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9 December 2025

Interspecific and Intergeneric Crosses for Clubroot Resistance in Brassica Crops

and
1
Department of Horticultural Crop Breeding, the National Institute of Horticulture Research, Konstytucji 3 Maja 1/3 Str., 96-100 Skierniewice, Poland
2
Library, the National Institute of Horticulture Research, Konstytucji 3 Maja 1/3 Str., 96-100 Skierniewice, Poland
*
Author to whom correspondence should be addressed.
Agronomy2025, 15(12), 2827;https://doi.org/10.3390/agronomy15122827
This article belongs to the Section Crop Breeding and Genetics
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Abstract

Clubroot disease, caused by Plasmodiophora brassicae, is a major global threat, causing severe yield losses of up to 100% in heavily infested fields. Interspecific hybridization is essential for the transfer of clubroot resistance genes among the Brassica species. This review aimed to describe the sources of clubroot resistance, categorize their types in Brassica crops, and identify the most effective techniques and underutilized sources for both intergeneric and interspecific hybridization. A systematic literature review served as the foundation for expert analysis, encompassing a comprehensive list of known sources of resistance and a detailed description of their characteristics, including monogenic, polygenic, dominant, and recessive traits. In addition, this review specifies techniques suitable for gene transfer, such as markers, embryo rescue, somatic hybridization, and CRISPR/Cas. Based on the literature, underutilized directions for genetic crosses have been proposed. These conclusions suggest that combining biotechnological methods, including markers, CRISPR/Cas, and embryo rescue, with intergeneric crosses offers the potential to transfer resistance genes from previously untapped sources.

1. Introduction

1.1. Background

Clubroot disease, caused by the obligate biotrophic protist Plasmodiophora brassicae (P. brassicae), is a major threat to Brassica crops worldwide, including oilseed rape (Brassica napus), cabbage (Brassica oleracea), and Chinese cabbage (Brassica rapa). The disease is characterized by the formation of galls on the roots, which leads to reduced nutrient and water uptake and, ultimately, severe yield losses [1,2,3]. Symptoms of clubroot primarily affect the roots, leading to the development of galls (clubs) in the infected root tissues, which are characterized by abnormal proliferation. Developing galls act as strong metabolic sinks, actively drawing carbohydrates, amino acids, and minerals from the shoots and surrounding healthy roots; this redirected nutrient flow, combined with disruption of vascular tissue, markedly impairs the plant’s ability to transport water and minerals. Consequently, the aboveground portions of afflicted plants exhibit yellowing, wilting, and eventual demise [4].

1.2. Significance

The socioeconomic impact of clubroot is significant as it affects major agricultural commodities. For instance, in regions such as Latin America and Australia, where Brassica crops are extensively cultivated, the disease poses substantial challenges, leading to economic losses and necessitating extensive management efforts [1,5]. In China, Brassicaceae crops suffer yield losses of 20–30% due to this disease [6]. Clubroot can cause up to 100% yield loss in heavily infested fields planted with susceptible canola cultivars [7].

1.3. Challenges in Clubroot Management

Environmental conditions, such as temperature and soil moisture, play crucial roles in the incidence and severity of clubroot, and climate change may exacerbate its spread by creating more favorable conditions for P. brassicae [8].
One of the challenges in managing clubroot disease is the longevity of the resting spores of P. brassicae, which can persist in soil for up to 20 years. This persistence combined with the ability of the pathogen to rapidly evolve and overcome host resistance makes clubroot a particularly challenging disease to control [8,9,10].
So far, there are no chemical control strategies for clubroot in Brassicaceae that can be considered both effective and sustainable. Thus, cultivation of resistant varieties has become the primary approach to prevent the occurrence of clubroot disease.

1.4. Genetic Resistance and Sustainable Solution

Control strategies for clubroot include integrated disease management such as crop rotation, the application of lime to raise soil pH to levels unfavorable for pathogen development, and the use of resistant cultivars. However, managing the disease remains challenging due to the persistence of long-lived resting spores and the substantial genetic diversity of Plasmodiophora brassicae, which results in multiple pathotypes with varying virulence and host specificity [4,10,11,12,13,14,15,16,17].
This variability further complicates control efforts, necessitating the development of broad-spectrum and durable resistance strategies. Genetic differences among regional isolates lead to variation in pathogenicity, underscoring the need for detailed pathotype classification. To better characterize this diversity and improve resistance breeding, several differential systems—including the Williams system, the European Clubroot Differential (ECD) set, the Canadian Clubroot Differential (CCD) set, the Somé et al. set, and the Sinitic Clubroot Differential (SCD) set—enable more precise classification of clubroot populations [18,19,20].
Classical differential-host studies documented distinct pathogenicity patterns among races [21], whereas recent advances, including a telomere-to-telomere genome assembly of strain Pb3A, provide a foundation for dissecting infection mechanisms [22]. Transcriptomic analyses reveal hormone-signaling and defense pathways underlying resistance in Brassica rapa [6,23]. Current research emphasizes developing rapid molecular pathotyping tools to complement phenotypic assays, supporting more precise detection and sustainable management of P. brassicae [24].
Genetic studies of Benoit Landry provided the first evidence that clubroot resistance could be mapped to discrete loci, forming the conceptual foundation for later QTL and marker-based analyses. Current resistance strategies face challenges from rapidly evolving pathotypes, highlighting the need for novel resistance sources. Breeding resistant cultivars, including interspecific and intergeneric crosses, offers a sustainable approach by tapping diverse Brassicaceae genetic resources [4,10,12,17,18,19,20,21,22]. Genetic resistance is more durable and cost-effective than chemical or cultural controls, providing protection without added input costs and avoiding environmental contamination [7,23,24]. Pyramiding multiple resistance genes can better address pathogen diversity, and integrating genetic resistance with other methods enhances overall disease management. Breeding allows incorporation of new resistance genes to keep pace with evolving P. brassicae populations [4,10,17,25,26].

1.5. Role of Wide Hybridization

Wide hybridization—including both interspecific crosses and intergeneric crosses expands the accessible genetic variation by enabling the transfer of agronomically valuable traits from wild relatives or related species [4,27,28,29,30,31,32,33,34,35]. These approaches allow breeders to introgress resistance genes and other beneficial traits into cultivated Brassica crops, strengthening their resilience to pathogens and pests and providing access to resistance sources absent in domesticated germplasm [36,37,38].
In Brassicaceae, interspecific hybridization plays a central role in transferring clubroot resistance genes among Brassica species [26,39,40,41,42,43,44,45]. Successful introgression has improved crop performance while reducing dependence on chemical control measures. Continued exploration of wild relatives and related genera offers the potential to uncover additional resistance sources, supporting further progress in disease management and crop productivity [46,47].
Wide hybridization also enhances the genetic diversity of Brassica species. Genomic consequences such as chromosomal rearrangements, retrotransposon activation, and homeologous recombination contribute to novel genomic configurations that broaden phenotypic variability [48]. This increased diversity facilitates the introduction of stress-tolerance and agronomic traits, overcoming genetic bottlenecks in cultivated forms and supporting long-term crop improvement [49,50].
Despite its value, wide hybridization is constrained by biological barriers that limit fertilization success, embryo development, and hybrid fertility. Post-zygotic incompatibilities—particularly endosperm failure—often cause embryo abortion, making embryo-rescue techniques essential for recovering viable hybrids [17,51]. Early studies demonstrated that intergeneric Brassica × Sinapis hybrids could be obtained only when immature ovules were excised and cultured, greatly improving hybrid survival [52]. Similar approaches enabled introgression of powdery mildew resistance from B. carinata into B. oleracea, confirming that embryos from wide crosses rarely mature without intervention [51]. Beyond embryo recovery, chromosome doubling is critical for stabilizing recombinant genomes. Colchicine treatment of isolated microspores in B. napus can yield doubling efficiencies up to 70%, facilitating the production of doubled haploids that fix introgressed chromosomal segments [53]. Nevertheless, wide hybrids frequently exhibit sterility, aneuploidy, and irregular homeologous pairing, limiting fertility and the efficiency of introgression [54,55,56]. Crossability barriers are often asymmetric, as shown in Brassica × Sinapis crosses, where viable hybrids were obtained mainly when Brassica served as the female parent [52].
Collectively, these studies highlight that embryo and ovule culture, chromosome engineering, amphidiploid formation, and fertility restoration are essential components of successful interspecific and intergeneric hybridization pipelines in Brassicaceae [27,57,58,59].

