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Inheritance of Characteristics☆
Inheritance of Characteristics☆ Thomas Debener, Leibniz University of Hannover, Hannover, Germany r 2017 Elsevier Inc. All rights reserved.
Introduction Since the rediscovery of Mendel's laws in 1901 by Correns, Tschernak and DeVries, genetic analyses have greatly increased our understanding of the basic principles of plant biology. Starting with traits that could be screened very easily, including flower color and structural characters, both the methods of analysis and the genetic strategies were constantly refined, finally leading to the complete analysis of a plant genome in the Arabidopsis sequencing project. A molecular analysis alone rarely identifies the function of a given DNA sequence without the proper genetic experiments. Therefore, the classical genetic analysis of a particular trait is often the key step in the analysis of gene structure and function.
The Genetic System of Roses Amongst 150 or more different species of the genus Rosa, the genetic system is not uniform. Ploidy levels can range from the diploid to the octoploid level. Due to the polyploid nature of most cultivated roses, the partial apomictic reproduction in some species of the section Caninae, self-incompatibility and fertility barriers between some species, thorough genetic analyses have been an exception in roses to date. Therefore, information on the inheritance of important rose characters is scarce. The complexity of genetic segregation patterns increases exponentially with the ploidy level of the segregating populations. The simpler cases are found in segregating progeny derived within diploid roses. Nevertheless, genetic analysis is restricted by the self-incompatibility of many diploid species and varieties, which is an obstacle to the use of self-fertilization to create F2 progenies. Thus the alternative “double-pseudo-testcross” strategy is used, in which unrelated parents with a high degree of heterozygosity are crossed with up to four alleles segregating in the progeny. In addition, backcrosses are also possible which will segregate for up to three alleles. In these cases segregation distortion has to be expected, as the presence of self-incompatibility factors similar to the gametophytic self-incompatibility system of Prunus would exclude the S-alleles shared and all alleles linked to them. Another disadvantage to genetic model systems is the small number of seeds produced by most of the diploid species which make the generation of sufficiently large populations very laborious. Furthermore, most diploid species and many diploid hybrids are not recurrent-flowering. This means that backcrosses can often be made only in the second year after sowing the F1 seedlings. The segregation of traits in tetraploids is much more complex than in diploids. Theoretically, up to eight different alleles per locus may segregate in the progeny of crosses between unrelated parents. In contrast to diploids, self-fertilization is possible in many tetraploid genotypes. However, even for characters determined by single dominant genes, much larger populations are required for tetraploids than for diploids to obtain the same genetic resolution (Table 1). Recently the mode of inheritance in segregating populations from crosses between garden roses was analyzed with molecular markers which indicated mainly tetrasomic inheritance although disomic inheritance for some genomic regions could not be excluded. If a particular character is determined by more than one gene and dominance is incomplete, genes have additive effects and a huge number of possible genotypes can be expected in the progeny (Table 2). This tremendous difference between the possible number of genetic combinations in diploids and tetraploids also explains the difficulties of genetic analysis in tetraploids as compared to diploids. A feature independent of the ploidy level was observed in a number of progeny from interspecific crosses. Here, several characters, such as the shape and number of prickles and the presence of glandular trichomes, are not inherited in an intermediate way but are rather inherited only through the female line, i.e., the offspring resemble the phenotype of the maternal plant. In some Table 1 Phenotypic ratios expected for the segregation of single loci in the tetraploid population Mating
Segregation of phenotypes
AAaa selfed Aaaa selfed AAaa Aaaa AAaa aaaa Aaaa aaaa Aa Aa Aa aa
35A: 1a 3A: 1a 11A: 1a 5A: 1a 1A: 1a 3A: 1a 1A: 1a
☆ Change History: January 2016. Thomas Debener updated the Affiliation, Abstract, Table 3, Sections: “The Genetic System of Roses,” “Flower Structure,” “Prickles,” “Flower Color,” “Recurrent Flowering,” “Resistance to Black Spot,” “Resistance to Powdery Mildew,” “Implications for Rose Biology,” and “Further Reading.”
Reference Module in Life Sciences
doi:10.1016/B978-0-12-809633-8.05047-0
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Table 2 Maximum number of different gametes that diploid and tetraploid roses may produce if all loci under consideration are heterozygous and multiallelic (for example, a1a2 for diploids and a1a2a3a4 for tetraploids) Number of loci
1 2 4 8 n
Table 3
Number of different types of gametes In diploids
In tetraploids
2 4 16 256 2n
6 36 1296 1,679,616 6n
Rose characters that were analyzed in genetic experiments
Character
Mode of inheritance
References
Recurrent flowering
Monogenic recessive
Yellow flower color Pink flower color Double flowers
Monogenic dominant Monogenic codominant Monogenic dominant Quantitative Monogenic dominant Quantitative Monogenic recessive Monogenic dominant Monogenic dominant Monogenic dominant
Semeniuk (1971a,b), De Vries and Dubois (1984), Debener (1999), Crespel et al. (2002), Iwata et al. (2012) De Vries and Dubois (1984) Debener (1999), Henz et al. (2015) Debener (1999), Crespel et al. (2002) Oyant et al. (2008), Roman et al. (2015) Debener (1999), Rajapakse et al. (2001) Crespel et al. (2002) Rajapakse et al. (2001) Dubois and De Vries (1987) De Vries and Dubois (1984) von Malek and Debener (1998), Whitaker et al. (2010), Terefe-Ayana et al. (2011) Linde and Debener (2003) Dugo et al. (2005), Yan et al. (2006), Moghaddam et al. (2012) Svejda (1977a,b,1979) Yan et al. (2005, 2007) Wang et al. (2004) Dugo et al. (2005) Dugo et al. (2005) Dugo et al. (2005), Oyant et al. (2008) Cherri-Martin et al. (2007), Spiller et al. (2010) Carvalho et al. (2015) Kawamura et al. (2015)
Prickles on stems Prickles on petioles Dwarf phenotype Moss phenotype Resistance to black spot Resistance to powdery mildew Winter hardiness Vigor Nematode resistance Flower size Leaf size Flowering time Fragrance Stomatal function Plant architecture
Monogenic dominant Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative
cases these F1 hybrids are morphologically indistinguishable from their mother and only molecular markers may reveal their hybrid nature. Up to now, the biological basis of this phenomenon is unclear but one may speculate that processes connected to genetic imprinting and selective gene silencing may be involved. The most simple explanation, cytoplasmic inheritance, can largely be excluded because of the large number of characters involved, some of which have been shown to be nuclear-inherited (for example, the presence of prickles) and the observation that these complexes of characters will segregate in later generations. Many speculations about the inheritance of morphological and physiological parameters have been published over the last century. However, most of these were based on observations of very few progeny and, thus, were not amenable to statistical analysis. On the other hand, the knowledge of commercial rose breeders based on decades of experience with genetic crosses and selection within segregating populations probably comprises a large amount of information about the inheritance of particular characters. But this information remains a company secret and is not available to the general public. However, over the last 15 years the availability of molecular markers in roses stimulated many genetic analysis in controlled crosses in both diploid and tetraploid progeny. In the following article, only those characters will be considered which were investigated in controlled crosses and for which the methods of analysis meet the basic requirements for genetic experiments (Table 3).
