Diversity and selection of the continuous-flowering gene, RoKSN, in rose

Abstract

Blooming seasonality is an important trait in ornamental plants and was selected by humans. Wild roses flower only in spring whereas most cultivated modern roses can flower continuously. This trait is explained by a mutation of a floral repressor gene, RoKSN, a TFL1 homologue. In this work, we studied the origin, the diversity and the selection of the RoKSN gene. We analyzed 270 accessions, including wild and old cultivated Asian and European roses as well as modern roses. By sequencing the RoKSN gene, we proposed that the allele responsible for continuous-flowering, RoKSN^copia, originated from Chinese wild roses (Indicae section), with a recent insertion of the copia element. Old cultivated Asian roses with the RoKSN^copia allele were introduced in Europe, and the RoKSN^copia allele was progressively selected during the 19th and 20th centuries, leading to continuous-flowering modern roses. Furthermore, we detected a new allele, RoKSN^A181, leading to a weak reblooming. This allele encodes a functional floral repressor and is responsible for a moderate accumulation of RoKSN transcripts. A transient selection of this RoKSN^A181 allele was observed during the 19th century. Our work highlights the selection of different alleles at the RoKSN locus for recurrent blooming in rose.

References

[1] Andres, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639 (2012).

[2] Shrestha, R., Gómez-Ariza, J., Brambilla, V. & Fornara, F. Molecular control of seasonal flowering in rice, Arabidopsis and temperate cereals. Ann. Bot. 114, 1445-1458 (2014).

[3] Khan, M. R. G., Ai, X.-Y. & Zhang, J.-Z. Genetic regulation of flowering time in annual and perennial plants. WIREs RNA 5, 347-359 (2014).

[4] Weller, J. L. & Ortega Martínez, R. Genetic control of flowering time in legumes. Front. Plant Sci. 6, 207 (2015).

[5] Toomajian, C. et al. A Nonparametric Test Reveals Selection for Rapid Flowering in the Arabidopsis Genome. PLoS Biol. 4, e137 (2006).

[6] Caicedo, A. L., Stinchcombe, J. R., Olsen, K. M., Schmitt, J. & Purugganan, M. D. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc. Natl Acad. Sci. USA 101, 15670-15675 (2004).

[7] Izawa, T. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J. Exp. Bot. 58, 3091-3097 (2007).

[8] Li, P. et al. Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes Dev. 28, 1635-1640 (2014).

[9] Tian, Z. et al. Artificial selection for determinate growth habit in soybean. Proc. Natl Acad. Sci. USA 107, 8563-8568 (2010).

[10] Blackman, B. K., Strasburg, J. L., Raduski, A. R., Michaels, S. D. & Rieseberg, L. H. The role of recently derived FT paralogs in sunflower domestication. Curr. Biol. 20, 629-635 (2010).

[11] Cutler, R. R. Secondary Metabolites | Culinary Uses and Nutritional Value. in Encyclopedia of Rose Science (ed Roberts, A. V.) 707-716 (Elsevier, 2003).

[12] Pemberton, H. B. Production and Marketing | Overview of Roses and Culture. in Encyclopedia of Rose Science (ed Roberts, A. V.) 570-573 (Elsevier, 2003).

[13] Pline l’ancien. Histoire naturelle. Stéphane Schmitt (editing and translation) (Gallimard, 2013).

[14] Touw, M. Roses in the middle ages. Econ. Bot. 36, 71-83 (1982).

[15] Goody, J . The Culture of Flowers (Cambridge University Press, 1993).

[16] Miller, P. The Gardeners Dictionary, the 8th edn. Printer for the author (1768).

[17] Wang, G. A study on the history of Chinese roses from ancient works and images. Acta Horticulturae 751, 347-356 (2007).

[18] Wylie, A. P. The history of garden roses. J. R. Horticulural Soc. 79, 555-571 (1954).

[19] Lemmonier, D. Le livre des roses. Histoire des roses de nos jardins (Belin, 2014).

