Abstract
Plant shape, and thereby plant architecture, is a major component of the visual quality of ornamental plants. We have been developing a new method for analyzing the entire plant architecture by 3D digitalization that allows an almost exhaustive description of rose bush architecture and generates a large number of variables, many of them inaccessible manually. We carried out a QTL analysis using this original phenotyping method. In order to evaluate a broader allelic variability as well as the effect of the genetic background on QTL detection, we used two connected, segregating, recurrent blooming populations. The number of QTLs per variable varied from three for the number of determined axes (NbDetA) to seven for the branching angle of order 2 long axes (AngLA2), the two populations taken together. Five new QTLs, located on the linkage groups (LGs) 2, 6, and 7, were detected for the branching angle of axes, and the QTL located on LG7 co-localized with RhBRC1, a branching repressor. Branching and stem elongation QTLs also co-located with RhBRC1, suggesting its pleiotropic nature. Year-specific QTLs were also revealed, that explained the genotype × year interactions observed for the number of order 3 short axes (NbSA3) and AngLA2 from a genetic point of view. We also evidenced an effect of the genetic background on QTL detection. This new knowledge should help to better reason the genetic improvement programs for rose bush architecture and, therefore, rose bush shape.
Similar content being viewed by others
References
Aguilar-Martinez JA, Poza-Carrion C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472. https://doi.org/10.1105/tpc.106.048934
Allard A, Bink MCAM, Martinez S, Kelner JJ, Legave JM, di Guardo M, Di Pierro EA, Laurens F, van de Weg EW, Costes E (2016) Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population. J Exp Bot 67:2875–2888. https://doi.org/10.1093/jxb/erw130
Alméras T, Costes E, Salles JC (2004) Identification of biomechanical factors involved in stem shape variability between apricot tree varieties. Ann Bot 93:455–468. https://doi.org/10.1093/aob/mch054
Banerjee S, Yandell BS, Yi N (2008) Bayesian quantitative trait loci mapping for multiple traits. Genetics 179:2275–2289. https://doi.org/10.1534/genetics.108.088427
Barbier F, Péron T, Lecerf M, Perez-Garcia MD, Barrière Q, Rolík J, Boutet-Mercy S, Citerne S, Lemoine R, Porcheron B, Roman H, Leduc N, Le Gourriérec J, Bertheloot J, Sakr S (2015) Sucrose modulates the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida. J Exp Bot 66:2569–2582. https://doi.org/10.1093/jxb/erv047
Beavis WD, Grant D, Albertsen M, Fincher R (1991) Quantitative trait loci for plant height in four maize populations and their associations with qualitative genetic loci. Theor Appl Genet 83:141–145
Ben Sadok I, Celton JM, Essalouh L, El Aabidine AZ, Garcia G, Martinez S, Grati-Kamoun N, Rebai A, Costes E, Khadari B (2013) QTL mapping of flowering and fruiting traits in olive. PLoS One 8:e62831. https://doi.org/10.1371/journal.pone.0062831
Billotte N, Jourjon MF, Marseillac N, Berger A, Flori A, Asmady H, Adon B, Singh R, Nouy B, Potier F, Cheah SC, Rohde W, Ritter E, Courtois B, Charrier A, Mangin B (2010) QTL detection by multi-parent linkage mapping in oil palm (Elaeis guineensis Jacq.) Theor Appl Genet 120:1673–1687. https://doi.org/10.1007/s00122-010-1284-y
