Rice in vivo RNA structurome reveals RNA secondary structure conservation and divergence in plants
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1 Rice in vivo RN structurome reveals RN secondary structure conservation and divergence in plants Hongjing Deng 1,2,,5, Jitender heema 3, Hang Zhang 2, Hugh Woolfenden 2, Matthew Norris 2, Zhenshan Liu 2, Qi Liu 2, Xiaofei Yang 2, Minglei Yang 2, Xian Deng 1, Xiaofeng ao 1,5, Yiliang Ding 2,5 1 State Key Laboratory of Plant enomics and National enter for Plant ene Research, S enter for Excellence in Molecular Plant Sciences, Institute of enetics and Developmental Biology, hinese cademy of Sciences. Beijing 111, hina 2 Department of ell and Developmental Biology, John Innes entre, Norwich Research Park, Norwich NR 7H, nited Kingdom 3 Department of omputational and Systems Biology, John Innes entre, Norwich Research Park, Norwich NR 7H, nited Kingdom ollege of Life Sciences, niversity of hinese cademy of Sciences, 19, Beijing, hina 5 S-JI entre of Excellence for Plant and Microbial Science (EPMS), John Innes entre, Norwich NR 7H, nited Kingdom orresponding author: X.. (xfcao@genetics.ac.cn) or Y.D. (yiliang.ding@jic.ac.uk). Running title: RN secondary structurome in rice 1
2 15 min DMS - % ddt dd dd dd () () () () Lane
3 Supplemental Figure 1 Preliminary experiment for optimizing concentration of DMS treatment. The fragment from nt to 1 33 nt of 18S rrn was analyzed. Lanes 1-5:,.75, 1.5, 2.5, % (v/v) DMS concentration, respectively, for 15 min at 28 ; lanes 6 to 9: /// sequencing lanes. The red and blue stars show the obviously modified and in concentration course, respectively.
4 B DMS S Reactivity DMS - + P =.6 P = 5.57E S Lane P =.89 P < 2.2E Relative DMS reactivity el reactivity Nucleotide position Reactivity Nucleotide position Lane Relative DMS reactivity el reactivity
5 Supplemental Figure 2 High agreement between Structure-seq and conventional gel-based RN secondary structure probing. () Left: gel-based probing. Right: the comparison of Structure-seq (purple bars) and gel-based probing (orange line) from nt to 1 3 nt of 18S rrn. (B) Left: gel-based probing. Right: the comparison of Structure-seq (purple bars) and gel-based probing (orange line) from 156 nt to 253 nt of 25S rrn. Lane 1 and 2, without and with 2.5% DMS treatment; lane 3 to 6, /// sequencing lanes. The positions of each well-visible and are coloured by red and blue stars, respectively. P and P values were shown in the corresponding region.
6 B F1 score Sensitivity P = PPV 75 1 D PPV F1 score Sensitivity P = P = PPV 75 1 P = PPV 75 1
7 Supplemental Figure 3 High correlation of PPV with sensitivity and F1 score. ()-(B) orrelation of PPV with sensitivity () and F1 score (B) in rice. Both P values are less than 2.2E-16. ()-(D) orrelation of PPV with sensitivity () and F1 score (D) in rabidopsis. Both P values are less than 2.2E-16.
