Volume 27, 2020
|Number of page(s)||12|
|Published online||23 September 2020|
Validated markers for sunflower (Helianthus annuus L.) breeding
Marqueurs validés pour la sélection du tournesol (Helianthus annuus L.)
Department of Plant Breeding and Genetics, College of Agriculture, University of Sargodha-Pakistan,
2 USDA ARS Corn Host Plant Research, Resistance Unit, Mississippi, Mississippi State, USA
* Corresponding author: firstname.lastname@example.org
Accepted: 13 August 2020
Sunflower is native to North America and is now grown around the world for edible oil, seed roasting, confectionary products and bird food. Genetic diversity in cultivated and wild germplasm is characterized for use with various breeding objectives. Molecular markers have been developed to facilitate sunflower breeding. This review was undertaken to discuss molecular markers, which have been validated in different genetic backgrounds for traits of economic interest in sunflower. Markers found to be linked to monogenic traits in mapping populations may be used to select plants with those traits; review of the literature identified markers available for several monogenic traits including resistance against pests and pathogens. Markers linked to Quantitative Trait Loci (QTL) for many disease resistance and economically important traits that have also been identified in specific populations and target environments are also reported here. These identified linked markers should be validated in different genetic backgrounds and environments to ensure widespread utility. Publicly available inbred lines carrying traits of interest and validated markers related to them are summarized in this review, which also highlights traits for which these resources are still lacking, possibly due to lack of funding despite the importance of this hybrid crop. Genomic sequence data is now available for sunflower, which must now be exploited to develop new SNP based markers linked to genes of interest to mine allelic diversity related to economically important traits, especially traits well studied in other organisms, such as seed oil content and resistance genes.
Le tournesol est originaire d’Amérique du Nord et est maintenant cultivé dans le monde entier comme source d’huile alimentaire, pour la torréfaction de ses graines, les tournesols de bouche et les aliments pour oiseaux. La diversité génétique du matériel végétal cultivé et sauvage a été caractérisée pour être utilisée à des fins de sélection diverses. Des marqueurs moléculaires ont été développés pour faciliter la sélection du tournesol. Cet article a pour objectif de discuter des marqueurs moléculaires qui ont été validés dans différents contextes génétiques pour les caractères d’intérêt économique du tournesol. Les marqueurs qui se sont avérés liés à des traits monogéniques dans les populations de cartographie peuvent être utilisés pour sélectionner des plantes présentant ces traits ; l’examen de la littérature a permis d’identifier les marqueurs disponibles pour plusieurs traits monogéniques, notamment la résistance aux parasites et aux agents pathogènes. Les marqueurs liés à des locus de caractères quantitatifs (QTL pour quantitative trait loci) pour de nombreuses résistances aux maladies et des caractères économiquement importants qui ont également été identifiés dans des populations spécifiques et des environnements cibles sont également mentionnés. Ces marqueurs liés identifiés doivent être validés dans différents contextes et environnements génétiques pour garantir une utilité généralisée. Les lignées consanguines disponibles de manière publique portant des traits d’intérêt et les marqueurs validés qui leur sont liés sont résumés dans cette revue, qui met également en évidence les traits pour lesquels ces ressources font encore défaut, peut-être en raison d’un manque de financement malgré l’importance de cette culture hybride. Les données de séquences génomiques sont maintenant disponibles pour le tournesol, qui doivent maintenant être exploitées pour développer de nouveaux marqueurs basés sur des SNP liés aux gènes d’intérêt pour exploiter la diversité allélique liée aux caractères économiquement importants, en particulier les caractères bien étudiés dans d’autres organismes, tels que la teneur en huile de graines et les gènes de résistance.
Key words: QTL / disease resistance / gene pyramiding / single nucleotide polymorphism / introgression
Mots clés : QTL / résistance aux maladies / pyramide des gènes / polymorphisme d’un seul nucléotide / introgression
© S. Rauf et al., Hosted by EDP Sciences, 2020
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Sunflower is an important oilseed or confectionary crop consumed by a large percentage of the world’s people. It is ranked as the fourth most popular oilseed crop after palm, soybean and rapeseed (FAOSTAT, 2016), and supplies 10% of the total edible oil produced in the world (FAOSTAT, 2018). Sunflower oil is a rich source of linoleic acid, which is excellent for human health. Its oil contains about 90% fatty acids, 9% phytosterols and 1% vitamin E, which is known to reduce low density lipids, improve immunity and helps to protect against cardiovascular disease (Staughton, 2019). The plant is native to eastern North America, with some evidence also supporting domestication in Mexico (Harter et al., 2004). Wild sunflower is spread across the entire United States, Northern Canada and the Trans-Mexican Volcanic Belt. It was used as a food source and for curing of diseases and wounds by Native Americans. Spanish travelers brought this crop to Europe where it was adapted as an ornamental plant.
The real potential of sunflower as a crop was not realized until it reached Russia (the former Soviet Union). V.S. Pustovoit used half seed reserve selection methods for the improvement of oil content in achenes. He was able to improve oil content from 30 to 40% from 1935 to 1944 with further improvement to 54% in the next decade (Kaya et al., 2012). High oil content lines from Russia were used as source of breeding material to develop new oilseed varieties in many parts of the world. Another breakthrough in sunflower breeding came with the discovery of cytoplasmic male sterility by Leclercq in Helianthus petiolaris (Leclercq, 1969; 1979), followed by the discovery of fertility restoration by Kinman (1970). This opened a new window for hybrid development, which increased the achene yield potential without sacrificing oil content. Sunflower is now cultivated in more than 70 countries with total oil production of 15.85 million tons. World average production stands at 1700. kg ha−1. Ukraine and Russia are the major growers of sunflower, and collectively produced 47% of the world production (FAOSTAT, 2016).
Sunflower breeding has been facilitated by the use of markers (Dimitrijevic and Horn, 2018). Good markers are highly polymorphic, generally co-dominant, have a strong linkage with the trait of interest, measurable at all growth stages, and phenotypically neutral. Many studies in sunflower have documented the importance of markers in marker-assisted selection (MAS), estimation of genetic diversity (Mandel et al., 2011), identification of inbred lines in heterosis breeding (Yue et al., 2007) and understanding heterotic patterns (Iqbal et al., 2010). Markers potentially suitable for MAS have been identified via Quantitative Trait Loci (QTL) mapping of economically important traits including yield and oil content (Abdi et al., 2012; Bert et al., 2004; Mokrani et al., 2002; León et al., 2003; Yu et al., 2003); disease resistance including head and stalk rot (Micic et al., 2005a), downy mildew (Brahm and Friedt, 2000; Liu et al., 2012a) and rust (Talukder et al., 2014); nutritional quality such as high oleic acid level (Schuppert et al., 2006; Dimitrijević et al., 2017), β-tocopherol content (Vera-Ruiz et al., 2006), and γ-tocopherol content (García-Moreno et al., 2006); herbicide resistance (Bulos et al., 2013b); Orobanche resistance (Lu et al., 2000; Iuoras et al., 2004); and selection of cytoplasmic male sterility (Schnabel et al., 2008), nuclear male sterility (Chen et al., 2006) or fertility restorer sources (Horn et al., 2003; Yue et al., 2010; Liu et al., 2012b). Many of these traits are discussed below.
