A current view on long noncoding RNAs in yeast and filamentous fungi

Abstract

Long noncoding RNAs (lncRNAs) are crucial players in epigenetic regulation. They were initially discovered in human, yet they emerged as common factors involved in a number of central cellular processes in several eukaryotes. For example, in the past decade, research on lncRNAs in yeast has steadily increased. Several examples of lncRNAs were described in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Also, screenings for lncRNAs in ascomycetes were performed and, just recently, the first full characterization of a lncRNA was performed in the filamentous fungus Trichoderma reesei. In this review, we provide a broad overview about currently known fugal lncRNAs. We make an attempt to categorize them according to their functional context, regulatory strategies or special properties. Moreover, the potential of lncRNAs as a biotechnological tool is discussed.

Keywords: Long noncoding RNA; Saccharomyces cerevisiae; Schizosaccharomyces pombe; Trichoderma reesei; Yeast; lncRNA.

Fig. 1

Regulation of meiotic gene expression in S. pombe by meiRNA. Two isoforms of meiRNA differing in length result from variation of the polyadenylation sites: meiRNA-L and meiRNA-S. The long version meiRNA-L has the more striking role in meiosis progression. Upon the onset of meiosis, meiRNA-L accumulates with its binding partner Mei2 at the sme2 locus that governs baiting and inhibition of the key-silencing factor Mmi1. Thus, meiosis specific genes, which are destabilized by Mmi1 during mitosis, are stably expressed. Moreover, meiRNA-L mediates chromosome pairing during the meiotic prophase. During mitosis, Mei2 is not produced and meiRNA is destabilized by Mmi1-directed exosome degradation. Thus, Mmi1 is active and causes gene silencing by mediating exosome degradation, recruitment of the RNA degradation complexes MTREC and NURS, as well as the RNAi machinery (the histone methyltransferase Clr4 and the RNAi effector complex RITS) and by promoting heterochromatin formation

Fig. 2

Response to extracellular inorganic phosphate in S. pombe. a Inversely correlated expression of tgp1 and the lncRNA nc-tgp1 in the presence or absence of phosphate. Under phosphate-rich conditions, the lncRNA nc-tgp1 is transcribed and blocks the expression of its sense gene tgp1 by modulation of the local nucleosome arrangement and promoting the dissociation of the central transactivator Pho7. Upon phosphate starvation, nc-tgp1 initiation is prevented, thus allowing binding of Pho7 and expression of tgp1. b Inversely correlated expression of pho84 and the lncRNA prt2 as well as pho1 and the lncRNA prt in the presence or absence of phosphate. Under phosphate-rich conditions, the lncRNA prt2 is transcribed and blocks the expression of its sense gene pho84 by an unknown mechanism. Similarly, the adjacent lncRNA prt is transcribed and blocks the expression of its sense gene pho1 by promoting the dissociation of the central transactivator Pho7. Upon phosphate starvation, prt2 initiation is prevented; thus, Pho84 is produced and in turn acts as a repressor of prt transcription, finally resulting in the expression of pho1

Fig. 3

Regulation of cellulase gene expression by the lncRNA HAX1 in T. reesei. Three isoforms of HAX1 differing in length result from variation of the transcription start point in different T. reesei strains: HAX1_QM6a, HAX1_QM9414 and HAX1_Rut-C30. They act as activators of cellulase expression. The longest version HAX1_Rut-C30 has a higher impact on the cellulase activity compared to HAX1_QM9414 and HAX1_QM6a (indicated by triple, double and single plus symbols, respectively). The regulatory mechanism of HAX1 is unknown, yet an interplay with the main transactivator Xyr1 is supposed. For details, see text