Bink MCAM, Jansen J, Madduri M, Voorrips RE, Durel CE, Kouassi AB, Laurens F, Mathis F, Gessler C, Gobbin D, Rezzonico F, Patocchi A, Kellerhals M,·Boudichevskaia A, Dunemann F, Peil A, Nowicka A, Lata B, Stankiewicz-Kosy M, Jeziorek K, Pitera E, Soska A, Tomala K, Evans KM, Fernández-Fernández F, Guerra W, Korbin M, Keller S, Lewandowski M, Plocharski W, Rutkowski K, Zurawicz E, Costa F, Sansavini S, Tartarini S, Komjanc M, Mott D, Antofie A, Lateur M, Rondia A, Gianfranceschi L, van de Weg WE (2014). Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet 127, 1073–1090. doi:https://doi.org/10.1007/s00122-014-2281-3
Blanc G, Charcosset A, Mangin B, Gallais A, Moreau L (2006) Connected populations for detecting quantitative trait loci and testing for epistasis: an application in maize. Theor Appl Genet 113:206–224. https://doi.org/10.1007/s00122-006-0287-1
Boumaza R, Demotes-Mainard S, Huche-Thelier L, Guerin V (2009) Visual characterization of the esthetic quality of the rosebush. J Sens Stud 24:774–796. https://doi.org/10.1111/j.1745-459X.2009.00238.x
Bredmose NB (1998) Growth flowering and postharvest performance of single stemmed rose (Rosa hybrida L.) in response to light quantum integral and plant population density. J Amer Soc Hort Sci 123:569–576
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. https://doi.org/10.1111/j.1469-8137.2011.03823.x
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
Crespel L, Sigogne M, Donès N, Relion D, Morel P (2013) Identification of relevant morphological, topological and geometrical variables to characterize the architecture of rose bushes in relation to plant shape. Euphytica 191:129–140. https://doi.org/10.1007/s10681-013-0902-6
Crespel L, Le Bras C, Relion D, Morel P (2014) Genotype × year interaction and broad-sense heritability of architectural characteristics in rose bush. Plant Breed 133:412–418. https://doi.org/10.1111/pbr.12157
Dai B, Guo H, Huang C, Ahmed MM, Lin Z (2017) Identification and characterization of segregation distortion loci on cotton chromosome 18. Front Plant Sci 7:2037. https://doi.org/10.3389/fpls.2016.02037
De Vienne D, Causse M (1998) La cartographie et la caractérisation des locus contrôlant la variation des caractères quantitatifs. In de Vienne (ed) Les marqueurs moléculaires en génétique et biotechnologies végétales, 2nd edn. INRA, pp 89–118
Debener T, Linde M (2009) Exploring complex ornamental genomes: the rose as a model plant. Crit Rev Plant Sci 28:267–280. https://doi.org/10.1080/07352680903035481
Debener T, Bretzke M, Spiller M, Linde M, Kaufmann H, Berger RG, Krings U (2010) Genetic and molecular analyses of key loci involved in self-incompatibility and floral scent in roses. Acta Hortic 870:183–190
Demotes-Mainard S, Huché-Thélier L, Morel P, Boumaza R, Guérin V, Sakr S (2013) Temporary water restriction or light intensity limitation promotes branching in rose bush. Sci Hortic 150:432–440. https://doi.org/10.1016/j.scienta.2012.12.005
Demotes-Mainard S, Péron T, Corot A, Bertheloot J, Le Gourrierec J, Pelleschi-Travier S, Crespel L, Morel P, Huché-Thélier L, Boumaza R, Vian A, Guérin V, Leduc N, Sakr S (2016) Plant responses to red and far-red lights, applications in horticulture. Environ Exp Bot 121:4–21. https://doi.org/10.1016/j.envexpbot.2015.05.010
Djennane S, Hibrand-Saint Oyant L, Kawamura K, Lalanne D, Laffaire M, Thouroude T, Chalain S, Sakr S, Boumaza R, Foucher F, Leduc N (2013) Impacts of light and temperature on shoot branching gradient and expression of strigolactone synthesis and signalling genes in rose. Plant Cell Environ 37:742–757. https://doi.org/10.1111/pce.12191
Donès N, Adam B, Sinoquet H (2006) PiafDigit software. http://www1.clermont.inra.fr/piaf/fr/telechargement/telecharger.php. Accessed 25 Apr 2017
Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ (2010) Phytochrome regulation of branching in Arabidopsis. Plant Physiol 152:1914–1927. https://doi.org/10.1104/pp.109.148833
Girault T, Bergougnoux V, Combes D, Viemont JD, Leduc N (2008) Light controls shoot meristem organogenic activity and leaf primordia growth during bud burst in Rosa sp. Plant Cell Environ 31:1534–1544. https://doi.org/10.1111/j.1365-3040.2008.01856.x
Gitonga VW, Koning-Boucoiran CFS, Verlinden K, Dolstra O, Visser RGF, Maliepaard C, Krens FA (2014) Genetic variation, heritability and genotype by environment interaction of morphological traits in a tetraploid rose population. BMC Genet 15:146. https://doi.org/10.1186/s12863-014-0146-z
Godin C, Caraglio Y (1998) A multiscale model of plant topological structures. J Theor Biol 191:1–46
Godin C, Costes E, Sinoquet H (1999) A method for describing plant architecture which integrates topology and geometry. Ann Bot 84:343–357. https://doi.org/10.1006/anbo.1999.0923
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194. https://doi.org/10.1038/nature07271
Gudin S (2000) Rose: genetics and breeding. Plant Breed Rev 17:159–189
Henry C, Rabot A, Laloi M, Mortreau E, Sigogne M, Leduc N, Lemoine R, Sakr S, Vian A, Pelleschi-Travier S (2011) Regulation of RhSUC2, a sucrose transporter, is correlated with the light control of bud burst in Rosa sp. Plant Cell Environ 34:1776–1789. https://doi.org/10.1111/j.1365-3040.2011.02374.x
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. https://doi.org/10.1007/s11295-007-0084-2
Huang YF, Doligez A, Fournier-Level A, Le Cunff L, Bertrand Y, Canaguier A, Morel C, Miralles V, Veran F, Souquet JM, Cheynier V, Terrier N, This P (2012) Dissecting genetic architecture of grape proanthocyanidin composition through quantitative trait locus mapping. BMC Plant Biol 12:30. https://doi.org/10.1186/1471-2229-12-30
Huché-Thélier L, Boumaza R, Demotes-Mainard S, Canet A, Symoneaux R, Douillet O, Guérin V (2011) Nitrogen deficiency increases basal branching and modifies visual quality of the rose bushes. Sci Hortic 130:325–334. https://doi.org/10.1016/j.scienta.2011.07.007
Huché-Thélier L, Crespel L, Le Gourrierec J, Morel P, Sakr S, Leduc N (2016) Light signaling and plant responses to blue and UV radiations—perspectives for applications in horticulture. Environ Exp Bot 121:22–38. https://doi.org/10.1016/j.envexpbot.2015.06.009
Iwata H, Gaston A, Remay A, Thouroude T, Jeauffre J, Kawamura K, Hibrand Saint-Oyant L, Araki T, Denoyes B, Foucher F (2012) The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J 69:116–125. https://doi.org/10.1111/j.1365-313X.2011.04776.x
Kawamura K, Hibrant-Saint Oyant L, Crespel L, Thouroude T, Lalanne D, Foucher F (2011) Quantitative trait loci for flowering time and inflorescence architecture in rose. Theor Appl Genet 122:661–675. https://doi.org/10.1007/s00122-010-1476-5
Kawamura K, Hibrand-Saint Oyant L, Thouroude T, Jeauffre J, Foucher F (2015) Inheritance of garden rose architecture and its association with flowering behaviour. Tree Genet Genomes 11:1–12. https://doi.org/10.1007/s11295-015-0844-3
Klie M, Menz I, Linde M, Debener T (2015) Strigolactone pathway genes and plant architecture: association analysis and QTL detection for horticultural traits in chrysanthemum. Mol Gen Genomics 291:957–969. https://doi.org/10.1007/s00438-015-1155-y
Knapp SJ, Bridges WC (1990) Using molecular markers to estimate quantitative trait locus parameters: power and genetic variances for unreplicated and replicated progeny. Genetics 126:769–777