Mapped markers included amplified fragment length polymorphism (AFLP), single nucleotide polymorphism (SNP), cleaved amplified polymorphism (CAP), simple sequence repeat (SSR), and sequence characterized amplified region (SCAR). Markers mapped within or very tightly linked to monogenic traits may be directly useful for MAS in multiple genetic backgrounds. However, markers identified linked to quantitative traits in specific populations (i.e., mapping populations of F2:3, RILs or doubled haploids), should be validated in other genetic backgrounds and possibly other environments before use. Moreover, markers should only be used to move resistance genes from the same donor source they were originally mapped, or from any line derived from that same source (Lande and Thompson, 1990). The linkage between the good allele of a marker and the good allele of a gene only works in the mapped or derived lines, except for perfect markers, which are completely linked to the actual causal mutation. Genotyping by sequence (GBS) has allowed large-scale of identification of SNP based diversity within genomes, which may be used to mine resistance genes, and identified SNP markers may be validated in other populations (Celik et al., 2016). This review will consolidate information about mapped and validated sunflower markers in the sections below, which will be a useful resource in the genetic improvement of sunflower.
Rust diseases are caused by the fungus Puccinia helianthi (Fig. 1A), and are prevalent in many parts of the world including the USA, Australia and South Africa. There are high levels of diversity within rust races; 29 races are endemic to its center of origin in the USA and races 300, 304 and 324 are the most prevalent in this region (Friskop et al., 2015). However, race 777 has been the most virulent, able to infect more than nine differentials (which are sunflower genotypes used to determine the various races of the pathogen, including inbred lines 7350, MC-90, MC-29, P-386, HA-R1, HA-R2, HA-R3, HA-R4, HA-R5; Qi et al., 2011). These differentials have been accepted by the ad hoc committee of the International Sunflower Association in 1987 (and reviewed by Gulya, 2006) as containing diverse rust resistance genes. Development of resistant hybrids is the only economical solution to control the disease without use of fungicides, which are expensive, dangerous for farmers to apply, and potentially hazardous to the environment (Bulos et al., 2013b). Phenotyping of resistance levels to determine presence of the resistant allele of rust resistance genes is difficult and laborious, making the development of molecular markers for selection highly desirable.
More than a dozen rust resistance genes have been identified in various accessions of sunflower, including R1–R5, R11–R13, R13a, R13b, R14, R15, Radv, RP1, Pu6, RSx53, and RRD6 (Zhang et al., 2016). The chromosomal locations of all R genes have been reported in a review by Jan et al. (2014) and markers have been developed for all mapped rust resistance genes. The genes for which linked markers have been validated in other populations (R1, R2, R4, R4u, R5, R11, R12, R13a, R13b, and RHAR6) are shown in Table 1, which can be used as a reference of donor lines for resistance breeding programs. Studies have shown that the resistance provided by race specific genes can be overcome by the evolution of the pathogen into new pathotypes. This process can be slowed by the use of breeding lines containing multiple resistance genes to achieve durable resistance. The creation of new inbred parental lines with multiple resistance genes is only possible through gene pyramiding with the help of molecular markers, since once one resistance gene is fixed for the resistant allele, phenotypic selection cannot differentiate lines fixed for a single gene from lines with additional resistance alleles from other genes (Qi and Ma, 2020).
New lines have been developed having multiple resistance genes identified originally in one line each, such as MC29, HA-R2, and HA-R6. These multiply resistant lines (HA-R12 and HA-R13) were developed by the pedigree method and molecular marker assisted selection. HA-R12 contains genes R2 from MC29 (AUS) and R13a from HA-R6. HA-R13 contains R5 from HA-R2 and R13a from HA-R6. Both HA-12 and HA-13 showed high levels of resistance to rust races 336 and 777 (Ma et al., 2016). Sunflower confection lines HA-DM2 (carrying the genes R12 and PlARG) and HA-DM3 (carrying the genes R13a and Pl17) carry rust resistance and downy mildew genes and were developed through pedigree and marker assisted selection (Ma et al., 2019). Gene stacking has been carried out by crossing parents carrying multiple rust resistance genes such as RO18 × MC29 carrying gene pair R18 and R2, and linked markers were used in the segregating generations to select lines with multiple rust resistance genes (Lawson et al., 2003). Similarly, an F2 population originating from HAR2 × MC29 carrying rust resistance genes R5 and R2 were genotyped using molecular markers ORS-316, ORS-630, ORS-333, SFW-00211 and SFW-01272 for the selection of multiple rust resistance genes (according to Tab. 1). Recently, a study showed the successful pyramiding of five rust resistance genes in homozygous condition and in various combinations (PlArg: R4/R12/PlArg, R5/R12/PlArg, R13b/R12/PlArg, R15/R12, and R13b/R15) selected via SSR and SNP markers (Qi and Ma, 2020). Three combinations included rust and downy mildew resistance genes.
(A) Rust symptoms on the underside of a leaf (Dr. Mehdi Ghafferi, Iran), (B) symptoms of downy mildew (photo donated: Dr. Yalcin Kaya, Trakya University, Turkey), (C) Sclerotinia basal stalk rot, (D) Sclerotinnia white mold head rot (Dr. Yalcin Kaya, Trakya University, Turkey) and (E) Orobanche plants within sunflower (Dr. Yalcin Kaya, Trakya University, Turkey).
List of validated markers for rust (Puccinia helianthi) resistance breeding.
Downy mildew (DM) is one of the most destructive diseases of sunflower, caused by an obligate biotroph, which induces damage to sunflower leaves (Fig. 1B). It was first reported in late 1890s in Northeastern US and is now present in all sunflower-producing countries of the world with the exception of Australia (Spring, 2019). It has been known to cause 50% yield losses under artificial inoculation trials (Spring, 2019). A total of 36 Pl resistance genes (R genes), Pl1–Pl35 and PlArg, have been reported in sunflower to date (Qi et al., 2019). However, in the past four decades, a total of 44 P. halstedii races have been identified globally, with the highest diversity of races present in North America and France (Trojanová et al., 2017; Viranyi et al., 2015). Resistance genes induce complete resistance against downy mildew; however, markers have been validated for only a few genes (PlArg, Pl1, Pl2, Pl5, Pl8, Pl16–Pl20, Pl34, and Pl35; Tab. 2). Resistance genes Pl8, Pl35 and PlARG originated from the wild species H. argophyllus. PlARG confers resistance to all races of downy mildew, and Pl35 has been introgressed into cultivated germplasm.
The mapped position of resistance genes were reported by Dimitrijevic and Horn (2018) and Talukder et al. (2019) and are presented in Table 2. MAS and backcrossing were used to develop two resistant confection sunflower lines. HA-DM5 contained Pl19 and HA-DM6 contained Pl35 (Qi et al., 2020). Durable resistance could be achieved by pyramiding two or more genes into a single line using the markers below. SNPs markers were used to develop line with three resistance genes i.e. Pl8, PlARG and R12 in F2 segregating populations from a cross between RHA 340 × RHA 464 (Qi et al., 2017). Dominant makers ORS-1008 and HT-636 were recommended for selection of Pl16 and Pl13 genes, respectively, in their mapping lines as well as new sunflower germplasm (Liu et al., 2012a). Utilization of genomic data and development of SNP markers for DM resistance genes has also been successful following recent studies utilizing the new SNP markers developed for sunflower for GWAS (Pecrix et al., 2018). For instance, resistance genes of two wild and eight domesticated ecotypes of sunflower were mapped on to the sunflower reference genome creating a genotyping array of 49 449 SNPs; this was used to identify 10 resistance genes, (Pecrix et al., 2018).
