Tuning the ribosome: The influence of rRNA modification on eukaryotic ribosome biogenesis and function

Figures & data

Table 1. Inventory of rRNA modifications in yeast. The rRNA, position (Posn.) and type (Mod.) of the modification and the enzyme/snoRNP(s) that introduce it are given, with information on whether partial modification was observed (✓; <85%)²¹ or not (x), and whether modification occurs early/chromatin-associated (E),¹⁸ in late nucleolar/nuclear (LN) particles or in the cytoplasm (C). A lack of information on the timing is indicated by “–.” Enzymes/snoRNPs targeting the same position sequentially are separated by “,” and alternative enzymes/snoRNPs that can install a single modification at a given site are separated by “/”. The information presented in this table is compiled from various references cited in the text.

rRNA	Posn.	Mod.	Enzyme/snoRNP	Partial	Timing	rRNA	Posn.	Mod.	Enzyme/snoRNP	Partial	Timing
18S	28	Am	snR74	x	E	18S	1415	Ψ	snR83	✓	—
18S	100	Am	snR51	✓	LN	18S	1428	Gm	snR56	x	E
18S	106	Ψ	snR44	x	—	18S	1572	Gm	snR57	x	E
18S	120	Ψ	snR49	x	—	18S	1575	m^7G	Bud23	x	—
18S	211	Ψ	snR49	✓	—	18S	1639	Cm	snR70	✓	E
18S	302	Ψ	snR49	x	—	18S	1773	ac^4C	Kre33	x	—
18S	414	Cm	U14	x	E	18S	1781	m2^6A	Dim1	x	C
18S	420	Am	snR52	x	E	18S	1782	m2^6A	Dim1	x	C
18S	436	Am	snR87	✓	E	5.8S	73	Ψ	snR43	✓	—
18S	466	Ψ	snR189	✓	—	25S	645	m^1A	Rrp8 (Bmt1)	x	—
18S	541	Am	snR41	x	E	25S	649	Am	U18	x	E
18S	562	Gm	?	✓	E	25S	650	Cm	U18	x	E
18S	578	Um	snR77	x	E	25S	663	Cm	snR58	✓	E
18S	619	Am	snR47	x	E	25S	776	Ψ	snR80	x	—
18S	632	Ψ	snR161	✓	—	25S	805	Gm	snR39b	x	E
18S	759	Ψ	snR80	x	—	25S	807	Am	snR39/snR59	x	E
18S	766	Ψ	snR161	x	—	25S	817	Am	snR60	x	LN
18S	796	Am	snR53	x	E	25S	867	Gm	snR50	✓	LN
18S	974	Am	snR54	x	E	25S	876	Am	snR72	✓	LN
18S	999	Ψ	snR31	✓	—	25S	898	Um	snR40	x	LN
18S	1007	Cm	snR79	x	E	25S	908	Gm	snR60	x	E
18S	1126	Gm	snR41	x	E	25S	956	m^3U	Bmt5	x	—
18S	1181	Ψ	snR85	x	—	25S	960	Ψ	snR8	x	—
18S	1187	Ψ	snR36	x	—	25S	966	Ψ	snR43	x	—
18S	1191	m^1acp^3Ψ	snR35,Emg1,Tsr3	x	E,LN,C	25S	986	Ψ	snR8	x	—
18S	1269	Um	snR55	x	E	25S	990	Ψ	snR49	x	—
18S	1271	Gm	snR40	x	E	25S	1004	Ψ	snR5	✓	—
18S	1280	ac^4C	Kre33	✓	—	25S	1042	Ψ	snR33	x	—
18S	1290	Ψ	snR83	x	—	25S	1052	Ψ	snR81	x	—
25S	1056	Ψ	snR44	x	—	25S	2351	Ψ	snR82	x	—
25S	1110	Ψ	snR82	✓	—	25S	2416	Ψ	snR11	x	—
25S	1124	Ψ	snR5	x	—	25S	2417	Um	snR66	x	E
25S	1133	Am	snR61	x	E	25S	2421	Um	snR78	x	LN
25S	1437	Cm	U24	x	E	25S	2619	Gm	snR67	x	E
25S	1449	Am	U24	x	E	25S	2634	m^3U	Bmt5	x	—
25S	1450	Gm	U24	x	E	25S	2640	Am	snR68	x	LN
25S	1888	Um	snR62	x	—	25S	2724	Um	snR67	x	E
25S	2129	Ψ	snR3	x	—	25S	2729	Um	snR51	✓	E
25S	2133	Ψ	snR3	x	—	25S	2735	Ψ	snR189	x	—
25S	2142	m^1A	Bmt2	x	—	25S	2791	Gm	snR48	x	E
25S	2191	Ψ	snR32	x	—	25S	2793	Gm	snR48	x	E
25S	2197	Cm	snR76	x	E	25S	2815	Gm	snR38	x	E
25S	2220	Am	snR47	x	E	25S	2826	Ψ	snR34	x	—
25S	2256	Am	snR63	x	LN	25S	2843	m^3U	Bmt6	x	—
25S	2258	Ψ	snR191	x	—	25S	2865	Ψ	snR46	x	—
25S	2260	Ψ	snR191	x	—	25S	2870	m^5C	Nop2 (Bmt4)	x	—
25S	2264	Ψ	snR3	x	—	25S	2880	Ψ	snR34	x	—
25S	2266	Ψ	snR84	x	—	25S	2921	Um	snR52/Sbp1	x	E
25S	2278	m^5C	Rcm1 (Bmt3)	x	—	25S	2922	Gm	Sbp1	x	LN
25S	2280	Am	snR13	x	E	25S	2923	Ψ	snR10	x	—
25S	2281	Am	snR13	x	E	25S	2944	Ψ	snR37	✓	—
25S	2288	Gm	snR75	x	E	25S	2946	Am	snR71	x	E
25S	2314	Ψ	snR86	x	—	25S	2948	Cm	snR69	x	E
25S	2337	Cm	snR64	x	—	25S	2959	Cm	snR73	x	E
25S	2340	Ψ	snR9	x	—	25S	2975	Ψ	snR42	x	—
25S	2347	Um/Ψ/Ψm	snR65,snR9	x	—	5S	50	Ψ	Pus7	x	—
25S	2349	Ψ	snR82	x	—