1.6. Objectives of the Review

This review aims to evaluate the success of interspecific and intergeneric hybridization in developing clubroot-resistant Brassica crops and to identify promising yet underutilized genetic resources and techniques for future breeding efforts.

3. Methods for the Interspecific and Intergeneric Hybridization for Clubroot Resistance

Utilizing new sources of resistance genes from wild Brassica relatives and related species often requires overcoming hybridization barriers and addressing challenges, such as linkage drag. Advanced breeding techniques are crucial for facilitating the introgression of resistance genes from wild relatives into cultivated Brassica crops [10,26,27,64,68,69].

3.1. Embryo Rescue

Embryo rescue is used to produce interspecific and intergeneric hybrids, overcome reproductive barriers, and incorporate beneficial alleles into cultivated species [27]. The advent of embryo rescue techniques in the late 20th century greatly facilitated the success of wide crosses by overcoming the post-zygotic barriers that cause embryo abortion, which were previously challenging [49,51,52,70,71,72]. This method not only aids in obtaining interspecific and intergeneric hybrids but also supports the production of haploid and doubled haploid plants, which are crucial for plant breeding programs [57,71]. Embryo rescue techniques in Brassicaceae have been used to breed biotic and abiotic stress-resistant lines, including synthetic amphidiploid and alien gene introgression lines for genetic studies [27]. The transfer of clubroot resistance genes from resistant Chinese cabbage to B. napus via distant hybridization and embryo rescue has been described by Liu et al. (2018) [73]. This approach has successfully identified true hybrids with clubroot resistance.

3.2. Polyploid Breeding

Polyploid breeding plays a significant role in enabling intergeneric and interspecific crosses for clubroot resistance in Brassica species [40,73,74,75,76,77]. Interspecific and intergeneric hybridization within Brassicaceae enables the production of synthetic amphidiploids and other engineered chromosomal lines. These lines, developed through polyploid breeding strategies, serve as valuable genetic resources for studying the effects of chromosomes on plant traits and for improving crop resistance to biotic stresses such as clubroot [27]. In polyploid Brassica species, the formation of double haploid (DH) lines allows for fixation and stability of clubroot resistance traits. DH lines are genetically uniform, facilitating the mapping and stable expression of resistance genes across generations [39]. Several studies have mapped clubroot resistance loci across various chromosomes of B. napus, thereby revealing the polygenic resistance mechanisms. Polyploidy can help stabilize these diverse resistance loci by providing multiple copies of homologous chromosomes, allowing for more complex gene interactions that contribute to resistance [29]. Diederichsen and Sacristan crossed resistant B. rapa with B. oleracea and created synthetic B. napus lines that were resistant to P. brassicae. The broad resistance of these synthetic lines suggests durable protection against P. brassicae pathotypes [78]. Masud Karim and Yu (2024) resynthesized B. napus lines using a B. rapa donor carrying race-specific resistance genes and B. oleracea donors harboring race-non-specific QTLs. All resynthesized and semi-resynthesized lines showed high resistance to multiple P. brassicae races, confirming the effective transfer and stacking of resistance loci [79]. Polyploid breeding facilitates intergeneric crosses between radish (Raphanus sativus) and B. oleracea and the development of allotetraploid Brassicoraphanus (RRCC). This artificial polyploid is resistant to various clubroot pathotypes. The significant homeologous recombination observed suggests the potential for transferring resistance traits from radish to Brassica napus, thereby improving clubroot resistance [56].

3.3. Protoplast Fusion

Somatic hybridization is a prominent method that utilizes protoplast electrofusion, resulting in hybrid plants that exhibit a high resistance to clubroot. This technique has been employed in interspecific or intergeneric crosses to overcome sexual incompatibility and introduce desired traits such as clubroot resistance. This allows the merging of genetic material from different species, such as B. rapa and B. oleracea, to enhance resistance traits against diseases [80]. The integration of clubroot resistance traits from various Brassica species through protoplast fusion allows the combination of different resistance loci. This technique effectively creates hybrids with enhanced disease resistance by providing genetic diversity that stabilizes resistance traits against multiple pathotypes of Plasmodiophora brassicae [81]. Asymmetric protoplast fusion between B. nigra and B. napus, performed by Sacristán et al. (1989), resulted in asymmetric somatic hybrids with the aim of co-transfer of disease-resistance traits, such as resistance to Phoma lingam and Plasmodiophora brassicae [82]. Protoplast fusion has been used to create intergeneric hybrids of red cabbage (B. oleracea) and radish (R. sativus). The resulting hybrids inherited chloroplasts from radish and exhibited male sterility and other traits, demonstrating cytoplasmic inheritance patterns. Notably, some hybrids from Japanese radish and cauliflower (B. oleracea) have demonstrated the ability to produce seeds when backcrossed with the parent species, indicating their potential for transferring clubroot resistance genes to Brassica crops [83,84]. Using protoplast fusion, resynthesized B. napus lines were developed to incorporate clubroot resistance from B. rapa and B. oleracea. These lines exhibited broad resistance against P. brassicae, with effectiveness depending on the combination of resistance genes from both parental species [85].

3.4. Molecular Markers

Molecular markers are essential tools for transferring and validating clubroot resistance across Brassica species and intergeneric hybrids. They enable precise mapping of resistance loci, assist in tracking desirable alleles during wide crosses, and accelerate breeding through marker-assisted selection. Various marker systems—including SNPs, RAPDs, SCARs, RFLPs, SSRs, IPs, and QTL-associated markers—have been applied to identify, map, and introgress clubroot resistance genes from diverse Brassicaceae germplasm, greatly improving the efficiency and accuracy of resistance breeding [42,86,87,88,89] (Table 1).
Table 1. Overview of molecular markers used in clubroot resistance breeding in Brassica crops.

4. Sources of Clubroot Resistance

Genetic resistance to clubroot occurs across numerous Brassica species [97] and remains a cornerstone of sustainable disease management [25,73]. Interspecific hybridization and genetic mapping have greatly expanded the accessible diversity of resistance, enabling gene transfer both within and beyond the Triangle of U.
The following section summarizes the principal resistance sources and their relevance for resistance breeding (Table 2).
Table 2. Sources of clubroot resistance.

4.1. Marker-Assisted Selection (MAS)

Marker-assisted selection (MAS) enhances the efficiency of breeding for clubroot resistance by enabling the selection of alleles linked to CR genes or QTLs. MAS is particularly valuable for traits with complex inheritance or difficult phenotyping and supports early-generation selection, thereby accelerating breeding progress [10,86].
In B. napus, SSR and intron-polymorphic (IP) markers linked to clubroot resistance loci have been developed and successfully used for trait introgression and validation [73]. Mapping efforts in B. rapa, R. sativus, and other Brassica species have identified multiple CR QTLs, providing marker sets that facilitate the targeted transfer of resistance across species and breeding pools [26,98].
Although MAS increases precision, its effectiveness may be constrained by linkage drag and marker–trait recombination, emphasizing the need for fine mapping and high-resolution markers in clubroot resistance breeding.

4.2. Cloned Clubroot Resistance (CR) Genes and Their Relevance for Resistance Breeding

Several clubroot resistance (CR) genes have been cloned from Brassica species, most of them belonging to the TIR–NB–LRR (Toll/interleukin-1 receptor–nucleotide-binding–leucine-rich repeat) family and serving as core resources for marker-assisted breeding. In B. rapa, the CRa/CRb locus on chromosome A03 comprises a cluster of NLR genes; CRa has been shown to be identical to CRb and confers resistance to pathotype group 3. This locus has been finely mapped and is routinely deployed in Chinese cabbage improvement [45,99,100]. The Crr1a gene encodes a TIR–NB–LRR protein active in hypocotyls and roots, and gain-of-function analyses confirmed its role in race-specific resistance, while a truncated allele underlies susceptibility [101].
The Rcr1 gene, also located on A03, mediates a distinct, calcium-independent defense pathway supported by proteomic and transcriptomic studies and is widely used in breeding resistant canola cultivars [102,103]. The dominant CRd gene, mapped upstream of Crr3, provides resistance to local race 4 isolates and enables efficient marker-assisted selection [104]. In B. oleracea, QTL-seq and RNA-seq approaches identified three major QTLs on C07, with two inducible candidate genes allowing the development of functional markers for cabbage [105].

