title: Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus.
abstract: Divergence of developmental mechanisms within populations could lead to hybrid developmental failure, and might be a factor driving speciation in angiosperms. We investigate patterns of endosperm and embryo development in Mimulus guttatus and the closely related, serpentine endemic Mimulus nudatus, and compare them to those of reciprocal hybrid seed. We address whether disruption in hybrid seed development is the primary source of reproductive isolation between these sympatric taxa. M. guttatus and M. nudatus differ in the pattern and timing of endosperm and embryo development. Some hybrid seeds exhibit early disruption of endosperm development and are completely inviable, while others develop relatively normally at first, but later exhibit impaired endosperm proliferation and low germination success. These developmental patterns are reflected in mature hybrid seeds, which are either small and flat (indicating little to no endosperm) or shriveled (indicating reduced endosperm volume). Hybrid seed inviability forms a potent reproductive barrier between M. guttatus and M. nudatus. We shed light on the extent of developmental variation between closely related species within the M. guttatus species complex, an important ecological model system, and provide a partial mechanism for the hybrid barrier between M. guttatus and M. nudatus.
authors.affiliation: Department of Biology, Duke University, 3319 French Family Science Center, 125 Science Drive, Durham, NC, 27705, USA.
authors.forename: Elen
authors.identifier: http://orcid.org/0000-0002-6522-9741
authors.initials: E
authors.lastname: Oneal
authors.affiliation: Department of Biology, Duke University, 3319 French Family Science Center, 125 Science Drive, Durham, NC, 27705, USA.
authors.forename: John H
authors.initials: JH
authors.lastname: Willis
authors.affiliation: Department of Plant and Microbial Biology, North Carolina State University, 2548 Thomas Hall, Raleigh, NC, 27695, USA.
authors.forename: Robert G
authors.initials: RG
authors.lastname: Franks
mesh_terms: D003433:Crosses, Genetic; D056625:Endosperm / Q000196:embryology*; D005638:Fruit / Q000254:growth & development; D018525:Germination; D006824:Hybridization, Genetic; D032241:Mimulus / Q000196:embryology* / Q000235:genetics*; D010641:Phenotype; D053205:Pollen Tube / Q000254:growth & development; D057945:Self-Fertilization; D013194:Staining and Labeling; D061350:Sympatry
keywords: Mimulus guttatus (monkeyflower); endosperm; hybrid inviability; pollen-pistil interactions; postzygotic isolation; seed development
references.citation: Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):11910-5
references.pmid: 10518550
references.citation: Plant Physiol. 2000 Dec;124(4):1570-81
references.pmid: 11115875
references.citation: Curr Opin Plant Biol. 2001 Feb;4(1):14-20
references.pmid: 11163162
references.citation: Curr Opin Plant Biol. 2001 Feb;4(1):21-7
references.pmid: 11163163
references.citation: Proc Biol Sci. 2001 Apr 22;268(1469):861-7
references.pmid: 11345333
references.citation: C R Acad Sci III. 2001 Jun;324(6):507-15
references.pmid: 11460830
references.citation: Nature. 2002 Apr 25;416(6883):844-7
references.pmid: 11976682
references.citation: Semin Cell Dev Biol. 2003 Feb;14(1):77-84
references.pmid: 12524010
references.citation: Genes Dev. 2003 Jun 15;17(12):1540-53
references.pmid: 12815071
references.citation: Evolution. 2003 Jul;57(7):1520-34
references.pmid: 12940357
references.citation: J Evol Biol. 2003 May;16(3):536-40
references.pmid: 14635855
references.citation: Trends Plant Sci. 2004 Oct;9(10):507-14
references.pmid: 15465686
references.citation: Plant J. 2005 Apr;42(1):111-23
references.pmid: 15773857
references.citation: Am Nat. 2005 Sep;166(3):330-8
references.pmid: 16224688
references.citation: Plant Physiol. 1991 Jul;96(3):985-9
references.pmid: 16668285
references.citation: Curr Biol. 2006 Jul 11;16(13):1322-8
references.pmid: 16824920
references.citation: Plant Cell. 2007 Mar;19(3):779-90
references.pmid: 17337627
references.citation: Heredity (Edinb). 2008 Feb;100(2):220-30
references.pmid: 17551519
references.citation: Science. 2007 Aug 17;317(5840):910-4
references.pmid: 17702935
references.citation: Science. 1982 Jul 30;217(4558):446-8
references.pmid: 17782980
references.citation: PLoS Biol. 2007 Sep;5(9):e236
references.pmid: 17803357
references.citation: Evolution. 2008 Dec;62(12):2958-70
references.pmid: 18691263
references.citation: J Integr Plant Biol. 2009 Jan;51(1):21-8
references.pmid: 19166490
references.citation: New Phytol. 2009 Aug;183(3):729-39
references.pmid: 19453433
references.citation: PLoS Genet. 2009 Sep;5(9):e1000663
references.pmid: 19779546
references.citation: New Phytol. 2010 Apr;186(1):54-62
references.pmid: 19925558
references.citation: Trends Genet. 2010 Mar;26(3):142-8
references.pmid: 20089326
references.citation: New Phytol. 2010 Jun;186(4):817-31
references.pmid: 20406407
references.citation: Philos Trans R Soc Lond B Biol Sci. 2010 Aug 27;365(1552):2469-78
references.pmid: 20643736
references.citation: PLoS Biol. 2010 Sep 28;8(9):null
references.pmid: 20927411
references.citation: Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1755-62
references.pmid: 21257907
references.citation: CSH Protoc. 2007 Jan 01;2007:pdb.prot4685
references.pmid: 21356937
references.citation: Am J Bot. 2009 Jan;96(1):144-65
references.pmid: 21628181
references.citation: Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20826-31
references.pmid: 22143805
references.citation: Annu Rev Plant Biol. 2012;63:331-52
references.pmid: 22404470
references.citation: Development. 2012 Jun;139(11):2031-9
references.pmid: 22535409
references.citation: Nat Methods. 2012 Jul;9(7):671-5
references.pmid: 22930834
references.citation: Protoplasma. 2013 Aug;250(4):863-73
references.pmid: 23178998
references.citation: PLoS Genet. 2013;9(1):e1003163
references.pmid: 23326241
references.citation: PLoS Biol. 2013;11(2):e1001497
references.pmid: 23468595
references.citation: Annu Rev Cell Dev Biol. 2013;29:189-211
references.pmid: 23641801
references.citation: Plant Cell. 2013 Jun;25(6):2037-55
references.pmid: 23898028
references.citation: Mol Ecol. 2014 Jun;23(11):2844-60
references.pmid: 24796267
references.citation: Front Plant Sci. 2014 Jun 26;5:281
references.pmid: 25018757
references.citation: New Phytol. 2014 Dec;204(4):1013-27
references.pmid: 25103615
references.citation: Nature. 2014 Oct 30;514(7524):624-7
references.pmid: 25209660
references.citation: Development. 2014 Dec;141(23):4580-9
references.pmid: 25377553
references.citation: PLoS Genet. 2015 Jun 18;11(6):e1005295
references.pmid: 26086217
references.citation: Evolution. 1990 Sep;44(6):1424-1435
references.pmid: 28564312
references.citation: Crit Rev Food Sci Nutr. 1986;24(4):401-49
references.pmid: 3536314
references.citation: Annu Rev Genet. 1993;27:181-204
references.pmid: 8122901
references.citation: Development. 1998 Sep;125(17):3329-41
references.pmid: 9693137