#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Gene Family Derived from Transposable Elements during Early Angiosperm Evolution Has Reproductive Fitness Benefits in


The benefits of ever-growing numbers of sequenced eukaryotic genomes will not be fully realized until we learn to decipher vast stretches of noncoding DNA, largely composed of transposable elements. Transposable elements persist through self-replication, but some genes once encoded by transposable elements have, through a process called molecular domestication, evolved new functions that increase fitness. Although they have conferred numerous adaptations, the number of such domesticated transposable element genes remains unknown, so their evolutionary and functional impact cannot be fully assessed. Systematic searches that exploit genomic signatures of natural selection have been employed to identify potential domesticated genes, but their predictions have yet to be experimentally verified. To this end, we investigated a family of domesticated genes called MUSTANG (MUG), identified in a previous bioinformatic search of plant genomes. We show that MUG genes are functional. Mutants of Arabidopsis thaliana MUG genes yield phenotypes with severely reduced plant fitness through decreased plant size, delayed flowering, abnormal development of floral organs, and markedly reduced fertility. MUG genes are present in all flowering plants, but not in any non-flowering plant lineages, such as gymnosperms, suggesting that the molecular domestication of MUG may have been an integral part of early angiosperm evolution. This study shows that systematic searches can be successful at identifying functional genetic elements in noncoding regions and demonstrates how to combine systematic searches with reverse genetics in a fruitful way to decipher eukaryotic genomes.


Vyšlo v časopise: A Gene Family Derived from Transposable Elements during Early Angiosperm Evolution Has Reproductive Fitness Benefits in. PLoS Genet 8(9): e32767. doi:10.1371/journal.pgen.1002931
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002931

Souhrn

The benefits of ever-growing numbers of sequenced eukaryotic genomes will not be fully realized until we learn to decipher vast stretches of noncoding DNA, largely composed of transposable elements. Transposable elements persist through self-replication, but some genes once encoded by transposable elements have, through a process called molecular domestication, evolved new functions that increase fitness. Although they have conferred numerous adaptations, the number of such domesticated transposable element genes remains unknown, so their evolutionary and functional impact cannot be fully assessed. Systematic searches that exploit genomic signatures of natural selection have been employed to identify potential domesticated genes, but their predictions have yet to be experimentally verified. To this end, we investigated a family of domesticated genes called MUSTANG (MUG), identified in a previous bioinformatic search of plant genomes. We show that MUG genes are functional. Mutants of Arabidopsis thaliana MUG genes yield phenotypes with severely reduced plant fitness through decreased plant size, delayed flowering, abnormal development of floral organs, and markedly reduced fertility. MUG genes are present in all flowering plants, but not in any non-flowering plant lineages, such as gymnosperms, suggesting that the molecular domestication of MUG may have been an integral part of early angiosperm evolution. This study shows that systematic searches can be successful at identifying functional genetic elements in noncoding regions and demonstrates how to combine systematic searches with reverse genetics in a fruitful way to decipher eukaryotic genomes.


Zdroje

1. AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

2. LanderES, LintonLM, BirrenB, NusbaumC, ZodyMC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860–921.

3. DoolittleWF, SapienzaC (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–603.

4. OrgelLE, CrickFH (1980) Selfish DNA: the ultimate parasite. Nature 284: 604–607.

5. WickerT, SabotF, Hua-VanA, BennetzenJL, CapyP, et al. (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973–982.

6. VolffJ-N (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28: 913–922.

7. FeschotteC (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 397–405.

8. SinzelleL, IzsvakZ, IvicsZ (2009) Molecular domestication of transposable elements: From detrimental parasites to useful host genes. Cell Mol Life Sci 66: 1073–1093.

9. VolffJN (2009) Cellular genes derived from Gypsy/Ty3 retrotransposons in mammalian genomes. Ann N Y Acad Sci 1178: 233–243.

10. Hua-VanA, Le RouzicA, BoutinTS, FileeJ, CapyP (2011) The struggle for life of the genome's selfish architects. Biology direct 6: 19.

11. FeschotteC, PrithamEJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41: 331–368.

12. WhitelamGC, JohnsonE, PengJ, CarolP, AndersonML, et al. (1993) Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5: 757–768.

13. HudsonM, RingliC, BoylanMT, QuailPH (1999) The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev 13: 2017–2027.

14. HudsonME, LischDR, QuailPH (2003) The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 34: 453–471.

15. BundockP, HooykaasP (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436: 282–284.

16. ZdobnovE, CampillosM, HarringtonE, TorrentsD, BorkP (2005) Protein coding potential of retroviruses and other transposable elements in vertebrate genomes. Nucleic Acids Res 33: 946–954.

17. CowanR, HoenD, SchoenD, BureauT (2005) MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol 22: 2084–2089.

18. MuehlbauerGJ, BhauBS, SyedNH, HeinenS, ChoS, et al. (2006) A hAT superfamily transposase recruited by the cereal grass genome. Mol Genet Genomics 275: 553–563.

19. SaccaroNL, Van SluysM-A, de Mello VaraniA, RossiM (2007) MudrA-like sequences from rice and sugarcane cluster as two bona fide transposon clades and two domesticated transposases. Gene 392: 117–125.

20. PiriyapongsaJ, Marino-RamirezL, JordanIK (2007) Origin and evolution of human microRNAs from transposable elements. Genetics 176: 1323–1337.

21. BenjakA, ForneckA, CasacubertaJM (2008) Genome-wide analysis of the “cut-and-paste” transposons of grapevine. PLoS ONE 3: e3107 doi:10.1371/journal.pone.0003107..