4.3. Transfer of Clubroot Resistance Inside the Triangle of U

4.3.1. Brassica rapa

Numerous accessions included in the European clubroot differential (ECD) set show high levels of resistance [26], and the species has been the major contributor of dominant, race-specific resistance genes used across Brassica breeding programs [4,12,29,35,44,45,101,106,107,108,109,110,111]. Resistance loci are distributed across several chromosomes, with the A3 and A8 regions representing major hotspots. Continued screening has identified additional loci in diverse wild B. rapa accessions [26,41,44,112].
Interspecific hybridization and MAS have enabled efficient transfer of B. rapa resistance into B. napus and B. oleracea. The locus CRd has been introgressed into canola backgrounds, including transfers from highly resistant turnip cultivar ECD04 and Chinese cabbage sources [25,56,73,78,113]. Complementary loci originating from B. rapa, including Crr1 and Crr2, have also been successfully introduced into cabbage via embryo rescue approaches [110,114]. Resistance alleles derived from B. rapa have been incorporated into synthetic and natural amphiploids such as resynthesized B. napus [68,115], although some alleles may be diluted depending on genome context [116].

4.3.2. Brassica oleracea

Although resistance in B. oleracea is generally more quantitative than that of the A genome, extensive germplasm evaluations—especially of kale and cabbage types—have revealed multiple valuable QTLs across the C2, C3, C5, C7, and C9 regions [14,29,105,117,118,119,120]. Several major-effect QTLs on C07 and C08 (e.g., qCRc7-2, qCRc7-3, qCRc7-4) have been functionally characterized, with candidate genes showing resistance-associated expression following infection [105,111,118]. Wild relatives such as B. macrocarpa further expand the available diversity, providing loci that can be integrated into cultivated backgrounds [111].
Despite occasional breakdown of resistance by virulent pathotypes [4,15,100,121], B. oleracea remains essential for pyramiding strategies, particularly for combining quantitative resistance with major genes transferred from B. rapa [68,117,122].

4.3.3. Brassica nigra and Related Genera

The B genome carries fewer documented resistance loci than the A or C genomes [123], yet B. nigra possesses pathotype-specific resistance that enhances the diversity of available sources [42,86,87,88,89]. The dominant gene Rcr6, identified in a region syntenic to A08 [108,123,124], represents the first major CR gene described for the B genome. Its introgression into B. napus is feasible with MAS, although amphidiploids containing the B genome (e.g., B. juncea, B. carinata) often show susceptibility [125], indicating that additional strategies are required for stable transfer. A recently identified CR locus in the B genome, together with the work of Hu et al. (2024), who demonstrated the efficient, marker-free CRISPR/Cas9-mediated incorporation of Rcr1 from B. rapa into B. napus, highlights the growing potential of genome editing in CR breeding [41].

4.3.4. Brassica juncea

B. juncea generally lacks inherent resistance but can acquire it through crosses with B. rapa and other Brassica species. Distant hybridization and embryo rescue enabled stable integration of resistance loci into the AABB background, with mapping studies identifying several genomic regions associated with resistance to Plasmodiophora brassicae [26,125].

4.3.5. Resynthesis of Brassica Species for Clubroot Resistance

Resynthesized Brassica species enable the combination of multiple resistance alleles, improving resilience through allele stacking and diversification. Resynthesized B. napus derived from B. rapa × B. oleracea crosses is particularly valuable for overcoming species barriers in resistance introgression [67,115]. Numerous QTLs detected via associative transcriptomics and classical mapping—including major loci on A02 and A03—serve as targets for pyramiding in modern canola breeding [18]. However, the expression of A- and C-genome resistance can vary depending on epistatic interactions [26,29,39,115,126].

4.4. Transfer of Clubroot Resistance Outside the Triangle of U

4.4.1. Raphanus sativus

Radish provides the most significant non-Brassica source of clubroot resistance, with broad-spectrum resistance documented across many accessions [59,83,127,128,129]. Several QTLs and loci—such as Crs1—have been mapped in radish germplasm [34,98,120]. Intergeneric hybrids such as Brassicoraphanus (RRCC) have facilitated stable introgression of radish-derived resistance into B. napus and B. oleracea [4,27,29,59,65,130]. Cytogenetic studies have demonstrated recombination between radish and Brassica chromosomes, confirming the feasibility of transferring radish-derived loci [65,97,131,132]. MAALs and backcrossed progenies have enabled targeted introgression of radish resistance regions, expanding the genomic toolkit for resistance breeding [29,65,98] (Table 3).
Table 3. Examples of successful interspecific introgression of clubroot resistance.

4.4.2. Arabidopsis and Other Cruciferous Species

No major resistance sources have yet been identified outside Brassica and radish, but ongoing exploration of wild crucifers continues to expand the genetic basis for resistance breeding. A range of species—including B. juncea, has been screened as potential donors in hybridization programs with B. napus [73]. Mechanistic studies of Arabidopsis thaliana identified genes such as RPB1 and regulators such as SnRK1.1 as contributors to partial or broad-spectrum resistance [126,127,128,129,130,131,132,133,134,135,136,137], offering insights into conserved pathways relevant to Brassica breeding.

5. Perspectives and Future Directions

Future progress in developing durable clubroot resistance will depend on effectively integrating diverse genetic resources with advanced genomic and gene-editing technologies. A central priority will be the continued expansion of the genetic base through interspecific and intergeneric introgression, which offers access to additional CR genes from cruciferous species beyond Brassica and Raphanus [101]. The use of synthetic hybrids and distant crosses complements this effort by enabling the transfer of resistance alleles that are otherwise inaccessible through conventional breeding, thereby enhancing resilience to diverse P. brassicae pathotypes.
At the same time, advances in genomic mapping will play a pivotal role in guiding more targeted resistance introgression. Approaches such as QTL-Seq and BSA provide rapid means of identifying CR loci suitable for strategic intercrossing [101], while high-density linkage maps, QTL analyses, and synteny comparisons with A. thaliana deepen understanding of conserved resistance mechanisms and support the efficient deployment of beneficial alleles [12,101]. These tools are complemented by transcriptomic strategies, including associative transcriptomics, which continues to be instrumental in identifying candidate genes underlying resistance variation [25]. As genomic platforms evolve, next-generation sequencing and GWAS will further accelerate the discovery of novel loci and enhance the predictive capacity of modern breeding pipelines [42,138,139,140].
A key issue in interpreting newly reported clubroot resistance genes is the strong possibility that several of them are not truly novel but correspond to previously described loci. Because many studies use different mapping populations, marker systems, and race differentials, resistance loci appearing under new names—especially those repeatedly detected on chromosomes A02, A03, and A08—may represent the same underlying gene [26,81,113,130]. This ambiguity is further amplified by high synteny and the presence of homeologous genome regions across Brassica species, which frequently place resistance factors in conserved chromosomal blocks [12,25,42,106,140].
To avoid redundant naming and overestimating the diversity of available resistance sources, future work should emphasize high-resolution mapping, comparative genomics, and sequence-level validation. Functional confirmation through allele sequencing, haplotype comparison, or CRISPR-mediated gene disruption will be essential to determine whether a locus is genuinely novel [69,99,100,108]. Clarifying these relationships is critical for breeding programs, as misidentification of CR genes can compromise pyramiding strategies and lead to ineffective combinations of resistance sources.
CRISPR/Cas9 should be viewed as a potential alternative to interspecific crosses for the development of clubroot resistance (CR). In contrast to conventional introgression, which requires wide crosses and is constrained by linkage drag, genome editing enables direct modification of resistance loci within adapted genetic backgrounds. Effective application of this approach in polyploid Brassica species depends on precise characterization of the targeted CR locus and its homeologous copies at the sequence level, as similar challenges have been widely documented for other polyploid crops [141,142,143,144,145,146]. Because multiple homeologous gene copies must often be edited simultaneously, guide RNA design must be informed by sequence comparison among all alleles, and target sites require validation for on-target activity [136,137]. Additional methodological considerations include appropriate delivery of CRISPR/Cas reagents and strategies to ensure efficient editing across complex polyploid genomes [138]. When these requirements are met, CRISPR/Cas9 provides a means to reconstruct or modify known CR alleles and to combine multiple resistance factors without the genetic constraints associated with interspecific hybridization.
Taken together, these developments point toward a future in which Brassica breeding programs can more effectively assemble broad and durable resistance to clubroot. The convergence of expanded germplasm exploration, high-resolution genomic tools, and precision gene editing will be essential not only for enhancing cultivar resilience but also for ensuring long-term agricultural sustainability in clubroot-affected production systems.

