Parental-genome dosage effects on the transcriptome of F1 hybrid triploid embryos of Arabidopsis thaliana

Plant Journal

Volumn 92, Issue 6, 2017, Pages 1044-1058

  Fort, Antoine ^a   Tuteja, Reetu ^a   Braud, Martin ^a   McKeown, Peter C ^a   Spillane, Charles ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Arabidopsis thaliana; epigenetic; genome dosage; genomic imprinting; heterosis; parental effect; seed development

Indexed keywords

GENE EXPRESSION; PLANTS (BOTANY); SEED; TISSUE;

ARABIDOPSIS THALIANA; EPIGENETIC; GENOMIC IMPRINTING; HETEROSIS; PARENTAL EFFECT; SEED DEVELOPMENT;

GENES;

GENOTYPES; NUTRIENTS; PLANTS;

TRANSCRIPTOME;

ALLELE; ARABIDOPSIS; DIPLOIDY; ENDOSPERM; EPIGENETICS; GENETICS; GENOME IMPRINTING; GROWTH, DEVELOPMENT AND AGING; PLANT GENOME; PLANT SEED; SEQUENCE ANALYSIS; TRIPLOIDY;

ALLELES; ARABIDOPSIS; DIPLOIDY; ENDOSPERM; EPIGENOMICS; GENOME, PLANT; GENOMIC IMPRINTING; SEEDS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME; TRIPLOIDY;

EID: 85037329162     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13740     Document Type: Article

References (79)

