The identification of the Rosa S-locus provides new insights into the breeding and wild origins of continuous-flowering roses

Koji Kawamura , Yoshihiro Ueda , Shogo Matsumoto , Takanori Horibe , Shungo Otagaki , Li Wang , Guoliang Wang , Laurence Hibrand-Saint Oyant , Fabrice Foucher , Marcus Linde , Thomas Debener

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac155

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac155 DOI: 10.1093/hr/uhac155
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The identification of the Rosa S-locus provides new insights into the breeding and wild origins of continuous-flowering roses
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Abstract

This study aims to: (i) identify the Rosa S-locus controlling self-incompatibility (SI); (ii) test the genetic linkage of the S-locus with other loci controlling important ornamental traits, such as the continuous-flowering (CF) characteristic; (iii) identify the S-alleles (SC) of old Chinese CF cultivars (e.g, Old Blush, Slater’s Crimson China) and examine the changes in the frequency of cultivars with Sc through the history of breeding; (iv) identify wild species carrying the Sc-alleles to infer wild origins of CF cultivars. We identified a new S- RNase (SC2) of Rosa chinensis in a contig from a genome database that has not been integrated into one of the seven chromosomes yet. Genetic mapping indicated that SC2 is allelic to the previously-identified S-RNase (SC1) in chromosome 3. Pollination experiments with half-compatible pairs of roses confirmed that they are the pistil-determinant of SI. The segregation analysis of an F1-population indicated genetic linkage between the S-locus and the floral repressor gene KSN. The non-functional allele ksn is responsible for the CF characteristic. A total of five S-alleles (SC1–5) were identified from old CF cultivars. The frequency of cultivars with SC dramatically increased after the introgression of ksn from Chinese to European cultivars and remains high (80%) in modern cultivars, suggesting that S-genotyping is helpful for effective breeding. Wild individuals carrying SC were found in Rosa multiflora (SC1), Rosa chinensis var . spontanea (SC3), and Rosa gigantea (SC2, SC4), supporting the hypothesis of hybrid origins of CF cultivars and providing a new evidence for the involvement of Rosa multiflora.

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Koji Kawamura, Yoshihiro Ueda, Shogo Matsumoto, Takanori Horibe, Shungo Otagaki, Li Wang, Guoliang Wang, Laurence Hibrand-Saint Oyant, Fabrice Foucher, Marcus Linde, Thomas Debener. The identification of the Rosa S-locus provides new insights into the breeding and wild origins of continuous-flowering roses. Horticulture Research, 2022, 9 (1) : uhac155 DOI:10.1093/hr/uhac155

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References

[1]

Young MA, Schorr P, Baer R . Modern Roses 12 . Shreveport: American Rose Society; 2007.

[2]

Leus L, Van Laere K, De Riek J et al. Ornamental crops. In: Van Huylenbroeck J (ed.), Handbook of Plant Breeding Vol. 11. Cham: Springer, 2018, 719-67.

[3]

Zlesak DC . Rose. In: Anderson NO, ed. Flower Breeding and Genetics.Springer: Dordrecht, 2006, 695-740.

[4]

Debener T, Linde M . Exploring complex ornamental genomes, the rose as a model plant. Crit Rev Plant Sci. 2009; 28: 267-80.

[5]

Hibrand Saint-Oyant L, Ruttink T, Hamama L et al. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat Plants. 2018; 4: 473-84.

[6]

Raymond O, Gouzy J, Just J et al. The Rosa genome provides new insights into the domestication of modern roses. Nat Genet. 2018; 50: 772-7.

[7]

Nakamura N, Hirakawa H, Sato S et al. Genome structure of Rosa multiflora, a wild ancestor of cultivated roses. DNA Res. 2018; 25: 113-21.

[8]

Scalliet G, Piola F, Douady CJ et al. Scent evolution in Chinese roses. PNAS. 2008; 105: 5927-32.

[9]

Magnard JL, Roccia A, Caissard JC et al. Biosynthesis of monoterpene scent compounds in roses. Science. 2015; 349: 81-3.

[10]

Iwata H, Gaston A, Remay A et al. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry . Plant J. 2012; 69: 116-25.

[11]

François L, Verdenaud M, Fu X et al. A miR172 target-deficient AP2-like gene correlates with the double flower phenotype in roses. Sci Rep. 2018; 8: 12912.

[12]

Sassa H. Molecular mechanism of the S-RNase-based gametophytic self-incompatibility in fruit trees of Rosaceae. Breed Sci. 2016; 66: 116-21.

[13]

Kubo K, Entani T, Takara A et al. Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science. 2010; 330: 796-9.

[14]

Akagi T, Henry IM, Morimoto T et al. Insights into the Prunus-specific S-RNase-based self-incompatibility system from a genome-wide analysis of the evolutionary radiation of S locus-related F-box genes . Plant Cell Physiol. 2016; 57: 1281-94.

[15]

Vieira J, Pimenta J, Gomes A et al. The identification of the Rosa S-locus and implications on the evolution of the Rosaceae gametophytic self-incompatibility systems . Sci Rep. 2021; 11: 3710.

[16]

Chen F, Su L, Hu S et al. A chromosome-level genome assembly of rugged rose (Rosa rugosa) provides insights into its evolution, ecology, and floral characteristics . Hortic Res. 2021; 8: 141.

[17]

Du J, Ge C, Li T et al. Molecular characteristics of S-RNase alleles as the determinant of self-incompatibility in the style of Fragaria viridis . Hortic Res. 2021; 8: 185.