Author Contributions

P.K.: Conceptualization, methodology, project administration, visualization, writing—original draft, review, and editing; M.K.: methodology. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by statutory funds from The National Institute of Horticultural Research, Skierniewice, Poland, and in the frame of subsidy of the Ministry of Agriculture and Rural Development special-purpose—Task 3.3: “The development of breeding materials for white head cabbage with higher resistance to drought stress under field conditions, cytoplasmic male sterility and increased tolerance to bacterial rot”.

Data Availability Statement

No new data were created or analyzed in this study.

Conflicts of Interest

The authors declare that they have no affiliations with or involvement in any organization or entity with any financial interest in the subject matter or materials discussed in this manuscript.

References

  1. Zotero, A.; García, C.; Gossen, B.D.; Strelkov, S.E.; Todd, C.D.; Bonham-Smith, P.C.; Pérez-López, E. Clubroot disease in Latin America: Distribution and management strategies. Plant Pathol. 2019, 68, 827–833. [Google Scholar] [CrossRef]
  2. Salih, R.; Brochu, A.-S.; Labbé, C.; Strelkov, S.E.; Franke, C.; Bélanger, R.; Pérez-López, E. A hydroponic-based bioassay to facilitate Plasmodiophora brassicae phenotyping. Plant Dis. 2024, 108, 131–138. [Google Scholar] [CrossRef] [PubMed]
  3. Xu, X.; Wu, C.; Zhang, F.; Yao, J.; Fan, L.; Liu, Z.; Yao, Y. Comprehensive review of Plasmodiophora brassicae: Pathogenesis, pathotype diversity, and integrated control methods. Front. Microbiol. 2025, 16, 1531393. [Google Scholar] [CrossRef] [PubMed]
  4. Diederichsen, E.; Frauen, M.; Linders, E.G.A.; Hatakeyama, K.; Hirai, M. Status and perspectives of clubroot resistance breeding in crucifer crops. J. Plant Growth Regul. 2009, 28, 265–281. [Google Scholar] [CrossRef]
  5. Donald, E.C.; Porter, I.J. Clubroot in Australia: The history and impact of Plasmodiophora brassicae in Brassica crops and research efforts directed towards its control. Can. J. Plant Pathol. 2014, 36, 66–84. [Google Scholar] [CrossRef]
  6. Chai, A.L.; Xie, X.W.; Shi, Y.X.; Li, B.J. Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Can. J. Plant Pathol. 2014, 36, 142–153. [Google Scholar] [CrossRef]
  7. Bruce, T.J.A. GM as a route for delivery of sustainable crop protection. J. Exp. Bot. 2012, 63, 537–541. [Google Scholar] [CrossRef]
  8. Struck, C.; Rüsch, S.; Streklov, B. Control strategies of clubroot disease caused by Plasmodiophora brassicae. Microorganisms 2022, 10, 620. [Google Scholar] [CrossRef]
  9. Dixon, G.R. Clubroot (Plasmodiophora brassicae Woronin)—An agricultural and biological challenge worldwide. Can. J. Plant Pathol. 2014, 36, 5–18. [Google Scholar] [CrossRef]
  10. Hasan, J.; Megha, S.; Rahman, H. Clubroot in Brassica: Recent advances in genomics, breeding, and disease management. Genome 2021, 64, 735–760. [Google Scholar] [CrossRef]
  11. Ahmed, H.U.; Hwang, S.F.; Strelkov, S.E.; Gossen, B.D.; Peng, G.; Howard, R.J.; Turnbull, G.D. Assessment of bait crops to reduce inoculum of clubroot (Plasmodiophora brassicae) of canola. Can. J. Plant Sci. 2011, 91, 545–551. [Google Scholar] [CrossRef]
  12. Ueno, H.; Matsumoto, E.; Aruga, D.; Kitagawa, S.; Matsumura, H.; Hayashida, N. Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol. Biol. 2012, 80, 621–629. [Google Scholar] [CrossRef]
  13. Dakouri, A.; Lamara, M.; Karim, M.M.; Wang, J.; Chen, Q.; Gossen, B.D.; Strelkov, S.E.; Hwang, S.-F.; Peng, G.; Yu, F. Identification of resistance loci against new pathotypes of Plasmodiophora brassicae in Brassica napus based on genome-wide association mapping. Sci. Rep. 2021, 11, 85836. [Google Scholar] [CrossRef] [PubMed]
  14. Farid, M.; Yang, R.-C.; Kebede, B.; Rahman, H. Evaluation of Brassica oleracea accessions for resistance to Plasmodiophora brassicae and identification of genomic regions associated with resistance. Genome 2020, 63, 91–101. [Google Scholar] [CrossRef] [PubMed]
  15. Hollman, K.B.; Hwang, S.F.; Manolii, V.P.; Strelkov, S.E. Pathotypes of Plasmodiophora brassicae collected from clubroot-resistant canola (Brassica napus L.) cultivars in Western Canada in 2017–2018. Can. J. Plant Pathol. 2021, 43, 622–630. [Google Scholar] [CrossRef]
  16. Holtz, M.D.; Hwang, S.-F.; Strelkov, S.E. Genotyping of Plasmodiophora brassicae reveals the presence of distinct populations. BMC Genom. 2018, 19, 254. [Google Scholar] [CrossRef]
  17. Zeng, L.; Zhang, Y.; Wu, Y.; Zhang, X.; Zhao, C.; Ren, L.; Huang, J.; Cheng, X.; Liu, S.; Liu, L. Pathotype characterization of Plasmodiophora brassicae by European Clubroot Differential and Williams sets in China. Plant Dis. 2024, 108, 847–851. [Google Scholar] [CrossRef]
  18. Askarian, H.; Hwang, S.-F.; Akhavan, A.; Manolii, V.P.; Strelkov, S.E.; Cao, T. Virulence spectrum of single-spore and field isolates of Plasmodiophora brassicae able to overcome resistance in canola (Brassica napus). Plant Dis. 2021, 105, 43–52. [Google Scholar] [CrossRef]
  19. Jones, D.R.; Ingram, D.S.; Dixon, G.R. Factors affecting tests for differential pathogenicity in populations of Plasmodiophora brassicae. Plant Pathol. 1982, 31, 229–238. [Google Scholar] [CrossRef]
  20. Pang, W.; Liang, Y.; Zhan, Z.; Li, X.; Piao, Z. Development of a Sinitic clubroot differential set for the pathotype classification of Plasmodiophora brassicae. Front. Plant Sci. 2020, 11, 568771. [Google Scholar] [CrossRef]
  21. Ayers, G.W. Races of Plasmodiophora brassicae. Can. J. Bot. 1957, 35, 923–932. [Google Scholar] [CrossRef]
  22. Javed, M.A.; Pérez-López, E.; Mukhopadhyay, S.; Normandeau, E.; Brochu, A.-S. Telomere-to-telomere genome assembly of the clubroot pathogen Plasmodiophora brassicae. Genome Biol. Evol. 2024, 16, evae122. [Google Scholar] [CrossRef] [PubMed]
  23. Jia, H.; Zhang, X.; Wang, Z.; Wei, X.; Yuan, Y.; Yang, Y.; Wei, F.; Tian, B.; Zhao, Y.; Yang, S.; et al. Root RNA-seq analysis reveals a distinct transcriptome landscape between clubroot-susceptible and clubroot-resistant Chinese cabbage lines after Plasmodiophora brassicae infection. Plant Soil 2017, 421, 93–105. [Google Scholar] [CrossRef]