1. Alonso-Peral, M.M., Trigueros, M., Sherman, B., Ying, H., Taylor, J.M., James Peacock, W. and Dennis, E.S. (2017) Patterns of gene expression in developing embryos of Arabidopsis hybrids. Plant J. 89, 927–939. https://doi.org/10.1111/tpj.13432.
2. Arondel, V., Vergnolle, C., Cantrel, C. and Kader, J.-C. (2000) Lipid transfer proteins are encoded by a small multigene family in Arabidopsis thaliana. Plant Sci. 157(1), 1–12. https://doi.org/10.1016/S0168-9452(00)00232-6.
3. Baroux, C., Spillane, C. and Grossniklaus, U. (2002) Evolutionary origins of the endosperm in flowering plants. Genome Biol. 3(9), reviews1026.
4. Baroux, C., Pecinka, A., Fuchs, J., Schubert, I. and Grossniklaus, U. (2007) The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell, 19(6), 1782–1794. https://doi.org/10.1105/tpc.106.046235.
5. Bauer, M.J. (2006) The interploidy hybridization barrier in Zea mays L. University of Missouri—Columbia.
6. Belmonte, M.F., Kirkbride, R.C., Stone, S.L., Pelletier, J.M., Bui, A.Q., Yeung, E.C., Hashimoto, M., Fei, J., Harada, C.M. and Munoz, M.D. (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc. Natl Acad. Sci. USA 110(5), E435–E444.
7. Berger, F. (2011) Imaging fertilization in flowering plants, not so abominable after all. J. Exp. Bot. 62(5), 1651–1658. https://doi.org/10.1093/jxb/erq305.
8. Birchler, J.A. (2014) Interploidy hybridization barrier of endosperm as a dosage interaction. Front. Plant Sci. 5, 281.
9. Birchler, J.A. and Hart, J.R. (1987) Interaction of endosperm size factors in maize. Genetics, 117(2), 309–317.
10. Bosemark, N.O. (1971) Haploids and homozygous diploids, triploids and tetraploids in sugar beet. Hereditas, 69(2), 193–203. https://doi.org/10.1111/j.1601-5223.1971.tb02433.x.
11. Boyle, E.I., Weng, S., Gollub, J., Jin, H., Botstein, D., Cherry, J.M. and Sherlock, G. (2004) GO::TermFinder—open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics, 20(18), 3710–3715. https://doi.org/10.1093/bioinformatics/bth456.
12. Burkart-Waco, D., Ngo, K., Dilkes, B., Josefsson, C. and Comai, L. (2013) Early disruption of maternal–zygotic interaction and activation of defense-like responses in Arabidopsis interspecific crosses. The Plant Cell Online, 25(6), 2037–2055.
13. Casneuf, T., De Bodt, S., Raes, J., Maere, S. and Van de Peer, Y. (2006) Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol. 7(2), R13. https://doi.org/10.1186/gb-2006-7-2-r13.
14. Costa, L.M., Yuan, J., Rouster, J., Paul, W., Dickinson, H. and Gutierrez-Marcos, J.F. (2012) Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr. Biol. 22(2), 160–165. https://doi.org/10.1016/j.cub.2011.11.059.
15. Dabney, A. and Storey, J.D. (2015) q-Value: Q-Value Estimation for False Discovery Rate Control.
16. Dilkes, B.P. and Comai, L. (2004) A differential dosage hypothesis for parental effects in seed development. Plant Cell, 16(12), 3174–3180. https://doi.org/10.1105/tpc.104.161230.
17. Donoghue, M.T., Fort, A., Clifton, R., Zhang, X., McKeown, P.C., Voigt-Zielinksi, M.L., Borevitz, J.O. and Spillane, C. (2014) C(m)CGG methylation-independent parent-of-origin effects on genome-wide transcript levels in isogenic reciprocal F1 triploid plants. DNA Res. 21(2), 141–151. https://doi.org/10.1093/dnares/dst046.
18. Erilova, A., Brownfield, L., Exner, V., Rosa, M., Twell, D., Scheid, O.M., Hennig, L. and Köhler, C. (2009) Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet. 5(9), e1000663.
19. Feil, R. and Berger, F. (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genet. 23(4), 192–199. https://doi.org/10.1016/j.tig.2007.02.004.
20. Florez-Rueda, A.M., Paris, M., Schmidt, A., Widmer, A., Grossniklaus, U. and Stadler, T. (2016) Genomic imprinting in the endosperm is systematically perturbed in abortive hybrid tomato seeds. Mol. Biol. Evol. 33(11), 2935–2946. https://doi.org/10.1093/molbev/msw175.
21. Fort, A., Ryder, P., McKeown, P.C., Wijnen, C., Aarts, M.G., Sulpice, R. and Spillane, C. (2016) Disaggregating polyploidy, parental-genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana. New Phytol. 209, 590–599. https://doi.org/10.1111/nph.13650.
22. Friedman, W.E. (1995) Organismal duplication, inclusive fitness theory, and altruism: understanding the evolution of endosperm and the angiosperm reproductive syndrome. Proc. Natl Acad. Sci. USA 92(9), 3913–3917.
23. Garnier, O., Laoueillé-Duprat, S. and Spillane, C. (2008) Genomic imprinting in plants. Epigenetics, 3(1), 14–20.
24. Gehring, M. and Satyaki, P.R.V. (2017) Endosperm and imprinting, inextricably linked. Plant Physiol. 173, 143–154. https://doi.org/10.1104/pp.16.01353.
25. Gehring, M., Bubb, K.L. and Henikoff, S. (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science (New York, NY), 324(5933), 1447–1451. https://doi.org/10.1126/science.1171609.