Leduc N, Roman H, Barbier F, Péron T, Huché-Thélier L, Lothier J, Demotes-Mainard S, Sakr S (2014) Light signaling in bud outgrowth and branching inplants. Plants 3:223–250
Li YL, Niu SZ, Dong YB, Cui DQ, Wang YZ, Liu YY, Wei MG (2007) Identification of trait-improving quantitative trait loci for grain yield components from a dent corn inbred line in an advanced backcross BC2F2 population and comparison with its F2:3 population in popcorn. Theor Appl Genet 115:129–140. https://doi.org/10.1007/s00122-007-0549-6
Li YL, Li XH, Li JZ, Fu JF, Wang YZ, Wei MG (2009) Dent corn genetic background influences QTL detection for grain yield and yield components in high-oil maize. Euphytica 169:273–284. https://doi.org/10.1007/s10681-009-9966-8
Li-Marchetti C, Le Bras C, Relion D, Citerne S, Huché-Thélier L, Sakr S, Morel P, Crespel L (2015) Genotypic differences in architectural and physiological responses to water restriction in rose bush. Front Plant Sci 6:355. https://doi.org/10.3389/fpls.2015.00355
Lorieux M, Goffinet B, Perrier X, Gonzalez de Leon D, Lanaud C (1995a) Maximum likelihood models for mapping genetic markers showing segregation distortion. 1. Backcross population. Theor Appl Genet 90:73–80
Lorieux M, Perrier X, Goffinet B, Lanaud C, Gonzalez de Leon D (1995b) Maximum likelihood models for mapping genetic markers showing segregation distortion. 2. F2 population. Theor Appl Genet 90:81–89
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. https://doi.org/10.1007/s10592-009-9871-7
Meyer JDF, Snook MEK, Houchins E, Rector BG, Widstrom NW, McMullen MD (2007) Quantitative trait loci for maysin synthesis in maize (Zea mays L.) lines selected for high silk maysin content. Theor Appl Genet 115:119–128. https://doi.org/10.1007/s00122-007-0548-7
Moghaddam HH, Leus L, De Riek J, Van Huylenbroeck J, Van Bockstaele E (2012) Construction of a genetic linkage map with SSR, AFLP and morphological markers to locate QTLs controlling pathotype-specific powdery mildew resistance in diploid roses. Euphytica 184:413–427. https://doi.org/10.1007/s10681-011-0616-6
Morel P, Galopin G, Donès N (2009) Using architectural analysis to compare the shape of two hybrid tea rose genotypes. Sci Hortic 120:391–398. https://doi.org/10.1016/j.scienta.2008.11.039
Morel P, Crespel L, Galopin G, Moulia B (2012) Effect of mechanical stimulation on the growth and branching of garden rose. Sci Hortic 135:59–64. https://doi.org/10.1016/j.scienta.2011.12.007
Nanson A (1970) L’héritabilité et le gain d’origine génétique dans quelques types d’expériences. Silvae Genet 19:113–121
Niwa M, Daimon Y, Kurotani K, Higo A, Pruneda-Paz JL, Breton G, Mitsuda N, Kay SA, Ohme-Takagi M, Endo M, Arakia T (2013) BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25:1228–1242. https://doi.org/10.1105/tpc.112.109090
Pauly L, Flajoulot S, Garon J, Julier B, Béguier V, Barre P (2012) Detection of favorable alleles for plant height and crown rust tolerance in three connected populations of perennial ryegrass (Lolium perenne L.) Theor Appl Genet 124:1139–1153. https://doi.org/10.1007/s00122-011-1775-5
Rameau C, Bertheloot J, Leduc N, Andrieu B, Foucher F, Sakr S (2015) Multiple pathways regulate shoot branching. Front Plant Sci 5:741. https://doi.org/10.3389/fpls.2014.00741
Roman H, Rapicault M, Miclot AS, Larenaudie M, Kawamura K, Thouroude T, Chastellier A, Lemarquand A, Dupuis F, Foucher F, Loustau S, Hibrand-Saint Oyant L (2015) Genetic analysis of the flowering date and number of petals in rose. Tree Genet Genomes 11:85. https://doi.org/10.1007/s11295-015-0906-6
