Apomictic and Sexual Germline Development Differ with Respect to Cell Cycle, Transcriptional, Hormonal and Epigenetic Regulation

English version České info

In flowering plants, asexual reproduction through seeds (apomixis) likely evolved from sexual ancestors several times independently. Only three key developmental steps differ between sexual reproduction and apomixis. In contrast to sexual reproduction, in apomicts the first cell of the female reproductive lineage omits or aborts meiosis (apomeiosis) to initiate gamete formation. Subsequently, the egg cell develops into an embryo without fertilization (parthenogenesis), and endosperm formation can either be autonomous or depend on fertilization. Consequently, the offspring of apomicts is genetically identical to the mother plant. The production of clonal seeds bears great promise for agricultural applications. However, the targeted manipulation of reproductive pathways for seed production has proven difficult as knowledge about the underlying gene regulatory processes is limited. We performed cell type-specific transcriptome analyses to study apomictic germline development in Boechera gunnisoniana, an apomictic species closely related to Arabidopsis thaliana. To facilitate these analyses, we first characterized a floral reference transcriptome. In comparison, we identified several regulatory pathways, including core cell cycle regulation, protein degradation, transcription factor activity, and hormonal pathways to be differentially regulated between sexual and apomictic plants. Apart from new insights into the underlying transcriptional networks, our dataset provides a valuable starting point for functional investigations.

Vyšlo v časopise: Apomictic and Sexual Germline Development Differ with Respect to Cell Cycle, Transcriptional, Hormonal and Epigenetic Regulation. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004476
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004476

Souhrn

Zdroje

1. Nogler GA (1984) Gametophytic apomixis. In: Embryology of Angiosperms. Edited by Johri BM. Berlin: Springer; pp. 475–518.

2. SavidanY (2000) Apomixis: Genetics and breeding. Plant Breeding Reviews 18: 13–86.

3. SpillaneC, SteimerA, GrossniklausU (2001) Apomixis in agriculture: The quest for clonal seeds. Sex Plant Reprod 14: 179–87.

4. BicknellRA, KoltunowAM (2004) Understanding apomixis: Recent advances and remaining conundrums. Plant Cell 16: 228–245.

5. SpillaneC, CurtisMD, GrossniklausU (2004) Apomixis technology development - virgin births in farmers' fields? Nat Biotechnol 22: 687–691.

6. KoltunowA, GrossniklausU (2003) Apomixis: A developmental perspective. Annu Rev Plant Biol 54: 547–574.

7. Grossniklaus U (2001) From sexuality to apomixis: molecular and genetic approaches. In: The Flowering of Apomixis: From Mechanisms to Genetic Engineering. Edited by Savidan Y, Carman J, Dresselhaus T. Mexico DF: CIMMYT; pp.168–211.

8. SprunckS, Gross-HardtR (2011) Nuclear behavior, cell polarity, and cell specification in the female gametophyte. Sex Plant Reprod 24: 123–136.

9. KoltunowAM (1993) Apomixis: Embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5: 1425–1437.

10. RodkienwiczB (1970) Callose in cell walls during megasporogenesis in angiosperms. Planta 93: 39–47.

11. WüstSE, VijverbergK, SchmidtA, WeissM, GheyselinckJ, et al. (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20: 506–512.

12. SchmidtA, WüstSE, VijverbergK, BarouxC, KleenD, et al. (2011) Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol 9: e1001155.

13. SchmidMW, SchmidtA, KlostermeierUC, BarannM, RosenstielP, et al. (2012) A powerful method for transcriptional profiling of specific cell types in eukaryotes: laser-assisted microdissection and RNA sequencing. PLoS ONE 7: e29685.

14. GrossniklausU, NoglerGA, van DijkPJ (2001) How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell 2001 13: 1491–1498.

15. SavidanY (1982) Nature et hérédité de l' apomixie chez Panicum maximum Jacq. Trav. & Doc. Orstom 153: 1–159.

16. NoglerGA (1984) Genetics of apospory in apomictic Ranunculus auricomus. V Conclusion Bot Helv 94: 411–422.

17. SherwoodRT, BergCC, YoungBA (1994) Inheritance of apospory in buffelgrass. Crop Sci 34: 1490–1494.

18. GrimanelliD, LeblancO, EspinosaE, PerottiE, González de LeónD, et al. (1998) Mapping diplosporous apomixis in tetraploid Tripsacum: one gene or several genes? Heredity 80: 33–39.

