study. Y.L. and D.S. performed the experiments. Z.M. conducted the bioinformatics analysis. B.S., Y.N. and H.K. helped with the confocal experiments. K.Y., L.W., M.Z., S.Z., X.Y., J.H. and Q.X. provided the experimental materials and intellectual input. Y.L., D.S. and Z.W. analysed the data. Y.L. and X.Z. wrote the paper.

Corresponding authors

Correspondence to Zhiye Wang or Xiuren Zhang.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Yijun Qi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Experimental validation of the SE-PAG1 interaction.

a, peptides of PAG1 recovered from MS analysis of SE immunoprecipitates. b, c, the specific SE-PAG1 interaction was confirmed in N. benthamiana by luciferase complementation (LCI) (b) and FRET (c). In (b), the infiltration scheme of leaves shows different combinations of constructs fused to either N-terminal (nLUC) or C-terminal (cLUC) regions of luciferase. LUC, bright field, and merged photograph (Merge) are shown. The red arrows and color bar indicate the infiltration positions and the signal intensity, respectively. A combination of CHR2 and SE17 serves as a positive control. In (c), CFP, SE-CFP as a donor fluorescence; YFP, PAG1-YFP as an acceptor fluorescence; nFRET, the FRET fluorescence. The color bars indicate the scale of the signal strength. (Scale bars, 10 μm). The last image was analyzed by imageJ to show the FRET signal intensity after background calibration. d, Co-IP assays to detect the SE-PAG1 interaction in Arabidopsis. In (b, c, d), the experiments were independently repeated three times with similar results. e, Y2H assays between PAG1 and truncated variants of SE, HYL1 and DCL1. (f) confocal imaging shows that PAG1 is distributed in nucleus and cytoplasm in root tip and elongated root of PPAG1-gPAG1-eYFP transgenic plants (Scale bars, 100 μm). At least 10 independent colonies for each interaction (e) and 16 independent transgenic plants (f) were examined and showed similar results. Source data

Extended Data Fig. 2 Genotypes and phenotypes of pag1-2 mutants.

a, three artificial miRNAs (pag1-2-a, -b, and -c) specifically target PAG1. The sequence alignment of the artificial miRNAs (red) and their complementary sequences (blue). b, pag1-2-a and pag1-2-b lines have the same phenotype as pag1-2-c, which refers to pag1-2 thereafter (Scale bars, 0.5 cm); c, sRNA blot analysis of artificial miRNA accumulation in pag1-2 transgenic lines (top). U6 is a loading control and qRT-PCR analysis of PAG1 transcript in pag1-2 relative to Col-0 (bottom). Data are presented as mean ± SD, n = 3 biologically independent replicates. The asterisk (*) indicates the significance between mutants and Col-0 control (*P < 0.05; unpaired, two-tailed Student’s t-test). d, the knockdown lines overexpressing artificial miRNA targeting PAG1 showed normal flowering time. The experiment was independently repeated at least three times with similar results. e, severely retarded root growth of pag1-2. Data are presented as mean ± SD, n = 16 biologically independent samples. The asterisk (*) indicates the significance between mutants and Col-0 control (***P < 0.001; unpaired, two-tailed Student’s t-test). Source data

Extended Data Fig. 3 RNA-seq analysis of se-2, pag1-2 and apc8-1.

a, numbers of differentially expressed genes in pag1-2 and se-2 mutants compared to Col-0. Also see in Supplementary Table 2 and 3. b, c, the number of reads (RNA-seq reads per million) of PAG1 (b) and SE (c) recovered from RNA-seq analysis of Col-0 and indicated mutants from three biological replicates. The asterisk (*) indicates the significance between mutants and Col-0 control (**P = 0.00304; unpaired, two-tailed Student’s t-test). d, overlapping of upregulated and downregulated genes between apc8-1 and se-2 mutants. e, comparative analysis shows significant overlapping between SE binding loci and PAG1-regulated genes. The data were derived from three biological replicates.

