title: Natural variation in epigenetic pathways affects the specification of female gamete precursors in Arabidopsis.
abstract: In angiosperms, the transition to the female gametophytic phase relies on the specification of premeiotic gamete precursors from sporophytic cells in the ovule. In Arabidopsis thaliana, a single diploid cell is specified as the premeiotic female gamete precursor. Here, we show that ecotypes of Arabidopsis exhibit differences in megasporogenesis leading to phenotypes reminiscent of defects in dominant mutations that epigenetically affect the specification of female gamete precursors. Intraspecific hybridization and polyploidy exacerbate these defects, which segregate quantitatively in F2 populations derived from ecotypic hybrids, suggesting that multiple loci control cell specification at the onset of female meiosis. This variation in cell differentiation is influenced by the activity of ARGONAUTE9 (AGO9) and RNA-DEPENDENT RNA POLYMERASE6 (RDR6), two genes involved in epigenetic silencing that control the specification of female gamete precursors. The pattern of transcriptional regulation and localization of AGO9 varies among ecotypes, and abnormal gamete precursors in ovules defective for RDR6 share identity with ectopic gamete precursors found in selected ecotypes. Our results indicate that differences in the epigenetic control of cell specification lead to natural phenotypic variation during megasporogenesis. We propose that this mechanism could be implicated in the emergence and evolution of the reproductive alternatives that prevail in flowering plants.
authors.affiliation: Grupo de Desarrollo Reproductivo y Apomixis, Laboratorio Nacional de Genómica para la Biodiversidad y Departamento de Ingeniería Genética de Plantas, Cinvestav Irapuato CP36821 Guanajuato, Mexico.
authors.forename: Daniel
authors.initials: D
authors.lastname: Rodríguez-Leal
authors.affiliation: Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional del Instituto Politécnico Nacional, Unidad Michoacán, CP 59510 Jiquilpan, Mexico.
authors.forename: Gloria
authors.initials: G
authors.lastname: León-Martínez
authors.affiliation: Grupo de Desarrollo Reproductivo y Apomixis, Laboratorio Nacional de Genómica para la Biodiversidad y Departamento de Ingeniería Genética de Plantas, Cinvestav Irapuato CP36821 Guanajuato, Mexico.
authors.forename: Ursula
authors.initials: U
authors.lastname: Abad-Vivero
authors.affiliation: Grupo de Desarrollo Reproductivo y Apomixis, Laboratorio Nacional de Genómica para la Biodiversidad y Departamento de Ingeniería Genética de Plantas, Cinvestav Irapuato CP36821 Guanajuato, Mexico vielle@ira.cinvestav.mx.
authors.forename: Jean-Philippe
authors.initials: JP
authors.lastname: Vielle-Calzada
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D060565:Argonaute Proteins / Q000235:genetics / Q000378:metabolism; D002454:Cell Differentiation / Q000235:genetics / Q000502:physiology; D044127:Epigenesis, Genetic / Q000235:genetics*; D056130:Gametogenesis, Plant / Q000235:genetics / Q000502:physiology; D018506:Gene Expression Regulation, Plant / Q000235:genetics / Q000502:physiology; D012324:RNA-Dependent RNA Polymerase / Q000235:genetics / Q000378:metabolism
chemical_list: C548461:AGO9 protein, Arabidopsis; D029681:Arabidopsis Proteins; D060565:Argonaute Proteins; C514575:RDR6 protein, Arabidopsis; D012324:RNA-Dependent RNA Polymerase
references.citation: Trends Plant Sci. 2010 Feb;15(2):57-71
references.pmid: 20080432
references.citation: Annu Rev Plant Biol. 2003;54:547-74
references.pmid: 14503003
references.citation: Nat Rev Genet. 2013 Jul;14(7):471-82
references.pmid: 23752794
references.citation: Plant Signal Behav. 2010 Nov;5(11):1476-9
references.pmid: 21057207
references.citation: Plant Cell. 2010 Oct;22(10):3249-67
references.pmid: 21037104
references.citation: Proc Natl Acad Sci U S A. 2012 May 1;109(18):7109-14
references.pmid: 22493265
references.citation: Curr Biol. 2011 Jun 21;21(12):1009-17
references.pmid: 21658947
references.citation: Genes Dev. 2009 Mar 1;23(5):549-54
references.pmid: 19270155
references.citation: PLoS Biol. 2011 Sep;9(9):e1001155
references.pmid: 21949639
references.citation: Trends Plant Sci. 2008 Jul;13(7):350-8
references.pmid: 18508405
references.citation: Nature. 2010 Jun 3;465(7298):627-31
references.pmid: 20336072
references.citation: Plant Cell. 2010 Feb;22(2):321-34
references.pmid: 20173091
references.citation: Plant Cell. 2003 Aug;15(8):1728-39
references.pmid: 12897248
references.citation: PLoS One. 2011;6(10):e25730
references.pmid: 21998686
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12360-5
references.pmid: 21690400
