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Inheritance of garden rose architecture and its association with flowering behaviour

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Abstract

Understanding the genetic basis of plant architecture is limited for woody plants due to the challenges of assessing the inheritance of their complex architecture. We aimed to evaluate the genetic variability of plant form and stature in a garden rose population, analyse the inheritance of plant architecture and its linkage with flowering behaviour and identify the quantitative trait loci (QTLs) controlling garden rose architecture. A total of 98 F 1 hybrids were derived from the cross between two diploid roses, The Fairy (TF) and Rosa × wichurana (RW) that differed in stature and flowering behaviour. The TF exhibits continuous flowering (CF) and has erect stature. The RW is once flowering (OF) and prostrate in stature. Three clones per genotype were multiplied, and a total of 300 plants were cultivated in a field. Flowering behaviour, plant form, plant height, stem diameter and internode length were scored during each of 2 years. All architectural traits had significant genetic variances (29–61 % of their respective phenotypic variances), and their broad-sense heritability estimates were 0.76–0.92. The majority of CF progeny was erect, whereas the OF progeny was prostrate, suggesting a linkage between plant form and flowering behaviour. The QTL analysis identified eight major QTLs controlling architectural traits. Several candidate genes involved in gibberellin biosynthesis and auxin signalling were identified in the vicinity of the QTLs. High heritability estimates obtained for garden rose architecture indicated that architectural characteristics are feasible targets of rose breeding. Linkage of plant form and flowering behaviour, however, prevents independent selection of these traits. The candidate genes identified can be good targets for future physiological studies.

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References

  • Ando K, Grumet R, Terpstra K, Kelly JD (2007) Manipulation of plant architecture to enhance crop disease control. CAB Rev 2:1–8

    Article  Google Scholar 

  • Auld TD, Morrison DA (1992) Genetic determination of erect and prostrate growth habit in five shrubs from windswept headlands in the Sydney region. Aust J Bot 40:1–11

    Article  Google Scholar 

  • Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375–407

    Article  PubMed Central  PubMed  Google Scholar 

  • Beavis WD (1998) QTL analyses: power, precision, and accuracy. In: Paterson AH (ed) Molecular dissection of complex traits. CRC Press, New York, pp 145–162

    Google Scholar 

  • Bendahmane M, Dubois A, Raymond O, Le Bris M (2013) Genetics and genomics of flower initiation and development in roses. J Exp Bot 64:847–885

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043

    Article  PubMed  Google Scholar 

  • Boumaza R, Demotes-Mainard S, Huché-Thélier L, Guérin V (2009) Visual characterization of the esthetic quality of the rosebush. J Sens Stud 24:774–796

    Article  Google Scholar 

  • Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83

    Article  CAS  PubMed  Google Scholar 

  • Buck-Sorlin G, de Visser PHB, Henke M, Sarlikioti V, van der Heijden GWAM, Marcelis LFM, Vos J (2011) Towards a functional–structural plant model of cut-rose: simulation of light environment, light absorption, photosynthesis and interference with the plant structure. Ann Bot 108:1121–1134

    Article  PubMed Central  PubMed  Google Scholar 

  • Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Busov VB, Brunner AM, Strauss S (2008) Genes for control of plant stature and form. New Phytol 177:589–607

    Article  CAS  PubMed  Google Scholar 

  • Costes E, Lauri PE, Laurens F, Moutier N, Belouin A, Delort F, Legave JM, Regnard JL (2004) Morphological and architectural traits on fruit trees which could be relevant for genetic studies: a review. Acta Horticult 663:349–355

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Crespel L, Le Bras C, Relion D, Morel P (2014) Genotype x year interaction and broad-sense heritability of architectural characteristics in rose bush. Plant Breed 133:412–418

    Article  Google Scholar 

  • Debener T (2003) Genetics: Inheritance of characteristics. In: Roberts AV, Debener T, Gudin S (eds) Encyclopedia of Rose Science, vol 1. Elsevier, Oxford, pp 286–292

    Chapter  Google Scholar 

  • Debener T, Linde M (2009) Exploring complex ornamental genomes: the rose as a model plant. Crit Rev Plant Sci 28:267–280

    Article  CAS  Google Scholar 

  • Dieters MJ, White TL, Littell RC, Hedge GR (1995) Application of approximate variances of variance-components and their ratios in genetic tests. Theor Appl Genet 91:15–24

