Skip to main content
Log in

CaAP2 transcription factor is a candidate gene for a flowering repressor and a candidate for controlling natural variation of flowering time in Capsicum annuum

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The APETALA2 transcription factor homolog CaAP2 is a candidate gene for a flowering repressor in pepper, as revealed by induced-mutation phenotype, and a candidate underlying a major QTL controlling natural variation in flowering time.

Abstract

To decipher the genetic control of transition to flowering in pepper (Capsicum spp.) and determine the extent of gene function conservation compared to model species, we isolated and characterized several ethyl methanesulfonate (EMS)-induced mutants that vary in their flowering time compared to the wild type. In the present study, we report on the isolation of an early-flowering mutant that flowers after four leaves on the primary stem compared to nine leaves in the wild-type ‘Maor’. By genetic mapping and sequencing of putative candidate genes linked to the mutant phenotype, we identified a member of the APETALA2 (AP2) transcription factor family, CaAP2, which was disrupted in the early-flowering mutant. CaAP2 is a likely ortholog of AP2 that functions as a repressor of flowering in Arabidopsis. To test whether CaAP2 has an effect on controlling natural variation in the transition to flowering in pepper, we performed QTL mapping for flowering time in a cross between early and late-flowering C. annuum accessions. We identified a major QTL in a region of chromosome 2 in which CaAP2 was the most significant marker, explaining 52 % of the phenotypic variation of the trait. Sequence comparison of the CaAP2 open reading frames in the two parents used for QTL mapping did not reveal significant variation. In contrast, significant differences in expression level of CaAP2 were detected between near-isogenic lines that differ for the flowering time QTL, supporting the putative function of CaAP2 as a major repressor of flowering in pepper.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alvarez J, Guli CL, Yu XH, Smyth DR (1992) TERMINAL FLOWER: a gene affecting inflorescence development in Arabidopsis thaliana. Plant J 2:103–116

    Article  Google Scholar 

  • Ashrafi H, Hill T, Stoffel K, Kozik A, Yao JQ, Chin-Wo SR, Van Deynze A (2012) De novo assembly of the pepper transcriptome (Capsicum annuum): a benchmark for in silico discovery of SNPs, SSRs and candidate genes. BMC Genomics 13:571

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aukerman MJ, Sakai S (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, Klein P, Giovannoni J (2010) A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J 64:936–947

    Article  CAS  PubMed  Google Scholar 

  • Cohen O, Borovsky Y, David-Schwartz R, Paran I (2012) CaJOINTLESS is a MADS-box gene involved in suppression of vegetative growth in all shoot meristems in pepper. J Exp Bot 63:4947–4957

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen O, Borovsky Y, David-Schwartz R, Paran I (2014) Capsicum annuum S (CaS) promotes reproductive transition and is required for flower formation in pepper (Capsicum annuum). New Phytol 202:1014–1023

    Article  CAS  PubMed  Google Scholar 

  • Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  CAS  PubMed  Google Scholar 

  • Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES (2011) FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA 108:6680–6685

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Elitzur T, Nahum H, Borovsky Y, Pekker I, Eshed Y, Paran I (2009) Co-ordinated regulation of flowering time, plant architecture and growth by FASCICULATE: the pepper orthologue of SELF PRUNING. J Exp Bot 60:869–880

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Golovnina KA, Kondratenko EY, Blinov AG, Goncharov NP (2010) Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Biol 10:168

    Article  PubMed Central  PubMed  Google Scholar 

  • Gul Khan MR, Ai XY, Zhang JZ (2014) Genetic regulation of flowering time in annual and perennial plants. Wiley Interdiscip Rev RNA 5:347–359

    Article  Google Scholar 

  • Hung H-Y, Shannon LM, Tian F et al (2012) ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA 109:E1913–E1921

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jeifetz D, David-Schwartz R, Borovsky Y, Paran I (2011) CaBLIND regulates axillary meristem initiation and transition to flowering in pepper. Planta 234:1227–1236

    Article  CAS  PubMed  Google Scholar 

  • Jung JH, Lee S, Yun J, Lee M, Park CM (2014) The miR172 target TOE3 represses AGAMOUS expression during Arabidopsis floral patterning. Plant Sci 215–216:29–38

    Article  PubMed  Google Scholar 

  • Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, deMaagd RA (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923–941

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim S, Park M, Yeom S-I et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Li D, Liu C, Shen L et al (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15:110–120

    Article  CAS  PubMed  Google Scholar 

  • Lu L, Yan W, Xue W, Shao D, Xing Y (2012) Evolution and association analysis of Ghd7 in rice. PLoS One 7:e34021

