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Genetics of Floral Development An Evo-Devo Approach Biology 317 Kelsey Galimba 8.5.2013 Why are flowering plants so diverse? Why are flowering plants so diverse? http://www.botanicalgarden.ubc.ca/potd/ Evolution of Development (Evo-Devo) The Logic ! Morphology is the product of development ! Development results from genetic regulatory programs. ! Evolution of diversity is directly related to the evolution of genetic regulatory programs. ! A limited number of genetic pathways have been used and re-used to build different body plans. Using the Evo-Devo Approach to study floral diversity Developmental processes that occur in the flowers different taxa. Infer evolutionary events that led to the differences or similarities. Zahn et al. (2005) Floral morphology can be described with different characteristics Phyllotaxy Symmetry Organ Fusion Whorl Number Organ Elaboration Organ Identity Floral Symmetry Bilateral Symmetry has evolved many times Carl Linneaus 1707-1778 Cubas 2004 Linaria vulgaris peloric mutant Linaria vulgaris L. vulgaris peloric mutations caused by methylation of CYCLOIDEA Floral Symmetry controlled by CYCLOIDEA(CYC) and DICHOTOMA(DICH) Antirrhinum majus WT Peloric CYC expression in developing flowers Luo et al. 1996 Mohavea confertiflora - Changes in symmetry with an evolutionary effect Cubas 2004 Hileman et al. 2003 M. confertiflora mimics a radial species. Mohavea confertiflora Mentzelia involucrata CYC affects symmetry in Helianthus Cubas 2004 Changes in CYC expression cause “Van Gogh's sunflowers” Chapman et al. 2012 Summary • Bilateral symmetry has evolved many time independently. • CYC homologs appear to have been recruited as symmetry genes in all cases of bilateral symmetry within the core eudicots. Floral Organ Identity Sepal – 1st Whorl Petal – 2nd Whorl Stamen – 3rd Whorl Carpel – 4th Whorl Different phases of shoot growth are regulated by environmental and endogenous signals Developmental Biology, Seventh Edition, Figure 20.38 Floral Organ Identity genes are MADS Box genes = Transcription Factors HOX Genes MADS-Box genes in flowers are HOX genes in animals are important for important for correct organ identity. correct body-plan formation. MIKC-type MADS-Box genes MADS I K C Highly conserved 60 Alpha-helical K-box, amino acid domain involved in protein involved in DNA dimerization. binding and protein dimerization. Generally divergent domain with small “Intervening” domain, highly conserved motifs, plays role in dimerization recently implicated specificity. as mediator of ternary protein complex formation. MIKC-type MADS-Box genes are involved in many aspects of plant development Smaczniak et al. (2012) “ABC” Model of Flower Development ! Arabidopsis thaliana Antirrhinum majus 'A' genes control the sepals 'A' and 'B' genes in combination control the petals 'B' and 'C' genes in combination control the stamens 'C' genes control the carpels ! Homeotic Mutants – used to study HOX genes in Drosophila WT HOX Genes antennapedia Carroll et al. (2005) Floral homeotic mutants How the ABCE Model was determined Krizek & Fletcher Nature Reviews Genetics (2005). 6(9), 688–698. “Sliding Boundary” model is one modification to the ‘ABC’ Model Kramer et al. (2003) Explaining diversity with the ABC model Transference of genetic identity from one structure to another B! A! C! SE PE ST CA B! A! C! PE PE ST CA Thalictrum thalictroides is a good model system for studying Floral Evo-Devo • Pivotal phylogenetic position - Ranunculales • High success with gene silencing techniques (VIGS) • Many horticultural mutants available • Numerous duplications of Floral Organ Identity Genes Soltis et al. Am J Bot 2009 T. thalictroides Horticultural Mutants Wildtype ‘Shoaff’s Double’ ‘Betty Blake’ ‘Green Dragon’ ‘Double White’ C-class and D-class Function in Thalictrum Floral Organ Identity Genes control development along the floral axis Sepal!