26. Gehring, M., Missirian, V. and Henikoff, S. (2011) Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS ONE, 6(8), e23687.
27. Goff, L.A., Trapnell, C. and Kelley, D. (2012) CummeRbund: visualization and exploration of Cufflinks high-throughput sequencing data. R package version 2 (0).
28. Gutierrez-Marcos, J.F., Pennington, P.D., Costa, L.M. and Dickinson, H.G. (2003) Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358(1434), 1105–1111. https://doi.org/10.1098/rstb.2003.1292.
29. Gutierrez-Marcos, J.F., Constancia, M. and Burton, G.J. (2012) Maternal to offspring resource allocation in plants and mammals. Placenta, 33(Suppl 2), e3–e10. https://doi.org/10.1016/j.placenta.2012.08.006.
30. Haig, D. and Westoby, M. (1989) Parent-specific gene expression and the triploid endosperm. Am. Nat. 134, 147–155.
31. Haig, D. and Westoby, M. (1991) Genomic imprinting in endosperm: its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 333(1266), 1–13.
32. Hsieh, T.F., Shin, J., Uzawa, R., Silva, P., Cohen, S., Bauer, M.J., Hashimoto, M., Kirkbride, R.C., Harada, J.J. and Zilberman, D. (2011) Regulation of imprinted gene expression in Arabidopsis endosperm. Proc. Natl Acad. Sci. USA 108(5), 1755.
33. Hundertmark, M. and Hincha, D.K. (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom. 9, 118. https://doi.org/10.1186/1471-2164-9-118.
34. Hurst, L.D. and McVean, G.T. (1998) Do we understand the evolution of genomic imprinting? Curr. Opin. Genet. Dev. 8(6), 701–708.
35. Iwasa, Y. (1998) The conflict theory of genomic imprinting: how much can be explained? Curr. Top. Dev. Biol. 40, 255–293.
36. Jackson, S. and Chen, Z.J. (2010) Genomic and expression plasticity of polyploidy. Curr. Opin. Plant Biol. 13(2), 153–159. https://doi.org/10.1016/j.pbi.2009.11.004.
37. Jahnke, S. and Scholten, S. (2009) Epigenetic resetting of a gene imprinted in plant embryos. Curr. Biol. 19(19), 1677–1681. https://doi.org/10.1016/j.cub.2009.08.053.
38. Jullien, P.E. and Berger, F. (2010) Parental-genome dosage imbalance deregulates imprinting in Arabidopsis. PLoS Genet. 6(3), e1000885.
39. Kang, I.-H., Steffen, J.G., Portereiko, M.F., Lloyd, A. and Drews, G.N. (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. The Plant Cell Online, 20(3), 635–647.
40. Kato, A. and Birchler, J.A. (2006) Induction of tetraploid derivatives of maize inbred lines by nitrous oxide gas treatment. J. Hered. 97(1), 39–44.
41. Kim, I., Hempel, F.D., Sha, K., Pfluger, J. and Zambryski, P.C. (2002) Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development, 129(5), 1261–1272.
42. van der Klei, H., Van Damme, J., Casteels, P. and Krebbers, E. (1993) A fifth 2S albumin isoform is present in Arabidopsis thaliana. Plant Physiol. 101(4), 1415–1416.
43. Köhler, C., Wolff, P. and Spillane, C. (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Annu. Rev. Plant Biol. 63, 331–352.
44. Kradolfer, D., Wolff, P., Jiang, H., Siretskiy, A. and Köhler, C. (2013) An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev. Cell, 26(5), 525–535. https://doi.org/10.1016/j.devcel.2013.08.006.
45. Lafon-Placette, C. and Köhler, C. (2014) Embryo and endosperm, partners in seed development. Curr. Opin. Plant Biol. 17, 64–69.
46. Li, Y., Zheng, L., Corke, F., Smith, C. and Bevan, M.W. (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev. 22(10), 1331–1336.
47. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G. and Durbin, R. (2009) The sequence alignment/map format and SAMtools. Bioinformatics, 25(16), 2078–2079.
48. Luo, M., Taylor, J.M., Spriggs, A., Zhang, H., Wu, X., Russell, S., Singh, M. and Koltunow, A. (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 7(6), e1002125. https://doi.org/10.1371/journal.pgen.1002125.
49. McKeown, P., Laouielle-Duprat, S., Prins, P., Wolff, P., Schmid, M., Donoghue, M., Fort, A., Duszynska, D., Comte, A. and Lao, N. (2011) Identification of imprinted genes subject to parent-of-origin specific expression in Arabidopsis thaliana seeds. BMC Plant Biol. 11(1), 113.
50. ®. In Plant Epigenetics and Epigenomics: Methods and Protocols (Spillane, C. and McKeown, P.C., eds). Totowa, NJ: Humana Press, pp 85–104. https://doi.org/10.1007/978-1-62703-773-0_6.
51. Miller, M., Zhang, C. and Chen, Z.J. (2012) Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3 (Bethesda), 2(4):505–513.
52. Nguyen, T.-P., Cueff, G., Hegedus, D.D., Rajjou, L. and Bentsink, L. (2015) A role for seed storage proteins in Arabidopsis seed longevity. J. Exp. Bot. 66(20), 6399–6413. https://doi.org/10.1093/jxb/erv348.
53. O'Connell, M.J., Loughran, N.B., Walsh, T.A., Donoghue, M.T., Schmid, K.J. and Spillane, C. (2010) A phylogenetic approach to test for evidence of parental conflict or gene duplications associated with protein-encoding imprinted orthologous genes in placental mammals. Mamm. Genome 21(9–10), 486–498. https://doi.org/10.1007/s00335-010-9283-5.