  24. Tso, H.H.; Strelkov, S.E.; Galindo-González, L. Current and future pathotyping platforms for Plasmodiophora brassicae in Canada. Plants 2021, 10, 1446. [Google Scholar] [CrossRef]
  25. Hejna, O.; Havlickova, L.; He, Z.; Bancroft, I.; Curn, V. Analysing the genetic architecture of clubroot resistance variation in Brassica napus by associative transcriptomics. Mol. Breed. 2019, 39, 1021–1034. [Google Scholar] [CrossRef]
  26. Hirani, A.H.; Gao, F.; Liu, J.; Fu, G.; Wu, C.; McVetty, P.B.E.; Duncan, R.W.; Li, G. Combinations of independent dominant loci conferring clubroot resistance in four turnip accessions (Brassica rapa) from the European Clubroot Differential set. Front. Plant Sci. 2018, 9, 1628. [Google Scholar] [CrossRef]
  27. Kaneko, Y.; Bang, S.W. Interspecific and intergeneric hybridization and chromosomal engineering of Brassicaceae crops. Breed. Sci. 2014, 64, 14–22. [Google Scholar] [CrossRef]
  28. Mehraj, H.; Akter, A.; Miyaji, N.; Miyazaki, J.; Shea, D.J.; Fujimoto, R.; Doullah, M.A.-U. Genetics of clubroot and fusarium wilt disease resistance in Brassica vegetables: The application of marker-assisted breeding for disease resistance. Plants 2020, 9, 726. [Google Scholar] [CrossRef]
  29. Piao, Z.; Ramchiary, N.; Lim, Y.P. Genetics of clubroot resistance in Brassica species. J. Plant Growth Regul. 2009, 28, 252–264. [Google Scholar] [CrossRef]
  30. Pilet-Nayel, M.-L.; Moury, B.; Caffier, V.; Montarry, J.; Kerlan, M.-C.; Fournet, S.; Durel, C.-E.; Delourme, R. Quantitative resistance to plant pathogens in pyramiding strategies for durable crop protection. Front. Plant Sci. 2017, 8, 1838. [Google Scholar] [CrossRef]
  31. Reglinski, T.; Havis, N.; Rees, H.J.; de Jong, H. The practical role of induced resistance for crop protection. Phytopathology 2023, 113, 719–731. [Google Scholar] [CrossRef] [PubMed]
  32. Botero-Ramirez, A.; Kirk, B.; Strelkov, S.E. Optimizing clubroot management and the role of canola cultivar mixtures. Pathogens 2024, 13, 640. [Google Scholar] [CrossRef] [PubMed]
  33. Peng, G.; Lahlali, R.; Hwang, S.-F.; Pageau, D.; Hynes, R.K.; McDonald, M.R.; Gossen, B.D.; Strelkov, S.E. Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Can. J. Plant Pathol. 2014, 36, 99–112. [Google Scholar] [CrossRef]
  34. Ma, Y.; Wang, H.; Song, J.; Yang, W.; Jia, H.; Agerbirk, N.; Chen, Y.; Li, C.; Piao, Y.; Li, S.; et al. Identification of clubroot-resistant germplasm in a radish (Raphanus sativus L.) core collection. Agronomy 2024, 14, 157. [Google Scholar] [CrossRef]
  35. Neik, T.X.; Barbetti, M.J.; Batley, J. Current status and challenges in identifying disease resistance genes in Brassica napus. Front. Plant Sci. 2017, 8, 1788. [Google Scholar] [CrossRef]
  36. Ahuja, I.; Rohloff, J.; Bones, A.M. Defence mechanisms of Brassicaceae: Implications for plant–insect interactions and potential for integrated pest management—A review. Agron. Sustain. Dev. 2010, 30, 311–348. [Google Scholar] [CrossRef]
  37. Lamichhane, J.R.; Arseniuk, E.; Boonekamp, P.; Czembor, J.; Decroocq, V.; Enjalbert, J.; Finckh, M.R.; Korbin, M.; Koppel, M.; Kudsk, P.; et al. Advocating a need for suitable breeding approaches to boost integrated pest management: A European perspective. Pest Manag. Sci. 2018, 74, 1219–1227. [Google Scholar] [CrossRef]
  38. Rato, C.; Carvalho, M.F.; Azevedo, C.; Oblessuc, P.R. Genome editing for resistance against plant pests and pathogens. Transgenic Res. 2021, 30, 427–459. [Google Scholar] [CrossRef]
  39. Fredua-Agyeman, R.; Rahman, H. Mapping of the clubroot disease resistance in spring Brassica napus canola introgressed from European winter canola cv. ‘Mendel’. Euphytica 2016, 211, 201–213. [Google Scholar] [CrossRef]
  40. Hirai, M.; Harada, T.; Kubo, N.; Tsukada, M.; Suwabe, K.; Matsumoto, S. A novel locus for clubroot resistance in Brassica rapa and its linkage markers. Theor. Appl. Genet. 2004, 108, 639–643. [Google Scholar] [CrossRef]
  41. Hu, H.; Zhang, Y.; Yu, F. A CRISPR/Cas9-based vector system enables fast breeding of selection marker-free canola with Rcr1-rendered clubroot resistance. J. Exp. Bot. 2024, 75, 1347–1363. [Google Scholar] [CrossRef] [PubMed]
  42. Kopec, P.M.; Mikolajczyk, K.; Jajor, E.; Perek, A.; Nowakowska, J.; Obermeier, C.; Chawla, H.S.; Korbas, M.; Bartkowiak-Broda, I.; Karlowski, W.M. Local duplication of TIR-NBS-LRR gene marks clubroot resistance in Brassica napus cv. Tosca. Front. Plant Sci. 2021, 12, 639631. [Google Scholar] [CrossRef] [PubMed]
  43. Kuginuki, Y.; Ajisaka, H.; Yui, M.; Yoshikawa, H.; Hida, K.-I.; Hirai, M. RAPD markers linked to a clubroot-resistance locus in Brassica rapa L. Euphytica 1997, 98, 149–154. [Google Scholar] [CrossRef]
  44. Nguyen, M.L.; Monakhos, G.F.; Komakhin, R.A.; Monakhos, S.G. The new clubroot resistance locus is located on chromosome A05 in Chinese cabbage (Brassica rapa L.). Russ. J. Genet. 2018, 54, 296–304. [Google Scholar] [CrossRef]
  45. Zhang, T.; Zhao, Z.; Zhang, C.; Pang, W.; Choi, S.R.; Lim, Y.P.; Piao, Z. Fine genetic and physical mapping of the CRb gene conferring resistance to clubroot disease in Brassica rapa. Mol. Breed. 2014, 34, 1173–1183. [Google Scholar] [CrossRef]
  46. Hajjar, R.; Hodgkin, T. The use of wild relatives in crop improvement: A survey of developments over the last 20 years. Euphytica 2007, 156, 1–13. [Google Scholar] [CrossRef]
  47. Quezada-Martinez, D.; Addo Nyarko, C.P.; Schiessl, S.V.; Mason, A.S. Using wild relatives and related species to build climate resilience in Brassica crops. Theor. Appl. Genet. 2021, 134, 1711–1728. [Google Scholar] [CrossRef]
  48. Zou, J.; Gao, S.; Zhang, B.; Ge, W.; Zhang, J.; Ji, R. Chinese cabbage BrCAP has potential resistance against Plasmodiophora brassicae. Horticulturae 2023, 9, 517. [Google Scholar] [CrossRef]
  49. Hu, D.; Jing, J.; Snowdon, R.J.; Mason, A.S.; Shen, J.; Meng, J.; Zou, J. Exploring the gene pool of Brassica napus by genomics-based approaches. Plant Biotechnol. J. 2021, 19, 1693–1712. [Google Scholar] [CrossRef]