Inheritance of Structural Characters Structural characters and flower colors are easily observed and, therefore, were the first targets for genetic analysis of rose characters. Many observations have been made on leaf shape, moss character, whole-plant architecture, flower and inflorescence morphology,
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prickles and several other morphological features. However, the modes of inheritance have only been elucidated for flower morphology, moss character, the dwarf phenotype and prickles.
Flower Structure Flower morphology consists of a large number of parameters, including the number and shape of petals, number of stamens, petal size and the number and arrangement of styles and ovaries. Some of these characters, for example, the size of floral organs, seem to be controlled by several genes, whereas single (five petals) versus double (410 petals) was shown to be inherited by a single gene. Wild rose species (with the exception of Rosa sericea and Rosa omeiensis) normally have five petals but a variable number of stamens and styles. In genotypes with double (multipetalled) flowers which have been selected several times during the early history of rose breeding, a certain number of stamens seems to have undergone homeotic transitions to petals, with some intermediate forms between both organ types. This is consistent with other plant species where these homeotic transformations have been observed for a long time. In roses these intermediate organ morphologies are common but the indefinite number of stamens makes it difficult to correlate stamen and petal numbers. However, diploid crosses between double (410 petals) and single (o6 petals) flowered genotypes revealed negative correlations between the number of stamens and petals (Fig. 1) supporting the concept of homeotic transformation. Whether or not this concept is accepted, it has been shown both in large diploid and tetraploid segregating populations that the double-flower phenotype is inherited as a single dominant gene (Fig. 2). In these populations where double flowers are caused by a single dominant gene, the number of petals in double-flowered genotypes displays a large variation, exceeding the values of the parental genotypes (so-called transgressive variation). By means of several marker based QTL analyses it could be shown that, in double flowers, differences between genotypes with respect to the
Fig. 1 Regression curve demonstrating the negative correlation between the number of petals and the number of stamens in a diploid population segregating for a single dominant gene for double flowers and quantitative factors influencing the number of petals. Note that the distribution of stamen numbers for flowers with five petals indicates the variable number of organs.
Fig. 2 Segregation of double flowers and flower color in a diploid population. Parental genotypes¼93/1-117 (pink, single) and 93/1-119 (pink, double), 94/1¼individual plants from the segregating progeny.
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Fig. 3 Segregation of the presence of prickles in a diploid population. Upper row, prickled and unprickled parents. Lower row, segregating progeny. Each group of three canes represents a single plant.
mean number of petals per flower are not only due to environmental conditions but are also modulated by additional genes. These seem to be present in the genetic background of both double- and single-flowered genotypes.
The Moss Phenotype The moss phenotype is characterized by the presence of a dense covering of glandular mossy protuberances on calyx tubes, petals, stems, petioles and pedicels. The character originated in the late 17th century as a sport of the cabbage rose Rosa centifolia L. Crosses between the tetraploid moss roses and tetraploid hybrid teas, originally performed to introduce recurrent flowering into the genetic background of the moss roses, revealed that the moss character is inherited as a single dominant gene.
Prickles As for many other morphological characters of roses, prickles display an enormous variability in shape as well as in quantity and distribution. They are, therefore, used as a key character for the taxonomic distinction of some species and varieties. Several studies have shown that prickles are inherited as a multi gene characteristic. Despite this complex inheritance, genotypes without prickles have been discovered relatively frequently, especially in diploid genotypes. Recent results based on the analysis of diploid segregating populations from crosses between prickled and unprickled plants (Fig. 3) demonstrate the inheritance of prickles on the stems as a single dominant gene at least in these genotypes. As the prickled parental genotypes used for this study represent a very limited gene pool, it cannot be excluded that additional genes may be involved in other genetic backgrounds. Furthermore, genetic analyses conducted in diploid and tetraploid populations indicate that the presence of prickles on the stem and on the petiole are inherited independently.
Dwarf Phenotypes Dwarf phenotypes mainly derived from the species Rosa chinensis minima (Sims) Voss. have been extensively used to breed miniature roses. The ease with which dwarf genotypes have been selected from crosses with diploid and tetraploid plants in the past and the observation that single-gene mutations cause dwarf phenotypes in plant models, such as Arabidopsis thaliana (L.) Heynh. would already imply simple inheritance of dwarfing in roses. Detailed genetic analysis of rose diploid populations indicated that the dwarf character is inherited as monogenic-dominant. Due to the different number of genes found in plant model systems, it cannot be excluded, as for the inheritance of prickles, that mutations in several different genes may lead to dwarf phenotypes.
Inheritance of Physiological Characters Flower Color Rose petals contain a number of different pigments that determine their color. In the 1970s, paper chromatography analyses of tetraploid rose cultivars revealed differences in the amounts of carotenoids, anthocyanidins (pelargonidin, cyanidin) and flavonols (kaempherol, quercetin) and the inheritance of petal color was postulated to be multigenic. However, in addition to several studies indicating quantitative inheritance of color intensity, the inheritance of yellow flower color in tetraploid as well as pink
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flower color in diploid populations was also shown to be controlled by major dominant and codominant genes, respectively (Table 3; Fig. 2). Although the pigment composition of the latter populations may have been very simple, refined methods which distinguish not only general pigment classes but also their various glycosides may resolve even complex petal colorations into simple segregation patterns of individual pigment components.
Recurrent Flowering Recurrent flowering was probably introduced into rose cultivars by introgression from R. chinensis Jaquin and Rosa odorata (Crép.) Rehd. and Wils. in the early 19th century. As it affects the requirement for vernalization of rose shoots to induce flowering and significantly increases the flowering period, it is an extremely important character which greatly influenced modern rose breeding. It is relatively easy to obtain recurrent-flowering progeny from crosses between recurrent and nonrecurrent cultivars. Therefore, theories about the inheritance of this character as a recessive gene date back to the early 1940s and were favoured, for example, by Hurst. But it was only since 1971 that the first clear-cut genetic analysis in diploid Rosa wichurana Crép. crosses demonstrated that a single recessive gene was responsible for the observed variation. Since then, several other studies in both tetraploid and diploid populations confirmed these results. It is assumed that most genes for recurrent flowering were derived from the few original sources. In a breakthrough discovery (Iwata et al., 2012) showed that the major control point between seasonal flowering and recurrent flowering is the TFL1 (Terminal Flower 1) orthologue which in several recurrent flowering mutants is mutated by the insertion of a retrotransposon. However, additional factors influence extend and duration of flowering as well.
Fragrance A specific characteristic of roses important for its commercial value is flower fragrance. In scented varieties fragrance is composed of up to more than one hundred volatiles. Several studies have analyzed genes involved in the biosynthesis of these volatiles, but only a few studies focused on the inheritance of volatiles in controlled crosses. These studies demonstrated that most volatiles segregated as polygenic traits but some also displayed monogenic segregation.