22. LeQH, WrightS, YuZ, BureauT (2000) Transposon diversity in Arabidopsis thaliana. Proc Natl Acad Sci U S A 97: 7376–7381.

23. YuZ, WrightSI, BureauTE (2000) Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution. Genetics 156: 2019–2031.

24. RossiM, AraujoPG, de JesusEM, VaraniAM, Van SluysMA (2004) Comparative analysis of Mutator -like transposases in sugarcane. Molecular genetics and genomics : MGG 272: 194–203.

25. BoguskiMS, LoweTM, TolstoshevCM (1993) dbEST–database for “expressed sequence tags”. Nat genet 4: 332–333.

26. BabuMM, IyerLM, BalajiS, AravindL (2006) The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res 34: 6505–6520.

27. Hua-VanA, CapyP (2008) Analysis of the DDE Motif in the Mutator Superfamily. J Mol Evol 67: 670–681.

28. OrrHA (2009) Fitness and its role in evolutionary genetics. Nature reviews Genetics 10: 531–539.

29. SmithAM, StittM (2007) Coordination of carbon supply and plant growth. Plant, cell & environment 30: 1126–1149.

30. LinR, DingL, CasolaC, RipollDR, FeschotteC, et al. (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318: 1302–1305.

31. SimonSA, MeyersBC (2011) Small RNA-mediated epigenetic modifications in plants. Curr Opin Plant Biol 14: 148–155.

32. ListerR, O'MalleyRC, Tonti-FilippiniJ, GregoryBD, BerryCC, et al. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523–536.

33. ZhangX, YazakiJ, SundaresanA, CokusS, ChanSW, et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126: 1189–1201.

34. GregoryBD, O'MalleyRC, ListerR, UrichMA, Tonti-FilippiniJ, et al. (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Developmental cell 14: 854–866.

35. de AraujoP, RossiM, de JesusE, SaccaroN, KajiharaD, et al. (2005) Transcriptionally active transposable elements in recent hybrid sugarcane. Plant J 44: 707–717.

36. JiaoY, DengXW (2007) A genome-wide transcriptional activity survey of rice transposable element-related genes. Genome Biol 8: R28.

37. OuyangX, LiJ, LiG, LiB, ChenB, et al. (2011) Genome-Wide Binding Site Analysis of FAR-RED ELONGATED HYPOCOTYL3 Reveals Its Novel Function in Arabidopsis Development. Plant Cell 23: 2514–2535.

38. LinR, TengY, ParkH-J, DingL, BlackC, et al. (2008) Discrete and essential roles of the multiple domains of Arabidopsis FHY3 in mediating phytochrome A signal transduction. Plant Physiol 148: 981–992.

39. HoenDR, ParkKC, ElroubyN, YuZ, MohabirN, et al. (2006) Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol Biol Evol 23: 1254–1268.

40. CordauxR, UditS, BatzerMA, FeschotteC (2006) Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. P Natl Acad Sci U S A 103: 8101–8106.

41. SwarbreckD, WilksC, LameschP, BerardiniTZ, Garcia-HernandezM, et al. (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic acids res 36: D1009–1014.

42. SalamovAA, SolovyevVV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10: 516–522.

43. TanakaT, AntonioBA, KikuchiS, MatsumotoT, NagamuraY, et al. (2008) The Rice Annotation Project Database (RAP-DB): 2008 update. Nucleic Acids Res 36: D1028–1033.

44. PatersonAH, BowersJE, BruggmannR, DubchakI, GrimwoodJ, et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551–556.

45. Marchler-BauerA, LuS, AndersonJB, ChitsazF, DerbyshireMK, et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225–229.

46. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. Journal of molecular biology 215: 403–410.

47. MingR, HouS, FengY, YuQ, Dionne-LaporteA, et al. (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991–996.

48. JaillonO, AuryJM, NoelB, PolicritiA, ClepetC, et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463–467.

49. CannonSB, SterckL, RombautsS, SatoS, CheungF, et al. (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proceedings of the National Academy of Sciences of the United States of America 103: 14959–14964.

50. GoodsteinDM, ShuS, HowsonR, NeupaneR, HayesRD, et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic acids research 40: D1178–1186.

51. SchnablePS, WareD, FultonRS, SteinJC, WeiF, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115.

52. TIBI (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463: 763–768.

53. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research 32: 1792–1797.

54. CastresanaJ (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular biology and evolution 17: 540–552.

55. DereeperA, GuignonV, BlancG, AudicS, BuffetS, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465–469.

56. GuindonS, GascuelO (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology 52: 696–704.

57. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.

58. RossoMG, LiY, StrizhovN, ReissB, DekkerK, et al. (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53: 247–259.

59. AlonsoJM, StepanovaAN, LeisseTJ, KimCJ, ChenH, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

60. MurashigeT, SkoogF (1962) A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia plantarum 15: 473–497.

61. Alonso-BlancoC, AartsM, BentsinkL, KeurentjesJ, ReymondM, et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell Online 21: 1877.

62. ShindoC, BernasconiG, HardtkeCS (2008) Intraspecific competition reveals conditional fitness effects of single gene polymorphism at the Arabidopsis root growth regulator BRX. New Phytol 180: 71–80.

63. DonohueK (2002) Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology 83: 1006–1016.

64. PigliucciM, SchlichtingCD (1996) Reaction norms of Arabidopsis IV. Relationships between plasticity and fitness. Heredity 76(Pt 5):427–436.

65. ShawRG, ChangS-M (2006) Gene action of new mutations in Arabidopsis thaliana. Genetics 172: 1855–1865.

66. MackinneyG (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140: 315–322.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#