Figure 1. Structures of box C/D and box H/ACA sRNP complexes. (A) Structural model of an H/ACA box sRNP from Pyrococcus furiosus (PDB 3HAY)¹⁵⁴ A surface view of the protein components is shown and sRNA and rRNA are indicated in dark gray and red, respectively. (B) Structural model of a Sulfolobus solfataricus box C/D sRNP (PDB 3PLA)¹⁵⁵ is shown as in A. The modified nucleotide is shown in surface view. Note, that archaeal L7Ae is an ortholog of eukaryotic Snu13 and in eukaryotes, Nop56 and Nop58 are orthologous to archaeal Nop5.

Figure 2. Base modifications in rRNA and the enzymes that install them. (A) Chemical structures of the 4 nucleotides and the modifications that are added in yeast rRNAs. The additional chemical groups are marked in red and the enzymes that introduce them in yeast are indicated above the arrow (yellow) and in humans below the arrow (green). (B) Three-step modification pathway for U1191 of the 18S rRNA in yeast.

Figure 3. Distribution of rRNA modifications on the yeast ribosome. The S. cerevisiae 80S ribosome (PBD 4V88)⁶ is shown – 40S in teal and 60S in gray. The positions of 2′-O-methylations (purple), pseudouridines (blue) and base modification installed by stand-alone enzymes (orange) are indicated. Three functionally important regions of the ribosome, the peptidyltransferase center (PTC), the decoding site and the intersubunit bridge eB14, are also shown in a magnified view.

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