Arabidopsis small nucleolar RNA monitors the efficient pre-rRNA processing during ribosome biogenesis

Abstract

Ribosome production in eukaryotes requires the complex and precise coordination of several hundred assembly factors, including many small nucleolar RNAs (snoRNAs). However, at present, the distinct role of key snoRNAs in ribosome biogenesis remains poorly understood in higher plants. Here we report that a previously uncharacterized C (RUGAUGA)/D (CUGA) type snoRNA, HIDDEN TREASURE 2 (HID2), acts as an important regulator of ribosome biogenesis through a snoRNA–rRNA interaction. Nucleolus-localized HID2 is actively expressed in Arabidopsis proliferative tissues, whereas defects in HID2 cause a series of developmental defects reminiscent of ribosomal protein mutants. HID2 associates with the precursor 45S rRNA and promotes the efficiency and accuracy of pre-rRNA processing. Intriguingly, disrupting HID2 in Arabidopsis appears to impair the integrity of 27SB, a key pre-rRNA intermediate that generates 25S and 5.8S rRNA and is known to be vital for the synthesis of the 60S large ribosomal subunit and also produces an imbalanced ribosome profile. Finally, we demonstrate that the antisense-box of HID2 is both functionally essential and highly conserved in eukaryotes. Overall, our study reveals the vital and possibly conserved role of a snoRNA in monitoring the efficiency of pre-rRNA processing during ribosome biogenesis.

Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

“…Intriguingly, the predicted HID2 methylation target site in the 25S rRNA sequence is not affected in the hid2 mutant. HID2 is thought to play a role in promoting pre-rRNA processing and minimizing the production of aberrant rRNA species (Zhu et al, 2016).…”

Ribosomal RNA Biogenesis and Its Response to Chilling Stress in Oryza sativa

“…Three sites (P, P9, and A1 [P2]) exist in the 59 ETS, four (D, A2, A3, and B1) in ITS1, three (E, C2, and C1) in ITS2, and two in the 39 ETS (B2 and B0;Sáez-Vasquez et al, 2004a, 2004bZakrzewska-Placzek et al, 2010;Lange et al, 2011;Weis et al, 2015aWeis et al, , 2015bSikorski et al, 2015;Tomecki et al, 2017). Moreover, functional studies of ribosome biogenesis mutants have identified the series of rRNA intermediates that occur during pre-rRNA processing (Lange et al, 2008(Lange et al, , 2011Abbasi et al, 2010;Zakrzewska-Placzek et al, 2010;Ohbayashi et al, 2011;Kumakura et al, 2013;Missbach et al, 2013;Hang et al, 2014;Weis et al, 2014Weis et al, , 2015bSikorski et al, 2015;Zhu et al, 2016). The high abundance of the P-A3 intermediate, which is easily detected in vivo, defines the major ITS1-first pathway in Arabidopsis, in which ITS1 cleavage at A3 occurs before complete removal of the 59 ETS in the 35S(P) primary transcript (Zakrzewska-Placzek et al, 2010;Lange et al, 2011;Sikorski et al, 2015).…”

Maize Urb2 protein is required for kernel development and vegetative growth by affecting pre‐ribosomal RNA processing

“…NRO assay was performed as described by Zhu et al (2016). To determine the transcription rate of 35S pre-rRNA, the isolated nuclei were incubated in 0.8 mM biotin-UTP (Roche), 4 mM A/G/CTP (New England Biolabs) and 1 U ll À1 RNase for 20 min at 30°C.…”

“…For example, TOGR1 (Thermotolerant Growth Required 1), a DEAD‐box RNA helicase that functions as a key chaperone for rRNA biogenesis, is required for rice thermotolerance, and TOGR1 overexpression significantly improves rice growth under hot conditions (Wang et al ., ). An Arabidopsis C/D box snoRNA, HIDDEN TREASURE 2 (HID2), is associated with the precursor 45S rRNA and promotes the efficiency and accuracy of pre‐rRNA processing; knockdown of HID2 impairs normal growth and development of Arabidopsis (Zhu et al ., ). In another example, a circularly permuted order of GTPase, LSG1‐2, physically associates with ribosomes, and the lsg1‐2 loss‐of‐function mutant has three cotyledons and upward curled leaves (Weis et al ., ).…”