54. Okushima, Y., Mitina, I., Quach, H.L. and Theologis, A. (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J, 43(1), 29–46.
55. Orozco-Arroyo, G., Paolo, D., Ezquer, I. and Colombo, L. (2015) Networks controlling seed size in Arabidopsis. Plant Reprod. 28(1), 17–32. https://doi.org/10.1007/s00497-015-0255-5.
56. Pang, P.P., Pruitt, R.E. and Meyerowitz, E.M. (1988) Molecular cloning, genomic organization, expression and evolution of 12S seed storage protein genes of Arabidopsis thaliana. Plant Mol. Biol. 11(6), 805–820. https://doi.org/10.1007/BF00019521.
57. Pennington, P.D., Costa, L.M., Gutierrez-Marcos, J.F., Greenland, A.J. and Dickinson, H.G. (2008) When genomes collide: aberrant seed development following maize interploidy crosses. Ann. Bot. 101(6), 833–843.
58. Raissig, M.T., Bemer, M., Baroux, C. and Grossniklaus, U. (2013) Genomic imprinting in the arabidopsis embryo is partly regulated by PRC2. PLoS Genet. 9(12), e1003862. https://doi.org/10.1371/journal.pgen.1003862.
59. Ravi, M. and Chan, S.W. (2010) Haploid plants produced by centromere-mediated genome elimination. Nature, 464(7288), 615–618.
60. Schneeberger, K., Ossowski, S., Ott, F., Klein, J.D., Wang, X., Lanz, C., Smith, L.M., Cao, J., Fitz, J. and Warthmann, N. (2011) Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proc. Natl Acad. Sci. USA 108(25), 10249–10254.
61. Scholten, S. (2010) Genomic imprinting in plant embryos. Epigenetics, 5(6), 455–459. https://doi.org/10.4161/epi.5.6.12313.
62. Schon, M.A. and Nodine, M. (2017) Widespread contamination of Arabidopsis embryo and endosperm transcriptome datasets. Plant Cell, 29, 608–617. https://doi.org/10.1105/tpc.16.00845.
63. Schruff, M.C., Spielman, M., Tiwari, S., Adams, S., Fenby, N. and Scott, R.J. (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development, 133(2), 251–261.
64. Scott, R.J., Spielman, M., Bailey, J. and Dickinson, H.G. (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development, 125(17), 3329.
65. Sekine, D., Ohnishi, T., Furuumi, H., Ono, A., Yamada, T., Kurata, N. and Kinoshita, T. (2013) Dissection of two major components of the post-zygotic hybridization barrier in rice endosperm. Plant J. 76(5), 792–799. https://doi.org/10.1111/tpj.12333.
66. Shewry, P.R., Napier, J.A. and Tatham, A.S. (1995) Seed storage proteins: structures and biosynthesis. Plant Cell, 7(7), 945–956.
67. Simon, P. (2003) Q-Gene: processing quantitative real-time RT–PCR data. Bioinformatics, 19(11), 1439–1440.
68. Stoute, A.I., Varenko, V., King, G.J., Scott, R.J. and Kurup, S. (2012) Parental-genome imbalance in Brassica oleracea causes asymmetric triploid block. Plant J. 71(3), 503–516.
69. Sweigart, A.L., Martin, N.H. and Willis, J.H. (2008) Patterns of nucleotide variation and reproductive isolation between a Mimulus allotetraploid and its progenitor species. Mol. Ecol. 17, 2089–2100.
70. Tiwari, S., Spielman, M., Schulz, R., Oakey, R.J., Kelsey, G., Salazar, A., Zhang, K., Pennell, R. and Scott, R.J. (2010) Transcriptional profiles underlying parent-of-origin effects in seeds of Arabidopsis thaliana. BMC Plant Biol. 10(1), 72. https://doi.org/10.1186/1471-2229-10-72.
71. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25(9), 1105–1111. https://doi.org/10.1093/bioinformatics/btp120.
72. Wang, X. and Clark, A. (2014) Using next-generation RNA sequencing to identify imprinted genes. Heredity, 113(2), 156–166.
73. Waters, A.J., Bilinski, P., Eichten, S.R., Vaughn, M.W., Ross-Ibarra, J., Gehring, M. and Springer, N.M. (2013) Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc. Natl Acad. Sci. USA 110, 19639–19644.
74. Wolf, J.B., Oakey, R.J. and Feil, R. (2014) Imprinted gene expression in hybrids: perturbed mechanisms and evolutionary implications. Heredity (Edinb) 113(2), 167–175. https://doi.org/10.1038/hdy.2014.11.
75. Wolff, P., Weinhofer, I., Seguin, J., Roszak, P., Beisel, C., Donoghue, M.T.A., Spillane, C., Nordborg, M., Rehmsmeier, M. and Köhler, C. (2011) High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet. 7(6), e1002126. https://doi.org/10.1371/journal.pgen.1002126.
76. Wolff, P., Jiang, H., Wang, G., Santos-González, J. and Köhler, C. (2015) Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana. Elife, 4. https://doi.org/10.7554/eLife.10074
77. Xia, T., Li, N., Dumenil, J., Li, J., Kamenski, A., Bevan, M.W., Gao, F. and Li, Y. (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell, 25(9), 3347–3359.
78. Yu, Z., Haberer, G., Matthes, M., Rattei, T., Mayer, K.F.X., Gierl, A. and Torres-Ruiz, R.A. (2010) Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 107(41), 17809–17814. https://doi.org/10.1073/pnas.1000852107.
79. Zhang, X. and Borevitz, J.O. (2009) Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics, 182(4), 943–954. https://doi.org/10.1534/genetics.109.103499.