19. Ozias-AkinsP, RocheD, HannaWW (1998) Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum implies genetic control of apospory by a divergent locus that may have no allelic form in sexual genotypes. Proc Natl Acad Sci U S A 95: 5127–5132.

20. NoyesRD, RiesebergLH (2000) Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics 155: 379–390.

21. Valle CB, Miles JW (2001) Breeding of apomictic species. In: The Flowering of Apomixis: From Mechanisms to Genetic Engineering. Edited by Savidan Y, Carman J, Dresselhaus T. Mexico DF: CIMMYT; pp. 137–152.

22. CáceresME, MatzkF, BustiA, PupilliF, ArcioniS (2001) Apomixis and sexuality in Paspalum simplex: characterization of the mode of reproduction in segregating progenies by different methods. Sex Plant Reprod 14: 201–206.

23. van DijkPJ, Bakx-SchotmanJM (2004) Formation of unreduced megaspores (diplospory) in apomictic dandelions (Taraxacum officinale, s.l.) is controlled by a sex-specific dominant locus. Genetics 166: 483–492.

24. KoltunowAM, JohnsonSD, RodriguesJC, OkadaT, HuY, TsuchiyaT, et al. (2011) Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. Plant J 66: 890–902.

25. SchranzME, KantamaL, de JongH, Mitchell-OldsT (2006) Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apomixis in Boechera (Brassicaceae). New Phytol 171: 425–438.

26. GrimanelliD, LeblancO, PerottiE, GrossniklausU (2001) Developmental genetics of gametophytic apomixis. Trends Genet 17: 597–604.

27. SharbelTF, VoigtML, CorralJM, ThielT, VarshneyA, et al. (2009) Molecular signatures of apomictic and sexual ovules in the Boechera holboellii complex. Plant J 104: 14026–14031.

28. SharbelTF, VoigtML, CorralJM, GallaG, KumlehnJ, et al. (2010) Apomictic and sexual ovules of Boechera display heterochronic global gene expression patterns. Plant Cell 22: 655–671.

29. LeblancO, ArmsteadI, PessinoS, OrtizJP, EvansC, et al. (1997) Non-radioactive mRNA fingerprinting to visualise gene expression in mature ovaries of Brachiaria hybrids derived from B. brizantha, an apomictic tropical forage. Plant Sci 126: 49–58.

30. RodriguesJC, CarbralGB, DusiDM, de MelloLV, RigdenDJ, et al. (2003) Identification of differentially expressed cDNA sequences in ovaries of sexual and apomictic plants of Brachiaria brizantha. Plant Mol Biol 53: 745–757.

31. OkadaT, HuY, TuckerMR, TaylorJM, JohnsonSD, et al. (2013) Enlarging cells initiating apomixis in Hieracium praealtum transition to an embryo sac program prior to entering mitosis. Plant Physiol 163: 216–31.

32. Vielle-CalzadaJP, NuccioML, BudimanMA, BursonBL, HusseyMA, et al. (1996) Comparative gene expression in sexual and apomictic ovaries of Pennisetum ciliare (L.) Link. Plant Mol Biol 32: 1085–1092.

33. SahuPP, GuptaS, MalaviyaDR, RoyAK, KaushalP, et al. (2012) Transcriptome analysis of differentially expressed genes during embryo sac development in apomeiotic non-parthenogenetic interspecific hybrid of Pennisetum glaucum. Mol Biotechnol 51: 262–271.

34. PessinoSC, EspinozaF, MartinezEJ, OrtizJP, ValleEM, et al. (2001) Isolation of cDNA clones differentially expressed in flowers of apomictic and sexual Paspalum notatum. Hereditas 134: 35–42.

35. PolegriL, CalderiniO, ArcioniS, PupilliF (2010) Specific expression of apomixis-linked alleles revealed by comparative transcriptomic analysis of sexual and apomictic Paspalum simplex Morong flowers. J Exp Bot 61: 1869–83.

36. OchogavíaAC, SeijoJG, GonzálezAM, PodioM, Duarte SilveiraE, et al. (2011) Characterization of retrotransposon sequences expressed in inflorescences of apomictic and sexual Paspalum notatum plants. Sex Plant Reprod 24: 231–246.

37. BarcacciaG, VarottoS, MeneghettiS, AlbertiniE, PorcedduA, et al. (2001) Analysis of gene expression during flowering in apomeiotic mutants of Medicago spp.: cloning ESTs and candidate genes for apomeiosis. Sex Plant Reprod 14: 233–238.