Winter Hardiness Although frequently used in the rose literature, the term “winter hardiness” is difficult to define precisely. The ability of roses to survive winter periods depends not only on the lowest temperatures, including frost tolerance (the ability to survive temperatures below freezing point), but also on the interplay of several other factors. These comprise the length of the acclimation period, humidity, periods of warm temperatures prevailing, frost factors and stress factors, including damage by pathogens and pests. Therefore, analyses of the percentage of winter kill in progeny derived from crosses between winter-hardy and nonhardy parents carried out in Canada in the 1970s displayed a broad variability, indicating an influence of multiple genes. However, estimates of heritability for different populations varied between 51 and 92%, implying the involvement of only a few or several closely linked loci.
Male Sterility In contrast to statements that evidence for an inheritance of male sterility as a single gene had been obtained, no conclusive genetic experiments have been reported. First results were reported in the early 1960s on a population that resulted from a cross between a male sterile genotype of Rosa setigera Michx. with a male fertile genotype of Rosa brunonii Lindl. About 96% of the 70 plants from the F1 progeny analyzed were male sterile. However, to elucidate the genetic basis of this trait, backcrosses and further crosses between the male sterile line and other genotypes would have been needed. Therefore, the genetic basis of male sterility remains obscure.
Inheritance of Resistance to Pathogens The study of plant resistance to pathogens involves higher levels of complexity than analyses of structural and physiological characters. Apart from genetic variation present in the host plant, the genetic constitution of the pathogen has to be considered as well. As was shown for numerous plant pathogen systems, the particular interaction between host and pathogen is often controlled by matching pairs of genes, following the so called “gene-for-gene” interaction. These gene-for-gene interactions are also termed “vertical resistance,” whereas resistance that is independent of the pathogen genotypes and controlled by many genes with additive effects is often termed “horizontal resistance”. Gene-for-gene interactions have been demonstrated for rose black spot and rose powdery mildew. Different pathogenic races may cause completely different reactions by the host plant and, therefore, polysporous isolates (i.e., mixtures of genetically diverse spores) often lead to host responses caused by several resistance genes simultaneously. As a consequence, genetic analyses focusing on these race-specific vertical resistance genes have to be performed under strictly controlled conditions with defined, genetically uniform strains of the pathogen. Apart from vertical resistance genes,
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quantitative or horizontal resistance genes acting on all pathogenic races may be present as well. This type of resistance is often less effective than vertical resistance in that it does not provide 100% protection against the pathogen but is generally expected to be more stable. It is also more difficult to manipulate in the breeding process because in most cases it is under polygenic control with different contributions of individual genes to the whole level of resistance.
Resistance to Black Spot Disease The first genetic analysis of resistance to rose pathogens was performed for black spot caused by the hemibiotrophic ascomycete Diplocarpon rosae Wolf. Black spot is the most severe fungal disease of field-grown roses, especially in areas with high annual precipitation. Screening of tetraploid as well as diploid populations carrying resistance from Rosa multiflora Thunb. with spores derived from a single conidial isolate revealed the presence of three single dominant genes Rdr1, Rdr2 and Rdr3 (Fig. 4). The data for Rdr1 have been confirmed, with several molecular markers cosegregating with the gene. These markers have been used to isolate and analyze the gene which turned out to be a TIR-NBS-LRR gene from a large gene family. In addition to the vertical race-specific resistance to black spot, horizontal resistance may be present as well. Observations in different laboratories show continuous variation in susceptibility between rose genotypes and even within segregating populations. However, quantitative genetic data on the transmission of partial resistance are not yet available.
Resistance to Powdery Mildew Powdery mildew, caused by the biotrophic ascomycete Podosphaera pannosa (Wallr.:Fr.) de Bary, formerly known as Sphaerotheca pannosa var. rosae, is the most important fungal disease of roses grown in greenhouses and also a serious disease in the field. Several studies on diploid and tetraploid segregating populations screened with single conidial isolates as well as natural inoculum revealed both the presence single major dominant genes as well as quantitative factors. Several of the underlying genes were located on various chromosomal maps constructed for roses by means of molecular markers.
Resistance to Crown Gall Disease The spread of crown gall disease, caused by Agrobacterium tumefaciens, is a serious problem in nursery stocks of southern European countries. Therefore, first analyses concerning the degree of susceptibility were made in a collection of 28 different genotypes and pronounced differences in susceptibility were found for some of the genotypes. However, no segregating progeny was analyzed and, therefore, no conclusions can be drawn concerning the inheritance of this character.
Implications for Rose Biology Even the limited amount of information about the inheritance of rose characters is an important first step for the understanding of biological functions. One example is the analysis of disease resistance showing that rose genes for black spot and powdery mildew resistance (both pathogens are obligate parasites) follow the scheme of the so-called gene-for-gene interactions. The
Fig. 4 Genotypes from a diploid population segregating for black spot resistance. Left, susceptible genotype displaying the typical black spot symptoms, like black spots and chlorosis. Right, resistant genotype without visible macroscopic symptoms. All plants were inoculated with spores from the single conidial Diplocarpon rosae isolate Dort E4, representing black spot race no. 5, at a density of 105 conidia mL1, and incubated for 10 days.
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demonstration of single-gene segregation has important implications for both the biology of the rose–pathogen interactions and future breeding strategies. Furthermore, this genetic information is the prerequisite for further analyses of the characters under investigation. For the rose disease resistance genes, for example, efforts to isolate and analyze the DNA sequences rely on the original genetic data. Another example are the genes known to influence the number of petals. The present data suggest that, apart from main switches deciding about double and single flowers, additional regulators determine the number of petals in double flowers. Utilizing the information about flower development in model plant species with several of the regulatory genes already cloned and analyzed, the information available for roses may be used to unravel the regulation of flower development in roses down to the molecular level. This approach would rely on the homology of the main regulatory networks, as demonstrated in comparative analysis between Arabidopsis, Antirrhinum and several other plant species. Another aspect under which genetic data from roses may facilitate structural and functional analyses of important genes is the concept of synteny. Synteny describes a conservation of gene order on chromosomal segments of different species from the same genus and even between different families. As genome sequences of Prunus, Fragaria, Malus and other rosaceous species are available and more to come, this information may soon help to detect and isolate a number of rose genes as well. Several initiatives are also working on a rose genome sequence and along with new sequencing techniques that allow complete transcriptome analysis this will speed up the identification of gene function in roses significantly.
Implications for Rose Breeding Rose breeding has mainly relied on very simple strategies. In order to develop more targeted approaches, information about the inheritance of the key traits is indispensable. This is of particular importance in cases where genes have to be introgressed from wild species to highly developed varieties via wide crosses. As an example, the mode of inheritance of a particular resistance gene is important to calculate the minimum population size necessary for obtaining progeny with both resistance and the appropriate combination of morphological characters. The more characters that are known in respect to their genetic basis, the more precise strategies considering the number of progeny and the number of generations can be developed. For traits that are difficult to screen, marker-assisted selection may be an alternative to the selection for the trait itself. Here again, markers can only be developed in populations segregating for a particular trait and in which precise knowledge about the inheritance is available.