–!1st!Whorl! Petal!–!2nd!Whorl! Stamen!–!3rd!Whorl! Carpel!–!4th!Whorl! ABC(D)E Model B! D! A! C! E! Ferrario et al. Curr Opin Plant Biol 2004 C-class function: conserved carpel and stamen identity across the angiosperms C-lineage D-lineage Arabidopsis C-class gene: AGAMOUS (AG) Kramer et al. 2004 AGAMOUS Subfamily Kramer et al. Genetics 2004 Bowman et al. Plant Cell 1989 Riechmann & Meyerowitz. Molec Biol Cell 1997 D-class function: ovule identity is mostly redundant among C- and D-lineage genes C-lineage D-lineage Petunia D-class genes: FBP7 & FBP11 AGAMOUS Subfamily Kramer et al. Genetics 2004 Angenent et al. Plant Cell 1995 Thalictrum has two AG homologs with different expression patterns. C-class Genes ThtAGAMOUS1 (ThtAG1) ThtAGAMOUS2 (ThtAG2) No D-class Genes ThdAG1 carpels stamens ThdAG2 ovule carpel Kramer et al. 2004 Di Stilio et al. 2005 Thalictrum has two AG homologs with different expression patterns. Hypothesis After the duplication event that led to ThAG1 and ThAG2: • ThAG1 kept the C-function role in stamen and carpel identity. • ThAG2 sub-functionalized to become an ovule identity gene. Kramer et al. 2004 Forward Genetics – ‘Double White’ has a defect in ThAG1 T. thalictroides T. thalictroides WT Double White Reverse Genetics – Down-regulating ThAG1 creates a ‘double flower’ phenotype Viral Induced Gene Silencing (VIGS) T. thalictroides WT T. thalictroides ‘Double White’ T. thalictroides TRV2ThAG1 Reverse Genetics – Down-regulating ThAG1 creates a ‘double flower’ phenotype T. thalictroides WT Conclusion: ThtAG1 does have the conserved C-function role in stamen and carpel identity. T. thalictroides ‘Double White’ T. thalictroides TRV2ThAG1 Double Flowers – the first recorded floral mutants T. thalictroides T. thalictroides WT Double White Theophrastus 371-287 BC Arabidopsis Arabidopsis WT agamous mutant VIGS of ThtAG2 does not result in a double-flower TRV1 ThtPDS Bleaching RB! LB! 2!x!35S! RdRp! MP! 16K! Rz! NOSt! TRV2 MCS! RB! LB! 2!x!35S! CP! Rz! NOSt! TRV2_ThtAG2_ThtPDS RB! LB! 2!x!35S! CP! ThtAG2' ThtPDS' Rz! NOSt! Untreated TRV2 Empty TRV2_ThtAG2_ThtPDS TRV2_ThtAG1 ThtAG2-silenced ovules have a carpel-like morphology and lack an embryo sac. ii oi ii es oi st-l ii nu oi WT Ovule ThtAG2 VIGS Ovule ThtAG2 VIGS Ovule sg Ovule Structure Carpel Structure oi = outer integument st = style st ii = inner integument sg = stigma es = embryo sac ov = ovule nu = nucellus st-l = style-like ov! WT Carpel ThtAG2-silenced ovules have a carpel-like morphology and lack an embryo sac. ii oi ii es oi st-l ii nu oi WT Ovule ThtAG2 VIGS Ovule ThtAG2 VIGS Ovule sg Conclusion: ThtAG2 has sub-functionalized st and is now an ovule identity gene. ov! WT Carpel Summary Down-regulation of ThtAG1 causes a double-flower phenotype. The horticultural mutant ‘Double White’ has a transposon disrupting ThtAG1. Down-regulation of ThtAG2 causes the loss of the embryo sac and the development of a carpel-like structure in place of the ovule. After the duplication that led to ThtAG1 and ThtAG2 • The C-class gene ThtAG1 kept the conserved C-function role in stamen and carpel development. • The C-class gene ThtAG2 has likely sub-functionalized to control ovule development – a role traditionally assigned to the D-class. .
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