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A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus

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Abstract

In several eudicots, including members of the Asteraceae family, the CYCLOIDEA (CYC) genes, which belong to the TCP class of transcription factors, are key players for floral symmetry. The sunflower inflorescence is heterogamous (radiate capitulum) with sterile monosymmetric ray flowers located in the outermost whorl of the inflorescence and hermaphrodite polysymmetric disk flowers. In inflorescence of Heliantheae tribe, flower primordia development initiates from the marginal ray flowers while disk flowers develop later in an acropetal fashion in organized parastichies along a number found to be one of Fibonacci patterns. Mutants for inflorescence morphology can provide information on the role of CYC-like genes in radiate capitulum evolution. The tubular ray flower (turf) mutant of sunflower shows hermaphrodite ray flowers with a nearly polysymmetric tubular-like corolla. Here, we demonstrate that this mutation is caused by the insertion in the TCP motif of a sunflower CYC-like gene (HaCYC2c) of non-autonomous transposable element (TE), belonging to the CACTA superfamily of transposons. We named this element Transposable element of turf1 (Tetu1). The Tetu1 insertion changes the reading frame of turf-HaCYC2c for the encoded protein and leads to a premature stop codon. Although in Tetu1 a transposase gene is lacking, our results clearly suggest that it is an active TE. The excision of Tetu1 restores the wild type phenotype or generates stable mutants. Co-segregation and sequence analysis in progenies of F2 and self-fertilized plants derived from reversion of turf to wild type clearly identify HaCYC2c as a key regulator of ray flowers symmetry. Also, HaCYC2c loss-of-function promotes the developmental switch from sterile to hermaphrodite flowers, revealing a novel and unexpected role for a CYC-like gene in the repression of female organs.

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References

  • Abbott RJ, James JK, Milne RI, Gillies ACM (2003) Plant introduction, hybridization and gene flow. Philos Trans R Soc B Biol Sci 358:1123–1132

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Anisimova IN, Tumanova LG, Gavrilova VA, Dyagileva AV, Pasha LI, Mitin VA, Timofeyeva GI (2009) Genomic instability in sunflower interspecific hybrids. Russ J Genet 45:934–943

    Article  CAS  Google Scholar 

  • Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL (2002) The pfam protein families database. Nucleic Acids Res 30:276–280

    Article  PubMed  CAS  Google Scholar 

  • Berti F, Fambrini M, Turi M, Bertini D, Pugliesi C (2005) Mutations of corolla symmetry affect carpel and stamen development in Helianthus annuus. Can J Bot 83:1065–1072

    Article  Google Scholar 

  • Broholm SK, Tähtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa P (2008) A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc Natl Acad Sci USA 105:9117–9122

    Article  PubMed  CAS  Google Scholar 

  • Busch A, Zachgo S (2009) Flower symmetry evolution: towards understanding the abominable mystery of angiosperm radiation. BioEssays 31:1181–1190

    Article  PubMed  CAS  Google Scholar 

  • Carlson SE, Howard DG, Donoghue MJ (2011) Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. BMC Evol Biol 11:325. doi:10.1186/1471-2148-11-325

    Article  PubMed  CAS  Google Scholar 

  • Carpenter R, Coen ES (1990) Floral Homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493

    Article  PubMed  CAS  Google Scholar 

  • Chapman MA, Leebens-Mack JH, Burke JM (2008) Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. Mol Biol Evol 25:1260–1273

    Article  PubMed  CAS  Google Scholar 

  • Citerne HL, Möller M, Cronk QCB (2000) Diversity of cycloidea-like genes in Gesneriaceae in relation to floral symmetry. Ann Bot 86:167–176

    Article  CAS  Google Scholar 

  • Citerne HL, Luo D, Pennington RT, Coen E, Cronk QCB (2003) A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae. Plant Physiol 131:1042–1053

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Nugent JM, Luo D, Bradley D, Cubas P, Chadwick M, Copsey L, Carpenter R (1995) Evolution of floral symmetry. Philos Trans R Soc B Biol Sci 350:35–38

    Article  Google Scholar 

  • Costa MMR, Fox S, Hana AI, Baxter C, Coen E (2005) Evolution of regulatory interactions controlling floral asymmetry. Development 132:5093–5101

    Article  PubMed  CAS  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999a) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    Article  PubMed  CAS  Google Scholar 

  • Cubas P, Vincent C, Coen E (1999b) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161

    Article  PubMed  CAS  Google Scholar 

  • Damerval C, Le Guilloux M, Jager M, Charon C (2007) Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in Papaveraceae. Plant Physiol 143:759–772

    Article  PubMed  CAS  Google Scholar 

  • Donoghue MJ, Ree RH, Baum DA (1998) Phylogeny and the evolution of flower symmetry in the Asteridae. Trends Plant Sci 3:311–317