Conclusions Our knowledge about the inheritance of important rose characters is still limited if compared to well-investigated plant species. However, the availability of diploid populations which have been used to analyze several important traits will increase the speed with which we can obtain more genetic information in the near future. In this process a genetic analysis will often remain a first necessary step which, often in connection with molecular methods, will lead to new insights into biological processes. Due to several unique characters of roses that cannot be analyzed in any model plant, detailed genetic analyses will remain indispensable over the next years. Apart from broadening our knowledge about principles of rose biology, information on the inheritance of key characters will be the prerequisite for the development of more advanced breeding strategies.
References Debener, T., 1999. Genetic analyses of important morphological and physiological characters in diploid roses. Gartenbauwissenschaft 64, 14–20. Carvalho, D.R.A., Koning-Boucoiran, C.F.S., Fanourakis, D., et al., 2015. QTL analysis for stomatal functioning in tetraploid Rosa x hybrida grown at high relative air humidity and its implications on postharvest longevity. Molecular Breeding 35, 172. Cherri-Martin, M., Julien, F., Heizmann, P., et al., 2007. Fragrance heritability in hybrid tea roses. Scientia Horticulturae 113, 177–181. Crespel, L., Chirollet, M., Durel, C.E., et al., 2002. Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theoretical and Applied Genetics 105, 1207–1214. De Vries, D.P., Dubois, L.A.M., 1984. Inheritance of the recurrent flowering and moss characters in F1 and F2 hybrid Tea Rosa centifolia muscosa (Aiton) seringe populations. Gartenbauwissenschaften 49, 97–100. Dubois, L.A.M., De Vries, D.P., 1987. On the inheritance of the dwarf character in Polyantha Rosa chinensis minima (Sims) Voss F1 populations. Euphytica 36, 535–539. Dugo, M.L., Satovic, Z., Millan, T., et al., 2005. Genetic mapping of QTLs controlling horticultural traits in diploid roses. Theoretical and Applied Genetics 111, 511–520. Henz, A., Debener, T., Linde, M., 2015. Identification of major stable QTLs for flower color in roses. Molecular Breeding 35. doi:10.1007/s11032-015-0382-6. Hibrand-Saint Oyant, L., Crespel, L., Rajapakse, S., et al., 2008. Genetic linkage maps of rose constructed with new microsatellite markers and locating QTL controlling flowering traits. Tree Genetics & Genomes 4, 11–23. Iwata, H., Gaston, A., Remay, A., et al., 2012. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant Journal 69, 116–125. Kawamura, K., Hibrand-Saint Oyant, L., Thouroude, T., et al., 2015. Inheritance of garden rose architecture and its association with flowering behavior. Tree Genetics & Genomes 11. Linde, M., Debener, T., 2003. Isolation and identification of eight races of powdery mildew of roses Podosphaera pannosa (Wallr.: Fr.) de Bary and the genetic analysis of the resistance gene Rppl. Theoretical and Applied Genetics 107, 256–262. Moghaddam, H.H., Leus, L., Riek, J., et al., 2012. Construction of a genetic linkage map with SSR, AFLP and morphological markers to locate QTLs controlling pathotypespecific powdery mildew resistance in diploid roses. Euphytica 184, 413–427.
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Rajapakse, S., Byrne, D., Zhang, L., et al., 2001. Two genetic linkage maps of tetraploid roses. Theoretical and Applied Genetics 103, 575–583. Roman, H., Rapicault, M., Miclot, A.S., et al., 2015. Genetic analysis of the flowering date and number of petals in rose. Tree Genetics & Genomes 11. Semeniuk, P., 1971a. Inheritance of recurrent blooming in R. wichuraiana. Journal of Heredity 62, 203–204. Semeniuk, P., 1971b. Inheritance of recurrent and non-recurrent blooming in “Goldilocks” Rosa wichuraiana progeny. Journal of Heredity 62, 319–320. Terefe-Ayana, T., Yasmin, A., Le, T.L., et al., 2011. Mining disease resistance genes in roses: Functional and molecular characterisation of the Rdr1 locus. Frontiers in Plant Biology 2, 35. doi:10.3389/fpls.2011.00035. Spiller, M., Berger, R.G., Debener, T., 2010. Genetic dissection of scent metabolic profiles in diploid rose populations. Theoretical and Applied Genetics 120, 1461–1471. doi:10.1007/s00122-010-1268-y. Svejda, F., 1977a. Breeding for improvement of flowering attributes of winterhardy Rosa rugosa hybrids. Euphytica 26, 697–701. Svejda, F., 1977b. Breeding for improvement of flowering attributes of winterhardy Rosa kordesii Wulf hybrids. Euphytica 26, 703–708. Svejda, F., 1979. Inheritance of winterhardiness in roses. Euphytica 28, 309–314. von Malek, B., Debener, T., 1998. Genetic analysis of resistance to blackspot (Diplocarpon rosae) in tetraploid roses. Theoretical and Applied Genetics 96, 228–231. Wang, X., Jacob, Y., Mastrantuono, S., et al., 2004. Spectrum and inheritance of resistance to the root-knot nematode Meloidogyne hapla in Rosa multiflora and R. indica. Plant Breeding 123, 79–83. doi:10.1046/j.0179-9541.2003.00930.x. Whitaker, V.M., Bradeen, J.M., Debener, T., et al., 2010. Rdr3, a novel locus conferring black spot disease resistance in tetraploid rose: Genetic analysis, LRR profiling, and SCAR marker development. Theoretical and Applied Genetics 120, 573–585. Yan, Z., Dolstra, O., Hendriks, T., et al., 2005. Vigor evaluation for genetics and breeding in rose. Euphytica 145, 339–347. Yan, Z., Dolstra, O., Prins, T., et al., 2006. Assessment of partial resistance to powdery mildew (Podosphaera pannosa) in a tetraploid rose population using a sporesuspension inoculation method. European Journal of Plant Pathology 114, 301–308. Yan, Z., Visser, P., Hendriks, T., et al., 2007. QTL: Analysis of variation for vigor in rose. Euphytica 154, 53–62.
Further Reading Debener, T., 1999. Genetic analyses of important morphological and physiological characters in diploid roses. Gartenbauwissenschaft 64, 14–20. De Vries, D.P., Dubois, L.A.M., 1996. Rose breeding: Past, present, prospects. Acta Horticulturae 424, 241–248. Gudin, S., 2000. Rose: Genetics and breeding plant. Breeding Reviews 17, 159–189. Iwata, H., Gaston, A., Remay, A., et al., 2012. The TFL1 homolog KSN is a regulator of continuous flowering in rose and strawberry. Plant Journal 69, 116–125. Krüssmann, G., 1974. Rosen, Rosen, Rosen. Berlin: Verlag Paul Parey. Lindstrom, E.W., 1936. Genetics of polyploidy. Botanical Review 2, 197–215.
