A Novel Candidate Cis-regulatory Motif Pair in the Promoters of Germline and Oogenesis Genes in C. Elegans

Overview

Journal Genome Res

Specialty Genetics

Date 2011 Sep 21

PMID 21930893

Citations 4

Authors

Chaim Linhart

Yonit Halperin

Amir Darom

Shahar Kidron

Limor Broday

Ron Shamir

Affiliations

Soon will be listed here.

Abstract

In this study we report on a novel pair of cis-regulatory motifs in promoter sequences of the nematode Caenorhabditis elegans. The motif pair exhibits extraordinary genomic traits: The order and the orientation of the two motifs are highly specific, and the distance between them is almost always one of two frequent distances. In contrast, the sequence between the motifs is variable across occurrences. Thus, the motif pair constitutes a nearly combinatorial sequence configuration. We further show that this module is conserved among, and unique to, the entire Caenorhabditis genus. By analyzing several gene expression data sets, our data suggest that this motif pair may function in germline development, oogenesis, and early embryogenesis. Finally, we verify that the motifs are indeed functional cis-regulatory elements using reporter constructs in transgenic C. elegans.

Citing Articles

Widespread transposon co-option in the germline regulatory network.

Carelli F, Cerrato C, Dong Y, Appert A, Dernburg A, Ahringer J Sci Adv. 2022; 8(50):eabo4082.

PMID: 36525485 PMC: 9757741. DOI: 10.1126/sciadv.abo4082.

Identification of Predictive Cis-Regulatory Elements Using a Discriminative Objective Function and a Dynamic Search Space.

Karnik R, Beer M PLoS One. 2015; 10(10):e0140557.

PMID: 26465884 PMC: 4605740. DOI: 10.1371/journal.pone.0140557.

Multiple small RNA pathways regulate the silencing of repeated and foreign genes in C. elegans.

Fischer S, Pan Q, Breen P, Qi Y, Shi Z, Zhang C Genes Dev. 2013; 27(24):2678-95.

PMID: 24352423 PMC: 3877757. DOI: 10.1101/gad.233254.113.

Regulatory elements of Caenorhabditis elegans ribosomal protein genes.

Sleumer M, Wei G, Wang Y, Chang H, Xu T, Chen R BMC Genomics. 2012; 13:433.

PMID: 22928635 PMC: 3575287. DOI: 10.1186/1471-2164-13-433.

References

Shostak Y, Van Gilst M, Antebi A, Yamamoto K . Identification of C. elegans DAF-12-binding sites, response elements, and target genes. Genes Dev. 2004; 18(20):2529-44. PMC: 529540. DOI: 10.1101/gad.1218504. View

Makeev V, Lifanov A, Nazina A, Papatsenko D . Distance preferences in the arrangement of binding motifs and hierarchical levels in organization of transcription regulatory information. Nucleic Acids Res. 2003; 31(20):6016-26. PMC: 219477. DOI: 10.1093/nar/gkg799. View

Ruvinsky I, Ruvkun G . Functional tests of enhancer conservation between distantly related species. Development. 2003; 130(21):5133-42. DOI: 10.1242/dev.00711. View

Inoue T, Wang M, Ririe T, Fernandes J, Sternberg P . Transcriptional network underlying Caenorhabditis elegans vulval development. Proc Natl Acad Sci U S A. 2005; 102(14):4972-7. PMC: 555976. DOI: 10.1073/pnas.0408122102. View

Praitis V . Creation of transgenic lines using microparticle bombardment methods. Methods Mol Biol. 2006; 351:93-107. DOI: 10.1385/1-59745-151-7:93. View

Kimble J, Crittenden S . Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol. 2007; 23:405-33. DOI: 10.1146/annurev.cellbio.23.090506.123326. View

Baugh L, Hill A, Slonim D, Brown E, Hunter C . Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development. 2003; 130(5):889-900. DOI: 10.1242/dev.00302. View

Kiontke K, Barriere A, Kolotuev I, Podbilewicz B, Sommer R, Fitch D . Trends, stasis, and drift in the evolution of nematode vulva development. Curr Biol. 2007; 17(22):1925-37. DOI: 10.1016/j.cub.2007.10.061. View

Brenner S . The genetics of Caenorhabditis elegans. Genetics. 1974; 77(1):71-94. PMC: 1213120. DOI: 10.1093/genetics/77.1.71. View

10.

Gaudet J, Mango S . Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science. 2002; 295(5556):821-5. DOI: 10.1126/science.1065175. View

11.

Halperin Y, Linhart C, Ulitsky I, Shamir R . Allegro: analyzing expression and sequence in concert to discover regulatory programs. Nucleic Acids Res. 2009; 37(5):1566-79. PMC: 2655690. DOI: 10.1093/nar/gkn1064. View

12.

Hubbard E, Greenstein D . Introduction to the germ line. WormBook. 2007; :1-4. PMC: 4781435. DOI: 10.1895/wormbook.1.18.1. View

13.

. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 1998; 282(5396):2012-8. DOI: 10.1126/science.282.5396.2012. View

14.

Merritt C, Rasoloson D, Ko D, Seydoux G . 3' UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol. 2008; 18(19):1476-82. PMC: 2585380. DOI: 10.1016/j.cub.2008.08.013. View

15.

Berman B, Nibu Y, Pfeiffer B, Tomancak P, Celniker S, Levine M . Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci U S A. 2002; 99(2):757-62. PMC: 117378. DOI: 10.1073/pnas.231608898. View

16.

Margalit A, Neufeld E, Feinstein N, Wilson K, Podbilewicz B, Gruenbaum Y . Barrier to autointegration factor blocks premature cell fusion and maintains adult muscle integrity in C. elegans. J Cell Biol. 2007; 178(4):661-73. PMC: 2064472. DOI: 10.1083/jcb.200704049. View

17.

Kimble J, White J . On the control of germ cell development in Caenorhabditis elegans. Dev Biol. 1981; 81(2):208-19. DOI: 10.1016/0012-1606(81)90284-0. View

18.

Hobert O . Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc Natl Acad Sci U S A. 2008; 105(51):20067-71. PMC: 2629285. DOI: 10.1073/pnas.0806070105. View

19.

Hansen D, Wilson-Berry L, Dang T, Schedl T . Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development. 2003; 131(1):93-104. DOI: 10.1242/dev.00916. View

20.

Swoboda P, Adler H, Thomas J . The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell. 2000; 5(3):411-21. DOI: 10.1016/s1097-2765(00)80436-0. View