Natural variation in epigenetic pathways affects the specification of female gamete precursors in arabidopsis

Plant Cell

Volumn 27, Issue 4, 2015, Pages 1034-1045

  Rodríguez Leal, Daniel ^a   León Martínez, Gloria ^b   Abad Vivero, Ursula ^a   Vielle Calzada, Jean Philippe ^a  

^a Lab Nac de Genomica Para la Biodiversidad y Departamento de Ingenieria Genetica de Plantas   (Mexico)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAGNOLIOPHYTA;

AGO9 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ARGONAUTE PROTEIN; RDR6 PROTEIN, ARABIDOPSIS; RNA DIRECTED RNA POLYMERASE;

ARABIDOPSIS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY; PLANT GAMETOGENESIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; CELL DIFFERENTIATION; EPIGENESIS, GENETIC; GAMETOGENESIS, PLANT; GENE EXPRESSION REGULATION, PLANT; RNA REPLICASE;

EID: 84928955639     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.133009     Document Type: Article

References (82)

1. Alonso-Blanco, C., Aarts, M.G.M., Bentsink, L., Keurentjes, J.J.B., Reymond, M., Vreugdenhil, D., and Koornneef, M. (2009). What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21: 1877–1896.
2. Anderson, J.T., Wagner, M.R., Rushworth, C.A., Prasad, K.V.S.K., and Mitchell-Olds, T. (2014). The evolution of quantitative traits in complex environments. Heredity (Edinb.) 112: 4–12.
3. Armenta-Medina, A., Demesa-Arévalo, E., and Vielle-Calzada, J.P. (2011). Epigenetic control of cell specification during female ga-metogenesis. Sex. Plant Reprod. 24: 137–147.
4. Atwell, S., et al. (2010). Genome-wide association study of 107 phe-notypes in Arabidopsis thaliana inbred lines. Nature 465: 627–631.
5. Bachelier, J.B., and Friedman, W.E. (2011). Female gamete competition in an ancient angiosperm lineage. Proc. Natl. Acad. Sci. USA 108: 12360–12365.
6. Bass, H.W., Marshall, W.F., Sedat, J.W., Agard, D.A., and Cande, W.Z. (1997). Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137: 5–18.
7. Birchler, J.A., Yao, H., Chudalayandi, S., Vaiman, D., and Veitia, R.A. (2010). Heterosis. Plant Cell 22: 2105–2112.
8. Bretagnolle, F., and Thompson, J.B. (1995). Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129: 1–22.
9. Brink, R.A. (1956). A genetic change associated with the R Locus in maize which is directed and potentially reversible. Genetics 41: 872–889.
10. Carman, J.G. (1997). Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and poly-embryony. Biol. J. Linn. Soc. Lond. 61: 51–94.
11. Carman, J.G., Jamison, M., Elliott, E., Dwivedi, K.K., and Naumova, T.N. (2011). Apospory appears to accelerate onset of meiosis and sexual embryo sac formation in sorghum ovules. BMC Plant Biol. 11: 9.
12. Chen, Z.J. (2007). Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 58: 377–406.
13. Chen, Z.J. (2010). Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15: 57–71.
14. Chen, Z.J. (2013). Genomic and epigenetic insights into the molecular bases of heterosis. Nat. Rev. Genet. 14: 471–482.
15. Chitwood, D.H., Nogueira, F.T., Howell, M.D., Montgomery, T.A., Carrington, J.C., and Timmermans, M.C. (2009). Pattern formation via small RNA mobility. Genes Dev. 23: 549–554.
16. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.
17. Cortijo, S., et al. (2014). Mapping the epigenetic basis of complex traits. Science 343: 1145–1148.
18. Cubas, P., Vincent, C., and Coen, E. (1999). An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.
19. Curtis, M.D., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462–469.
20. Drews, G.N., and Koltunow, A.M. (2011). The female gametophyte. The Arabidopsis Book. 9: e0155, doi/10.1199/tab.0155.
21. Durán-Figueroa, N., and Vielle-Calzada, J.P. (2010). ARGONAUTE9-dependent silencing of transposable elements in pericentromeric regions of Arabidopsis. Plant Signal. Behav. 5: 1476–1479.
22. Durand, S., Bouché, N., Perez Strand, E., Loudet, O., and Camilleri, C. (2012). Rapid establishment of genetic incompatibility through natural epigenetic variation. Curr. Biol. 22: 326–331.
23. Eames, A.J. (1961). Morphology of the Angiosperms. (New York: McGraw-Hill).
24. Eun, C., Lorkovic, Z.J., Naumann, U., Long, Q., Havecker, E.R., Simon, S.A., Meyers, B.C., Matzke, A.J., and Matzke, M. (2011). AGO6 functions in RNA-mediated transcriptional gene silencing in shoot and root meristems in Arabidopsis thaliana. PLoS ONE 6: e25730.
25. Ferrándiz, C., Pelaz, S., and Yanofsky, M.F. (1999). Control of carpel and fruit development in Arabidopsis. Annu. Rev. Biochem. 68: 321–354.