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • MacAlister CA, Park SJ, Jiang K, Marcel F, Bendahmane A, Izkovich Y, Eshed Y, Lippman ZB (2012) Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene. Nat Genet 44:1393–1398

    Article  CAS  PubMed  Google Scholar 

  • Maes T, Van de Steene N, Zethof J, Karimi M, D’Hauw M, Mares G, Van Montagu M, Gerats T (2001) Petunia Ap2-like genes and their role in flower and seed development. Plant Cell 13:229–244

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin A, Adam H, Diaz-Mendoza M, Zurczak M, Gonzalez-Schain ND, Suarez-Lopez P (2009) Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136:2873–2881

    Article  CAS  PubMed  Google Scholar 

  • Mathieu J, Yant LJ, Murdter F, Kuttner F, Schmid M (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7:e1000148. doi:10.1371/journal.pbio.1000148

    Article  PubMed Central  PubMed  Google Scholar 

  • Mendez-Vigo B, Martınez-Zapater JM, Alonso-Blanco C (2013) The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLoS Genet 9:e1003289. doi:10.1371/journal.pgen.1003289

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA 100:10102–10107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nelson CJ (1997) QGENE: software for marker-based genomic analysis and breeding. Mol Breed 3:229–235

    Article  Google Scholar 

  • Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci USA 102:3123–3128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Olsen KM, Wendel JF (2013) A bountiful harvest: genomic insights into crop domestication phenotypes. Ann Rev Plant Biol 64:47–70

    Article  CAS  Google Scholar 

  • Paran I, Borovsky Y, Nahon S, Cohen O (2007) The use of induced mutations to study shoot architecture in Capsicum. Isr J Plant Sci 55:125–131

    Article  Google Scholar 

  • Park SJ, Jiang K, Schatz MC, Lippman ZB (2012) Rate of meristem maturation determines inflorescence architecture in tomato. Proc Natl Acad Sci USA 109:639–644

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ripoll JJ, Roeder AHK, Ditta GS, Yanofsky MF (2011) A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development 138:5167–5176

    Article  CAS  PubMed  Google Scholar 

  • Rosas U, Mei Y, Xie Q et al (2014) Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS. Nat Commun. doi:10.1038/ncomms4651

    PubMed Central  PubMed  Google Scholar 

  • Salomé PA, Bomblies K, Laitinen RAE, Yant L, Mott R, Weigel D (2011) Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics 188:421–433

    Article  PubMed Central  PubMed  Google Scholar 

  • Salvi S, Sponza G, Morgante M et al (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104:11376–11381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Samach A, Lotan H (2007) The transition to flowering in tomato. Plant Biotechnol 24:71–82

    Article  Google Scholar 

  • Shrestha R, Ariza JG, Brambilla V, Fornara F (2014) Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals. Ann Bot. doi:10.1093/aob/mcu032

    PubMed  Google Scholar 

  • Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037

    Article  CAS  PubMed  Google Scholar 

  • Wu F, Eannetta NT, Xu Y, Durrett R, Mazourek M, Jahn MM, Tanksley SD (2009) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118:1279–1293

    Article  CAS  PubMed  Google Scholar 

  • Yant L, Mathieu J, Schmid M (2009) Just say no: floral repressors help Arabidopsis bide the time. Curr Opin Plant Biol 12:580–586

    Article  CAS  PubMed  Google Scholar 

  • Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22:2156–2170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zuellig MP, Kenney AM, Sweigart AL (2014) Evolutionary genetics of plant adaptation: insights from new model systems. Curr Opinion Plant Biol 18:44–50

    Article  Google Scholar 

Download references

Acknowledgments

We thank Aharon Bellalou for technical support, Arnon Brand for graphic design and Hanita Zemach for assistance with microscopic analyses. We thank Dr. Zach Lippman (Cold Spring Harbor Laboratory) for contributing the digital expression data of CaAP2 in ‘Maor’. This research was supported by The Israel Science Foundation (Grant No. 1349/10).

Conflict of interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ilan Paran.

Additional information

Communicated by J. Dubcovsky.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 111 kb)

Supplementary material 2 (XLSX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Borovsky, Y., Sharma, V.K., Verbakel, H. et al. CaAP2 transcription factor is a candidate gene for a flowering repressor and a candidate for controlling natural variation of flowering time in Capsicum annuum . Theor Appl Genet 128, 1073–1082 (2015). https://doi.org/10.1007/s00122-015-2491-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-015-2491-3

Keywords

Navigation