Introduction Since the rediscovery of Mendel's laws in 1901 by Correns, Tschernak and DeVries, genetic analyses have greatly increased our understanding of the basic principles of plant biology. Starting with traits that could be screened very easily, including flower color and structural characters, both the methods of analysis and the genetic strategies were constantly refined, finally leading to the complete analysis of a plant genome in the Arabidopsis sequencing project. A molecular analysis alone rarely identifies the function of a given DNA sequence without the proper genetic experiments. Therefore, the classical genetic analysis of a particular trait is often the key step in the analysis of gene structure and function.
The Genetic System of Roses Amongst 150 or more different species of the genus Rosa, the genetic system is not uniform. Ploidy levels can range from the diploid to the octoploid level. Due to the polyploid nature of most cultivated roses, the partial apomictic reproduction in some species of the section Caninae, self-incompatibility and fertility barriers between some species, thorough genetic analyses have been an exception in roses to date. Therefore, information on the inheritance of important rose characters is scarce. The complexity of genetic segregation patterns increases exponentially with the ploidy level of the segregating populations. The simpler cases are found in segregating progeny derived within diploid roses. Nevertheless, genetic analysis is restricted by the self-incompatibility of many diploid species and varieties, which is an obstacle to the use of self-fertilization to create F2 progenies. Thus the alternative “double-pseudo-testcross” strategy is used, in which unrelated parents with a high degree of heterozygosity are crossed with up to four alleles segregating in the progeny. In addition, backcrosses are also possible which will segregate for up to three alleles. In these cases segregation distortion has to be expected, as the presence of self-incompatibility factors similar to the gametophytic self-incompatibility system of Prunus would exclude the S-alleles shared and all alleles linked to them. Another disadvantage to genetic model systems is the small number of seeds produced by most of the diploid species which make the generation of sufficiently large populations very laborious. Furthermore, most diploid species and many diploid hybrids are not recurrent-flowering. This means that backcrosses can often be made only in the second year after sowing the F1 seedlings. The segregation of traits in tetraploids is much more complex than in diploids. Theoretically, up to eight different alleles per locus may segregate in the progeny of crosses between unrelated parents. In contrast to diploids, self-fertilization is possible in many tetraploid genotypes. However, even for characters determined by single dominant genes, much larger populations are required for tetraploids than for diploids to obtain the same genetic resolution (Table 1). Recently the mode of inheritance in segregating populations from crosses between garden roses was analyzed with molecular markers which indicated mainly tetrasomic inheritance although disomic inheritance for some genomic regions could not be excluded. If a particular character is determined by more than one gene and dominance is incomplete, genes have additive effects and a huge number of possible genotypes can be expected in the progeny (Table 2). This tremendous difference between the possible number of genetic combinations in diploids and tetraploids also explains the difficulties of genetic analysis in tetraploids as compared to diploids. A feature independent of the ploidy level was observed in a number of progeny from interspecific crosses. Here, several characters, such as the shape and number of prickles and the presence of glandular trichomes, are not inherited in an intermediate way but are rather inherited only through the female line, i.e., the offspring resemble the phenotype of the maternal plant. In some Table 1 Phenotypic ratios expected for the segregation of single loci in the tetraploid population Mating
Segregation of phenotypes
AAaa selfed Aaaa selfed AAaa Aaaa AAaa aaaa Aaaa aaaa Aa Aa Aa aa
35A: 1a 3A: 1a 11A: 1a 5A: 1a 1A: 1a 3A: 1a 1A: 1a
☆ Change History: January 2016. Thomas Debener updated the Affiliation, Abstract, Table 3, Sections: “The Genetic System of Roses,” “Flower Structure,” “Prickles,” “Flower Color,” “Recurrent Flowering,” “Resistance to Black Spot,” “Resistance to Powdery Mildew,” “Implications for Rose Biology,” and “Further Reading.”
Reference Module in Life Sciences
doi:10.1016/B978-0-12-809633-8.05047-0
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Table 2 Maximum number of different gametes that diploid and tetraploid roses may produce if all loci under consideration are heterozygous and multiallelic (for example, a1a2 for diploids and a1a2a3a4 for tetraploids) Number of loci
1 2 4 8 n
Table 3
Number of different types of gametes In diploids
In tetraploids
2 4 16 256 2n
6 36 1296 1,679,616 6n
Rose characters that were analyzed in genetic experiments
Character
Mode of inheritance
References
Recurrent flowering
Monogenic recessive
Yellow flower color Pink flower color Double flowers
Monogenic dominant Monogenic codominant Monogenic dominant Quantitative Monogenic dominant Quantitative Monogenic recessive Monogenic dominant Monogenic dominant Monogenic dominant
Semeniuk (1971a,b), De Vries and Dubois (1984), Debener (1999), Crespel et al. (2002), Iwata et al. (2012) De Vries and Dubois (1984) Debener (1999), Henz et al. (2015) Debener (1999), Crespel et al. (2002) Oyant et al. (2008), Roman et al. (2015) Debener (1999), Rajapakse et al. (2001) Crespel et al. (2002) Rajapakse et al. (2001) Dubois and De Vries (1987) De Vries and Dubois (1984) von Malek and Debener (1998), Whitaker et al. (2010), Terefe-Ayana et al. (2011) Linde and Debener (2003) Dugo et al. (2005), Yan et al. (2006), Moghaddam et al. (2012) Svejda (1977a,b,1979) Yan et al. (2005, 2007) Wang et al. (2004) Dugo et al. (2005) Dugo et al. (2005) Dugo et al. (2005), Oyant et al. (2008) Cherri-Martin et al. (2007), Spiller et al. (2010) Carvalho et al. (2015) Kawamura et al. (2015)
Prickles on stems Prickles on petioles Dwarf phenotype Moss phenotype Resistance to black spot Resistance to powdery mildew Winter hardiness Vigor Nematode resistance Flower size Leaf size Flowering time Fragrance Stomatal function Plant architecture
Monogenic dominant Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative Quantitative
cases these F1 hybrids are morphologically indistinguishable from their mother and only molecular markers may reveal their hybrid nature. Up to now, the biological basis of this phenomenon is unclear but one may speculate that processes connected to genetic imprinting and selective gene silencing may be involved. The most simple explanation, cytoplasmic inheritance, can largely be excluded because of the large number of characters involved, some of which have been shown to be nuclear-inherited (for example, the presence of prickles) and the observation that these complexes of characters will segregate in later generations. Many speculations about the inheritance of morphological and physiological parameters have been published over the last century. However, most of these were based on observations of very few progeny and, thus, were not amenable to statistical analysis. On the other hand, the knowledge of commercial rose breeders based on decades of experience with genetic crosses and selection within segregating populations probably comprises a large amount of information about the inheritance of particular characters. But this information remains a company secret and is not available to the general public. However, over the last 15 years the availability of molecular markers in roses stimulated many genetic analysis in controlled crosses in both diploid and tetraploid progeny. In the following article, only those characters will be considered which were investigated in controlled crosses and for which the methods of analysis meet the basic requirements for genetic experiments (Table 3).