26. Fujimoto, R., Taylor, J.M., Shirasawa, S., Peacock, W.J., and Dennis, E.S. (2012). Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc. Natl. Acad. Sci. USA 109: 7109–7114.
27. Fujimoto, R., Sasaki, T., Kudoh, H., Taylor, J.M., Kakutani, T., and Dennis, E.S. (2011). Epigenetic variation in the FWA gene within the genus Arabidopsis. Plant J. 66: 831–843.
28. García-Aguilar, M., Michaud, C., Leblanc, O., and Grimanelli, D. (2010). Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22: 3249–3267.
29. García-Aguilar, M., Dorantes-Acosta, A., Pérez-España, V., and Vielle-Calzada, J.-P. (2005). Whole-mount in situ mRNA localization in developing ovules and seeds of Arabidopsis. Plant Mol. Biol. Rep. 23: 279–289.
30. Ghildiyal, M., and Zamore, P.D. (2009). Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10: 94–108.
31. Grimanelli, D., Leblanc, O., Perotti, E., and Grossniklaus, U. (2001). Developmental genetics of gametophytic apomixis. Trends Genet. 17: 597–604.
32. Grossniklaus, U., and Schneitz, K. (1998). The molecular and genetic basis of ovule and megagametophyte development. Semin. Cell Dev. Biol. 9: 227–238.
33. Groszmann, M., Gonzalez-Bayon, R., Greaves, I.K., Wang, L., Huen, A.K., Peacock, W.J., and Dennis, E.S. (2014). Intraspecific Arabidopsis hybrids show different patterns of heterosis despite the close relatedness of the parental genomes. Plant Physiol. 166: 265–280.
34. Havecker, E.R., Wallbridge, L.M., Hardcastle, T.J., Bush, M.S., Kelly, K.A., Dunn, R.M., Schwach, F., Doonan, J.H., and Baulcombe, D.C. (2010). The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22: 321–334.
35. Hojsgaard, D., Greilhuber, J., Pellino, M., Paun, O., Sharbel, T.F., and Hörandl, E. (2014). Emergence of apospory and bypass of meiosis via apomixis after sexual hybridisation and polyploidisation. New Phytol. 204: 1000–1012.
36. Huang, B.-Q., and Russell, S.D. (1992). Female germ unit: Organization, isolation, and function. Int. Rev. Cytol. 140: 233–293.
37. Karpechenko, G.D. (1927). The production of polyploid gametes in hybrids. Hereditas 9: 349–368.
38. Koltunow, A.M., and Grossniklaus, U. (2003). Apomixis: a developmental perspective. Annu. Rev. Plant Biol. 54: 547–574.
39. Latzel, V., Allan, E., Bortolini Silveira, A., Colot, V., Fischer, M., and Bossdorf, O. (2013). Epigenetic diversity increases the productivity and stability of plant populations. Nat. Commun. 4: 2875.
40. Li, C.F., Pontes, O., El-Shami, M., Henderson, I.R., Bernatavichute, Y.V., Chan, S.W., Lagrange, T., Pikaard, C.S., and Jacobsen, S.E. (2006). An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93–106.
41. Li, X., Wei, Y., Nettleton, D., and Brummer, E.C. (2009). Comparative gene expression profiles between heterotic and non-heterotic hybrids of tetraploid Medicago sativa. BMC Plant Biol. 9: 107.
42. Lieber, D., Lora, J., Schrempp, S., Lenhard, M., and Laux, T. (2011). Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate. Curr. Biol. 21: 1009–1017.
43. Long, Q., et al. (2013). Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45: 884–890.
44. Lovell, J.T., Aliyu, O.M., Mau, M., Schranz, M.E., Koch, M., Kiefer, C., Song, B.H., Mitchell-Olds, T., and Sharbel, T.F. (2013). On the origin and evolution of apomixis in Boechera. Plant Reprod. 26: 309–315.
45. Madrid, E.N., and Friedman, W.E. (2009). The developmental basis of an evolutionary diversification of female gametophyte structure in Piper and Piperaceae. Ann. Bot. (Lond.) 103: 869–884.
46. Maheshwari, P. (1950). An Introduction to the Embryology of An-giosperms. (New York: MacGraw-Hill).
47. Mallory, A., and Vaucheret, H. (2010). Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22: 3879–3889.
48. Manning, K., Tör, M., Poole, M., Hong, Y., Thompson, A.J., King, G.J., Giovannoni, J.J., and Seymour, G.B. (2006). A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38: 948–952.
49. Meyer, R.C., et al. (2012). Heterosis manifestation during early Ara-bidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids. Plant J. 71: 669–683.
50. 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: 505–513.
51. Moore, S., and Lukens, L. (2011). An evaluation of Arabidopsis thaliana hybrid traits and their genetic control. 3 G 1: 571–579.
52. Nonomura, K., Miyoshi, K., Eiguchi, M., Suzuki, T., Miyao, A., Hirochika, H., and Kurata, N. (2003). The MSP1 gene is necessary to restrict the number of cells entering into male and female spo-rogenesis and to initiate anther wall formation in rice. Plant Cell 15: 1728–1739.