references.citation: BMC Plant Biol. 2009 Aug 13;9:107
references.pmid: 19678936
references.citation: Heredity (Edinb). 2014 Jan;112(1):4-12
references.pmid: 23612691
references.citation: Mol Cell. 2012 Jun 29;46(6):859-70
references.pmid: 22608924
references.citation: Sex Plant Reprod. 2011 Jun;24(2):137-47
references.pmid: 21484604
references.citation: Nature. 1999 Sep 9;401(6749):157-61
references.pmid: 10490023
references.citation: Genes Dev. 2006 Nov 15;20(22):3079-83
references.pmid: 17114581
references.citation: Plant J. 1998 Dec;16(6):735-43
references.pmid: 10069079
references.citation: Elife. 2014 Jul 03;3:e03198
references.pmid: 24994762
references.citation: BMC Plant Biol. 2011 Jan 11;11:9
references.pmid: 21223576
references.citation: G3 (Bethesda). 2011 Dec;1(7):571-9
references.pmid: 22384368
references.citation: Plant Cell. 1993 Oct;5(10):1291-1301
references.pmid: 12271029
references.citation: Development. 2012 Apr;139(8):1399-404
references.pmid: 22399683
references.citation: Curr Biol. 2012 Jan 24;22(2):166-70
references.pmid: 22206705
references.citation: Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11664-9
references.pmid: 10500234
references.citation: Curr Biol. 2012 Feb 21;22(4):326-31
references.pmid: 22285031
references.citation: Trends Genet. 2001 Oct;17(10):597-604
references.pmid: 11585667
references.citation: Semin Cell Dev Biol. 1998 Apr;9(2):227-38
references.pmid: 9599420
references.citation: Science. 2012 Aug 31;337(6098):1081-4
references.pmid: 22936775
references.citation: Genetics. 1996 Mar;142(3):1009-20
references.pmid: 8849906
references.citation: Arabidopsis Book. 2011;9:e0155
references.pmid: 22303279
references.citation: G3 (Bethesda). 2012 Apr;2(4):505-13
references.pmid: 22540042
references.citation: Annu Rev Plant Biol. 2007;58:377-406
references.pmid: 17280525
references.citation: Genetics. 1956 Nov;41(6):872-89
references.pmid: 17247669
references.citation: New Phytol. 2014 Dec;204(4):1000-12
references.pmid: 25081588
references.citation: Nature. 2010 Mar 25;464(7288):628-32
references.pmid: 20208518
references.citation: Sex Plant Reprod. 2012 Jun;25(2):97-109
references.pmid: 22367230
references.citation: Nat Rev Genet. 2009 Feb;10(2):94-108
references.pmid: 19148191
references.citation: PLoS One. 2011;6(5):e19949
references.pmid: 21625501
references.citation: Science. 2003 Jan 31;299(5607):716-9
references.pmid: 12522258
references.citation: Ann Bot. 2009 Apr;103(6):869-84
references.pmid: 19202137
references.citation: Genes Dev. 2004 Oct 1;18(19):2368-79
references.pmid: 15466488
references.citation: Plant Physiol. 2003 Oct;133(2):462-9
references.pmid: 14555774
references.citation: Plant Physiol. 2014 Sep;166(1):265-80
references.pmid: 25073707
references.citation: J Cell Biol. 1997 Apr 7;137(1):5-18
references.pmid: 9105032
references.citation: Science. 2014 Mar 7;343(6175):1145-8
references.pmid: 24505129
references.citation: Genes Dev. 2005 Sep 15;19(18):2164-75
references.pmid: 16131612
references.citation: Plant Reprod. 2013 Dec;26(4):309-15
references.pmid: 23783772
references.citation: Nature. 2010 Jun 3;465(7298):632-6
references.pmid: 20520716
references.citation: Plant J. 2012 Aug;71(4):669-83
references.pmid: 22487254
references.citation: Plant Cell. 2010 Jul;22(7):2105-12
references.pmid: 20622146
references.citation: PLoS Genet. 2013 Apr;9(4):e1003437
references.pmid: 23593031
references.citation: New Phytol. 1995 Jan;129(1):1-22
references.pmid: 33874422
references.citation: PLoS Biol. 2005 Jul;3(7):e196
references.pmid: 15907155
references.citation: Plant J. 2011 Jun;66(5):831-43
references.pmid: 21457364
references.citation: Nat Commun. 2013;4:2875
references.pmid: 24285012
references.citation: Plant Cell. 2007 Aug;19(8):2583-94
references.pmid: 17675402
references.citation: Cell. 2006 Jul 14;126(1):79-92
references.pmid: 16839878
references.citation: Plant Cell. 2010 Dec;22(12):3879-89
references.pmid: 21183704
references.citation: Nat Methods. 2012 Jul;9(7):671-5
references.pmid: 22930834
references.citation: Curr Opin Plant Biol. 2012 Nov;15(5):549-55
references.pmid: 23000434
references.citation: Nat Genet. 2006 Aug;38(8):948-52
references.pmid: 16832354
references.citation: Genes Dev. 1999 Nov 15;13(22):2971-82
references.pmid: 10580004
references.citation: Curr Biol. 2004 Jul 13;14(13):1214-20
references.pmid: 15242620
references.citation: Nat Genet. 2013 Aug;45(8):884-890
references.pmid: 23793030
references.citation: Cell. 2006 Jul 14;126(1):93-106
references.pmid: 16839879
references.citation: Plant Cell. 2009 Jul;21(7):1877-96
references.pmid: 19574434
references.citation: Annu Rev Biochem. 1999;68:321-54
references.pmid: 10872453