The persimmon genome reveals clues to the evolution of a lineage-specific sex determination system in plants

Autoři: Takashi Akagi aff001;  Kenta Shirasawa aff003;  Hideki Nagasaki aff003;  Hideki Hirakawa aff003;  Ryutaro Tao aff004;  Luca Comai aff005;  Isabelle M. Henry aff005
Působiště autorů: Graduate School of Environmental and Life Science, Okayama University, Okayama, Japan aff001;  Japan Science and Technology Agency (JST), PRESTO, Kawaguchi-shi, Saitama, Japan aff002;  Kazusa DNA Research Institute, Kazusa-Kamatari, Kisarazu, Chiba, Japan aff003;  Graduate School of Agriculture, Kyoto University, Kyoto, Japan aff004;  Genome Center and Department of Plant Biology, University of California Davis, Davis, California, United States of America aff005;  Genome Center and Department, Plant Biology, University of California Davis, Davis, California, United States of America aff005
Vyšlo v časopise: The persimmon genome reveals clues to the evolution of a lineage-specific sex determination system in plants. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008566
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008566


Most angiosperms bear hermaphroditic flowers, but a few species have evolved outcrossing strategies, such as dioecy, the presence of separate male and female individuals. We previously investigated the mechanisms underlying dioecy in diploid persimmon (D. lotus) and found that male flowers are specified by repression of the autosomal gene MeGI by its paralog, the Y-encoded pseudo-gene OGI. This mechanism is thought to be lineage-specific, but its evolutionary path remains unknown. Here, we developed a full draft of the diploid persimmon genome (D. lotus), which revealed a lineage-specific whole-genome duplication event and provided information on the architecture of the Y chromosome. We also identified three paralogs, MeGI, OGI and newly identified Sister of MeGI (SiMeGI). Evolutionary analysis suggested that MeGI underwent adaptive evolution after the whole-genome duplication event. Transformation of tobacco plants with MeGI and SiMeGI revealed that MeGI specifically acquired a new function as a repressor of male organ development, while SiMeGI presumably maintained the original function. Later, a segmental duplication event spawned MeGI’s regulator OGI on the Y-chromosome, completing the path leading to dioecy, and probably initiating the formation of the Y-chromosome. These findings exemplify how duplication events can provide flexible genetic material available to help respond to varying environments and provide interesting parallels for our understanding of the mechanisms underlying the transition into dieocy in plants.

Klíčová slova:

Arabidopsis thaliana – Flowering plants – Flowers – Gene mapping – Genome analysis – Lotus – Plant genomics – Sequence alignment


1. Renner SS. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an up-dated online database. Amer J Bot. 2014; 101: 1588–1596.

2. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, et al. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature. 2004; 427: 348–352. doi: 10.1038/nature02228 14737167

3. Wang J, Na J-K, Yu Q, Gschwend AR, Han J, Zeng F, et al. Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Nat Acad Sci USA. 2012; 109: 13710–13715. doi: 10.1073/pnas.1207833109 22869747

4. Kazama Y, Ishii K, Aonuma W, Ikeda T, Kawamoto H, et al. A new physical mapping approach refines the sex-determining gene positions on the Silene latifolia Y-chromosome. Sci Rep. 2016; 6: 18917. doi: 10.1038/srep18917 26742857

5. Akagi T, Henry IM, Tao R, Comai L. A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science. 2014; 346: 646–650. doi: 10.1126/science.1257225 25359977

6. Harkess A, Zhou J, Xu C, Bowers JE, Van der Hulst R, et al. The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nat Comm. 2017; 8: 1279.

7. Akagi T, Henry IM, Ohtani H, Morimoto T, Beppu K, Kataoka I, et al. A Y-encoded suppressor of feminization arose via lineage-specific duplication of a cytokinin response regulator in kiwifruit. Plant Cell. 2018; 30: 780–795. doi: 10.1105/tpc.17.00787 29626069

8. Charlesworth B, Charlesworth D. A model for the evolution of dioecy and gynodioecy. Amer Nat. 1978; 112: 975–997.

9. Charlesworth D, Charlesworth B. Population genetics of partial male-sterility and the evolution of monoecy and dioecy. Heredity. 1978; 41: 137–153.

10. Flagel LE, Wendel JF. Gene duplication and evolutionary novelty in plants. New Phytol. 2009; 183: 557–564. doi: 10.1111/j.1469-8137.2009.02923.x 19555435

11. Van de Peer Y, Mizrachi E, Marchal K. The evolutionary significance of polyploidy. Nat Rev Genet. 2017; 18: 411–424. doi: 10.1038/nrg.2017.26 28502977

12. The Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012; 485: 635–641. doi: 10.1038/nature11119 22660326

13. Olsen JL, Rouzé P, Verhelst B, Lin YC, Bayer T, et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature. 2016; 530: 331–335. doi: 10.1038/nature16548 26814964

14. Fraser LG, Tsang GK, Datson PM, De Silva HN, Harvey CF, Gill GP, et al. A gene-rich linkage map in the dioecious species Actinidia chinensis (kiwifruit) reveals putative X/Y sex-determining chromosomes. BMC Genom. 2009; 10: 102.

15. Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, et al. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Nat Acad Sci USA. 2007; 104: 1424–1429. doi: 10.1073/pnas.0608580104 17220272

16. Whipple CJ, Kebrom TH, Weber AL, Yang F, Hall D, Meeley R, grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses. Proc Nat Acad Sci USA. 2011; 108: E506–E512. doi: 10.1073/pnas.1102819108 21808030

17. Sakuma S, Pourkheirandish M, Hensel G, Kumlehn J, Stein N, Tagiri A, et al. Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley. New Phytol. 2013; 197: 939–948. doi: 10.1111/nph.12068 23293955

18. Tamura M, Tao R, Yonemori K, Ustunomiya N, Sugiura A. Ploidy level and genome size of several Diospyros species. J Jpn Soc Hortic Sci. 1998; 67: 306–312.

19. Huang S, Ding J, Deng D, Tang W, Sun H, Liu D, et al. Draft genome of the kiwifruit Actinidia chinensis. Nat Comm. 2013; 4: 2640.

20. Lyons E, Pedersen B, Kane J, Alam M, Ming R, Tang H, et al. Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with Rosids. Plant Physiol. 2008; 148: 1772–1781. doi: 10.1104/pp.108.124867 18952863

21. Iorizzo M, Ellison S, Senalik D, Zeng P, Satapoomin P, et al. A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat Genet. 2016; 48: 657–666. doi: 10.1038/ng.3565 27158781

22. Reyes-Chin-Wo S, Wang Z, Yang X, Kozik A, Arikit S, Song C, et al. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Comm. 2017; 8: 14953.

23. Vanneste K, Baele G, Maere S, Van De Peer Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary. Genome Res. 2014; 24: 1334–1347. doi: 10.1101/gr.168997.113 24835588

24. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, et al. The fate of duplicated genes in a polyploid plant genome. Plant J. 2013; 73: 143–153. doi: 10.1111/tpj.12026 22974547

25. Yang HW, Akagi T, Kawakatsu T, Tao R. Gene networks orchestrated by MeGI: a single‐factor mechanism underlying sex determination in persimmon. Plant J. 2019; 98: 97–111. doi: 10.1111/tpj.14202 30556936

26. Ariel FD, Manavella PA, Dezar CA, Chan RL. The true story of the HD-Zip family. Trends Plant Sci. 2007; 12: 419–426. doi: 10.1016/j.tplants.2007.08.003 17698401

27. Sakuma S, Salomon B, Komatsuda T. The domestication syndrome genes responsible for the major changes in plant form in the Triticeae crops. Plant Cell Physiol. 2011; 52: 738–749. doi: 10.1093/pcp/pcr025 21389058

28. Bartlett A., O'Malley R.C., Huang S.C., Galli M., Nery J.R., Gallavotti A. et al. Mapping genome-wide transcription-factor binding sites using DAP-seq. Nat Protoc. 2017; 1659–1672. doi: 10.1038/nprot.2017.055 28726847

29. Khan A, Fornes O, Stigliani A, Gheorghe M, Castro-Mondragon JA, van der Lee R, et al. JASPAR 2018: update of the open-access database of transcription factor binding profiles and its web framework. Nucleic Acids Res. 2018; D260–D266. doi: 10.1093/nar/gkx1126 29140473

30. Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman T-L, et al. Sex determination: why so many ways of doing it? PLoS Biol. 2014;

31. Wilf P, Labandeira CC, Johnson KR, Ellis B. Decoupled plant and insect diversity after the end-Cretaceous extinction. Science. 2006; 313: 1112–1115. doi: 10.1126/science.1129569 16931760

32. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE. 2012; 7: e37135. doi: 10.1371/journal.pone.0037135 22675423

33. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE. 2011; 6: e19379. doi: 10.1371/journal.pone.0019379 21573248

34. Shirasawa K, Hirakawa H, Isobe S. Analytical workflow of double-digest restriction site-associated DNA sequencing based on empirical and in silico optimization in tomato. DNA Res. 2016; 23: 145–153. doi: 10.1093/dnares/dsw004 26932983

35. O'Malley RC, Huang SC, Song L, Lewsey MG, Bartlett A, Nery JR, et al. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell. 2016; 165: 1280–1292. doi: 10.1016/j.cell.2016.04.038 27203113

36. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25: 1105–1111. doi: 10.1093/bioinformatics/btp120 19289445

37. Hoff KL, Lange S, Lomsadze A, Morodovsky M, Stanke M. BRAKER1: Unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics. 2016; 32: 767–769. doi: 10.1093/bioinformatics/btv661 26559507

38. Lomsadze A, Gemayel K, Tang S, Borodovsky M. Modeling leaderless transcription and atypical genes results in more accurate gene prediction in prokaryotes. Genome Res. 2018; 28: 1079–1089. doi: 10.1101/gr.230615.117 29773659

39. Stanke M, Waack S. Gene prediction with a Hidden-Markov model and a new intron submodel. Bioinformatics. 2003; 19: 215–225.