53. Nonomura, K., Morohoshi, A., Nakano, M., Eiguchi, M., Miyao, A., Hirochika, H., and Kurata, N. (2007). A germ cell specific gene of the ARGONAUTE family is essential for the progression of pre-meiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19: 2583–2594.
54. Nordborg, M., et al. (2005). The pattern of polymorphism in Arabi-dopsis thaliana. PLoS Biol. 3: e196.
55. Olmedo-Monfil, V., Durán-Figueroa, N., Arteaga-Vázquez, M., Demesa-Arévalo, E., Autran, D., Grimanelli, D., Slotkin, R.K., Martienssen, R.A., and Vielle-Calzada, J.P. (2010). Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628–632.
56. Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H.L., and Poethig, R.S. (2004). SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabi-dopsis. Genes Dev. 18: 2368–2379.
57. Pignatta, D., Erdmann, R.M., Scheer, E., Picard, C.L., Bell, G.W., and Gehring, M. (2014). Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. eLife 3: e03198.
58. Pontes, O., Li, C.F., Costa Nunes, P., Haag, J., Ream, T., Vitins, A., Jacobsen, S.E., and Pikaard, C.S. (2006). The Arabidopsis chro-matin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126: 79–92.
59. Prasad, K.V.S.K., et al. (2012). A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337: 1081–1084.
60. Ramsey, J., and Schemske, D.W. (1998). Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29: 467–501.
61. Reiser, L., and Fischer, R.L. (1993). The ovule and the embryo sac. Plant Cell 5: 1291–1301.
62. Rodríguez-Leal, D., and Vielle-Calzada, J.P. (2012). Regulation of apomixis: learning from sexual experience. Curr. Opin. Plant Biol. 15: 549–555.
63. Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., and Schneitz, K. (1999). Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 11664–11669.
64. Schmidt, A., Wuest, S.E., Vijverberg, K., Baroux, C., Kleen, D., and Grossniklaus, U. (2011). Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9: e1001155.
65. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9: 671-675.
66. Schneitz, K., Hülskamp, M., and Pruitt, R.E. (1995). Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J. 7: 731-749.
67. Sheridan, W.F., Avalkina, N.A., Shamrov, I.I., Batygina, T.B., and Golubovskaya, I.N. (1996). The mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics 142: 1009-1020.
68. Shindo, C, Lister, C, Crevillen, P., Nordborg, M., and Dean, C. (2006). Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev. 20: 3079-3083.
69. Silveira, A.B., Trontin, C, Cortijo, S., Barau, J., Del Bem, L.E., Loudet, O., Colot, V., and Vincentz, M. (2013). Extensive natural epigenetic variation at a de novo originated gene. PLoS Genet. 9: e1003437.
70. Strange, A., Li, P., Lister, C, Anderson, J., Warthmann, N., Shindo, C, Irwin, J., Nordborg, M., and Dean, C. (2011). Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions. PLoS ONE 6: e19949.
71. Todesco, M., et al. (2010). Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465: 632-636.
72. Todesco, M., Balasubramanian, S., Cao, J., Ott, F., Sureshkumar, S., Schneeberger, K., Meyer, R.C., Altmann, T., and Weigel, D. (2012). Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr. Biol. 22: 166-170.
73. Tucker, M.R., Okada, T., Hu, Y., Scholefield, A., Taylor, J.M., and Koltunow, A.M. (2012). Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139: 1399-1404.
74. Vandendries, R. (1909). Contribution á l’histoire du développement des crucifères. Cellule 25: 412-429.
75. Vaucheret, H. (2008). Plant ARGONAUTES. Trends Plant Sci. 13: 350-358.
76. Vielle-Calzada, J.-P., Thomas, J., Spillane, C, Coluccio, A., Hoeppner, M.A., and Grossniklaus, U. (1999). Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13: 2971-2982.
77. Voigt-Zielinski, M.L., Piwczynski, M., and Sharbel, T.F. (2012). Differential effects of polyploidy and diploidy on fitness of apomictic Boechera. Sex. Plant Reprod. 25: 97-109.
78. Walters, J.L. (1962). Megasporogenesis and gametophyte selection in Paeonia californica. Am. J. Bot. 49: 787-794.
79. Ye, R., Wang, W., Iki, T., Liu, C, Wu, Y., Ishikawa, M., Zhou, X., and Qi, Y. (2012). Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol. Cell 46: 859-870.
80. Yoshikawa, M., Peragine, A., Park, M.Y., and Poethig, R.S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19: 2164-2175.
81. Zilberman, D., Cao, X., and Jacobsen, S.E. (2003). ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719.
82. Zilberman, D., Cao, X., Johansen, L.K., Xie, Z., Carrington, J.C., and Jacobsen, S.E. (2004). Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr. Biol. 14: 1214-1220.