List of validated markers for downy mildew (Plasmopara halstedii).
Sclerotinia white mold is a major disease of sunflower in temperate areas, causing damage to all parts of the plant including the head (Fig. 1C–D). Resistance to the disease has been found in related wild species but is known to be of polygenic inheritance and was absent in cultivated germplasm until recently (Micic et al., 2005a). However, breeding lines such as HA-BSR1 have been registered, which have high tolerance to Sclerotinia basal stalk mold originating from parents HA 441/RHA 439 (Talukder et al., 2017). Narrow sense heritability ranged between 2–60% for Sclerotinia resistance (Zubrzycki and Maringolo, 2017), indicating the possibility for good gain from selection, and the possibility of identifying genes of major effect on resistance. Gene identification studies using different methods have been successful in this effort. Forty-three candidate genes have been identified through transcript profiling of sunflower and Brassica napus (Fusari et al., 2012). Association mapping showed that candidate gene HaRIC_B caused a 20% reduction in the head rot incidence. Several mapping studies were carried out to identify QTLs linked to Sclerotinia resistance (Davar et al., 2010; Zubrzycki and Maringolo, 2017). However, markers proposed by transcript profiling, association, or linkage mapping have not been validated in independent populations. Polygenic traits are generally affected by genotype × environment interactions so it is also important to validate lines containing proposed markers in different environments as well as different genetic backgrounds (Dimitrijevic and Horn, 2018).
Sunflower wild species H. tuberosus and H. maximiliani are known to carry resistance (Rönicke et al., 2004; Fusari et al., 2012). Breeding line TUB-5-3234 carrying partial resistance was developed from introgression and phenotypic selection. This line was then used to develop molecular markers related to Sclerotinia white mold resistance component traits such as decreased stem lesions, decreased leaf lesions and speed of fungal growth (Micic et al., 2005a). Markers such as ORS-337, ORS-1129 and ORS-588 were mapped to linkage group (LG) 4, LG10 and LG17 and found to be associated with traits related to white mold resistance (Tab. 3). QTLs were also validated in another population originating from the cross NDBLOSsel (partial resistance) × CM625; although these markers may be useful for the selection of white mold resistance, they must be validated in each genetic background the resistance will be moved into. Genome wide association studies developed 20 522 high quality bi-allelic SNPs suitable for use in diverse genetic backgrounds such as inbred lines, hybrids, open pollinated varieties, and landraces. The developed array was found superior to improve the Sclerotinia mid stalk rot resistance when compared with currently available tools for determining genetic diversity for disease resistance (Livaja et al., 2016).
List of validated markers for Sclerotinia sclerotiorum.
Broomrape is a parasitic plant, which causes significant economic damage to sunflower growers around the world, but specifically in Eastern Europe (Kaya, 2014; Fig. 1E). Unlike weeds, parasitic plants directly feed on the sunflower for food and shelter. This causes reduction in leaf area and head diameter, as many of the sunflower’s resources are being taken by the parasite. Various parasitic broomrape races denoted A through H has been characterized, and they differ on the basis of their virulence, with “H” being the most virulent pathotype (Kaya, 2014). Races F–H are the most prevalent in sunflower growing countries. Resistance is monogenic and race specific, and thus could be defeated by the origin of new races (Kaya, 2014). Multiple resistance genes have been identified and are denoted in the Or series (Tab. 4), and each gene induces vertical (race specific) resistance.
Several resistant hybrids have been developed to reduce yield losses due to the parasitic plants through conventional breeding methods of phenotypic screening and selection (Cvejić et al., 2020). The genomic tools may be further exploited to identify resistance genes and subsequent introduction in elite inbred lines, particularly to pyramid resistance and discourage evolution of new virulence types (Cvejić et al., 2020). SSR markers from LG3 showed strong association with various resistance genes i.e. Or2, Or5, and Or6 (Imerovski et al., 2013). The Or5 gene was identified on the telomeric end of LG3 and it was not possible to find flanking markers for this gene. Therefore, MAS was limited to one side of this gene, closer to the centromere, and four primers i.e. CRT-392, CRT-314, ORS-1034 and ORS-1040 were located within a 6.2 to 11.2 cM range (Tang et al., 2003). Primer ORS-683 was closely linked to gene orab-vl-8 with genetic distance of 1.5 cm on LG3 (Molinero-Ruiz et al., 2015). Primers sets such as C12Q1/6895 and C12Q1/6881 were patented by Gao, (2019) to select sunflower genotypes with increased Orobanche resistance (US Patent, No. 15/946,105; Gao et al., 2019). The primers allow selection of the resistant alleles of the OrDEB2 gene. Gene BRS11 was located on linkage group 4 (Hoeft et al., 2011), and the nomenclature of this gene has been changed to ORS11 for the purpose of consistency with identified genes (Martín-Sanz et al., 2020). The gene was linked to SNP marker M-4_30.40 on linkage group 4 (Martín-Sanz et al., 2020).
Markers linked to QTL for Orobanche resistance have also been identified, which explain less of the phenotypic variation for resistance but may be used to increase tolerance. These have been poorly validated in sunflower as compared to disease resistance genes for rust and downy mildew. Genotype-by-sequencing was used to map QTLs related to Orobanche resistance. Two major QTLs or3.1 and or3.2 were identified; or3.1 was mapped near the resistance gene Or5 while Or3.2 was identified for the first time. QTL Or3.1 region later fine-mapped with CAPS markers (Primer sequences presented in supplementary file S1; Imerovski et al., 2019). Exploration of 6.5 MB (31.9 to 38.48 Mb) of genomic sequence on LG3 where resistance QTLs in parental lines were overlapping identified 123 genes including two resistance genes, HanXRQChr03g0065701 and HanXRQChr03g0065841. In exploration of a 3.72 MB genomic region (97.13 and 100.85 Mb), another putative resistance gene HanXRQChr03g0076321 was identified (Imerovski et al., 2019).
List of validated markers for broomrape resistance.
The sunflower crop is protected from weeds generally by spraying pre-emergence and a few post emergence broad leaf herbicides to reduce infestation in the field (Kaya et al., 2012). Therefore, herbicide tolerance is a desirable trait in sunflower breeding to expand the range of herbicides including imidazolinones (IMI) and sulfonylureas (SU) applied to sunflower fields at various growth stages (Sala et al., 2018). Herbicide tolerance was observed in wild populations of sunflower, which survived in commercial fields of corn, soybean and other crops in Kansas and South Dakota, US (Al-Khatib et al., 1998; White et al., 2002). The trait was spontaneously induced in wild sunflower populations repeatedly treated with herbicides, which induced a partial dominant mutation at locus Ahasl1 (acetohydroxyacid synthase). The mutant allele of ahasl1, was subsequently introgressed into elite breeding lines through hybridization and selection.