40. Krishnakumar V, Hanlon MR, Contrino S, Ferlanti ES, Karamycheva S, Kim M, et al. Araport: the Arabidopsis information portal. Nucl Acids Res. 2015; 43: D1003–1009. doi: 10.1093/nar/gku1200 25414324

41. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnob EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31: 3210–3212. doi: 10.1093/bioinformatics/btv351 26059717

42. Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics. 2005; 21: Suppl 1 i351–358.

43. Bao W, Kojima KK, Kohany O. Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA. 2015; 6: 11. doi: 10.1186/s13100-015-0041-9 26045719

44. Hirakawa H, Shirasawa K, Miyatake K, Nunome T, Negoro S, Ohyama A, et al. Draft genome sequence of eggplant (Solanum melongena L.): the representative solanum species indigenous to the old world. DNA Res. 2014; 21: 649–660. doi: 10.1093/dnares/dsu027 25233906

45. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2009; 449: 463–467.

46. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinfo. 2004; 5: 113.

47. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17: 540–552. doi: 10.1093/oxfordjournals.molbev.a026334 10742046

48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol. 2013; 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

49. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9: 357–359. doi: 10.1038/nmeth.1923 22388286

50. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

51. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePistro MA, et al. The variant call format and VCFtools, Bioinformatics. 2011; 27: 2156–2158. doi: 10.1093/bioinformatics/btr330 21653522

52. Endelman JB, Plomion C. LPmerge: an R package for merging genetic maps by linear programming. Bioinformatics. 2014; 30: 1623–1624. doi: 10.1093/bioinformatics/btu091 24532720

53. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25: 1451–1452. doi: 10.1093/bioinformatics/btp187 19346325

54. Shirasawa K, Isuzugawa K, Ikenaga M, Saito Y, Yamamoto T, Hirakawa H, et al. The genome sequence of sweet cherry (Prunus avium) for use in genomics-assisted breeding. DNA Res. 2017; 24: 499–508. doi: 10.1093/dnares/dsx020 28541388

55. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets, Bioinformatics. 2011; 27: 863–864. doi: 10.1093/bioinformatics/btr026 21278185

56. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 2012; 6: 80–92. doi: 10.4161/fly.19695 22728672

57. Delcher AL, Phillippy A, Carlton J, Salzberg SL. Fast algorithms for large-scale genome alignment and comparison. Nucl Acids Res. 2002; 30: 2478–83. doi: 10.1093/nar/30.11.2478 12034836

58. Krzywinski M, Schein J, Birol İ, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009; 19: 1639–1645. doi: 10.1101/gr.092759.109 19541911

59. Bayer M, Milne I, Stephen G, Shaw P, Cardle L, Wright F, et al. Comparative visualization of genetic and physical maps with Strudel. Bioinformatics. 2011; 27: 1307–1308. doi: 10.1093/bioinformatics/btr111 21372085

60. Li L, Stoeckert CJ, Roos DS. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 2003; 13: 2178–2189. doi: 10.1101/gr.1224503 12952885

61. Tuskan GA, Difazio S, Jansson S, Bohlmann J, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006; 313: 1596–1604. doi: 10.1126/science.1128691 16973872

62. Shi T, Huang H, Barker MS. Ancient genome duplications during the evolution of kiwifruit (Actinidia) and related Ericales. Annals Bot. 2010; 106: 497–504.

63. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Appl Biosci. 1997; 13: 555–556.

64. Esumi T, Tao R, Yonemori K. Relationship between floral development and transcription levels of LEAFY and TERMINAL FLOWER 1 homologs in Japanese pear (Pyrus pyrifolia Nakai) and quince (Cydonia oblonga Mill.). J Jpn Soc Hortic Sci. 2007; 76: 294–304.

65. Christophel DC, Basinger JF. Earliest floral evidence for the Ebenaceae in Australia. Nature. 1982; 296: 439–441.

Článek vyšel v časopise

PLOS Genetics

2020 Číslo 2
Nejčtenější tento týden
Nejčtenější v tomto čísle

Zvyšte si kvalifikaci online z pohodlí domova

Deprese u dětí a adolescentů
nový kurz
Autoři: MUDr. Vlastimil Nesnídal

Konsenzuální postupy v léčbě močových infekcí

COVID-19 up to date
Autoři: doc. MUDr. Vladimír Koblížek, Ph.D., MUDr. Mikuláš Skála, prof. MUDr. František Kopřiva, Ph.D., prof. MUDr. Roman Prymula, CSc., Ph.D.

Betablokátory a Ca antagonisté z jiného úhlu
Autoři: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Chronické žilní onemocnění a možnosti konzervativní léčby

Všechny kurzy
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se