38. ChenL, MiyazakiC, KojimaA, SaitoA, AdachiT (1999) Isolation and characterization of a gene expressed during early embryo sac development in apomictic Guinea grass (Panicum maximum). J Plant Physiol 154: 55–62.

39. AlbertiniE, MarconiG, BarcacciaG, RaggiL, FalcinelliM (2004) Isolation of candidate genes for apomixis in Poa pratensis L. Plant Mol Biol 56: 879–894.

40. AlbertiniE, MarconiG, RealeL, BarcacciaG, PorcedduA, et al. (2005) SERK and APOSTART. Candidate genes for apomixis in Poa pratensis. Plant Physiol 138: 2185–2199.

41. TuckerMR, AraujoAC, PaechNA, HechtV, SchmidtED, et al. (2003) Sexual and apomictic reproduction in Hieracium subgenus pilosella are closely interrelated developmental pathways. Plant Cell 15: 1524–1537.

42. Olmedo-MonfilV, Durán-FigueroaN, Arteaga-VázquezM, Demesa-ArévaloE, AutranD, et al. (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628–632.

43. Garcia-AguilarM, MichaudC, LeblancO, GrimanelliD (2010) Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22: 3249–3267.

44. SinghM, GoelS, MeeleyRB, DantecC, ParrinelloH, et al. (2011) Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23: 443–458.

45. RaviM, MarimuthuMP, SiddiqiI (2008) Gamete formation without meiosis in Arabidopsis. Nature 451: 1121–1124.

46. d'ErfurthI, JolivetS, FrogerN, CatriceO, NovatchkovaM, et al. (2009) Turning meiosis into mitosis. PLoS Biol 7: e1000124.

47. MatzkF, MeisterA, SchubertI (2010) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J 21: 97–108.

48. RoyBA (1995) The breeding system of six species of Arabis (Brassicaceae). Am J Bot 82: 869–877.

49. TaskinKM, TurgutK, ScottRJ (2004) Apomictic development in Arabis gunnisoniana. Isr J Plant Sci 52: 155–160.

50. AliyuOM, SchranzME, SharbelTF (2010) Quantitative variation for apomictic reproduction in the genus Boechera (Brassicaceae). Am J Bot 97: 1719–1731.

51. Johnston AJ (2007) Functional genomics of sexual and asexual reproduction in Arabidopsis and relatives. PhD Thesis, University of Zürich, Switzerland.

52. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol 29: 644–654.

53. ConesaA, GötzS, García-GómezJM, TerolJ, TalónM, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676.

54. KentWJ (2002) BLAT-the BLAST-like alignment tool. Genome Res 12: 656–664.

55. Bar-OrC, CzosnekH, KoltaiH (2007) Cross-species microarray hybridizations: a developing tool for studying species diversity. Trends Genet 23: 200–207.

56. TangF, BarbacioruC, WangY, NordmanE, LeeC, et al. (2009) mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6: 377–382.

57. TarazonaS, García-AlcaldeF, DopazoJ, FerrerA, ConesaA (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21: 2213–2223.

58. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.

59. WijnkerE, SchnittgerA (2013) Control of the meiotic cell division program in plants. Plant Reprod 26: 143–158.

60. VandepoeleK, RaesJ, De VeylderL, RouzéP, RombautsS, et al. (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14: 903–916.

61. GutierrezC (2009) The Arabidopsis cell division cycle. Arabidopsis Book 7: e0120.

62. NodineMD, BartelDP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24: 2678–2692.

63. ChenC, FarmerAD, LangleyRJ, MudgeJ, CrowJA, et al. (2010) Meiosis-specific gene discovery in plants: RNA-Seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol 10: 280.

64. TortiS, FornaraF, VincentC, AndrésF, NordströmK, et al. (2012) Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24: 444–462.

65. FilichkinSA, PriestHD, GivanSA, ShenR, BryantDW (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20: 45–58.

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

67. KoszegiD, JohnstonAJ, RuttenT, CzihalA, AltschmiedL, et al. (2011) Members of the RKD transcription factor family induce an egg cell-like gene expression program. Plant J 67: 280–91.

68. ImaiA, MatsuyamaT, HanzawaY, AkiyamaT, TamaokiM, et al. (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135: 1565–1573.

69. WuXB, WangJ, LiuJH, DengXX (2009) Involvement of polyamine biosynthesis in somatic embryogenesis of Valencia sweet orange (Citrus sinensis) induced by glycerol. J Plant Physiol 166: 52–62.

70. De-la-PeñaC, Galaz-AvalosRM, Loyola-VargasVM (2008) Possible role of light and polyamines in the onset of somatic embryogenesis of Coffea canephora. Mol Biotechnol 39: 215–24.