Subsequently, three alleles were discovered, including AhasIl-1, which confers moderate levels of tolerance against IMI and SU herbicides and contained a C to T mutation in codon 205 (Kolkman et al., 2004); AhasIl-2, which conferred high levels of tolerance to SU and contained a C to T mutation in codon 197; and AhasIl-3, which contained a G to A mutation in codon 122 and showed high levels of resistance to IMI (Kolkman et al., 2004). Herbicide resistance was also induced through treatment of mutagen ethyl methane sulfonate to seeds and subsequent selection with imazapyr herbicide in an M2 population (Sala et al., 2008). A homozygous resistant line (CLHA-PLUS) was developed from the selection in a treated population (Sala et al., 2008). Allele AhasIl-3 or allelic combination of AhasIl-1plus AhasIl-3 was sufficient to exploit the herbicide tolerance in hybrids for IMI resistance in sunflower. Marker assisted selection may help to introgress various variants of the AhasI1 gene into elite breeding lines to exploit the trait in hybrid breeding (Bulos et al., 2013b). The SSR primers p-AHAS18 and p-AHAS19, which were initially developed by Kolkman et al. (2004) were validated and found to be polymorphic in lines carrying the alleles AhasIl-1 and AhasIl-3 (Bulos et al., 2013b). Co-dominant inheritance of these SSRs allowed identification of heterozygous hybrids. Two SNP primers p-AHASNidF and pAHAS122TWT were polymorphic in lines carrying the ahasl1, Ahasl1-1, and Ahasl1-2 alleles while two other primers p-AHASNidF with pAHAS122TMU may be used to amplify Ahasl1-3 (Bulos et al., 2013b; Jacob et al., 2017). SSR primer pair AHAS16 and AHAS17 was originally reported by Kolkman et al. (2004) and were validated to study the size variation for allele Ahasl1-1 in wild germplasm (Jacob et al., 2017).
Development of high oleic acid lines is an important breeding objective for sunflower. Historically, sunflower contains about 18–25% oleic acid (Rauf et al., 2017). Because oleic acid is beneficial to human health, the high oleic acid trait was created through mutation breeding and then introgressed into new hybrids. “Pervenet” breeding lines contain a dominant mutation, which increases oleic acid content to more than 89% in the sunflower oil. Commercial varieties with high oleic acid content are available and now account for up to 4% of the total sunflower oil production, and generally enjoy a premium in price (Rauf et al., 2017). Selection for high oleic acid is expensive and slow due to the laborious gas chromatography and nuclear infrared resonance protocols. The use of molecular markers could greatly facilitate selection in early segregating generations, and only desirable plants would be carried forward into the next generation. Primer sets such as NI-3F/N2-IR have been used successfully to select for the defective version of the A12- desaturase or FAD2-1D gene which causes the accumulation of high levels of high oleic acid in the sunflower seeds. The primers are perfect markers for this trait, because they are completely linked to the causal mutation. This allows genotypes to be selected in all segregating material for which the trait exists and simplifies the use of this trait (Tab. 5).
List of validated markers for the selection of high oleic acid contents.
Sunflower is the second biggest crop after maize cultivated through hybrid seed (Dimitrijevic and Horn, 2018). Commercial hybrid seed production is dependent on cytoplasmic male sterility (CMS) and male fertility restorer (RF) lines. Fertility restorer genes are nuclear based and tend to overcome the cytoplasmic male sterility in the F1 generation. A satisfactory restoration of fertility is necessary for high grain filling percentage. There are more than 70 cytoplasmic male sterility sources developed for sunflower, and some of them have been reviewed by Rauf (2019). These CMS sources can only be exploited with suitable restorer genes. Generally, hybrid sunflower breeding is dependent on the Rf1 gene obtained from line T66006-2-1-B (Kinman, 1970). Diversification of cytoplasmic and fertility restorer genes is major breeding goal to reduce genetic vulnerability to diseases and pathogens. A range of fertility restorer genes (Rf1–Rf7, Rf-PEF1) have been identified from various sources which are compatible with different CMS sources (Talukder et al., 2019). Some of the validated markers to select various RF genes and their assigned linkage group are shown in Table 6.
Validated markers for selection of restorer genes in various populations of sunflower.
Tocopherols are vitamin E active compounds with antioxidant activity and are highly abundant in sunflower oil (Rauf et al., 2017). There are four derivatives (α, β, γ, δ) of fat-soluble tocopherol with vitamin E activity. These tocopherols protect cells as well as oil from oxidative damage, thus prolonging the shelf life of both seed and oil (Rauf et al., 2017). Sunflower seed is predominantly comprised of α-tocopherol; however, substituting the α-tocopherol with γ-tocopherol has improved the shelf life of the oil (García-Moreno et al., 2012).
The selection for oil with modified tocopherols content is expensive and laborious due to the laboratory protocols and the complicated inheritance of interacting loci which encode various tocopherol derivatives (García-Moreno et al., 2012). DNA based markers will provide a cost effective way to select desired oil ratios and levels (Vera-Ruiz et al., 2006). High β-tocopherol content is controlled by recessive alleles at the Tph1 gene. DNA marker based studies showed that three SSR markers (ORS-1093, ORS-222 and ORS-598) on LG1 are tightly linked with Tph1. ORS-716 successfully differentiated the low β-tocopherol genotype (CAS-12) from high β-tocopherol genotypes (i.e., T-589; Vera-Ruiz et al., 2006). Four inbred lines containing high γ-tocopherol content (85%) were developed and reported by García-Moreno et al. (2006). γ-tocopherol content is controlled by recessive alleles at Tph2, which is tightly linked to SSR markers ORS-312 and ORS-599 on LG8 (García-Moreno et al., 2006). The heterozygous recessive genotype tph1tph2 was superior to the homozygous genotype at this locus due to ability to produce both types of β- and γ-tocopherols. A primer combination of γ-TMT-F1/F2/R24 showed polymorphism between two high γ-tocopherols parents i.e. IAST-1 and nmsT2100, concluding that both parents had maximized γ-tocopherols at different loci and were polymorphic in an F2 population created by crossing the two lines. A list of polymorphic validated primer is presented in Table 7.
Validated markers available for tocopherol contents in sunflower.
Sunflower belongs to a highly diverse genus with species that include extremophiles, which may be useful donors of genes to fulfill various sunflower-breeding objectives (Warburton et al., 2017). However, most of the diversity within the germplasm pool is as yet unexplored due to lack activity in the characterization and transfer of valuable genes from related species. Marker assisted selection can overcome drawbacks of phenotypic selection, and MAS for monogenic traits is particularly straightforward. Introgression via MAS can be carefully targeted and include lower linkage drag and allow gene pyramiding, which usually cannot be done through conventional breeding procedures. Today’s breeders are selecting multiple disease resistance genes in segregating populations with markers. Despite these successes, large parts of the genomes and of the collections of cultivated and wild species are as yet uncharacterized and under-utilized due to lack of structural and functional genomic information. The international consortium on sunflower genomics has been able to create a genomic database of 3.6 GB of sequence data available to the public (https://www.ncbi.nlm.nih.gov/assembly/GCF_002127325.1/). This database may help speed the scanning of the sunflower genome to mine resistance genes in sunflower, using information from related species, including model species for which considerably more genetic information is available.
Genomic data has aided in the elucidation of the evolutionary history of sunflower, and the genetic architecture of at least two important traits (flowering time and the metabolism of oil content) is now better understood (Badouin et al., 2017; Bonnafous et al., 2018). Genome sequences of several of breeding lines showed that the cultivated pan genome is comprised of 61 205 genes, and 27% of these genes vary between breeding lines (Hübner et al., 2019). A small percentage (1.5%) of the genes are introgressed from wild species, and majority of these genes induce biotic resistance in sunflower (Hübner et al., 2019). A genetic analysis of male and female lines used in development of sunflower hybrids and compared to open pollinated varieties (OPV) showed male lines had a higher percentage of introgressed genes from wild species than did the females or OPVs. Genetic analysis of male and female lines also revealed differentiation for biotic resistance, which was complementary to provide better resistance in hybrids (Owens et al., 2019).
