HMO1 is a high-mobility group B protein that plays a role in transcription of genes encoding rRNA and ribosomal proteins (RPGs) in Saccharomyces cerevisiae. This study uses genome-wide chromatin immunoprecipitation to study the roles of HMO1, FHL1, and RAP1 in transcription of these genes as well as other RNA polymerase II-transcribed genes in yeast. The results show that HMO1 associates with the 35S rRNA gene in an RNA polymerase I-dependent manner and that RPG promoters (138 in total) can be classified into several distinct groups based on HMO1 abundance at the promoter and the HMO1 dependence of FHL1 and/or RAP1 binding to the promoter. FHL1, a key regulator of RPGs, binds to most of the HMO1-enriched and transcriptionally HMO1-dependent RPG promoters in an HMO1-dependent manner, whereas it binds to HMO1-limited RPG promoters in an HMO1-independent manner, irrespective of whether they are transcribed in an HMO1-dependent manner. Reporter gene assays indicate that these functional properties are determined by the promoter sequence.The yeast ribosome is composed of four rRNAs and 79 ribosomal proteins (RPs) (58, 73). Yeast rRNA genes occur as a tandem repeat of approximately 150 copies. The 25S, 18S, and 5.8S RNAs are transcribed by RNA polymerase I (Pol I), 5S RNA is transcribed by RNA Pol III, and the 138 RP genes (RPGs) are transcribed by RNA Pol II (58,73). In a rapidly growing cell, transcription of rRNA and RPGs accounts for approximately 60% of total transcription and 50% of Pol IImediated transcription, respectively (73), representing a large fraction of the total energy consumption of the cell. Little is known about the regulatory mechanisms involved in coordinating the transcription of rRNA and RPGs under various growth conditions. Recent studies showed that the TOR complex 1 (TORC1) plays a central role in regulating transcription of rRNA and RPGs in response to changes in the abundance of extracellular nutrients (44). Under favorable nutrient conditions, TORC1 is localized to the nucleus and directly binds to the 35S rDNA promoter to activate transcription by Pol I (36). TORC1 also indirectly regulates Pol II-mediated RPG transcription by recruiting IFH1, a coactivator for FHL1 (45,58,60,72). FHL1 was originally identified as a suppressor of a Pol III mutant (24) and was later shown to be important for RPG transcription (27,34,45,58,60,72). Under poor nutrient conditions, TORC1 is exported from the nucleus to the cytoplasm, so that the synthesis of 35S rRNA is substantially diminished (36). Concurrently, CRF1, a corepressor for FHL1, displaces IFH1 from RPG promoters to inhibit RPG transcription (45).HMO1 is a member of the high-mobility group B (HMGB) protein family, which include nonhistone proteins that bind to and have diverse roles in eukaryotic chromatin. HMGB proteins contain one or more distinctive DNA-binding motifs known as "HMG boxes" (11, 69). The HMG box is a conserved protein structural motif, in which three alpha helices are arranged in an L shape (55, 74). As the HMG box domain binds...

Saccharomyces cerevisiae HMO1, a high mobility group B (HMGB) protein, associates with the rRNA locus and with the promoters of many ribosomal protein genes (RPGs). Here, the Sos recruitment system was used to show that HMO1 interacts with TBP and the N-terminal domain (TAND) of TAF1, which are integral components of TFIID. Biochemical studies revealed that HMO1 copurifies with TFIID and directly interacts with TBP but not with TAND. Deletion of HMO1 (Δhmo1) causes a severe cold-sensitive growth defect and decreases transcription of some TAND-dependent genes. Δhmo1 also affects TFIID occupancy at some RPG promoters in a promoter-specific manner. Interestingly, over-expression of HMO1 delays colony formation of taf1 mutants lacking TAND (taf1ΔTAND), but not of the wild-type strain, indicating a functional link between HMO1 and TAND. Furthermore, Δhmo1 exhibits synthetic growth defects in some spt15 (TBP) and toa1 (TFIIA) mutants while it rescues growth defects of some sua7 (TFIIB) mutants. Importantly, Δhmo1 causes an upstream shift in transcriptional start sites of RPS5, RPS16A, RPL23B, RPL27B and RPL32, but not of RPS31, RPL10, TEF2 and ADH1, indicating that HMO1 may participate in start site selection of a subset of class II genes presumably via its interaction with TFIID.