  50. Snowdon, R.J. Cytogenetics and genome analysis in Brassica crops. Chromosome Res. 2007, 15, 85–95. [Google Scholar] [CrossRef]
  51. Tonguç, M.; Griffiths, P.D. Development of Black Rot Resistant Interspecific Hybrids between Brassica oleracea L. Cultivars and Brassica Accession A 19182, Using Embryo Rescue. Euphytica 2004, 136, 313–318. [Google Scholar] [CrossRef]
  52. Momotaz, A.; Kato, M.; Kakihara, F. Production of Intergeneric Hybrids between Brassica and Sinapis Species by Means of Embryo Rescue Techniques. Euphytica 1998, 103, 123–130. [Google Scholar] [CrossRef]
  53. Chen, Z.Z.; Snyder, S.; Loh, W.H.; Fan, Z.G. Efficient Production of Doubled Haploid Plants through Chromosome Doubling of Isolated Microspores in Brassica napus. Plant Breed. 1994, 113, 217–221. [Google Scholar] [CrossRef]
  54. Leflon, M.; Coriton, O.; Jenczewski, E.; Huteau, V.; Eber, F.; Chèvre, A.M.; Letanneur, J.C.; Chelysheva, L.; Barker, G.; Ryder, C.D. Pairing and recombination at meiosis of Brassica rapa (AA) × Brassica napus (AACC) hybrids. Theor. Appl. Genet. 2006, 113, 1467–1480. [Google Scholar] [CrossRef]
  55. Zou, J.; Yang, T.; Xia, W.; Li, R.; Qian, W.; Pires, J.C.; Mason, A.S.; Park, B.S.; Fu, D.; Lim, Y.P.; et al. De novo genetic variation associated with retrotransposon activation, genomic rearrangements and trait variation in a recombinant inbred line population of Brassica napus derived from interspecific hybridization with Brassica rapa. Plant J. 2011, 68, 212–224. [Google Scholar] [CrossRef]
  56. Zhan, Z.; Nwafor, C.C.; Hou, Z.; Gong, J.; Zhu, B.; Jiang, Y.; Zhou, Y.; Wu, J.; Piao, Z.; Tong, Y.; et al. Cytological and Morphological Analysis of Hybrids between Brassicoraphanus, and Brassica napus for Introgression of Clubroot Resistant Trait into Brassica napus L. PLoS ONE 2017, 12, e0177470. [Google Scholar] [CrossRef]
  57. Rogo, U.; Fambrini, M.; Pugliesi, C. Embryo Rescue in Plant Breeding. Plants 2023, 12, 3106. [Google Scholar] [CrossRef]
  58. Chalhoub, B.; Denoeud, F.; Liu, S.; Parkin, I.A.; Golicz, A.A.; Tang, H.; Wang, X.; Chiquet, J.; Belcram, H.; Tong, H.; et al. Plant genetics. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 2014, 345, 950–953. [Google Scholar] [CrossRef]
  59. Katche, E. Interspecific Hybridization for Brassica Crop Improvement. Crop Breed. Genet. Genom. 2019, 1, e190007. [Google Scholar] [CrossRef]
  60. Cheng, F.; Wu, J.; Wang, X. Genome Triplication Drove the Diversification of Brassica Plants. Hortic. Res. 2014, 1, 14024. [Google Scholar] [CrossRef]
  61. Nikolov, L.A. Brassicaceae Flowers: Diversity amid Uniformity. J. Exp. Bot. 2019, 70, 2623–2635. [Google Scholar] [CrossRef] [PubMed]
  62. Hu, D.; Zhang, W.; Zhang, Y.; Chang, S.; Chen, L.; Chen, Y.; Shi, Y.; Shen, J.; Meng, J.; Zou, J. Reconstituting the Genome of a Young Allopolyploid Crop, Brassica napus, with Its Related Species. Plant Biotechnol. J. 2019, 17, 1106–1118. [Google Scholar] [CrossRef] [PubMed]
  63. Chen, S.; Nelson, M.N.; Chèvre, A.-M.; Jenczewski, E.; Li, Z.; Mason, A.S.; Meng, J.; Plummer, J.A.; Pradhan, A.; Siddique, K.H.M.; et al. Trigenomic Bridges for Brassica Improvement. Crit. Rev. Plant Sci. 2011, 30, 524–547. [Google Scholar] [CrossRef]
  64. Wei, Z.; Wang, M.; Chang, S.; Wu, C.; Liu, P.; Meng, J.; Zou, J. Introgressing Subgenome Components from Brassica rapa and B. carinata to B. juncea for Broadening Its Genetic Base and Exploring Intersubgenomic Heterosis. Front. Plant Sci. 2016, 7, 1677. [Google Scholar] [CrossRef]
  65. Zou, J.; Hu, D.; Mason, A.S.; Shen, X.; Wang, X.; Wang, N.; Grandke, F.; Wang, M.; Chang, S.; Snowdon, R.J.; et al. Genetic Changes in a Novel Breeding Population of Brassica napus Synthesized from Hundreds of Crosses between B. rapa and B. carinata. Plant Biotechnol. J. 2018, 16, 507–519. [Google Scholar] [CrossRef]
  66. Kamiński, P.; Marasek-Ciołakowska, A.; Podwyszyńska, M.; Nowakowska, M.; Nowak, K.; Szczechura, W.; Kowalska, U. Development and Characteristics of Intergeneric Brassica rapa L. subsp. pekinensis × Sinapis alba Hybrids as a New Germplasm for the Breeding. Sci. Hortic. 2025, 344, 114102. [Google Scholar] [CrossRef]
  67. Pelletier, G.; Primard, C.; Vedel, F. Intergeneric Cytoplasm Hybridization in Cruciferae by Protoplast Fusion. In Protoplasts 1983; Potrykus, I., Harms, C.T., Hinnen, A., Hütter, R., King, P.J., Shillito, R.D., Eds.; Birkhäuser: Basel, Switzerland, 1983; pp. 286–287. ISBN 978-3-0348-6557-9. [Google Scholar]
  68. Crisp, P.; Crute, I.R.; Sutherland, R.A.; Angell, S.M.; Bloor, K.; Burgess, H.; Gordon, P.L. The Exploitation of Genetic Resources of Brassica oleracea in Breeding for Resistance to Clubroot (Plasmodiophora brassicae). Euphytica 1989, 42, 215–226. [Google Scholar] [CrossRef]
  69. Matsumoto, E.; Ueno, H.; Aruga, D.; Sakamoto, K.; Hayashida, N. Accumulation of Three Clubroot Resistance Genes through Marker-Assisted Selection in Chinese Cabbage (Brassica rapa ssp. pekinensis). J. Jpn. Soc. Hortic. Sci. 2012, 81, 184–190. [Google Scholar] [CrossRef]
  70. Cardoza, V.; Stewart, C.N. Brassica Biotechnology: Progress in Cellular and Molecular Biology. Vitr. Cell. Dev. Biol.-Plant 2004, 40, 542–551. [Google Scholar] [CrossRef]
  71. Sharma, D.R.; Kaur, R.; Kumar, K. Embryo Rescue in Plants—A Review. Euphytica 1996, 89, 325–337. [Google Scholar] [CrossRef]
  72. Snowdon, R.J.; Friedt, W. Molecular Markers in Brassica Oilseed Breeding: Current Status and Future Possibilities. Plant Breed. 2004, 123, 1–8. [Google Scholar] [CrossRef]
  73. Liu, Y.; Xu, A.; Liang, F.; Yao, X.; Wang, Y.; Liu, X.; Zhang, Y.; Dalelhan, J.; Zhang, B.; Qin, M.; et al. Screening of Clubroot-Resistant Varieties and Transfer of Clubroot Resistance Genes to Brassica napus Using Distant Hybridization. Breed. Sci. 2018, 68, 258–267. [Google Scholar] [CrossRef] [PubMed]
  74. Chiang, M.S.; Chiang, B.Y.; Grant, W.F. Transfer of Resistance to Race 2 of Plasmodiophora brassicae from Brassica napus to Cabbage (B. oleracea Var. Capitata). I. Interspecific Hybridization between B. napus and B. oleracea Var. Capitata. Euphytica 1977, 26, 319–336. [Google Scholar] [CrossRef]