8 ini index DMS reactivity DMS reactivity DMS reactivity DMS reactivity DMS reactivity. P = 2.118E- P < 2.2E B 5 TR DS... DS 3 TR Position Position Spliced events nspliced events end of 5 exon 5 end of 3 exon Position 5 splice site 3 splice site Position D E 5 5 TR DS 3 TR 3 3 Magnitude Period (nucleotide) Magnitude Period (nucleotide) High - 5 TR High - DS High - 3 TR Low - 5 TR Low - DS Low - 3 TR Magnitude Period (nucleotide) High - 5 TR High - DS High - 3 TR Low - 5 TR Low - DS Low - 3 TR F P < 2.2E-16 P =.955 P = 2.1E-1 No m 6 Single m 6 Multiple m 6 s..3.2 MM P = 9.E-13 m 6 ontrol Position
9 Supplemental Figure lobal pattern of mrn structurome in rice. () verage DMS reactivity in selected regions of mrns with more than one stop per nucleotide mrns filtered by length were used for this analysis. Wilcoxon rank-sum test (when alternative hypothesis was "less") was used for P value calculation between 5 TR and DS, DS and 3 TR. P values were shown in the corresponding region. (B) verage DMS reactivity around the alternative splice sites between spliced and unspliced events in 5 splice site and spliced and 6 35 unspliced events in 3 splice site. ()-(E) Discrete Fourier transform (DFT) of average DMS reactivity of selected regions in all the mrns (), mrns with high and low mrn content (D), mrns with high and low translation efficiency (E). (F) Effect of the number of m 6 peaks on ini index in 3 TR. (Yellow) 7 38 transcripts without m 6 peaks; (orange) 2 6 transcripts with single m 6 peak; (red) 2 75 transcripts with multiple m 6 peaks. P values were calculated by Wilcoxon rank-sum test. () DMS reactivity pattern around the conserved motif (MM, M = or ) identified in m 6 -seq (Li et al., 21). 221 motifs with m 6 and 19 motifs without m 6 were analyzed. P values were calculated by Kolmogorov-Smirnov (KS) test.
10 DMS reactivity DMS reactivity content content 1 High content Low content TR DS... DS 3 TR Position Position.2 B.5 High content Low content P =.2657 P =.19 P = 3.26E-7 P = 1.11E TR DS... DS 3 TR Position Position.1 3 Magnitude Period (nucleotide) High - 5 TR High - DS High - 3 TR Low - 5 TR Low - DS Low - 3 TR
11 Supplemental Figure 5 Effect of content on the global pattern of mrn structurome in rabidopsis. ()-(B) verage content () and average DMS reactivity (B) of transcripts with the highest 15% and lowest 15% mrn content with more than one stop per nucleotide (11 27 in total) in rabidopsis. P values between two groups were calculated by KS test. () DFT of average DMS reactivity of selected regions in mrns with high and low mrn content.
12 O. sativa DMS - + B. thaliana DMS P =.66 P = 1.385E-6 1 el reactivity O. sativa. thaliana Lane P =.77 P = 7.389E Sequence identity: O. sativa. thaliana Relative DMS reactivity Nucleotide position Lane Nucleotide position O. sativa thaliana Structure-Seq DMS reactivity.8.2 /
13 Supplemental Figure 6 omparison of 25S rrn fragment in rice and rabidopsis. The fragments are from 695 nt to 8 nt in rice and from 73 nt to 85 nt in rabidopsis. () el-based probing in rice and rabidopsis. Lane 1 and 2, without and with 2.5% DMS treatment; lane 3 to 6, /// sequencing lanes. The positions of each well-visible and are coloured by red and blue, respectively. (B) omparison of gel reactivity (top) and relative DMS reactivity (bottom) in rice and rabidopsis. In the sequence alignment, mismatches are highlighted in a green background, best matches are highlighted in a purple background, and the region with highly conserved in vivo RN secondary structure is marked in white. Pairwise alignments were performed in EMBOSS Needle. P and P value were shown in the corresponding region. () Phylogenetic structure of the fragments coloured by DMS reactivity. The orange line represents the highly conserved structure probing region identified in gel-based probing and Structure-seq analysis. The probed sites using gel-based probing (Supplemental Figure 6 and 6B top) and Structure-seq (Supplemental Figure 6B bottom) show very similar DMS modification patterns between rice and rabidopsis. The pattern of DMS reactivity is consistent with the phylogeny-derived structures (Supplemental Figure 6).
14 B Reactivity Reactivity 1.5 T LO_Os2g T Sequence identity: T Reactivity 2.5 Reactivity LO_Os9g735.1 LO_Os2g LO_Os9g735.1 T Sequence identity:.5 LO_Os2g in vivo LO_Os9g735.1 in vivo T in vivo T in vivo
15 Supplemental Figure 7 Two individual examples for two kinds of relationship between sequence identity and structure similarity. High sequence identity and high structure similarity (group-1) () and low sequence identity and low structure similarity (group-) (B) exhibit two kinds of relationship between sequence identity and structure similarity. The results in rice are coloured with red and the ones in rabidopsis with blue. The reactivity is compared based on the sequence alignment of selected regions. Best matched regions are coloured in a light purple background, the mismatches on and in a green background, and the mismatches on and in a yellow background. rc diagrams were shown to compare in vivo RN secondary structure in the selected regions.
