The Orphan Gene Regulates Dauer Development and Intraspecific Competition in Nematodes by Copy Number Variation

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The nematode dauer stage represents the major survival and dispersal strategy, and had a remarkable impact in the evolutionary and ecological success of nematodes. Our recent work in Pristionchus pacificus revealed substantial natural variation in various aspects of dauer development, i.e. pheromone production and sensing and dauer longevity and fitness, including a strain from Ohio with extremely long-lived dauers, very high fitness and high dauer formation in response to other strains´ pheromones. However, the molecular mechanisms associated with natural variation in dauer development are currently unknown. Using quantitative-trait-loci analysis, we discovered that the orphan gene dauerless controls dauer formation by copy number variation. Strains with one dauerless copy show high dauer formation, whereas strains with two copies have strongly reduced dauer formation. Transgenic animals expressing multiple copies do not form dauers. dauerless is exclusively expressed in CAN neurons, and both CAN ablation and dauerless mutations increase dauer formation. Strikingly, dauerless underwent several duplications and acts in parallel or downstream of steroid-hormone signaling but upstream of the nuclear-hormone-receptor daf-12. Our findings reveal the importance of gene duplications and copy number variations for orphan gene function and suggest daf-12 as major target for dauer regulation.

Vyšlo v časopise: The Orphan Gene Regulates Dauer Development and Intraspecific Competition in Nematodes by Copy Number Variation. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005146
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005146

Souhrn

Zdroje

1. Sommer RJ, Ogawa A. Hormone Signaling and Phenotypic Plasticity in Nematode Development and Evolution. Curr Biol. 2011;21: R758–R766. doi: 10.1016/j.cub.2011.06.034 21959166

2. Cassada RC, Russell RL. The Dauerlarva, a Post-Embryonic Developmental Variant of the Nematode Caenorhabditis elegans. Dev Biol. 1975;46: 326–342. 1183723

3. Herrmann M, Mayer WE, Hong RL, Kienle S, Minasaki R, Sommer RJ. The Nematode Pristionchus pacificus (Nematoda: Diplogastridae) Is Associated with the Oriental Beetle Exomala orientalis (Coleoptera: Scarabaeidae) in Japan. Zool Sci. 2007;24: 883–889. 17960992

4. Morgan K, McGaughran A, Villate L, Herrmann M, Witte H, Bartelmes G, et al. Multi locus analysis of Pristionchus pacificus on La Réunion Island reveals an evolutionary history shaped by multiple introductions, constrained dispersal events and rare outcrossing. Mol Ecol. 2012;21: 250–266. doi: 10.1111/j.1365-294X.2011.05382.x 22126624

5. Perry RN, Wharton DA. Molecular and Physiological Basis of Nematode Survival. Chippenham: CABI; 2011.

6. Hu PJ. Dauer. In: WormBook. The C. elegans Research Community; 2007.

7. Schroeder FC. Modular Assembly of Primary Metabolic Building Blocks: A Chemical Language in C. elegans. Chem Biol. 2015. In press.

8. Antebi A, Yeh W- H, Tait D, Hedgecock EM, Riddle DL. daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev. 2000;14: 1512–1527. 10859169

9. Motola DL, Cummins CL, Rottiers V, Sharma KK, Li T, Li Y, et al. Identification of Ligands for DAF-12 that Govern Dauer Formation and Reproduction in C. elegans. Cell. 2006;124: 1209–1223. 16529801

10. Mahanti P, Bose N, Bethke A, Judkins JC, Wollam J, Dumas KJ, et al. Comparative metabolomics reveals endogenous ligands of DAF-12, a nuclear hormone receptor, regulating C. elegans development and lifespan. Cell Metab. 2014;19: 73–83. doi: 10.1016/j.cmet.2013.11.024 24411940

11. Bose N, Meyer JM, Yim JJ, Mayer MG, Markov GV, Ogawa A, et al. Natural Variation in Dauer Pheromone Production and Sensing Supports Intraspecific Competition in Nematodes. Curr Biol. 2014;24: 1536–1541. doi: 10.1016/j.cub.2014.05.045 24980503

12. Bose N, Ogawa A, von Reuss SH, Yim JJ, Ragsdale EJ, Sommer RJ, et al. Complex Small-Molecule Architectures Regulate Phenotypic Plasticity in a Nematode. Angew Chem. 2012;51: 12438–12443.