[18]

Smulders MJM, Arens P, Bourke PM et al. In the name of the rose, a roadmap for rose research in the genome era. Hortic Res. 2019; 6: 65.

[19]

Kawamura K, Hibrand-Saint Oyant L, Crespel L et al. Quantitative trait loci for flowering time and inflorescence architecture in rose. Theor Appl Genet. 2011; 122: 661-75.

[20]

Debener T, Bretzke M, Dreier M et al. Genetic and molecular analyses of key loci involved in self incompatibility and floral scent in roses. Acta Hortic. 2010; 870: 183-90.

[21]

Zhou NN, Tang KX, Jeauffre J et al. Genetic determinism of prickles in rose. Theor Appl Genet. 2020; 133: 3017-35.

[22]

Lopez Arias DC, Chastellier A, Thouroude T et al. Characterization of black spot resistance in diploid roses with QTL detection, meta-analysis and candidate-gene identification. Theor Appl Genet. 2020; 133: 3299-321.

[23]

Randoux M, Davière JM, Jeauffre J et al. RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol. 2014; 202: 161-73.

[24]

Soufflet-Freslon V, Araou E, Jeauffre J et al. Diversity and selection of the continuous-flowering gene, RoKSN, in rose. Hortic Res. 2021; 8: 76.

[25]

Hurst CC . Notes on the origin and evolution of our garden roses. J Roy Hort Soc. 1941; 66: 73-82, 242-250, 282-289.

[26]

Liorzou M, Pernet A, Li S 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. 2016; 67: 4711-25.

[27]

Meng J, Fougère-Danezan M, Zhang LB et al. Untangling the hybrid origin of the Chinese tea roses, evidence from DNA sequences of single-copy nuclear and chloroplast genes. Plant Syst Evol. 2011; 297: 157-70.

[28]

Zhu ZM, Gao XF, Fougère-Danezan M. Phylogeny of Rosa sections Chinenses and Synstylae (Rosaceae) based on chloroplast and nuclear markers . Mol Phylogenet Evol. 2015; 87: 50-64.

[29]

Tan J, Wang J, Luo L et al. Genetic relationships and evolution of old Chinese garden roses based on SSRs and chromosome diversity. Sci Rep. 2017; 7: 15437.

[30]

Yang C, Ma Y, Cheng B et al. Molecular evidence for hybrid origin and phenotypic variation of Rosa section Chinenses . Genes. 2020; 11: 996.

[31]

Debray K, Le Paslier MC, Bérard A et al. Unveiling the patterns of reticulated evolutionary processes with phylogenomics: hybridization and polyploidy in the genus Rosa . Syst Biol. 2022; 71: 547-69.

[32]

Cui W-H, Du XY, Zhong MC et al. Complex and reticulate origin of edible roses (Rosa, Rosaceae) in China . Hortic Res. 2022; 9: uhab051.

[33]

Meng J, He SL, Li DZ et al. Nuclear genetic variation of Rosa odorata var. gigantea (Rosaceae), population structure and conservation implications . Tree Genet Genomes. 2016; 12: 65.

[34]

Jian HY, Zhao L, Zhang H et al. Phylogeography and population genetics of Rosa chinensis var. spontanea and R. lucidissima Complex, the important ancestor of modern roses . Front Plant Sci. 2022; 13: 851396.

[35]

Schueler S, Tusch A, Scholz F . Comparative analysis of the within-population genetic structure in wild cherry (Prunus avium L.) at the self-incompatibility locus and nuclear microsatellites . Mol Ecol. 2006; 15: 3231-43.

[36]

Aguiar B, Vieira J, Cunha AE et al. Convergent evolution at the gametophytic self-incompatibility system in Malus and Prunus . PLoS One. 2015; 10: e0126138.

[37]

Price MN, Dehal PS, Arkin AP . FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009; 26: 1641-50.

[38]

Prince MN, Dehal PS, Arkin AP . FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One. 2010; 5: e9490.

[39]

Zang F, Ma Y, Tu X et al. A high-quality chromosome-level genome of wild Rosa rugosa . DNA Res. 2021; 28: dsab017.

[40]

Lyons E, Freeling M . How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 2008; 53: 661-73.

[41]

Debener T, Mattiesch L . Construction of a genetic linkage map for roses using RAPD and AFLP markers. Theor Appl Genet. 1999; 99: 891-9.

[42]

Liang M, Cao Z, Zhu A et al. Evolution of self-compatibility by a mutant Sm -RNase in citrus . Nat Plants. 2020; 6: 131-42.

[43]

Navarro A, Betran E, Barbadilla A et al. Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics. 1997; 146: 695-709.

[44]

Ueckert J, Byrne DH, Crosby K et al. The utilization of the polyploid nature of roses. Acta Hortic. 2015; 1064: 73-8.

[45]

Zlesak DC . Pollen diameter and guard cell length as predictors of ploidy in diverse rose cultivars, species, and breeding lines. Flori Ornam Biotech. 2009; 3: 53-70.

[46]

Dubois A, Raymond O, Maene M et al. Tinkering with the C-function, a molecular frame for the selection of double flowers in cultivated roses. PLoS One. 2010; 5: e9288.

[47]

Kawamura K, Hibrand-Saint Oyant L, Thouroude T et al. Inheritance of garden rose architecture and its association with flowering behaviour. Tree Genet Genomes. 2015; 11: 22.

[48]

Kawamura K, Hibrand-Saint Oyant L, Foucher F et al. Kernel methods for phenotyping complex plant architecture. J Theor Biol. 2014; 342: 83-92.

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