71. DutraNT, SilveiraV, de AzevedoIG, Gomes-NetoLR, FaçanhaAR, et al. (2013) Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. Physiol Plant 148: 121–32.

72. HaHC, SirisomaNS, KuppusamyP, ZweierJL, WosterPM, et al. (1998) The natural polyamine spermidine functions directly as free radical scavenger. Proc Natl Acad Sci USA 95: 11140–11145.

73. HörandlE, HadacekF (2013) The oxidative damage initiation hypothesis for meiosis. Plant Reprod DOI 10.1007s0049701302347/s00497-013-0234-7

74. MartinMV, FiolDF, SundaresanV, ZabaletaEJ, PagnussatGC (2013) oiwa, a female gametophytic mutant impaired in a mitochondrial manganese-superoxide dismutase, reveals crucial roles for reactive oxygen species during embryo sac development and fertilization in Arabidopsis. Plant Cell 25: 1573–1591.

75. ConnerJA, GoelS, GunawanG, Cordonnier-PrattMM, JohnsonVE, et al. (2008) Sequence analysis of bacterial artificial chromosome clones from the apospory-specific genomic region of Pennisetum and Cenchrus. Plant Physiol 147: 1396–1411.

76. GuilfoyleTJ, UlmasovT, HagenG (1998) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54: 619–627.

77. RademacherEH, MöllerB, LokerseAS, Llavata-PerisCI, van den BergW, et al. (2011) A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. Plant J 68: 597–606.

78. CraigKL, TyersM (1999) The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 72: 299–328.

79. LechnerE, AchardP, VansiriA, PotuschakT, GenschikP (2006) F-box proteins everywhere. Curr Opin Plant Biol 9: 631–638.

80. AmiteyeS, CorralJM, VogelH, SharbelTF (2011) Analysis of conserved microRNAs in floral tissues of sexual and apomictic Boechera species. BMC Genomics 12: 500.

81. SchallauA, ArzentonF, JohnstonAJ, HähnelU, KoszegiD, et al. (2010) Identification and genetic analysis of the APOSPORY locus in Hypericum perforatum L. Plant J 62: 773–784.

82. MladekC, GugerK, HauserMT (2003) Identification and characterization of the ARIADNE gene family in Arabidopsis. A group of putative E3 ligases. Plant Physiol 131: 27–40.

83. MarimuthuMP, JolivetS, RaviM, PereiraL, DavdaJN, et al. (2011) Synthetic clonal reproduction through seeds. Science 331: 876.

84. CrismaniW, GirardC, MercierR (2013) Tinkering with meiosis. J Exp Bot 64: 55–65.

85. CookGS, GrønlundAL, SicilianoI, SpadaforaN, AminiM, et al. (2013) Plant WEE1 kinase is cell cycle regulated and removed at mitosis via the 26S proteasome machinery. J Exp Bot 64: 2093–2106.

86. HeckmannS, LermontovaI, BerckmansB, De VeylderL, BäumleinH, et al. (2011) The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J 68: 646–656.

87. ZengY, ConnerJ, Ozias-AkinsP (2011) Identification of ovule transcripts from the Apospory-Specific Genomic Region (ASGR)-carrier chromosome. BMC Genomics 12: 206.

88. GrossniklausU, SchneitzK (1998) The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol 9: 227–238.

89. TuckerMR, OkadaT, JohnsonSD, TakaiwaF, KoltunowAM (2012) Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium. J Exp Bot 63: 3229–3241.

90. Vielle-CalzadaJ-P, ThomasJ, SpillaneC, ColuccioA, HoeppnerMA, GrossniklausU (1999) Maintenance of genomic imprinting at the Arabidopsis MEDEA locus requires zygotic DDM1 activity. Genes Dev 13: 2971–2982.

91. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

92. ParadisE, ClaudeJ, StrimmerK (2004) APE: Analysis of phylogenetics and evolution in the R language. Bioinformatics 20: 289–290.

93. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

94. RobinsonMD, OshlackA (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25.

95. WüstSE, O'MaoileidighDS, RaeL, KwasniewskaK, RaganelliA, HanczarykK, et al. (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci U S A 109: 13452–13457.

96. Alexa A, Rahnenführer J (2009) Gene set enrichment analysis with topGO. (www.bioconductor.org).

97. Warnes G, Bolker B, Lumley T (2010) gplots: Various R programming tools for plotting data. (www.bioconductor.org).

98. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.