  75. Matsumoto, E.; Yasui, C.; Ohi, M.; Tsukada, M. Linkage Analysis of RFLP Markers for Clubroot Resistance and Pigmentation in Chinese Cabbage (Brassica rapa Ssp. pekinensis). Euphytica 1998, 104, 79–86. [Google Scholar] [CrossRef]
  76. Rahman, H.; Shakir, A.; Jakir Hasan, M. Breeding for Clubroot Resistant Spring Canola (Brassica napus L.) for the Canadian Prairies: Can the European Winter Canola Cv. Mendel Be Used as a Source of Resistance? Can. J. Plant Sci. 2011, 91, 447–458. [Google Scholar] [CrossRef]
  77. Fredua-Agyeman, R.; Hwang, S.-F.; Strelkov, S.E.; Zhou, Q.; Feindel, D. Potential Loss of Clubroot Resistance Genes from Donor Parent Brassica rapa subsp. Rapifera (ECD 04) during Doubled Haploid Production. Plant Pathol. 2018, 67, 892–901. [Google Scholar] [CrossRef]
  78. Diederichsen, E.; Sacristan, M.D. Disease Response of Resynthesized Brassica napus L. Lines Carrying Different Combinations of Resistance to Plasmodiophora brassicae Wor. Plant Breed. 1996, 115, 5–10. [Google Scholar] [CrossRef]
  79. Karim, M.; Yu, F. Resynthesizing Brassica napus with race specific resistance genes and race non-specific QTLs to multiple races of Plasmodiophora brassicae. Sci. Rep. 2024, 14, 14627. [Google Scholar] [CrossRef]
  80. Ren, J.P.; Dickson, M.H.; Earle, E.D. Improved Resistance to Bacterial Soft Rot by Protoplast Fusion between Brassica rapa and B. oleracea. Theor. Appl. Genet. 2000, 100, 810–819. [Google Scholar] [CrossRef]
  81. Yu, F.; Zhang, Y.; Wang, J.; Chen, Q.; Karim, M.M.; Gossen, B.D.; Peng, G. Identification of Two Major QTLs in Brassica napus Lines with Introgressed Clubroot Resistance From Turnip Cultivar ECD01. Front. Plant Sci. 2022, 12, 785989. [Google Scholar] [CrossRef]
  82. Sacristán, M.D.; Gerdemann-Knörck, M.; Schieder, O. Incorporation of Hygromycin Resistance in Brassica Nigra and Its Transfer to B. napus through Asymmetric Protoplast Fusion. Theor. Appl. Genet. 1989, 78, 194–200. [Google Scholar] [CrossRef]
  83. Hagimori, M.; Nagaoka, M.; Kato, N.; Yoshikawa, H. Production and Characterization of Somatic Hybrids between the Japanese Radish and Cauliflower. Theor. Appl. Genet. 1992, 84, 819–824. [Google Scholar] [CrossRef]
  84. Kameya, T.; Kanzaki, H.; Toki, S.; Abe, T. Transfer of Radish (Raphanus sativus L.) Chloroplasts into Cabbage (Brassica oleracea L.) by Protoplast Fusion. Jpn. J. Genet. 1989, 64, 27–34. [Google Scholar] [CrossRef]
  85. Diederichsen, E.; Wagenblatt, B.; Schallehn, V.; Deppe, U.; Sacristan, M.D. Transfer of Clubroot Resistance from Resynthesised Brassica napus into Oilseed Rape—Identification of Race- Specific Interactions with Plasmodiophora brassicae. In Proceedings of the Acta Hortic; International Society for Horticultural Science: Leuven, Belgium, 1996; Volume 407, pp. 423–429. [Google Scholar]
  86. Francia, E.; Tacconi, G.; Crosatti, C.; Barabaschi, D.; Bulgarelli, D.; Dall’Aglio, E.; Valè, G. Marker Assisted Selection in Crop Plants. Plant Cell Tissue Organ Cult. 2005, 82, 317–342. [Google Scholar] [CrossRef]
  87. Jonas, E.; Koning, D.-J.D. Genomic Selection Needs to Be Carefully Assessed to Meet Specific Requirements in Livestock Breeding Programs. Front. Genet. 2015, 6, 49. [Google Scholar] [CrossRef]
  88. Neyhart, J.L.; Lorenz, A.J.; Smith, K.P. Multi-Trait Improvement by Predicting Genetic Correlations in Breeding Crosses. G3 2019, 9, 3153–3165. [Google Scholar] [CrossRef] [PubMed]
  89. Wang, Q.; Wang, Y.; Qian, H.; Zhang, Z.; Zhang, L. Evaluation of Germplasm and Development of Markers for Resistance to Plasmodiophora brassicae in Radish (Raphanus sativus L.). Agronomy 2022, 12, 554. [Google Scholar] [CrossRef]
  90. Figdore, S.S.; Ferreira, M.E.; Slocum, M.K.; Williams, P.H. Association of RFLP Markers with Trait Loci Affecting Clubroot Resistance and Morphological Characters in Brassica oleracea L. Euphytica 1993, 69, 33–44. [Google Scholar] [CrossRef]
  91. Nagaoka, T.; Doullah, M.A.U.; Matsumoto, S.; Kawasaki, S.; Ishikawa, T.; Hori, H.; Okazaki, K. Identification of QTLs That Control Clubroot Resistance in Brassica oleracea and Comparative Analysis of Clubroot Resistance Genes between B. rapa and B. oleracea. Theor. Appl. Genet. 2010, 120, 1335–1346. [Google Scholar] [CrossRef]
  92. Pang, W.; Fu, P.; Li, X.; Zhan, Z.; Yu, S.; Piao, Z. Identification and Mapping of the Clubroot Resistance Gene CRd in Chinese Cabbage (Brassica rapa ssp. pekinensis). Front. Plant Sci. 2018, 9, 653. [Google Scholar] [CrossRef]
  93. Kato, T.; Hatakeyama, K.; Fukino, N.; Matsumoto, S. Fine Mapping of the Clubroot Resistance Gene CRb and Development of a Useful Selectable Marker in Brassica rapa. Breed. Sci. 2013, 63, 116–124. [Google Scholar] [CrossRef]
  94. Werner, S.; Diederichsen, E.; Frauen, M.; Schondelmaier, J.; Jung, C. Genetic Mapping of Clubroot Resistance Genes in Oilseed Rape. Theor. Appl. Genet. 2008, 116, 363–372. [Google Scholar] [CrossRef]
  95. Shah, N.; Sun, J.; Yu, S.; Yang, Z.; Wang, Z.; Huang, F.; Dun, B.; Gong, J.; Liu, Y.; Li, Y.; et al. Genetic Variation Analysis of Field Isolates of Clubroot and Their Responses to Brassica napus Lines Containing Resistant Genes CRb and PbBa8.1 and Their Combination. Mol. Breed. 2019, 39, 153. [Google Scholar] [CrossRef]
  96. Xu, M.L.; Korban, S.S. Saturation Mapping of the Apple Scab Resistance Gene Vf Using AFLP Markers. Theor. Appl. Genet. 2000, 101, 844–851. [Google Scholar] [CrossRef]
  97. Zhang, H.; Feng, J.; Manolii, V.P.; Strelkov, S.E.; Hwang, S.-F. Characterization of a Gene Identified in Pathotype 5 of the Clubroot Pathogen Plasmodiophora brassicae. Phytopathology 2015, 105, 764–770. [Google Scholar] [CrossRef] [PubMed]
  98. Gan, C.; Deng, X.; Cui, L.; Yu, X.; Yuan, W.; Dai, Z.; Yao, M.; Pang, W.; Ma, Y.; Yu, X.; et al. Construction of a High-Density Genetic Linkage Map and Identification of QTLs Associated with Clubroot Resistance in Radish (Raphanus sativus L.). Mol. Breed. 2019, 39, 1020–1025. [Google Scholar] [CrossRef]
  99. Hatakeyama, K.; Niwa, T.; Kato, T.; Ohara, T.; Kakizaki, T.; Matsumoto, S. Tandem Repeated Organization of NB-LRR Genes in the Clubroot-Resistant CRb Locus in Brassica rapa L. Mol. Genet. Genom. 2017, 292, 397–405. [Google Scholar] [CrossRef] [PubMed]
