Abstract
Rose is the ornamental species with the highest financial impact. Floral traits such as the number of petals and the date of flowering are major characteristics of ornamental plants. Our objective is to study the genetic determinism of floral traits: date of flowering and number of petals, which are a major issue for rose breeders. The study was conducted on two interspecific populations interconnected by the male parent: H190 x hybrid of Rosa wichurana (referred to as HW) and “The Fairy” x hybrid of Rosa wichurana (referred to as FW). The number of petals and the date of flowering were scored over 2 and 8 years, respectively. A new HW genetic map covering 468 cM and the already available genetic map of the FW population (Kawamura et al. TAG Theor Appl Genet 122:661–675, 2011) were used for the genetic determinism studies. In each population, half of the hybrids exhibited single flowers (less than 10 petals), whereas the other half revealed double flowers. The number of petals is controlled by the NP gene located on LG3. Additionally, we detected two new major quantitative trait loci (QTLs) on LG2 and LG5, close to RoAP1b and RoRAG, respectively, two genes involved in the control of floral identity. For the date of flowering, three QTLs with a major effect and high stability between years were found on linkage groups 3, 4, and 6, indicating a high stability of QTLs to the changing environment. Candidate genes underlying these QTLs were investigated and key genes were identified. These major QTLs were linked to candidate genes, i.e., the identified QTL on LG4 was linked to RoFT, the one on LG3 to genes involved in gibberellin pathways, and the one on LG6 to RoFD. These QTLs, which are very stable over time, are good candidates to develop markers applicable in marker-assisted selection (MAS).
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References
Abe M et al (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056
Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092
Ahn JH et al (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614
Brachi B et al (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6:e1000940
Buckler ES et al (2009) The genetic architecture of maize flowering time. Science (Washington) 325:714–718
Campoy JA, Ruiz D, Egea J, Rees DJG, Celton JM, Martinez-Gomez P (2011) Inheritance of flowering time in apricot (Prunus armeniaca L.) and analysis of linked quantitative trait loci (QTLs) using simple sequence repeat (SSR) markers. Plant Mol Biol Report 29:404–410
Campoy JA, Ruiz D, Allderman L, Cook N, Egea J (2012) The fulfilment of chilling requirements and the adaptation of apricot (Prunus armeniaca L.) in warm winter climates: an approach in Murcia (Spain) and the Western Cape (South Africa). Eur J Agron 37:43–55
Celton JM, Martinez S, Jammes MJ, Bechti A, Salvi S, Legave JM, Costes E (2011) Deciphering the genetic determinism of bud phenology in apple progenies: a new insight into chilling and heat requirement effects on flowering dates and positional candidate genes. New Phytol 192:378–392
Chmelnitsky I, Colauzzi M, Algom R, Zieslin N (2001) Effects of temperature on phyllody expression and cytokinin content in floral organs of rose flowers. Plant Growth Regul 35:207–214
Colasanti J, Muszynski MG (eds) (2008) The maize floral transition vol 1. Handbook of maize: its biology. Springer Science, New York
Crespel L, Chirollet M, Durel CE, Zhang D, Meynet J, Gudin S (2002) Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theor Appl Genet 105:1207–1214
Debener T, Linde M (2009) Exploring complex ornamental genomes: the rose as a model plant. Crit Rev Plant Sci 28:267–280
Debener T, Mattiesch L (1999) Construction of a genetic linkage map for roses using RAPD and AFLP markers. Theor Appl Genet 99:891–899
Dirlewanger E et al (2012) Comparison of the genetic determinism of two key phenological traits, flowering and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity 109:280–292
Dubois A et al (2010) Tinkering with the C-function: a molecular frame for the selection of double flowers in cultivated roses. PLoS One 5:1–12
Dugo ML, Satovic Z, Millan T, Cubero JI, Rubiales D, Cabrera A, Torres AM (2005) Genetic mapping of QTLs controlling horticultural traits in diploid roses TAG. Theor Appl Genet 111:511–520