Inheritance of Structural Characters Structural characters and flower colors are easily observed and, therefore, were the first targets for genetic analysis of rose characters. Many observations have been made on leaf shape, moss character, whole-plant architecture, flower and inflorescence morphology,
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prickles and several other morphological features. However, the modes of inheritance have only been elucidated for flower morphology, moss character, the dwarf phenotype and prickles.
Flower Structure Flower morphology consists of a large number of parameters, including the number and shape of petals, number of stamens, petal size and the number and arrangement of styles and ovaries. Some of these characters, for example, the size of floral organs, seem to be controlled by several genes, whereas single (five petals) versus double (410 petals) was shown to be inherited by a single gene. Wild rose species (with the exception of Rosa sericea and Rosa omeiensis) normally have five petals but a variable number of stamens and styles. In genotypes with double (multipetalled) flowers which have been selected several times during the early history of rose breeding, a certain number of stamens seems to have undergone homeotic transitions to petals, with some intermediate forms between both organ types. This is consistent with other plant species where these homeotic transformations have been observed for a long time. In roses these intermediate organ morphologies are common but the indefinite number of stamens makes it difficult to correlate stamen and petal numbers. However, diploid crosses between double (410 petals) and single (o6 petals) flowered genotypes revealed negative correlations between the number of stamens and petals (Fig. 1) supporting the concept of homeotic transformation. Whether or not this concept is accepted, it has been shown both in large diploid and tetraploid segregating populations that the double-flower phenotype is inherited as a single dominant gene (Fig. 2). In these populations where double flowers are caused by a single dominant gene, the number of petals in double-flowered genotypes displays a large variation, exceeding the values of the parental genotypes (so-called transgressive variation). By means of several marker based QTL analyses it could be shown that, in double flowers, differences between genotypes with respect to the
Fig. 1 Regression curve demonstrating the negative correlation between the number of petals and the number of stamens in a diploid population segregating for a single dominant gene for double flowers and quantitative factors influencing the number of petals. Note that the distribution of stamen numbers for flowers with five petals indicates the variable number of organs.
Fig. 2 Segregation of double flowers and flower color in a diploid population. Parental genotypes¼93/1-117 (pink, single) and 93/1-119 (pink, double), 94/1¼individual plants from the segregating progeny.
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Fig. 3 Segregation of the presence of prickles in a diploid population. Upper row, prickled and unprickled parents. Lower row, segregating progeny. Each group of three canes represents a single plant.
mean number of petals per flower are not only due to environmental conditions but are also modulated by additional genes. These seem to be present in the genetic background of both double- and single-flowered genotypes.
The Moss Phenotype The moss phenotype is characterized by the presence of a dense covering of glandular mossy protuberances on calyx tubes, petals, stems, petioles and pedicels. The character originated in the late 17th century as a sport of the cabbage rose Rosa centifolia L. Crosses between the tetraploid moss roses and tetraploid hybrid teas, originally performed to introduce recurrent flowering into the genetic background of the moss roses, revealed that the moss character is inherited as a single dominant gene.
Prickles As for many other morphological characters of roses, prickles display an enormous variability in shape as well as in quantity and distribution. They are, therefore, used as a key character for the taxonomic distinction of some species and varieties. Several studies have shown that prickles are inherited as a multi gene characteristic. Despite this complex inheritance, genotypes without prickles have been discovered relatively frequently, especially in diploid genotypes. Recent results based on the analysis of diploid segregating populations from crosses between prickled and unprickled plants (Fig. 3) demonstrate the inheritance of prickles on the stems as a single dominant gene at least in these genotypes. As the prickled parental genotypes used for this study represent a very limited gene pool, it cannot be excluded that additional genes may be involved in other genetic backgrounds. Furthermore, genetic analyses conducted in diploid and tetraploid populations indicate that the presence of prickles on the stem and on the petiole are inherited independently.
Dwarf Phenotypes Dwarf phenotypes mainly derived from the species Rosa chinensis minima (Sims) Voss. have been extensively used to breed miniature roses. The ease with which dwarf genotypes have been selected from crosses with diploid and tetraploid plants in the past and the observation that single-gene mutations cause dwarf phenotypes in plant models, such as Arabidopsis thaliana (L.) Heynh. would already imply simple inheritance of dwarfing in roses. Detailed genetic analysis of rose diploid populations indicated that the dwarf character is inherited as monogenic-dominant. Due to the different number of genes found in plant model systems, it cannot be excluded, as for the inheritance of prickles, that mutations in several different genes may lead to dwarf phenotypes.
Inheritance of Physiological Characters Flower Color Rose petals contain a number of different pigments that determine their color. In the 1970s, paper chromatography analyses of tetraploid rose cultivars revealed differences in the amounts of carotenoids, anthocyanidins (pelargonidin, cyanidin) and flavonols (kaempherol, quercetin) and the inheritance of petal color was postulated to be multigenic. However, in addition to several studies indicating quantitative inheritance of color intensity, the inheritance of yellow flower color in tetraploid as well as pink
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flower color in diploid populations was also shown to be controlled by major dominant and codominant genes, respectively (Table 3; Fig. 2). Although the pigment composition of the latter populations may have been very simple, refined methods which distinguish not only general pigment classes but also their various glycosides may resolve even complex petal colorations into simple segregation patterns of individual pigment components.
Recurrent Flowering Recurrent flowering was probably introduced into rose cultivars by introgression from R. chinensis Jaquin and Rosa odorata (Crép.) Rehd. and Wils. in the early 19th century. As it affects the requirement for vernalization of rose shoots to induce flowering and significantly increases the flowering period, it is an extremely important character which greatly influenced modern rose breeding. It is relatively easy to obtain recurrent-flowering progeny from crosses between recurrent and nonrecurrent cultivars. Therefore, theories about the inheritance of this character as a recessive gene date back to the early 1940s and were favoured, for example, by Hurst. But it was only since 1971 that the first clear-cut genetic analysis in diploid Rosa wichurana Crép. crosses demonstrated that a single recessive gene was responsible for the observed variation. Since then, several other studies in both tetraploid and diploid populations confirmed these results. It is assumed that most genes for recurrent flowering were derived from the few original sources. In a breakthrough discovery (Iwata et al., 2012) showed that the major control point between seasonal flowering and recurrent flowering is the TFL1 (Terminal Flower 1) orthologue which in several recurrent flowering mutants is mutated by the insertion of a retrotransposon. However, additional factors influence extend and duration of flowering as well.
Fragrance A specific characteristic of roses important for its commercial value is flower fragrance. In scented varieties fragrance is composed of up to more than one hundred volatiles. Several studies have analyzed genes involved in the biosynthesis of these volatiles, but only a few studies focused on the inheritance of volatiles in controlled crosses. These studies demonstrated that most volatiles segregated as polygenic traits but some also displayed monogenic segregation.