Oil content is a highly economical but polygenic trait in sunflower. Genome wide association selection was used to identify several genes related to the metabolism of oil in sunflower. Utilization of newly developed SNP marker resources allowed identification of SNP markers for traits of interest, which can speed selection via marker assisted selection or targeted interventions of specific genes using gene editing. Genomic selection has been considered a useful way to increase breeding efficiency of uncharacterized parental lines and could be used as alternative to classical general combining ability analyses and phenotypic population selection, and may be helpful to reduce the labor and cost of phenotypic analysis for economical traits such as oil content (Mangin et al., 2017).
The Sunflower Genome Database (https://sunflowergenome.org/) and the XRQ genome (https://www.heliagene.org/HanXRQ-SUNRISE/) are available on the INRA Sunflower Bioinformatics Resources (https://www.heliagene.org/) and may be used to compare genomic regions of sunflower. Genomic resources regarding sunflower pest such as Orobanche cumana are also available which may provide a genomic insight to this pest, and helps to uncover genomic based diversity within various virulent races of this pest. Genomic resources may be used for expression analysis of genes under stress conditions, pathway and metabolism analysis of economically important traits, and gene sequences that may help finding SNPs linked to genes of interest.
Literature was reviewed and validated markers were sought for various traits in sunflower, and these are consolidated and presented here. Validated markers that are available for diverse monogenic traits including diseases resistance, Orobanche resistance, herbicide tolerance, high oleic acid, high tocopherol content, and fertility restorers were identified. Validated markers were also found to be available for the quantitative traits, Sclerotinia white mold and Orobanche resistance. Lists of all these markers are provided in Tables 1–7. These tables provide information on validated markers that will enable sunflower breeding to characterize, diversify and transfer genes between sunflower inbred lines within cultivated germplasm and from wild species without excessive linkage drag. Highly resistant germplasm is now available containing multiple resistance genes including rust, downy mildew and Sclerotinia white rot; these can be used as donor lines and the markers in Tables 1–7 can be used for marker assisted introgression of the beneficial alleles. Validated molecular markers are also available to modify tocopherol levels and fatty acids, which would help develop specialty sunflower lines at lower cost, and validated markers for fertility restorer genes may help to diversify the fertility restoration sources and may improve the performance of hybrids with better grain filling under various environments. The authors hope that the markers, available in one consolidated review article, will aid sunflower breeders around the world in the improvement of selection gain efficiency for traits of interest. Genome sequence resources are made available online which help to understand the evolution history of sunflower, sequence diversity within germplasm, and mine new genes of economic value. Genome sequencing may also be used to develop new SNP markers tightly linked with targeted traits or genes which could be validated and applied for MAS for improvement of sunflower populations.
The authors declare that they have no conflicts of interest in relation to this article.
This manuscript has not received any specific funding.
The authors would like to thank Drs. Gerald Seiler and Ziv Attia for their thoughtful review of the manuscript. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA that is an equal opportunity employer.
- Abdi N, Darvishzadeh R, Jafari M, et al. 2012. Genetic analysis and QTL mapping of agro-morphological traits in sunflower (Helianthus annuus L) under two contrasting water treatment conditions. Plant Omics 5(2): 149–158. [Google Scholar]
- Al-Khatib K, Baumgartner JR, Peterson DE, et al. 1998. Imazethapyr resistance in common sunflower (Helianthus annuus). Weed Sci 46: 403–407. [CrossRef] [Google Scholar]
- Badouin H, Gouzy J, Grassa CJ, et al. 2017. The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546(7656): 148–152. [Google Scholar]
- Bert PF, Dechamp-Guillaume G, Serre F, et al. 2004. Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L). Theor Appl Genet 109(4): 865–874. [CrossRef] [PubMed] [Google Scholar]
- Bonnafous F, Fievet G, Blanchet N, et al. 2018. Comparison of GWAS models to identify non-additive genetic control of flowering time in sunflower hybrids. Theor Appl Genet 131(2): 319–332. [CrossRef] [PubMed] [Google Scholar]
- Brahm L, Friedt W. 2000. PCR-based markers facilitating marker assisted selection in sunflower for resistance to downy mildew. Crop Sci 40(3): 676–682. [Google Scholar]
- Bulos M, Ramos ML, Altieri E, Sala CA. 2013a. Molecular mapping of a sunflower rust resistance gene from HAR6. Breed Sci 63(1): 141–146. [CrossRef] [PubMed] [Google Scholar]
- Bulos M, Sala CA, Altieri E, et al. 2013b. Marker assisted selection for herbicide resistance in Sunflower. Helia 36(59): 1–16. [CrossRef] [Google Scholar]
- Celik I, Bodur S, Frary A, et al. 2016. Genome-wide SNP discovery and genetic linkage map construction in sunflower (Helianthus annuus L) using a genotyping by sequencing (GBS) approach. Mol Breed 36(9): 133. Available from https://doi.org/10.1007/s11032-016-0558-8. [Google Scholar]
- Chen J, Hu J, Vick BA, et al. 2006. Molecular mapping of a nuclear male-sterility gene in sunflower (Helianthus annuus L) using TRAP and SSR markers. Theor Appl Genet 113(1): 122–127. [CrossRef] [PubMed] [Google Scholar]
- Cvejić S, Radanović A, Dedić B, et al. 2020. Genetic and genomic tools in sunflower breeding for broomrape resistance. Genes 11(2): 152. Available from https://doi.org/10.3390/genes11020152. [Google Scholar]
- Davar R, Darvishzadeh R, Ahmad MAJD, et al. 2010. QTL mapping of partial resistance to basal stem rot in sunflower using recombinant inbred lines. Phytopathol Mediterr 49(3): 330–341. [Google Scholar]
- Dimitrijevic A, Horn R. 2018. Sunflower hybrid breeding: from markers to genomic selection. Front Plant Sci 8: 2238. Available from https://doi.org/10.3389/fpls.2017.02238 [CrossRef] [PubMed] [Google Scholar]
