Selection is no more efficient in haploid than in diploid life stages of an angiosperm and a moss

Molecular Biology and Evolution

Volumn 30, Issue 8, 2013, Pages 1929-1939

  Szövényi, Péter ^a,b,c   Ricca, Mariana ^a,b   Hock, Zsófia ^a   Shaw, Jonathan A ^d   Shimizu, Kentaro K ^a   Wagner, Andreas ^a,b,e,f  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BIOINFORMATICS INSTITUTE   (Singapore)

^f SANTA FE INSTITUTE   (United States)

Author keywords

Biphasic life cycle; Diploid; Evolutionary rate; Expression breadth; Expression noise; Haploid; High throughput sequencing; Masking

Indexed keywords

ALLELE; ANGIOSPERM; ARABIDOPSIS THALIANA; ARTICLE; DIPLOIDY; EVOLUTIONARY RATE; FUNARIA HYGROMETRICA; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; HAPLOIDY; LIFE CYCLE; MOLECULAR EVOLUTION; MOSS; NATURAL SELECTION; NONHUMAN; ANIMAL; EVOLUTION; FEMALE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; MALE; BIPHASIC LIFE CYCLE; EXPRESSION BREADTH; EXPRESSION NOISE; HAPLOID; HIGH THROUGHPUT SEQUENCING; MASKING;

ANGIOSPERMS; ANIMALS; BIOLOGICAL EVOLUTION; BRYOPHYTA; DIPLOIDY; EVOLUTION, MOLECULAR; FEMALE; HAPLOIDY; LIFE CYCLE STAGES; MALE; POLYMORPHISM, GENETIC; SELECTION, GENETIC;

BIPHASIC LIFE CYCLE; DIPLOID; EVOLUTIONARY RATE; EXPRESSION BREADTH; EXPRESSION NOISE; HAPLOID; HIGH THROUGHPUT SEQUENCING; MASKING;

EID: 84888589655     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst095     Document Type: Article