    Article  CAS  PubMed  Google Scholar 

  • Djennane S, Hibrand-Saint Oyant L, Kawamura K, Lalanne D, Laffaire M, Thouroude T, Chalain S, Sakr S, Boumaza R, Foucher F, Leduc N (2014) 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

    Article  CAS  PubMed  Google Scholar 

  • Dubois LAM, De Vries DP (1987) On the inheritance of the dwarf character in polyantha x Rosa chinensis minima (SIMS) Voss F1-populations. Euphytica 36:535–539

    Article  Google Scholar 

  • Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, Banfield MJ, Rameau C (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15:2742–2754

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT, Tester M (2011) Phenomics: technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16:635–644

    Article  CAS  PubMed  Google Scholar 

  • Gudin S (2000) Rose: genetics and breeding. Plant Breed Rev 17:159–189

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Holland JB, Nyquist WE, Cervantes-Martinez CT (2003) Estimating and interpreting heritability for plant breeding: an update. Plant Breed Rev 22:9–111

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • James KR, Haritos N, Ades PK (2006) Mechanical stability of trees under dynamic loads. Am J Bot 93:1522–1530

    Article  PubMed  Google Scholar 

  • Kawamura K (2010) A conceptual framework for the study of modular responses to local environmental heterogeneity within the plant crown and a review of related concepts. Ecol Res 25:733–744

    Article  Google Scholar 

  • 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. Theor Appl Genet 122:661–675

    Article  PubMed  Google Scholar 

  • Kawamura K, Hibrand-Saint Oyant L, Foucher F, Thouroude T, Loustau S (2014) Kernel methods for phenotyping complex plant architecture. J Theor Biol 342:83–92

    Article  PubMed  Google Scholar 

  • Larson SR, Wu X, Jones TA, Jensen KB, Chatterton NJ, Waldron BL, Robins JG, Bushman BS, Palazzo AJ (2006) Comparative mapping of growth habit, plant height, and flowering QTLs in two interspecific families of Leymus. Crop Sci 46:2526–2539

    Article  CAS  Google Scholar 

  • Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161–164

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Watanabe S, Uchiyama T, Kong F, Kanazawa A, Xia Z, Nagamatsu A, Arai M, Yamada T, Kitamura K, Masuta C, Harada K, Abe J (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiol 153:198–210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCulloh KA, Sperry JS (2005) Patterns in hydraulic architecture and their implications for transport efficiency. Tree Physiol 25:257–267

    Article  PubMed  Google Scholar 

  • Mirzaie-Nodoushan H, Gordon IL, Rumball WB (1999) Inheritance of growth habit-related attributes in red clover (Trifolium pratense L.). J Hered 90:550–553

    Article  Google Scholar 

  • Mohamed R, Wang CT, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng X, Meilan R, Strauss SH, Brunner AM (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nakamura T, Saotome M, Ishiguro Y, Itoh R, Higurashi S, Hosono M, Ishii Y (1994) The effects of GA3 on weeping of growing shoots of the Japanese cherry, Prunus spachiana. Plant Cell Physiol 35:523–527

    CAS  Google Scholar 

  • Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–122

    Article  CAS  PubMed  Google Scholar 

  • Niwa M, Daimon Y, Kurotani K, Higo A, Pruneda-Paz JL, Breton G, Mitsuda N, Kay SA, Ohme-Takagi M, Endo M, Araki T (2013) BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25:1228–1242

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nugroho WD, Yamagishi Y, Nakaba S, Fukuhara S, Begum S, Marsoem SN, Ko JH, Jin HO, Funada R (2012) Gibberellin is required for the formation of tension wood and stem gravitropism in Acacia mangium seedlings. Ann Bot 110:887–895

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nybom H (2009) Introduction to Rosa. In: Folta KM, Gardiner SE (eds) Genetics and genomics of Rosaceae, Springer, pp 339-352

  • Pearcy RW, Muraoka H, Valladares F (2005) Crown architecture in sun and shade environments: assessing function and trade-offs with a three-dimensional simulation model. New Phytol 166:791–800

    Article  PubMed  Google Scholar 

  • Rajapakse S, Byrne DH, Zhang L, Anderson N, Arumuganathan K, Ballard RE (2001) Two genetic linkage maps of tetraploid roses. Theor Appl Genet 103:575–583