    Article  Google Scholar 

  • Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30:235–238

    Article  PubMed  CAS  Google Scholar 

  • Fambrini M, Bonsignori E, Rapparini F, Cionini G, Michelotti V, Bertini D, Baraldi R, Pugliesi C (2006) stem fasciated, a recessive mutation in sunflower (Helianthus annuus), alters plant morphology and auxin level. Ann Bot 98:715–730

    Article  PubMed  Google Scholar 

  • Fambrini M, Michelotti V, Pugliesi C (2007) The unstable tubular ray flower allele of sunflower: inheritance of reversion to wild type. Plant Breed 126:548–550

    Article  Google Scholar 

  • Fambrini M, Mariotti L, Parlanti S, Picciarelli P, Salvini M, Ceccarelli N, Pugliesi C (2011) The extreme dwarf phenotype of the GA-sensitive mutant of sunflower, dwarf2, is generated by a deletion in the ent-kaurenoic acid oxidase1 (HaKAO1) gene sequence. Plant Mol Biol 75:431–450

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Pritham EJ (2007) DNA-transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368

    Article  PubMed  CAS  Google Scholar 

  • Fick GN (1976) Genetics of floral color and morphology in sunflowers. J Hered 67:227–230

    Google Scholar 

  • Graham ET, Trentham R (1998) Staining paraffin extracted, alcohol rinsed and air dried plant tissue with aqueous mixture of three dyes. Biotech Histochem 73:178–185

    Article  PubMed  CAS  Google Scholar 

  • Harris EM (1995) Inflorescence and floral ontogeny in Asteraceae: a synthesis of historical and current concepts. Bot Rev 61:93–278

    Article  Google Scholar 

  • Howarth DG, Donoghue MJ (2006) Phylogenetic analisys of the “ECE” (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci USA 103:9101–9106

    Article  PubMed  CAS  Google Scholar 

  • Kane NC, Gill N, King MG, Bowers JE, Berges H, Gouzy J, Bachlava E, Langlade NB, Lai Z, Stewart M, Burke JM, Vincourt P, Knapp SJ, Rieseberg LH (2011) Progress towards a reference genome for sunflower. Botany 89:429–437

    Article  Google Scholar 

  • Kim M, Cui M-L, Cubas P, Gillies A, Lee K, Chapman MA, Abbott RJ, Coen E (2008) Regulatory genes control key morphological and ecological trait transferred between species. Science 322:1116–1119

    Article  PubMed  CAS  Google Scholar 

  • Knowles PF (1978) Morphology and anatomy. In: Carter JF (ed) Sunflower science and technology. ASA, CSSA, SSSA, Inc. Publishers, Madison, pp 55–87

  • Krizek EM, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698

    Article  PubMed  CAS  Google Scholar 

  • Lewin B (1997) Transposons. In: Lewin B (ed) Genes VI. Oxford University Press, New York, pp 563–595

    Google Scholar 

  • Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799

    Article  PubMed  CAS  Google Scholar 

  • Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen ES (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99:367–376

    Article  PubMed  CAS  Google Scholar 

  • Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39

    Article  PubMed  Google Scholar 

  • Muszynski MG, Gierl A, Peterson PA (1993) Genetic and molecular analysis of a three-component transposable-element system in maize. Mol Gen Genet 237:105–112

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  PubMed  CAS  Google Scholar 

  • Preston JC, Hileman LC (2009) Developmental genetics of floral symmetry evolution. Trends Plant Sci 14:147–154

    Article  PubMed  CAS  Google Scholar 

  • Roccaro M, Li Y, Masiero S, Saedler H, Sommer H (2005) ROSINA (RSI), a novel protein with DNA-binding capacity, acts during floral organ development in Antirrhinum majus. Plant J 43:238–250

    Article  PubMed  CAS  Google Scholar 

  • Roccaro M, Li Y, Sommer H (2007) ROSINA (RSI) is a part of a CACTA transposable element, TamRSI, and links flower development to transposon activity. Mol Genet Genomics 278:243–254

    Article  PubMed  CAS  Google Scholar 

  • Siebert PD, Chenchik A, Kellog DE, Lukyanov KA, Lukyanov SA (1995) An improved method for walking in uncloned genomic DNA. Nucleic Acids Res 23:1087–1088

    Article  PubMed  CAS  Google Scholar 

  • Tähtiharju S, Rijpkema AS, Vetterli A, Albert VA, Teeri TH, Elomaa P (2012) Evolution and diversification of the CYC/TB1 gene family in Asteraceae—a comparative study in gerbera (Mutisieae) and sunflower (Heliantheae). Mol Biol Evol 29:1155–1166

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Guyot R, Yahiaoui N, Keller B (2003) CACTA transposons in Triticeae. A diverse family of high-copy repetitive elements. Plant Physiol 132:52–63

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Claudio Pugliesi.

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Fambrini, M., Salvini, M. & Pugliesi, C. A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus . Genetica 139, 1521–1529 (2011). https://doi.org/10.1007/s10709-012-9652-y

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