Winter Hardiness Although frequently used in the rose literature, the term “winter hardiness” is difficult to define precisely. The ability of roses to survive winter periods depends not only on the lowest temperatures, including frost tolerance (the ability to survive temperatures below freezing point), but also on the interplay of several other factors. These comprise the length of the acclimation period, humidity, periods of warm temperatures prevailing, frost factors and stress factors, including damage by pathogens and pests. Therefore, analyses of the percentage of winter kill in progeny derived from crosses between winter-hardy and nonhardy parents carried out in Canada in the 1970s displayed a broad variability, indicating an influence of multiple genes. However, estimates of heritability for different populations varied between 51 and 92%, implying the involvement of only a few or several closely linked loci.
Male Sterility In contrast to statements that evidence for an inheritance of male sterility as a single gene had been obtained, no conclusive genetic experiments have been reported. First results were reported in the early 1960s on a population that resulted from a cross between a male sterile genotype of Rosa setigera Michx. with a male fertile genotype of Rosa brunonii Lindl. About 96% of the 70 plants from the F1 progeny analyzed were male sterile. However, to elucidate the genetic basis of this trait, backcrosses and further crosses between the male sterile line and other genotypes would have been needed. Therefore, the genetic basis of male sterility remains obscure.
Inheritance of Resistance to Pathogens The study of plant resistance to pathogens involves higher levels of complexity than analyses of structural and physiological characters. Apart from genetic variation present in the host plant, the genetic constitution of the pathogen has to be considered as well. As was shown for numerous plant pathogen systems, the particular interaction between host and pathogen is often controlled by matching pairs of genes, following the so called “gene-for-gene” interaction. These gene-for-gene interactions are also termed “vertical resistance,” whereas resistance that is independent of the pathogen genotypes and controlled by many genes with additive effects is often termed “horizontal resistance”. Gene-for-gene interactions have been demonstrated for rose black spot and rose powdery mildew. Different pathogenic races may cause completely different reactions by the host plant and, therefore, polysporous isolates (i.e., mixtures of genetically diverse spores) often lead to host responses caused by several resistance genes simultaneously. As a consequence, genetic analyses focusing on these race-specific vertical resistance genes have to be performed under strictly controlled conditions with defined, genetically uniform strains of the pathogen. Apart from vertical resistance genes,
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quantitative or horizontal resistance genes acting on all pathogenic races may be present as well. This type of resistance is often less effective than vertical resistance in that it does not provide 100% protection against the pathogen but is generally expected to be more stable. It is also more difficult to manipulate in the breeding process because in most cases it is under polygenic control with different contributions of individual genes to the whole level of resistance.
Resistance to Black Spot Disease The first genetic analysis of resistance to rose pathogens was performed for black spot caused by the hemibiotrophic ascomycete Diplocarpon rosae Wolf. Black spot is the most severe fungal disease of field-grown roses, especially in areas with high annual precipitation. Screening of tetraploid as well as diploid populations carrying resistance from Rosa multiflora Thunb. with spores derived from a single conidial isolate revealed the presence of three single dominant genes Rdr1, Rdr2 and Rdr3 (Fig. 4). The data for Rdr1 have been confirmed, with several molecular markers cosegregating with the gene. These markers have been used to isolate and analyze the gene which turned out to be a TIR-NBS-LRR gene from a large gene family. In addition to the vertical race-specific resistance to black spot, horizontal resistance may be present as well. Observations in different laboratories show continuous variation in susceptibility between rose genotypes and even within segregating populations. However, quantitative genetic data on the transmission of partial resistance are not yet available.
Resistance to Powdery Mildew Powdery mildew, caused by the biotrophic ascomycete Podosphaera pannosa (Wallr.:Fr.) de Bary, formerly known as Sphaerotheca pannosa var. rosae, is the most important fungal disease of roses grown in greenhouses and also a serious disease in the field. Several studies on diploid and tetraploid segregating populations screened with single conidial isolates as well as natural inoculum revealed both the presence single major dominant genes as well as quantitative factors. Several of the underlying genes were located on various chromosomal maps constructed for roses by means of molecular markers.
Resistance to Crown Gall Disease The spread of crown gall disease, caused by Agrobacterium tumefaciens, is a serious problem in nursery stocks of southern European countries. Therefore, first analyses concerning the degree of susceptibility were made in a collection of 28 different genotypes and pronounced differences in susceptibility were found for some of the genotypes. However, no segregating progeny was analyzed and, therefore, no conclusions can be drawn concerning the inheritance of this character.
Implications for Rose Biology Even the limited amount of information about the inheritance of rose characters is an important first step for the understanding of biological functions. One example is the analysis of disease resistance showing that rose genes for black spot and powdery mildew resistance (both pathogens are obligate parasites) follow the scheme of the so-called gene-for-gene interactions. The
Fig. 4 Genotypes from a diploid population segregating for black spot resistance. Left, susceptible genotype displaying the typical black spot symptoms, like black spots and chlorosis. Right, resistant genotype without visible macroscopic symptoms. All plants were inoculated with spores from the single conidial Diplocarpon rosae isolate Dort E4, representing black spot race no. 5, at a density of 105 conidia mL1, and incubated for 10 days.
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demonstration of single-gene segregation has important implications for both the biology of the rose–pathogen interactions and future breeding strategies. Furthermore, this genetic information is the prerequisite for further analyses of the characters under investigation. For the rose disease resistance genes, for example, efforts to isolate and analyze the DNA sequences rely on the original genetic data. Another example are the genes known to influence the number of petals. The present data suggest that, apart from main switches deciding about double and single flowers, additional regulators determine the number of petals in double flowers. Utilizing the information about flower development in model plant species with several of the regulatory genes already cloned and analyzed, the information available for roses may be used to unravel the regulation of flower development in roses down to the molecular level. This approach would rely on the homology of the main regulatory networks, as demonstrated in comparative analysis between Arabidopsis, Antirrhinum and several other plant species. Another aspect under which genetic data from roses may facilitate structural and functional analyses of important genes is the concept of synteny. Synteny describes a conservation of gene order on chromosomal segments of different species from the same genus and even between different families. As genome sequences of Prunus, Fragaria, Malus and other rosaceous species are available and more to come, this information may soon help to detect and isolate a number of rose genes as well. Several initiatives are also working on a rose genome sequence and along with new sequencing techniques that allow complete transcriptome analysis this will speed up the identification of gene function in roses significantly.
Implications for Rose Breeding Rose breeding has mainly relied on very simple strategies. In order to develop more targeted approaches, information about the inheritance of the key traits is indispensable. This is of particular importance in cases where genes have to be introgressed from wild species to highly developed varieties via wide crosses. As an example, the mode of inheritance of a particular resistance gene is important to calculate the minimum population size necessary for obtaining progeny with both resistance and the appropriate combination of morphological characters. The more characters that are known in respect to their genetic basis, the more precise strategies considering the number of progeny and the number of generations can be developed. For traits that are difficult to screen, marker-assisted selection may be an alternative to the selection for the trait itself. Here again, markers can only be developed in populations segregating for a particular trait and in which precise knowledge about the inheritance is available.