Fan SH, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR, Holland D, Abbott AG (2010) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol 185:917–930
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550–550.e552
Foster T, Johnston R, Seleznyova A (2003) A morphological and quantitative characterization of early floral development in apple (Malus x domestica Borkh.). Ann Bot 92:199–206
Foucher F, Chevalier M, Corre C, Soufflet-Freslon V, Legeai F, Hibrand-Saint Oyant L (2008) New resources for studying the rose flowering process. Genome 51:827–837
Garrod JF, Harris GP (1974) Studies on the glasshouse carnation: effects of temperature and growth substances on petal number. Ann Bot 38:1025–1031
Hanano S, Goto K (2011) Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell 23:3172–3184
Hibrand-Saint Oyant L, Crespel L, Rajapakse S, Zhang L, Foucher F (2008) Genetic linkage maps of rose constructed with new microsatellite markers and locating QTL controlling flowering traits. Tree Genet Genomes 4:11–23
Iwata H et al (2012) The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J 69:116–125
Jung C, Muller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14:563–573
Kawamura K, Hibrand-Saint Oyant L, Crespel L, Thouroude T, Lalanne D, Foucher F (2011) Quantitative trait loci for flowering time and inflorescence architecture in rose. TAG Theor Appl Genet 122:661–675
Koning-Boucoiran CFS et al (2012) The mode of inheritance in tetraploid cut roses. TAG Theor Appl Genet 125:591–607
Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66
Kotoda N et al (2010) Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus * domestica Borkh.). Plant Cell Physiol 51:561–575
Linde M, Hattendorf A, Kaufmann H, Debener T (2006) Powdery mildew resistance in roses: QTL mapping in different environments using selective genotyping. TAG Theor Appl Genet 113:1081–1092
Meng J, Li D, Yi T, Yang J, Zhao X (2009) Development and characterization of microsatellite loci for Rosa odorata var. gigantea Rehder & E. H. Wilson (Rosaceae). Conserv Genet 10:1973–1976
Meynet J, Barrade R, Duclos A, Siadous R (1994) Dihaploid plants of roses (Rosa * hybrida, cv ‘Sonia’) obtained by parthenogenesis induced using irradiated pollen and in vitro culture of immature seeds. Agronomie 14:169–175
Napp-Zinn K (1985) Arabidopsis thaliana. In: Halevy HA (ed) Handbook of flowering, vol 1. CRC Press, Boca Raton, pp 492–503
Nishikawa F, Endo T, Shimada T, Fujii H, Shimizu T, Omura M (2009) Differences in seasonal expression of flowering genes between deciduous trifoliate orange and evergreen Satsuma mandarin. Tree Physiol 29:921–926
Nishikawa F et al (2010) Transcriptional changes in CiFT-introduced transgenic trifoliate orange (Poncirus trifoliata L. Raf.). Tree Physiol 30:431–439
Oda A et al (2012) CsFTL3, a chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums. J Exp Bot 63:1461–1477
Quilot B, Wu BH, Kervella J, Genard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet 109:884–897
Randoux M et al (2012) Gibberellins regulate the transcription of the continuous flowering regulator, RoKSN, a rose TFL1 homologue. J Exp Bot 63:6543–6554
Remay A, Lalanne D, Thouroude T, le Couviour F, Hibrand-Saint Oyant L, Foucher F (2009) A survey of flowering genes reveals the role of gibberellins in floral control in rose. TAG Theor Appl Genet 119:767–781
Roberts AV, Blake PS, Lewis R, Taylor JM, Dunstan DI (1999) The effect of gibberellins on flowering in roses. J Plant Growth Regul 18:113–119
Romeu JF, Monforte AJ, Sanchez G, Granell A, Garcia-Brunton J, Badenes ML, Rios G (2014) Quantitative trait loci affecting reproductive phenology in peach. BMC Plant Biol 14:52
Samach A, Smith HM (2013) Constraints to obtaining consistent annual yields in perennials. II: Environment and fruit load affect induction of flowering. Plant Sci 207:168–176
Sanchez-Perez R, Howad W, Dicenta F, Arus P, Martinez-Gomez P (2007) Mapping major genes and quantitative trait loci controlling agronomic traits in almond. Plant Breed 126:310–318
Shen L, Chen Y, Su X, Zhang S, Pan H, Huang M (2012) Two FT orthologs from Populus simonii Carriere induce early flowering in Arabidopsis and poplar trees. Plant Cell Tiss Org Cult 108:371–379