Segura V, Cilas C, Laurens F, Costes E (2006) Phenotyping progenies for complex architectural traits: a strategy for 1-year-old apple trees (Malus x domestica Borkh.) Tree Genet Genomes 2:140–151. https://doi.org/10.1007/s11295-006-0037-1
Segura V, Denancé C, Durel CE, Costes E (2007) Wide range QTL analysis for complex architectural traits in 1-year-old apple progeny. Genome 50:159–171. https://doi.org/10.1139/G07-002
Shin HK, Lieth JH, Kim SH (2001) Effects of temperature on leaf area and flower size in rose. Acta Hortic 547:185–191
Souza VAB, Byrne DH, Taylor JF (1998) Heritability, genetic and phenotypic correlations, and predicted selection response of quantitative traits in peach: II. An analysis of several fruit traits. J Am Soc Hortic Sci 123:604–611
Spiller M, Linde M, Hibrand-Saint Oyant L, Tsai CJ, Byrne DH, Smulders MJM, Foucher F, Debener T (2011) Towards a unified genetic map for diploid roses. Theor Appl Genet 122:489–500. https://doi.org/10.1007/s00122-010-1463-x
Teichmann T, Muhr M (2015) Shaping plant architecture. Front Plant Sci 6:233. https://doi.org/10.3389/fpls.2015.00233
Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200. https://doi.org/10.1038/nature07272
Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349. https://doi.org/10.1017/S0016672311000279
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
White J (1979) The plant as a metapopulation. Annu Rev Ecol Syst 10:109–145. https://doi.org/10.1146/annurev.es.10.110179.000545
Yan Z, Denneboom C, Hattendorf A, Dolstra O, Debener T, Stam P, Visser PB (2005) Construction of an integrated map of rose with AFLP, SSR, PK, RGA, RFLP, SCAR and morphological markers. Theor Appl Genet 110:766–777. https://doi.org/10.1007/s00122-004-1903-6
Yan Z, Visser PB, Hendriks T, Prins TW, Stam P, Dolstra O (2007) QTL analysis of variation for vigour in rose. Euphytica 154:53–62. https://doi.org/10.1007/s10681-006-9269-2
Zhang L, Wang S, Li H, Deng Q, Zheng A, Li S, Li P, Li Z, Wang J (2010) Effects of missing marker and segregation distortion on QTL mapping in F2 populations. Theor Appl Genet 121:1071–1082. https://doi.org/10.1007/s00122-010-1372-z
Zieslin N, Mor Y (1990) Light on roses. A review. Scientia Hort 43:1–14
Acknowledgements
The authors would like to thank Rémi Gardet and his team of the IRHS experimental station (ImHorPhen) for their technical assistance in plant management, Muriel Bahut of the ANAN platform (SFR QuaSaV) and Charles Poncet of the Gentyane platform for SSR analyses, Hervé Autret and Marie-Sophie Neveux for their technical assistance, Valérie Le Clerc for proofreading this manuscript in depth, and Annie Buchwalter for proofreading the English language in this manuscript.
Funding information
This study was financed by the French Ministry of Agriculture and Fisheries (Compte d’Affectation Spéciale pour le Développement Agricole et Rural; CASDAR) within the framework of the ARIAGE project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Data archiving statement
All relevant data are within the article and supplementary material files.
Additional information
Communicated by D. Chagné
Rights and permissions
About this article
Cite this article
Li-Marchetti, C., Le Bras, C., Chastellier, A. et al. 3D phenotyping and QTL analysis of a complex character: rose bush architecture. Tree Genetics & Genomes 13, 112 (2017). https://doi.org/10.1007/s11295-017-1194-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-017-1194-0