[20] Liorzou, M. et al. Nineteenth century French rose (Rosa sp.) germplasm shows a shift over time from a European to an Asian genetic background. J. Exp. Bot. 67, 4711-4725 (2016).

[21] Oghina-Pavie, C. Rose and Pear Breeding in Nineteenth-Century France: The Practice and Science of Diversity. in New Perspective on the History of Life Sciences and Agriculture, 53-72 (Springer International Publishing, 2015).

[22] Semeniuk, P. Inheritance of recurrent blooming in Rosa wichuraiana. J. Heredity 62, 203-204 (1971).

[23] Li, S. et al. Inheritance of perpetual blooming in Rosa chinensis ‘Old Blush’. Horticultural Plant J. 1, 108-112 (2015).

[24] Iwata, H. et al. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J. 69, 116-125 (2012).

[25] Hibrand Saint-Oyant, L. et al. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat. Plants 4, 473-484 (2018).

[26] Horibe, T., Yamada, K., Otagaki, S., Matsumoto, S. & Kawamura, K. Molecular genetic studies on continuous-flowering roses that do not originate from Rosa chinensis. Acta Horticulturae 1064, 185-912 (2015).

[27] SanMiguel, P., Gaut, B. S., Tikhonov, A., Nakajima, Y. & Bennetzen, J. L. The paleontology of intergene retrotransposons of maize. Nat. Genet. 20, 43-45 (1998).

[28] Perlman, P. S. & Boeke, J. D. Ring around the retroelement. Science 303, 182 (2004).

[29] Taoka, K. et al. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476, 332-335 (2011).

[30] Ahn, J. H. et al. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 25, 605-614 (2006).

[31] Randoux, M. et al. RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. N. Phytol. 202, 161-173 (2014).

[32] Proïa, F., Pernet, A., Thouroude, T., Michel, G. & Clotault, J. On the characterization of flowering curves using Gaussian mixture models. J. Theor. Biol. 402, 75-88 (2016).

[33] Foucher, F. et al. 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 (2003).

[34] Osborn, T. C. The contribution of polyploidy to variation in Brassica species. Physiol. Plant. 121, 531-536 (2004).

[35] Pilu, R. Paramutation phenomena in plants. Semin. Cell Dev. Biol. 44, 2-10 (2015).

[36] Bruneau, A., Starr, J. R. & Joly, S. Phylogenetic relationships in the genus Rosa: new evidence from chloroplast DNA sequences and an appraisal of current knowledge. Syst. Bot. 32, 366-378 (2007).

[37] Oghina-Pavie, C. Les rosiers entre horticulture et science au XIXe siècle. in Roses, mettez-vous au parfum. 17-24 (SNHF, 2015).

[38] Hurst, C. C. Notes on the origin and evolution of our garden roses. J. R. Horticulural Soc. 66, 73-82 (1941).

[39] Mattock, R. ‘The Silk Road Hybrids’: Cultural linkage facilitated the transmigration of the remontant gene in Rosa x damascena, the Damask rose, in circa 3,500 BCE from the river Amu Darya watershed in Central Asia, the river Oxus valley of the Classics, to Rome by 300 BCE. Doctoral Thesis, 28 Sept 2017, Department of Architecture & Civil Engineering, (University of Bath, 2017)

[40] Neff, M. M., Turk, E. & Kalishman, M. Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 18, 613-615 (2002).

[41] Shannon, S. & Meeks-Wagner, D. R. A mutation in the arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3, 877 (1991).

[42] Hood, E. E., Gelvin, S. B., Melchers, L. S. & Hoekema, A. New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 2, 208-218 (1993).

[43] Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 (1998).

[44] Klie, M. & Debener, T. Identification of superior reference genes for data normalisation of expression studies via quantitative PCR in hybrid roses (Rosa hybrida). BMC Res. Notes 4, 518 (2011).

[45] Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45- e45 (2001).

[46] Raymond, O. et al. The Rosa genome provides new insights into the domestication of modern roses. Nat. Genet. 50, 772-777 (2018).

[47] Dubois, A. et al. Transcriptome database resource and gene expression atlas for the rose. BMC Genom. 13, 638 (2012).