Extended Data Fig. 4 In vitro cell-free and in vivo SE-decay assays.

a, western blot analysis of SE protein in three-week-old pag1-2 mutants with different severities using an anti-SE antibody. Actin serves as a loading control. bd, additional repeats for in vitro cell-free (b, c) and in vivo (d) SE-decay assays. Western blot analysis of SE protein was conducted with an anti-SE antibody. Actin is a loading control. In (d), the numbers below the gels indicated the relative mean signals of SE protein in different time points that were sequentially normalized to that of SE and actin at time 0 where the value was arbitrarily assigned a value of 1. The experiments were independently repeated twice (d) or three times (a, b and c) with similar results. Source data

Extended Data Fig. 5 DMS3 serves as a positive control for 26S proteasome degradation compared to SE in parallel experiments.

a, in vivo DMS3-decay assay. DMS3-YFP transgenic seedlings were treated with CHX (0.5 mM) with or without 50 μM PYR-41 for indicated time. YFP levels were determined with an anti-YFP antibody. Actin is a loading control. The numbers below the gels indicated the relative mean signals of SE protein in different time points that were sequentially normalized to that of YFP and actin at time 0 where the value was arbitrarily assigned a value of 1. b, detection of ubiquitin conjugated to DMS3, a positive control, in vivo. DMS3-YFP was IP-ed with an anti-YFP antibody. Western blot analysis of ubiquitin was conducted with an anti-ubiquitin antibody (Agrisera, AS08307). Actin is a loading control for input. The experiment was independently repeated twice (a) or three times (b) with similar results. Source data

Extended Data Fig. 6 Y2H assays between SE and additional 20S proteasome subunits and the 19S regulatory subunit RPN1a.

The interactions between SE and RPN1a, PAC1, PAF1 and PBD1 were detected by Y2H. At least 10 independent colonies for each interaction were tested and showed similar results.

Extended Data Fig. 7 Foldindex analysis of SE and in vitro SE- and HYL1-decay assays via purified 20S proteasome.

a, predicted disordered segment via Foldindex analysis. Amino acid residues with green or red colors indicate the predicted ordered and disordered segment, respectively. b, the activity of the isolated 26S and 20S proteasomes and control IPs. Data are presented as means ± SD, n = 3 biologically independent replicates. RFU, relative fluorescence units. Note: two control IPs had no activity but only one control IP is shown here. c, 6xHis-SUMO-SE was purified by gel filtration. SEC analysis was performed in a HiLoad 16/600 Superdex 200 column (GE Healthcare) based on the manufacture’s specification. The molecular weight of the SE protein in peak 2 is calculated as 189.3 kDa. The asterisk (*) indicates the nonspecific bands. d, SDS-PAGE of purified recombinant proteins HYL1. The experimental conditions for purifying SE (c) and HYL1 (d) were optimized for at least 10 times and the proteins were later purified and obtained for multiple times under the best optimized conditions; and the results were always consistent. e, an additional repeat for in vitro SE-decay assay. f, an additional repeat for in vitro HYL1-decay assay. g, an additional repeat for 20S proteasome degradation of 6xHis-SUMO-SE proteins in vitro. The arrows indicate truncated SE. The experiments were independently repeated three times (e, f and g) with similar results. Source data

Extended Data Fig. 8 The interaction between SE and DCL1 is compromised in pag1-2.

Additional figures for BiFC assays showed the different interactions pattern between SE and DCL1 in Col-0 and pag1-2 protoplasts. Scale bars, 10 μm. At least 14 independent protoplasts for each interaction were tested and showed similar results.

Extended Data Fig. 9 SE transcript but not PAG1 was significantly accumulated in SE overexpressed transgenic lines.

a, b, qRT-PCR analysis of SE (a) and PAG1 (b) transcripts in Col-0; 35S-FM-SE transgenic plants relative to Col-0. Data are presented as mean ± SD, n = 3 biologically independent replicates. The asterisk (*) indicates the significance between mutants and Col-0 control (**P < 0.01, ***P < 0.001; unpaired, two-tailed Student’s t-test). Source data

Extended Data Fig. 10 PAG1 mutation causes mis-location of SE between nucleus and cytoplasm.

An additional repeat for cell-fractionation analysis showed that the presence of SE protein in cytoplasm in addition to nucleus in the pag1-2 mutant, but not in Col-0 plants. The experiment was independently repeated three times with similar results. Source data

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Li, Y., Sun, D., Ma, Z. et al. Degradation of SERRATE via ubiquitin-independent 20S proteasome to survey RNA metabolism. Nat. Plants 6, 970–982 (2020). https://doi.org/10.1038/s41477-020-0721-4

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