- Dimitrijević A, Imerovski I, Miladinović D, et al. 2017. Oleic acid variation and marker-assisted detection of Pervenets mutation in high-and low-oleic sunflower cross. Crop Breed Appl Biotechnol 17(3): 235–241. [CrossRef] [Google Scholar]
- FAOSTAT. 2016. Statistical division. Rome, Italy: Food and Agriculture Organization of the United Nations. Available from http://www.fao.org/faostat/en/#homedata (retrieved on 12th February, 2020). [Google Scholar]
- FAOSTAT. 2018. Statistical division. Rome, Italy: Food and Agriculture Organization of the United Nations. Available from http://www.fao.org/faostat/en/#homedata (retrieved on 3rd February, 2020). [Google Scholar]
- Feng J, Jan CC. 2008. Introgression and molecular tagging of Rf4, a new male fertility restoration gene from wild sunflower Helianthus maximiliani L. Theor Appl Genet 117(2): 241. Available from https://doi.org/10.1007/s00122-008-0769-4. [CrossRef] [PubMed] [Google Scholar]
- Friskop AJ, Gulya TJ, Harveson RM, et al. 2015. Phenotypic diversity of Puccinia helianthi (sunflower rust) in the United States from 2011 and 2012. Plant Dis 99(11): 1604–1609. [CrossRef] [PubMed] [Google Scholar]
- Fusari CM, Di Rienzo JA, Troglia C, et al. 2012. Association mapping in sunflower for sclerotinia head rot resistance. BMC Plant Biol 12(1): 93. Available from http://www.biomedcentral.com/1471-2229/12/93. [CrossRef] [PubMed] [Google Scholar]
- Gao W, Ripley VL, Aradhya CC, et al. 2019. US Patent Application No. 15/946, 105. Washington, DC: US Patent and Trademark Office. [Google Scholar]
- García-Moreno MJ, Fernández-Martínez JM, Velasco L, et al. 2012. Genetic basis of unstable expression of high gamma-tocopherol content in sunflower seeds. BMC Plant Biol 12(1): 71. Available from http://www.biomedcentral.com/1471-2229/12/71. [CrossRef] [PubMed] [Google Scholar]
- García-Moreno MJ, Vera-Ruiz EM, Fernández-Martínez JM, et al. 2006. Genetic and molecular analysis of high gamma-tocopherol content in sunflower. Crop Sci 46(5): 2015–2021. [Google Scholar]
- Gong L, Hulke BS, Gulya TJ, et al. 2013. Molecular tagging of a novel rust resistance gene R12 in sunflower (Helianthus annuus L). Theor Appl Genet 126(1): 93–99. [CrossRef] [PubMed] [Google Scholar]
- Gulya TJ. 2006. The sunflower rust situation: current races in the northern and central Great Plains, and resistance in oilseed and confection hybrids. In: Proceedings of 28th sunflower research workshop Fargo, ND, pp. 11–12. [Google Scholar]
- Harter AV, Gardner KA, Falush D, et al. 2004. Origin of extant domesticated sunflowers in eastern North America. Nature 430(6996): 201–205. [PubMed] [Google Scholar]
- Hass CG, Tang S, Leonard S, et al. 2006. Three non-allelic epistatically interacting methyltransferase mutations produce novel tocopherol (vitamin E) profiles in sunflower. Theor Appl Genet 113(5): 767–782. [CrossRef] [PubMed] [Google Scholar]
- Hoeft E, Li Z, Tulsieram L. 2011. U.S. Patent No. 7,872,170. Washington, DC: U.S. Patent and Trademark Office. [Google Scholar]
- Horn R, Kusterer B, Lazarescu E, et al. 2003. Molecular mapping of the Rf1 gene restoring pollen fertility in PET1-based F 1 hybrids in sunflower (Helianthus annuus L). Theor Appl Genet 106(4): 599–606. [CrossRef] [PubMed] [Google Scholar]
- Horn R, Radanovic A, Fuhrmann L, et al. 2019. Development and validation of markers for the fertility restorer gene Rf1 in sunflower. Int J Mol Sci 20(6): 1260. Available from https://doi.org/10.3390/ijms20061260. [Google Scholar]
- Hübner S, Bercovich N, Todesco M, et al. 2019. Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nat Plants 5(1): 54–62. [CrossRef] [PubMed] [Google Scholar]
- Imerovski I, Dedić B, Cvejić S, et al. 2019. BSA-seq mapping reveals major QTL for broomrape resistance in four sunflower lines. Mol Breed 39: 41. Available from https://doi.org/10.1007/s11032-019-0948-9. [Google Scholar]
- Imerovski I, Dimitrijevic A, Miladinovic D, et al. 2013. Identification of PCR markers linked to different Or genes in sunflower. Plant Breed 132(1): 115–120. [Google Scholar]
- Imerovski I, Dimitrijevic A, Miladinovic D, et al. 2014. Identification and validation of breeder-friendly DNA markers for Pl arg gene in sunflower. Mol Breed 34(3): 779–788. [Google Scholar]
- Iqbal A, Sadaqat HA, Khan AS, et al. 2010. Identification of sunflower (Helianthus annuus, Asteraceae) hybrids using simple-sequence repeat markers. Genet Mol Res 10(1): 102–106. [Google Scholar]
- Iuoras M, Stanciu D, Ciucã M, et al. 2004. Preliminary studies related to the use of marker assisted selection for resistance to Orobanche cumana Wallr in sunflower. Rom Agric Res 21: 33–37. [Google Scholar]
- Jacob J, Sujatha M, Varaprasad SK. 2017. Screening of cultivated and wild Helianthus species reveals herbicide tolerance in wild sunflowers and allelic variation at Ahasl1 (acetohydroxyacid synthase 1 large subunit) locus. Plant Genet Res 15(5): 421–429. [CrossRef] [Google Scholar]
- Jan CC, Zhang M, Liu Z. 2014. Molecular mapping of the rust resistance gene in sunflower germplasm line PH3. In: Presentation at the National Sunflower Association Research Forum, January 8–9, 2014 Fargo, ND. [Google Scholar]
- Kaya Y, Jocic S, Miladinovic D. 2012. Sunflower. In: Technological innovations in major world oil crops, volume 1. New York, NY: Springer, pp. 85–129. [CrossRef] [Google Scholar]
- Kaya Y. 2014. Current situation of sunflower broomrape around the world. In: Proceedings of the 3rd International Symposium on Broomrape (Orobanche spp.) in Sunflower, pp. 9–18. [Google Scholar]
- Kinman ML. 1970. New development in the USDA and state experiment station sunflower breeding programs. In: Proc 4th Int Sunflower Conf, Memphis, TN, pp. 181–183. [Google Scholar]
- Kolkman JM, Slabaugh MB, Bruniard JM, et al. 2004. Acetohydroxyacid synthase mutations conferring resistance to imidazolinone or sulfonylurea herbicides in sunflower. Theor Appl Genet 109(6): 1147–1159. [CrossRef] [PubMed] [Google Scholar]
- Lande R, Thompson R. 1990. Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124(3): 743–756. [PubMed] [Google Scholar]
- Lawson W, Kong G, Shatte T, et al. 2003. Molecular markers for sunflower rust resistance genes − an update. In: 14th Australian Sunflower Association Conference Proceedings 1–6. [Google Scholar]
- Leclercq P. 1969. Cytoplasmic male sterility in sunflower. Ann Amelior Plant 19: 99–106. [Google Scholar]
- Leclercq P. 1979. Cytoplasmic male sterility in sunflower 2-genetical and environmental effects on fertility restoration. Ann Amelior Plantes 29: 201–212. [Google Scholar]
- León AJ, Andrade FH, Lee M. 2003. Genetic analysis of seed-oil concentration across generations and environments in sunflower. Crop Sci 43(1): 135–140. [Google Scholar]