References (65)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA. 2003. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol. 133: 713-725.
3. Bell G. 1997. The evolution of the life cycle of brown seaweeds. Biol J Linn Soc. 60:21-38.
4. Bell G. 2008. Selection: the mechanism of evolution, 2nd edition. Oxford: Oxford University Press.
5. Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH. 2011. Porphyra: a marine crop shaped by stress. Trends Plant Sci. 16:29-37.
6. Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijó JA, Becker JD. 2008. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148:1168-1181.
7. Byers DL, Waller DM. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Evol Syst. 30:479-513.
8. Charlesworth D, Charlesworth B. 1992. The effects of selection in the gametophyte stage on mutational load. Evolution 46:703-720.
9. Charlesworth D, Willis J. 2009. The genetics of inbreeding depression. Nat Rev Genet. 10:783-796.
10. Cook DL, Gerber AN, Tapscott SJ. 1998. Modeling stochastic gene expression: implications for haploinsufficiency. Proc Natl Acad Sci U S A. 95:15641-15646.
11. Destombe C, Godin J, Nocher M, Richerd S, Valero M. 1993. Differences in response between haploid and diploid isomorphic phases of Gracilaria verrucosa (Rhodophyta: Gigartinales) exposed to artificial environmental conditions. Hydrobiologia 261:131-137.
12. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
13. Gan X, Stegle O, Behr J, et al. (23 co-authors). 2011. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419-423.
14. Gene Ontology Consortium. 2005. Gene ontology: tool for the unification of biology. Nat Genet. 25:25-29.
15. Gerstein AC, Cleathero LA, Mandegar MA, Otto SP. 2011. Haploids adapt faster than diploids across a range of environments. J Evol Biol. 24:531-540.
16. Gossmann TI, Song BH, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A. 2010. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol Biol Evol. 27:1822-1832.
17. Grabherr MG, Haas BJ, Yassour M, et al. (21 co-authors). 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644-652.
18. Haerizadeh F, Wong CE, Bhalla PL, Gresshoff PM, Singh MB. 2009. Genomic expression profiling of mature soybean (Glycine max) pollen. BMC Plant Biol. 9:25.
19. Hafidh S, Breznenová K, Růžička P, Feciková J, Capková V, Honys D. 2012. Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biol. 12:24.
20. Henter HJ. 2003. Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa. Evolution 57:1793-1803.
21. Holloway AK, Lawniczak MKN, Mezey JG, Begun DJ, Jones CD. 2007. Adaptive gene expression divergence inferred from population genomics. PLoS Genet. 3:2007-2013.
22. Honys D, Twell D. 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132:640-652.
23. Hu TT, Pattyn P, Bakker EG, et al. (30 co-authors). 2011. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 43:476-481.
24. Johnston AJ, Meier P, Gheyselinck J, Wuest SE, Federer M, Schlagenhauf E, Becker JD, Grossniklaus U. 2007. Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol. 8:R204.
25. Kondrashov A, Crow J. 1991. Haploidy or diploidy - which is better. Nature 351:314-315.
26. Koonin EV. 2011. Are there laws of genome evolution? PLoS Comput Biol. 7:e1002173.
27. Krumbiegel R. 1979. Response of haploid and diploid protoplasts from Datura innoxia Mill. and Petunia hybrida L. to treatment with X-rays and a chemical mutagen. Environ Exp Bot. 19:99-103.
28. Lassmann T, Hayashizaki Y, Daub CO. 2009. TagDust - a program to eliminate artifacts from next generation sequencing data. Bioinformatics 25:2839-2840.
29. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323.
30. Ma J, Skibbe DS, Fernandes J, Walbot V. 2008. Male reproductive development: gene expression profiling of maize anther and pollen ontogeny. Genome Biol. 9:R181.
31. Mable BK, Otto SP. 2001. Masking and purging mutations following EMS treatment in haploid, diploid and tetraploid yeast (Saccharomyces cerevisiae). Genet Res. 77:9-26.
32. Muralla R, Lloyd J, Meinke D. 2011. Molecular foundations of reproductive lethality in Arabidopsis thaliana. PLoS One 6:e28398.
33. Onodera Y, Nakagawa K, Haag JR, Pikaard D, Mikami T, Ream T, Ito Y, Pikaars CS. 2008. Sex-biased lethality or transmission of defective transcription machinery in Arabidopsis. Genetics 180:207-218.
34. Orr HA, Otto SP. 1994. Does diploidy increase the rate of adaptation? Genetics 136:1475-1480.
35. Otto SP. 2004. Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proc Biol Sci. 271:705-714.
36. Otto SP, Gerstein AC. 2008. The evolution of haploidy and diploidy. Curr Biol. 18:R1121-R1124.
37. Park SG, Choi SS. 2010. Expression breadth and expression abundance behave differently in correlations with evolutionary rates. BMC Evol Biol. 10:241.
38. Pina C, Pinto F, Feijo JA, Becker JD. 2005. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol. 138:744-756.
39. R Development Core Team. 2011. R: a language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing [cited 2013 May 3]. Available from: http://www.R-project.org/
40. Rensing SA, Lang D, Zimmer AD, et al. (70 co-authors). 2008. The genome of the moss Physcomitrella patens reveals evolutionary insights into the conquest of land by plants. Science 319:64-69.
41. Rost B. 1999. Twilight zone of protein sequence alignments. Protein Eng. 12:85-94.
42. Russell SD, Gou X, Wong CE, Wang X, Yuan T, Wei X, Bhalla PL, Singh MB. 2012. Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol. 195:560-573.
43. Schein M, Yang Z, Mitchell-Olds T, Schmid KJ. 2004. Rapid evolution of a pollen-specific oleosin-like gene family from Arabidopsis thaliana and closely related species. Mol Biol Evol. 21:659-669.
44. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann J. 2005. A gene expression map of Arabidopsis development. Nat Genet. 37:501-506.
45. Seoighe C, Gehring C, Hurst LD. 2005. Gametophytic selection in Arabidopsis thaliana supports the selective model of intron length reduction. PLoS Genet. 1:e13.
46. Shaw AJ, Beer SC. 1997. Gametophyte-sporophyte variation and covariation in mosses. Adv Bryol. 6:35-63.
47. Shaw J, Szövényi P, Shaw B. 2011. Bryophyte diversity and evolution: windows into the early evolution of land plants. Am J Bot. 98:1-18.
48. Slotte T, Bataillon T, Hansen TT, Onge KR, Wright SI, Schierup MH. 2011. Genomic determinants of protein evolution and polymorphism in Arabidopsis. Gen Biol Evol. 3:1210-1219.
49. Sokal RR, Rohlf FJ. 2012. Biometry: the principles and practice of statistics in biological research, 4th ed. New York: W. H. Freeman and Co.
50. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609-W612.
51. Szövényi P, Rensing SA, Lang D, Shaw AJ, Wray G. 2011. Generation-biased gene expression in a bryophyte model system. Mol Biol Evol. 28:803-812.
52. Thornber CS. 2006. Functional properties of the isomorphic biphasic algal life cycle. Integr Comp Biol. 46:605-614.
53. Tortajada AM, Carmona MJ, Serra M. 2009. Does haplodiploidy purge inbreeding depression in rotifer populations? PLoS One 4:e8195.
54. Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH. 2008. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol. 148: 1201-1211.
55. Wang Z, Zhang J. 2011. Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc Natl Acad Sci U S A. 108:E67-E76.
56. Whittle CA, Johnston MO. 2003. Male-biased transmission of deleterious mutations in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 100: 4055-4059.
57. Wolff P, Weinhofer I, Seguin J, Roszak P, Beisel C, Donoghue MT, Spillane C, Nordborg M, Rehmsmeier M, Köhler C. 2011. High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet. 6:e102126.
58. Woody JL, Shoemaker RC. 2011. Gene expression: sizing it all up. Front Genet. 2:70.
59. Wright SI, Andolfatto P. 2008. The impact of natural selection on the genome: emerging patterns in Drosophila and Arabidopsis. Annu Rev Ecol Evol Systemat. 39:193-213.
60. Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenfuhrer J, von Mering C, Grossniklaus U. 2010. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol. 20:506-512.
61. Yanai I, Benjamin H, Shmoish M, et al. (12 co-authors). 2005. Genomewide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21:650-659.
62. Yang L, Gaut BS. 2011. Factors that contribute to variation in evolutionary rate among Arabidopsis genes. Mol Biol Evol. 28:2359-2369.
63. Yang Z. 2007. PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
64. Yin S, Wang P, Deng W, Zheng H, Hu L, Hurst LD, Kong X. 2009. Dosage compensation on the active X chromosome minimizes transcriptional noise of X-linked genes in mammals. Genome Biol. 10:R74.
65. Zeyl C, Vanderford T, Carter M. 2003. An evolutionary advantage of haploidy in large yeast populations. Science 299:555-558.