13. Mayer MG, Sommer RJ. Natural variation in Pristionchus pacificus dauer formation reveals cross-preference rather than self-preference of nematode dauer pheromones. Proc R Soc B. 2011;278: 2784–2790. doi: 10.1098/rspb.2010.2760 21307052

14. Dawkins R, Krebs JR. Arms Races between and within Species. Proc R Soc B. 1979;205: 489–511.

15. Schluter D. Ecology of Adaptive Radiation. Oxford: Oxford University Press; 2000.

16. Dubnau D, Losick R. Bistability in bacteria. Mol Microbiol. 2006;61: 564–572. 16879639

17. Srinivasan J, Sinz W, Lanz C, Brand A, Nandakumar R, Raddatz G, et al. A Bacterial Artificial Chromosome-Based Genetic Linkage Map of the Nematode Pristionchus pacificus. Genetics. 2002;162: 129–134. 12242228

18. Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, Dinkelacker I, et al. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet. 2008;40: 1193–1198. doi: 10.1038/ng.227 18806794

19. Rödelsperger C, Streit A, Sommer RJ. Structure, Function and Evolution of The Nematode Genome. In: eLS. Chichester: John Wiley & Sons, Ltd; 2013.

20. Sinha A, Sommer RJ, Dieterich C. Divergent gene expression in the conserved dauer stage of the nematodes Pristionchus pacificus and Caenorhabditis elegans. BMC Genomics. 2012;13: 254–270. doi: 10.1186/1471-2164-13-254 22712530

21. Borchert N, Dieterich C, Krug K, Schütz W, Jung S, Nordheim A, et al. Proteogenomics of Pristionchus pacificus reveals distinct proteome structure of nematode models. Genome Res. 2010;20: 837–846. doi: 10.1101/gr.103119.109 20237107

22. Rödelsperger C, Neher RA, Weller A, Eberhardt G, Witte H, Mayer WE, et al. Characterization of genetic diversity in the nematode Pristionchus pacificus from population-scale resequencing data. Genetics. 2014;196: 1153–1165. doi: 10.1534/genetics.113.159855 24443445

23. Witte H, Moreno E, Rödelsperger C, Kim J, Kim J, Streit A, et al. Gene inactivation using the CRISPR/Cas9 system in the nematode Pristionchus pacificus. Dev Genes Evol. 2015. In press.

24. Ogawa A, Streit A, Antebi A, Sommer RJ. A Conserved Endocrine Mechanism Controls the Formation of Dauer and Infective Larvae in Nematodes. Curr Biol. 2009;19: 67–71. doi: 10.1016/j.cub.2008.11.063 19110431

25. Carroll SB. Endless forms most beautiful. New York: Norton; 2005.

26. Sommer RJ, Streit A. Comparative Genetics and Genomics of Nematodes: Genome Structure, Development, and Lifestyle. Ann Rev Genet. 2011;45: 1–20. doi: 10.1146/annurev-genet-110410-132417 21721943

27. Schmid KJ, Tautz D. A screen for fast evolving genes from Drosophila. PNAS. 1997;94: 9746–9750. 9275195

28. Drosophila 12 Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 2007;450: 203–218. 17994087

29. Chain FJJ, Feulner PGD, Panchal M, Eizaguirre C, Samonte IE. Extensive Copy-Number Variation of Young Genes across Stickleback Populations. PLoS Genet. 2014;10: e1004830. doi: 10.1371/journal.pgen.1004830 25474574

30. Schlager B, Wang X, Braach G, Sommer RJ. Molecular cloning of a dominant roller mutant and establishment of DNA-mediated transformation in the nematode Pristionchus pacificus. Genesis. 2009;47: 300–304. doi: 10.1002/dvg.20499 19298013

31. West-Eberhard MJ. Developmental plasticity and evolution. New York: Oxford University Press; 2003.

32. Sommer RJ, Carta LK, Kim S-Y, Sternberg PW. Morphological, genetic and molecular description of Pristionchus pacificus sp. n. (Nematoda: Neodiplogastridae). Fund Appl Nemat. 1996;19: 511–521.

33. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 2003;19: 889–890. 12724300

34. Sommer RJ, Sternberg PW. Apoptosis and change of competence limit the size of the vulva equivalence group in Pristionchus pacificus: a genetic analysis. Curr Biol. 1996;6: 52–59. 8805221

35. Xie C, Tammi MT. CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics. 2009;10: 80. doi: 10.1186/1471-2105-10-80 19267900

36. Ragsdale EJ, Müller MR, Rödelsperger C, Sommer RJ. A Developmental Switch Coupled to the Evolution of Plasticity Acts through a Sulfatase. Cell. 2013;155: 922–933. doi: 10.1016/j.cell.2013.09.054 24209628

37. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7: 562–578. doi: 10.1038/nprot.2012.016 22383036

38. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res. 2004;32: 1792–1797. 15034147

39. Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27: 592–593. doi: 10.1093/bioinformatics/btq706 21169378

40. Darriba D, Taboada GL, Doallo R, Posada D. ProTest 3: fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27: 1164–1165 doi: 10.1093/bioinformatics/btr088 21335321