- Liu Z, Gulya TJ, Seiler GJ, et al. 2012a. Molecular mapping of the Pl16 downy mildew resistance gene from HA-R4 to facilitate marker-assisted selection in sunflower. Theor Appl Genet 125(1): 121–131. [CrossRef] [PubMed] [Google Scholar]
- Liu Z, Mulpuri S, Feng J, et al. 2012b. Molecular mapping of the Rf3 fertility restoration gene to facilitate its utilization in breeding confection sunflower. Mol Breed 29(2): 275–284. [Google Scholar]
- Liu Z, Wang D, Feng J, et al. 2013. Diversifying sunflower germplasm by integration and mapping of a novel male fertility restoration gene. Genetics 112. Available from https://doi.org/10.1534/genetics.112.146092. [Google Scholar]
- Livaja M, Unterseer S, Erath W, et al. 2016. Diversity analysis and genomic prediction of Sclerotinia resistance in sunflower using a new 25 K SNP genotyping array. Theor Appl Genet 129(2): 317–329. [CrossRef] [PubMed] [Google Scholar]
- Lu YH, Melero-Vara JM, García-Tejada JA, et al. 2000. Development of SCAR markers linked to the gene Or5 conferring resistance to broomrape (Orobanche cumana Wallr) in sunflower. Theor Appl Genet 100(3–4): 625–632. [Google Scholar]
- Ma GJ, Markell SG, Song QJ, et al. 2017. Genotyping-by-sequencing targeting of a novel downy mildew resistance gene Pl 20 from wild Helianthus argophyllus for sunflower (Helianthus annuus L). Theor Appl Genet 130(7): 1519–1529. [CrossRef] [PubMed] [Google Scholar]
- Ma GJ, Seiler GJ, Markell SG, et al. 2016. Registration of two double rust resistant germplasms, HA-R12 and HA-R13 for confection sunflower. J Plant Reg 10(1): 69–74. [CrossRef] [Google Scholar]
- Ma GJ, Seiler GJ, Markell SG, et al. 2019. Registration of three confection sunflower germplasm, HA-DM2, HA-DM3, and HA-DM4, resistant to downy mildew and rust. J Plant Reg 13(1): 103–108. [CrossRef] [Google Scholar]
- Ma GJ, Song QJ, Markell SG, et al. 2018. High-throughput genotyping-by-sequencing facilitates molecular tagging of a novel rust resistance gene, R 15, in sunflower (Helianthus annuus L). Theor Appl Genet 131(7): 1423–1432. [CrossRef] [PubMed] [Google Scholar]
- Mandel JR, Dechaine JM, Marek LF, et al. 2011. Genetic diversity and population structure in cultivated sunflower and a comparison to its wild progenitor, Helianthus annuus L. Theor Appl Genet 123(5): 693–704. [CrossRef] [PubMed] [Google Scholar]
- Mangin B, Bonnafous F, Blanchet N, et al. 2017. Genomic prediction of sunflower hybrids oil content. Front Plant Sci 8: 1633. Available from https://doi.org/10.3389/fpls.2017.01633. [CrossRef] [PubMed] [Google Scholar]
- Markin N, Usatov A, Makarenko M, et al. 2017. Study of informative DNA markers of the Rf1 gene in sunflower for breeding practice. Czech J Genet Plant Breed 53:69–75. [CrossRef] [Google Scholar]
- Martín-Sanz A, Pérez-Vich B, Rueda S, et al. 2020. Characterization of post-haustorial resistance to sunflower broomrape. Crop Sci 60(3): 1188–1198. [Google Scholar]
- Micic Z, Hahn V, Bauer E, et al. 2005a. Identification and validation of QTL for Sclerotinia midstalk rot resistance in sunflower by selective genotyping. Theor Appl Genet 111(2): 233–242. [CrossRef] [PubMed] [Google Scholar]
- Micic Z, Hahn V, Bauer E, et al. 2005b. QTL mapping of resistance to Sclerotinia midstalk rot in RIL of sunflower population NDBLOS sel × CM625. Theor Appl Genet 110(8): 1490–1498. [CrossRef] [PubMed] [Google Scholar]
- Mirzahosein-Tabrizi M. 2017. Identification of downy mildew resistance loci in sunflower germplasm. Not Sci Biol 9(4): 515–519. [CrossRef] [Google Scholar]
- Mokrani L, Gentzbittel L, Azanza F, et al. 2002. Mapping and analysis of quantitative trait loci for grain oil content and agronomic traits using AFLP and SSR in sunflower (Helianthus annuus L). Theor Appl Genet 106(1): 149–156. [CrossRef] [PubMed] [Google Scholar]
- Molinero-Ruiz L, Delavault P, Pérez-Vich B, et al. 2015. History of the race structure of Orobanche cumana and the breeding of sunflower for resistance to this parasitic weed: a review. Span J Agric Res 13: e10R01. [CrossRef] [Google Scholar]
- Nagarathna TK, Shadakshari YG, Ramanappa TM, 2011. Molecular analysis of sunflower (Helianthus annuus L) genotypes for high oleic acid using microsatellite markers. Helia 34(55): 63–68. [CrossRef] [Google Scholar]
- Najafabadi MS, Abedini R, Eskandari H, et al. 2015. Monitoring three Plasmopara halstedii resistance genes in Iranian sunflower inbred lines. Iran J Biotech 13(2): 45 e1047. [Google Scholar]
- Owens GL, Baute GJ, Hubner S, et al. 2019. Genomic sequence and copy-number evolution during hybrid crop development in sunflowers. Evol Appl 12: 54–65. [CrossRef] [PubMed] [Google Scholar]
- Pecrix Y, Penouilh-Suzette C, Muños S, et al. 2018. Ten broad spectrum resistances to downy mildew physically mapped on the sunflower genome. Front Plant Sci 9: 1780. Available from https://doi.org/10.3389/fpls.2018.01780. [CrossRef] [PubMed] [Google Scholar]
- Premnath A, Narayana M, Ramakrishnan C, et al. 2016. Mapping quantitative trait loci controlling oil content, oleic acid and linoleic acid content in sunflower (Helianthus annuus L). Mol Breed 36(7): 106. Available from https://doi.org/10.1007/s11032-016-0527-2. [Google Scholar]
- Qi L, Gulya T, Seiler GJ, et al. 2011. Identification of resistance to new virulent races of rust in sunflowers and validation of DNA markers in the gene pool. Phytopathology 101(2): 241–249. [CrossRef] [PubMed] [Google Scholar]
- Qi L, Ma G. 2020. Marker-assisted gene pyramiding and the reliability of using SNP markers located in the recombination suppressed regions of sunflower (Helianthus annuus L.). Genes 11(1): 10. Available from https://doi.org/10.3390/genes11010010. [Google Scholar]
- Qi LL, Foley ME, Cai XW, et al. 2016. Genetics and mapping of a novel downy mildew resistance gene, Pl 18, introgressed from wild Helianthus argophyllus into cultivated sunflower (Helianthus annuus L). Theor Appl Genet 129(4): 741–752. [CrossRef] [PubMed] [Google Scholar]
- Qi LL, Long YM, Jan CC, et al. 2015a. Pl17 is a novel gene independent of known downy mildew resistance genes in the cultivated sunflower (Helianthus annuus L). Theor Appl Genet 128: 757–767. [CrossRef] [PubMed] [Google Scholar]
- Qi LL, Ma GJ, Li XH, et al. 2019. Diversification of the downy mildew resistance gene pool by introgression of a new gene, Pl35, from wild Helianthus argophyllus into oilseed and confection sunflowers (Helianthus annuus L). Theor Appl Genet 132(9): 2553–2565. [CrossRef] [PubMed] [Google Scholar]