Socquet-Juglard D, Christen D, Devènes G, Gessler C, Duffy B, Patocchi A (2013) Mapping architectural, phenological, and fruit quality QTLs in apricot. Plant Mol Biol Report 31:387–397
Spiller M et al (2011) Towards a unified genetic map for diploid roses TAG. Theor Appl Genet 122:489–500
Sun Y, Fan Z, Li X, Li J, Yin H (2013) The APETALA1 and FRUITFUL homologs in Camellia japonica and their roles in double flower domestication. Mol Breed 33:821–834
Tanaka Y, Oshima Y, Yamamura T, Sugiyama M, Mitsuda N, Ohtsubo N, Ohme-Takagi M, Terakawa T (2013) Multi-petal cyclamen flowers produced by AGAMOUS chimeric repressor expression. Sci Rep 3:srep02641
Tanaka N et al (2014) Overexpression of Arabidopsis FT gene in apple leads to perpetual flowering. Plant Biotechnol 31:11–20
Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594
Van Ooijen JW (2004) MAPQTL® 5.0 software for the mapping of quantitative trait loci in experimental populations. Plant Research international, Wageningen
Van Ooijen JW (2006) JoinMap® 4.0 software for the calculation of genetic linkage maps in experimental populations. Plant Research international, Wageningen
Verde I, Quarta R, Cedrola C, Dettori MT (2002) QTL analysis of agronomic traits in a BC 1 peach population. Acta Horticult 592:291–297
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wigge PA, Kim M, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science (Washington) 309:1056–1059
Xing W, Wang Z, Wang X, Bao M, Ning G (2014) Over-expression of an FT homolog from Prunus mume reduces juvenile phase and induces early flowering in rugosa rose. Sci Hortic 172:68–72
Zhang F, Chen S, Jiang J, Guan Z, Fang W, Chen F (2013) Genetic mapping of quantitative trait loci underlying flowering time in chrysanthemum. PLoS One 8:e83023
Zieslin N (1992) Regulation of flower formation in rose plants: a reappraisal. Sci Hortic 49:305–310
Acknowledgments
We thank Claudine Foubert and the entire team of the experimental unit (INEM) of IRHS for their technical assistance in plant management. Christophe Brouard (UE Horti), Gilles Michel, and Sébastien Pineau are also gratefully acknowledged for their help in collecting data in the field. We thank the PTM ANAN (Muriel Bahut) of the SFR Quasav and the Gentyane platforms (especially Charles Poncet) for the SSR analyses. This research was supported by the CASDAR (compte d’affectation spéciale pour le développement agricole et rural No 1028). We thank Gail Wagman for her comments and the English correction of the manuscript.
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The authors declare that they have no conflict of interest.
Data archiving statement
Genetic map and QTL data are currently being submitted to GDR, Genome Database for Rosaceae (accession number=tfGDR1012).
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Communicated by A. M. Dandekar
This article is part of the Topical Collection on Germplasm Diversity
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Fig. 1S
Kendall correlations between the two years of the notations of the number of petals within the both populations HW (A, C) and FW (B, D). A scatterplot and correlation test were realized for both populations either the entire population (A, B) or the subgroup of progeny with double flower (C, D). (PPTX 56 kb)
Fig. S2
Distribution of the ADT (sum of the average daily temperatures) in the HW (A) and FW (B) populations over 7 years (2006 to 2012). Dates for the male parent Rw (♂) and the female parent (♀) are indicated. Only two dates (2012–2013) for the parent H190 are indicated. (PPTX 80 kb)
Fig. S3
Comparison of the date of flowering in the subgroups of R (recurrent blooming) and NR (non-recurrent blooming) of the two populations HW (A) and FW (B). The date of flowering was expressed as the mean of the ADT. (PPTX 43 kb)
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Roman, H., Rapicault, M., Miclot, A.S. et al. Genetic analysis of the flowering date and number of petals in rose. Tree Genetics & Genomes 11, 85 (2015). https://doi.org/10.1007/s11295-015-0906-6
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DOI: https://doi.org/10.1007/s11295-015-0906-6