Conclusions Our knowledge about the inheritance of important rose characters is still limited if compared to well-investigated plant species. However, the availability of diploid populations which have been used to analyze several important traits will increase the speed with which we can obtain more genetic information in the near future. In this process a genetic analysis will often remain a first necessary step which, often in connection with molecular methods, will lead to new insights into biological processes. Due to several unique characters of roses that cannot be analyzed in any model plant, detailed genetic analyses will remain indispensable over the next years. Apart from broadening our knowledge about principles of rose biology, information on the inheritance of key characters will be the prerequisite for the development of more advanced breeding strategies.
References Debener, T., 1999. Genetic analyses of important morphological and physiological characters in diploid roses. Gartenbauwissenschaft 64, 14–20. Carvalho, D.R.A., Koning-Boucoiran, C.F.S., Fanourakis, D., et al., 2015. QTL analysis for stomatal functioning in tetraploid Rosa x hybrida grown at high relative air humidity and its implications on postharvest longevity. Molecular Breeding 35, 172. Cherri-Martin, M., Julien, F., Heizmann, P., et al., 2007. Fragrance heritability in hybrid tea roses. Scientia Horticulturae 113, 177–181. Crespel, L., Chirollet, M., Durel, C.E., et al., 2002. Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theoretical and Applied Genetics 105, 1207–1214. De Vries, D.P., Dubois, L.A.M., 1984. Inheritance of the recurrent flowering and moss characters in F1 and F2 hybrid Tea Rosa centifolia muscosa (Aiton) seringe populations. Gartenbauwissenschaften 49, 97–100. Dubois, L.A.M., De Vries, D.P., 1987. On the inheritance of the dwarf character in Polyantha Rosa chinensis minima (Sims) Voss F1 populations. Euphytica 36, 535–539. Dugo, M.L., Satovic, Z., Millan, T., et al., 2005. Genetic mapping of QTLs controlling horticultural traits in diploid roses. Theoretical and Applied Genetics 111, 511–520. Henz, A., Debener, T., Linde, M., 2015. Identification of major stable QTLs for flower color in roses. Molecular Breeding 35. doi:10.1007/s11032-015-0382-6. Hibrand-Saint Oyant, L., Crespel, L., Rajapakse, S., et al., 2008. Genetic linkage maps of rose constructed with new microsatellite markers and locating QTL controlling flowering traits. Tree Genetics & Genomes 4, 11–23. Iwata, H., Gaston, A., Remay, A., et al., 2012. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant Journal 69, 116–125. Kawamura, K., Hibrand-Saint Oyant, L., Thouroude, T., et al., 2015. Inheritance of garden rose architecture and its association with flowering behavior. Tree Genetics & Genomes 11. Linde, M., Debener, T., 2003. Isolation and identification of eight races of powdery mildew of roses Podosphaera pannosa (Wallr.: Fr.) de Bary and the genetic analysis of the resistance gene Rppl. Theoretical and Applied Genetics 107, 256–262. Moghaddam, H.H., Leus, L., Riek, J., et al., 2012. Construction of a genetic linkage map with SSR, AFLP and morphological markers to locate QTLs controlling pathotypespecific powdery mildew resistance in diploid roses. Euphytica 184, 413–427.
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Rajapakse, S., Byrne, D., Zhang, L., et al., 2001. Two genetic linkage maps of tetraploid roses. Theoretical and Applied Genetics 103, 575–583. Roman, H., Rapicault, M., Miclot, A.S., et al., 2015. Genetic analysis of the flowering date and number of petals in rose. Tree Genetics & Genomes 11. Semeniuk, P., 1971a. Inheritance of recurrent blooming in R. wichuraiana. Journal of Heredity 62, 203–204. Semeniuk, P., 1971b. Inheritance of recurrent and non-recurrent blooming in “Goldilocks” Rosa wichuraiana progeny. Journal of Heredity 62, 319–320. Terefe-Ayana, T., Yasmin, A., Le, T.L., et al., 2011. Mining disease resistance genes in roses: Functional and molecular characterisation of the Rdr1 locus. Frontiers in Plant Biology 2, 35. doi:10.3389/fpls.2011.00035. Spiller, M., Berger, R.G., Debener, T., 2010. Genetic dissection of scent metabolic profiles in diploid rose populations. Theoretical and Applied Genetics 120, 1461–1471. doi:10.1007/s00122-010-1268-y. Svejda, F., 1977a. Breeding for improvement of flowering attributes of winterhardy Rosa rugosa hybrids. Euphytica 26, 697–701. Svejda, F., 1977b. Breeding for improvement of flowering attributes of winterhardy Rosa kordesii Wulf hybrids. Euphytica 26, 703–708. Svejda, F., 1979. Inheritance of winterhardiness in roses. Euphytica 28, 309–314. von Malek, B., Debener, T., 1998. Genetic analysis of resistance to blackspot (Diplocarpon rosae) in tetraploid roses. Theoretical and Applied Genetics 96, 228–231. Wang, X., Jacob, Y., Mastrantuono, S., et al., 2004. Spectrum and inheritance of resistance to the root-knot nematode Meloidogyne hapla in Rosa multiflora and R. indica. Plant Breeding 123, 79–83. doi:10.1046/j.0179-9541.2003.00930.x. Whitaker, V.M., Bradeen, J.M., Debener, T., et al., 2010. Rdr3, a novel locus conferring black spot disease resistance in tetraploid rose: Genetic analysis, LRR profiling, and SCAR marker development. Theoretical and Applied Genetics 120, 573–585. Yan, Z., Dolstra, O., Hendriks, T., et al., 2005. Vigor evaluation for genetics and breeding in rose. Euphytica 145, 339–347. Yan, Z., Dolstra, O., Prins, T., et al., 2006. Assessment of partial resistance to powdery mildew (Podosphaera pannosa) in a tetraploid rose population using a sporesuspension inoculation method. European Journal of Plant Pathology 114, 301–308. Yan, Z., Visser, P., Hendriks, T., et al., 2007. QTL: Analysis of variation for vigor in rose. Euphytica 154, 53–62.
Further Reading Debener, T., 1999. Genetic analyses of important morphological and physiological characters in diploid roses. Gartenbauwissenschaft 64, 14–20. De Vries, D.P., Dubois, L.A.M., 1996. Rose breeding: Past, present, prospects. Acta Horticulturae 424, 241–248. Gudin, S., 2000. Rose: Genetics and breeding plant. Breeding Reviews 17, 159–189. Iwata, H., Gaston, A., Remay, A., et al., 2012. The TFL1 homolog KSN is a regulator of continuous flowering in rose and strawberry. Plant Journal 69, 116–125. Krüssmann, G., 1974. Rosen, Rosen, Rosen. Berlin: Verlag Paul Parey. Lindstrom, E.W., 1936. Genetics of polyploidy. Botanical Review 2, 197–215.