- Qi LL, Ma GJ, Long YM, et al. 2015b. Relocation of a rust resistance gene R2 and its marker-assisted gene pyramiding in confection sunflower (Helianthus annuus L). Theor Appl Genet 128(3): 477–488. [CrossRef] [PubMed] [Google Scholar]
- Qi LL, Ma GJ, Seiler GJ. 2020. Registration of two confection sunflower germplasms, HA-DM5 and HA-DM6, resistant to sunflower downy mildew. J Plant Reg 14(1): 87–91. [CrossRef] [Google Scholar]
- Qi LL, Seiler GJ, Vick BA, et al. 2012. Genetics and mapping of the R11 gene conferring resistance to recently emerged rust races, tightly linked to male fertility restoration, in sunflower (Helianthus annuus L). Theor Appl Genet 125(5): 921–932. [CrossRef] [PubMed] [Google Scholar]
- Qi LL, Talukder ZI, Hulke BS, et al. 2017. Development and dissection of diagnostic SNP markers for the downy mildew resistance genes Pl Arg and Pl 8 and maker-assisted gene pyramiding in sunflower (Helianthus annuus L). Mol Genet Genom 292(3): 551–563. [CrossRef] [Google Scholar]
- Rauf S, Jamil N, Tariq SA, et al. 2017. Progress in modification of sunflower oil to expand its industrial value. J Sci Food Agric 97: 1997–2006. [CrossRef] [PubMed] [Google Scholar]
- Rauf S. 2019. Breeding strategies for sunflower (Helianthus annuus L.) genetic improvement. In: Advances in plant breeding strategies: industrial and food crops. Springer, Cham, pp. 637–673. [CrossRef] [Google Scholar]
- Rönicke S, Hahn V, Horn R, et al. 2004. Interspecific hybrids of sunflower as a source of Sclerotinia resistance. Plant Breed 123(2): 152–157. [Google Scholar]
- Sala C, Bulos M, Whitt SR, et al. 2018. US Patent No. 10, 017, 827. Washington, DC: US Patent and Trademark Office. [Google Scholar]
- Sala CA, Bulos M, Echarte AM. 2008. Genetic analysis of an induced mutation conferring imidazolinone resistance in sunflower. Crop Sci 48(5): 1817–1822. [Google Scholar]
- Schnabel U, Engelmann U, Horn R. 2008. Development of markers for the use of the PEF1 cytoplasm in sunflower hybrid breeding. Plant Breed 127(6): 587–591. [Google Scholar]
- Schuppert GF, Tang S, Slabaugh MB, et al. (2006) The sunflower high-oleic mutant Ol carries variable tandem repeats of FAD2-1, a seed-specific oleoyl-phosphatidyl choline desaturase. Mol Breed 17(3): 241–256. [Google Scholar]
- Solodenko A. 2018. Validation of microsatellite markers of Pl resistance genes to downy mildew of sunflower. Helia 41(68): 73–82. [CrossRef] [Google Scholar]
- Spring O. 2019. Spreading and global pathogenic diversity of sunflower downy mildew − Review. Plant Protect Sci 55(3): 149–158. [CrossRef] [Google Scholar]
- Staughton J. 2019. The amazing benefits of sunflower oil. Oilseeds Focus 5(2): 40–41. [Google Scholar]
- Talukder Z, Ma G, Hulke B, et al. 2019. Linkage mapping and genome-wide association studies of the Rf gene cluster in sunflower (Helianthus annuus L) and their distribution in world sunflower collections. Front Genet 10: 216. Available from https://doi.org/10.3389/fgene.2019.00216. [CrossRef] [PubMed] [Google Scholar]
- Talukder ZI, Gong L, Hulke BS, Pegadaraju V, Song Q, Schultz Q, Qi L. 2014. A high-density SNP map of sunflower derived from RAD-sequencing facilitating fine-mapping of the rust resistance gene R12. PLoS One 9(7): e98628. [CrossRef] [PubMed] [Google Scholar]
- Talukder ZI, Hu J, Seiler G J, et al. 2017. Registration of oilseed sunflower germplasm HA-BSR1 highly tolerant to Sclerotinia basal stalk rot. J Plant Regis 11(3): 315–319. [CrossRef] [Google Scholar]
- Tang S, Heesacker A, Kishore VK, et al. 2003. Genetic mapping of the Or5 gene for resistance to Orobanche race E in sunflower. Crop Sci 43(3): 1021–1028. [Google Scholar]
- Tilak IS, [Google Scholar]
- Trojanová Z, Sedlářová M, Gulya TJ, et al. 2017. Methodology of virulence screening and race characterization of Plasmopara halstedii, and resistance evaluation in sunflower: a review. Plant Path 66: 171–185. [CrossRef] [Google Scholar]
- Vera-Ruiz EM, Velasco L, Leon AJ, et al. 2006. Genetic mapping of the Tph1 gene controlling beta-tocopherol accumulation in sunflower seeds. Mol Breed 17(3): 291–296. [Google Scholar]
- Viranyi F, Gulya TJ, Tourieille DL. 2015. Recent changes in the pathogenic variability of Plasmopara halstedii (sunflower downy mildew) populations from different continents. Helia 38: 149–162. [CrossRef] [Google Scholar]
- Warburton ML, Rauf S, Marek L, et al. 2017. The use of crop wild relatives in maize and sunflower breeding. Crop Sci 57(3): 1227–1240. [Google Scholar]
- White AD, Owen MD, Hartzler RG, et al. 2002. Common sunflower resistance to acetolactate-inhibiting herbicides. Weed Sci 50:432–437. [CrossRef] [Google Scholar]
- Yu JK, Tang S, Slabaugh MB, et al. 2003. Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43(1): 367–387. [Google Scholar]
- Yue B, Miller JF, Hu J. 2007. Experimenting with marker assisted selection in confection sunflower germplasm enhancement. In: Proceeding of 29th Sunflower Research Forum. [Google Scholar]
- Yue B, Vick BA, Cai X, et al. 2010. Genetic mapping for the Rf1 (fertility restoration) gene in sunflower (Helianthus annuus L) by SSR and TRAP markers. Plant Breed 129(1): 24–28. [Google Scholar]
- Zhang M, Liu Z, Jan CC. 2016. Molecular mapping of a rust resistance gene R14 in cultivated sunflower line PH 3. Mol Breed 36(3): 32. Available from https://doi.org/10.1007/s11032-016-0456-0. [Google Scholar]
- Zhang ZW, Ma GJ, Zhao J, et al. 2017. Discovery and introgression of the wild sunflower-derived novel downy mildew resistance gene Pl 19 in confection sunflower (Helianthus annuus L.). Theor Appl Genet 130(1): 29–39. [CrossRef] [PubMed] [Google Scholar]
- Zubrzycki JE, Maringolo CA, Filippi CV, et al. 2017. Main and epistatic QTL analyses for Sclerotinia head rot resistance in sunflower. PLoS One 12(12): e0189859. [CrossRef] [PubMed] [Google Scholar]
Cite this article as: Rauf S, Warburton M, Naeem A, Kainat W. 2020. Validated markers for sunflower (Helianthus annuus L.) breeding. OCL 27: 47.
Supplementary Table S1. Supplementary sequence data of primers 5’–3’. (Access here)
(A) Rust symptoms on the underside of a leaf (Dr. Mehdi Ghafferi, Iran), (B) symptoms of downy mildew (photo donated: Dr. Yalcin Kaya, Trakya University, Turkey), (C) Sclerotinia basal stalk rot, (D) Sclerotinnia white mold head rot (Dr. Yalcin Kaya, Trakya University, Turkey) and (E) Orobanche plants within sunflower (Dr. Yalcin Kaya, Trakya University, Turkey).
|In the text|
Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.
Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.
Initial download of the metrics may take a while.