    Article  CAS  Google Scholar 

  • Randoux M, Davière JM, Jeauffre J, Thouroude T, Pierre S, Toualbia Y, Perrotte J, Reynoird JP, Jammes MJ, Hibrand-Saint Oyant L, Foucher F (2014) RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol 202:161–173

    Article  CAS  PubMed  Google Scholar 

  • Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615

    CAS  PubMed  Google Scholar 

  • 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. Theor Appl Genet 119:767–781

    Article  CAS  PubMed  Google Scholar 

  • Roberts AV, Blake PS, Lewis R, Talor JM, Dunstan DI (1999) The effect of gibberellins on flowering in roses. J Plant Growth Regul 18:113–119

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Matsuoka M (2004) Generating high-yielding varieties by genetic manipulation of plant architecture. Curr Opin Biotechnol 15:144–147

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Segura V, Cilas C, Costes E (2008) Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: mixed linear modeling of repeated spatial and temporal measures. New Phytol 178:302–314

    Article  PubMed  Google Scholar 

  • Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y, Lifschitz E (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci U S A 106:8392–8397

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spiller M, Linde M, Hibrand-Saint Oyant L, Tsai C-J, Byrne DH, Smulders MJM, Foucher F, Debener T (2011) Towards a unified genetic map for diploid roses. Theor Appl Genet 122:489–500

    Article  PubMed  Google Scholar 

  • Tan L, Li X, Liu F, Sun X, Li C, Zhu Z, Fu Y, Cai H, Wang X, Xie D, Sun C (2008) Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 40:1360–1364

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijen JW (2004) MAPQTL® 5.0 Software for the mapping of quantitative trait loci in experimental populations. Plant Research International, Wageningen

    Google Scholar 

  • Via S (1984) The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution 35:896–905

    Article  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Davis RE, Nuss DL, Zhao Y (2013) Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture. Proc Natl Acad Sci U S A 110:19149–19154

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • White J (1979) The plant as a metapopulation. Annu Rev Ecol Syst 10:109–145

    Article  Google Scholar 

  • Wissemann V, Gallenmüller F, Ritz C, Steinbrecher T, Speck T (2006) Inheritance of growth form and mechanical characters in reciprocal poplyploid hybrids of Rosa section Caninae—implications for the ecological niche differentiation and radiation process of hybrid offspring. Trees 20:340–347

    Article  Google Scholar 

  • Wolters PJ, Schouten HJ, Velasco R, Si-Ammour A, Baldi P (2013) Evidence for regulation of columnar habit in apple by a putative 2OG-Fe(II) oxygenase. New Phytol 200:993–999

    Article  CAS  PubMed  Google Scholar 

  • Wu R, Stettler RF (1997) Quantitative genetics of growth and development in Populus. II. The partitioning of genotype x environment interaction in stem growth. Heredity 78:124–134

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhang F, Jiang J, Chen S, Chen F, Fang W (2012a) Mapping single-locus and epistatic quantitative trait loci for plant architectural traits in chrysanthemum. Mol Breed 30:1027–1036

    Article  Google Scholar 

  • Zhang Y, Zhu J, Dai H (2012b) Characterization of transcriptional differences between columnar and standard apple trees using RNA-Seq. Plant Mol Biol Report 30:957–965

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Drs. Philippe Morel and Gilles Galopin (SAGAH, INRA Angers) for their helpful advice on plant measurements; Charles-Eric Durel, Sylvain Gaillard, Fabrice Dupuis and Alix Pernet (GenHort, INRA Angers) for the statistical analyses. This work was supported by grants from the Département de Génétique et d’Amélioration des Plantes, INRA, Région Pays de la Loire and Japan Society for the Promotion of Science KAKENHI (24688004).

Data Archiving Statement

Genetic map and QTL data are currently being submitted to GDR, Genome Database for Rosaceae (accession number = tfGDR1008).

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Correspondence to Koji Kawamura or Fabrice Foucher.

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Communicated by W.-W. Guo

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Kawamura, K., Hibrand-Saint Oyant, L., Thouroude, T. et al. Inheritance of garden rose architecture and its association with flowering behaviour. Tree Genetics & Genomes 11, 22 (2015). https://doi.org/10.1007/s11295-015-0844-3

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