16 Supplemental Table 1 libraries orrelation of stop counts in different replicates of Structure-seq Pearson correlation coefficient (P) 18S rrn a 25S rrn a (-) DMS replicate 1 vs. (-) DMS replicate (+) DMS replicate 1 vs. (+) DMS replicate (-) DMS replicate 1 vs. (+) DMS replicate (-) DMS replicate 2 vs. (+) DMS replicate a: ll the P values of P are less than 2.2E-16. 1
17 Supplemental Table 2 O enrichment of the highest and lowest 1% PPV in rice ID ene set name P value -log1(p value) Fold enrichment enes with the highest 1% PPV O:51171 Regulation of nitrogen compound metabolic process 1.68E O:6255 Regulation of macromolecule metabolic process 3.62E O:168 Regulation of gene expression 2.E O:6355 Regulation of transcription, DNdependent 1.51E O:1876 Lipid localization 3.77E enes with the lowest 1% PPV O:167 RN metabolic process 7.28E O:55 ell redox homeostasis.5e O:6811 Ion transport 1.E O:7165 Signal transduction 9.66E O:15979 Photosynthesis 6.13E
18 Supplemental Table 3 orrelation of m 6 modification and ini index in rice Region mrn a 5 TR b DS c 3 TR d m 6 enrichment vs. ini index P P value m 6 peak density vs. ini index P P value < 2.2E E E-8 < 2.2E-16 a: transcripts were analyzed; b: 282 transcripts were analyzed; c: transcripts were analyzed; d: 7 25 transcripts were analyzed. 3
19 Supplemental Table verage content a in our analyzed populations Region (mrn) (5' TR) (DS) (3' TR) Rice (n = 11,87).5 ± ± ±.91.1 ±.2. thaliana (n = 7,2).2 ± ± ± ±.38 a: Mean and SD are shown.
20 Supplemental Table 5 Details of enriched O terms listed in Figure 5B to 5E ID ene set name P value -log1(p value) Fold enrichment High sequence identity, high structure similarity O:3197 hromatin assembly 6.25E O:726 Small TPase mediated signal transduction 6.55E O:921 Ribonucleoside triphosphate biosynthetic process 3.76E O:61 Tricarboxylic acid cycle intermediate metabolic process 1.16E O:613 Translational initiation 1.75E O:6511 biquitin-dependent protein catabolic process 1.2E O:6352 DN-dependent transcription, initiation 3.3E High sequence identity, low structure similarity O:16192 Vesicle-mediated transport 1.5E O:283 Small molecule biosynthetic process 1.98E O:271 ellular nitrogen compound biosynthetic process 6.53E O:1651 arbohydrate biosynthetic process 2.1E O:925 lucan biosynthetic process 3.55E O:69 luconeogenesis 7.77E O:15995 hlorophyll biosynthetic process 1.81E Low sequence identity, high structure similarity O:6869 Lipid transport 9.81E O:51171 Regulation of nitrogen compound metabolic process 2.6E O:1556 Regulation of macromolecule biosynthetic process 3.E O:89 Regulation of primary metabolic process 6.7E O:6351 Transcription, DN-dependent 8.9E O:51252 Regulation of RN metabolic process 1.3E O:55 ell redox homeostasis 5.89E O:318 Nicotianamine biosynthetic process 7.99E Low sequence identity, low structure similarity O:5992 Trehalose biosynthetic process 1.8E O:6793 Phosphorus metabolic process 2.6E O:3687 Post-translational protein modification 3.7E O:2221 Response to chemical stimulus.88e O:668 Protein phosphorylation 1.5E O:6979 Response to oxidative stress 7.6E O:255 ell wall modification 8.3E
21 6
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