  100. Kato, T.; Hatakeyama, K.; Fukino, N.; Matsumoto, S. Identification of a Clubroot Resistance Locus Conferring Resistance to Plasmodiophora brassicae Pathotype Group 3 in Chinese Cabbage (Brassica rapa L.). Breed. Sci. 2012, 62, 282–287. [Google Scholar] [CrossRef]
  101. Hatakeyama, K.; Suwabe, K.; Tomita, R.N.; Kato, T.; Nunome, T.; Fukuoka, H.; Matsumoto, S. Identification and Characterization of Crr1a, a Gene for Resistance to Clubroot Disease in Brassica rapa L. PLoS ONE 2013, 8, e54745. [Google Scholar] [CrossRef]
  102. Chu, M.; Falk, K.C.; Peng, G.; Zhang, X.; Song, T.; Chang, A.; Lahlali, R.; Gossen, B.D.; Yu, F.; Liu, X.; et al. Fine Mapping of Rcr1 and Analyses of Its Effect on Transcriptome Patterns during Infection by Plasmodiophora brassicae. BMC Genom. 2014, 15, 1166. [Google Scholar] [CrossRef]
  103. Song, T.; Peng, G.; Yu, F.; Chu, M.; Lahlali, R. Shotgun Label-Free Proteomic Analysis of Clubroot Resistance Conferred by Rcr1 in Brassica rapa. Front. Plant Sci. 2016, 7, 1013. [Google Scholar] [CrossRef] [PubMed]
  104. Ce, F.; Mei, J.; He, H.; Zhao, Y.; Hu, W.; Yu, F.; Li, Q.; Ren, X.; Si, J.; Song, H.; et al. Identification of Candidate Genes for Clubroot Resistance in Brassica oleracea Using QTL-Seq. Front. Plant Sci. 2021, 12, 703520. [Google Scholar] [CrossRef]
  105. Chen, J.; Jing, J.; Zhan, Z.; Zhang, T.; Zhang, C.; Piao, Z. Identification of Novel QTLs for Isolate-Specific Partial Resistance to Plasmodiophora brassicae in Brassica rapa. PLoS ONE 2013, 8, e85307. [Google Scholar] [CrossRef] [PubMed]
  106. Fredua-Agyeman, R.; Jiang, J.; Hwang, S.-F.; Strelkov, S.E. QTL Mapping and Inheritance of Clubroot Resistance Genes Derived From Brassica rapa subsp. Rapifera (ECD 02) Reveals Resistance Loci and Distorted Segregation Ratios in Two F2 Populations of Different Crosses. Front. Plant Sci. 2020, 11, 899. [Google Scholar] [CrossRef] [PubMed]
  107. Karim, M.M.; Dakouri, A.; Zhang, Y.; Chen, Q.; Peng, G.; Strelkov, S.E.; Gossen, B.D.; Yu, F. Two Clubroot-Resistance Genes, Rcr3 and Rcr9wa, Mapped in Brassica rapa Using Bulk Segregant RNA Sequencing. Int. J. Mol. Sci. 2020, 21, 5033. [Google Scholar] [CrossRef]
  108. Lee, J.; Izzah, N.K.; Choi, B.-S.; Joh, H.J.; Lee, S.-C.; Perumal, S.; Seo, J.; Ahn, K.; Jo, E.J.; Choi, G.J.; et al. Genotyping-by-Sequencing Map Permits Identification of Clubroot Resistance QTLs and Revision of the Reference Genome Assembly in Cabbage (Brassica oleracea L.). DNA Res. 2015, 23, dsv034. [Google Scholar] [CrossRef]
  109. Suwabe, K.; Tsukazaki, H.; Iketani, H.; Hatakeyama, K.; Fujimura, M.; Nunome, T.; Fukuoka, H.; Matsumoto, S.; Hirai, M. Identification of Two Loci for Resistance to Clubroot (Plasmodiophora brassicae Woronin) in Brassica rapa L. Theor. Appl. Genet. 2003, 107, 997–1002. [Google Scholar] [CrossRef]
  110. Zhang, H.; Liu, X.; Zhou, J.; Strelkov, S.E.; Fredua-Agyeman, R.; Zhang, S.; Li, F.; Li, G.; Wu, J.; Sun, R.; et al. Identification of Clubroot (Plasmodiophora brassicae) Resistance Loci in Chinese Cabbage (Brassica rapa ssp. pekinensis) with Recessive Character. Genes 2024, 15, 274. [Google Scholar] [CrossRef]
  111. Hirani, A.H.; Gao, F.; Liu, J.; Fu, G.; Wu, C.; Yuan, Y.; Li, W.; Hou, J.; Duncan, R.; Li, G. Transferring Clubroot Resistance from Chinese Cabbage (Brassica rapa) to Canola (B. napus). Can. J. Plant Pathol. 2016, 38, 82–90. [Google Scholar] [CrossRef]
  112. Cheng, F.; Wu, J.; Cai, C.; Fu, L.; Liang, J.; Borm, T.; Zhuang, M.; Zhang, Y.; Zhang, F.; Bonnema, G.; et al. Genome Resequencing and Comparative Variome Analysis in a Brassica rapa and Brassica oleracea Collection. Sci. Data 2016, 3, 160119. [Google Scholar] [CrossRef]
  113. Rahman, H.; Peng, G.; Yu, F.; Falk, K.C.; Kulkarni, M.; Selvaraj, G. Special Issue: Genetics and Breeding for Clubroot Resistance in Canadian Spring Canola (Brassica napus L.). Can. J. Plant Pathol. 2014, 36, 122–134. [Google Scholar] [CrossRef]
  114. Chiang, B.Y.; Chiang, M.S.; Grant, W.F.; Crete, R. Transfer of Resistance to Race 2 of Plasmodiophora brassicae from Brassica napus to Cabbage (B. oleracea spp. Capitata). IV. A Resistant 18-Chromosome B1 Plant and Its B2 Progenies. Euphytica 1980, 29, 47–55. [Google Scholar] [CrossRef]
  115. Karim, M.M.; Yu, F. Identification of QTLs for Resistance to 10 Pathotypes of Plasmodiophora brassicae in Brassica oleracea Cultivar ECD11 through Genotyping-by-Sequencing. Theor. Appl. Genet. 2023, 136, 249. [Google Scholar] [CrossRef]
  116. Lindhout, P. The Perspectives of Polygenic Resistance in Breeding for Durable Disease Resistance. Euphytica 2002, 124, 217–226. [Google Scholar] [CrossRef]
  117. Kamei, A.; Tsuro, M.; Kubo, N.; Hayashi, T.; Wang, N.; Fujimura, T.; Hirai, M. QTL Mapping of Clubroot Resistance in Radish (Raphanus sativus L.). Theor. Appl. Genet. 2010, 120, 1021–1027. [Google Scholar] [CrossRef] [PubMed]
  118. Hirai, M. Genetic Analysis of Clubroot Resistance in Brassica Crops. Breed. Sci. 2006, 56, 223–229. [Google Scholar] [CrossRef]
  119. Peng, L.; Zhou, L.; Li, Q.; Wei, D.; Ren, X.; Song, H.; Mei, J.; Si, J.; Qian, W. Identification of Quantitative Trait Loci for Clubroot Resistance in Brassica oleracea with the Use of Brassica SNP Microarray. Front. Plant Sci. 2018, 9, 822. [Google Scholar] [CrossRef]
  120. Chang, A.; Lamara, M.; Wei, Y.; Hu, H.; Parkin, I.A.P.; Gossen, B.D.; Peng, G.; Yu, F. Clubroot Resistance Gene Rcr6 in Brassica Nigra Resides in a Genomic Region Homologous to Chromosome A08 in B. rapa. BMC Plant Biol. 2019, 19, 224. [Google Scholar] [CrossRef]
  121. Peng, G.; Falk, K.C.; Gugel, R.K.; Franke, C.; Yu, F.; James, B.; Strelkov, S.E.; Hwang, S.-F.; McGregor, L. Sources of Resistance to Plasmodiophora brassicae (Clubroot) Pathotypes Virulent on Canola. Can. J. Plant Pathol. 2014, 36, 89–99. [Google Scholar] [CrossRef]
  122. Jakir Hasan, M.; Strelkov, S.E.; Howard, R.J.; Rahman, H. Screening of Brassica Germplasm for Resistance to Plasmodiophora brassicae Pathotypes Prevalent in Canada for Broadening Diversity in Clubroot Resistance. Can. J. Plant Sci. 2012, 92, 501–515. [Google Scholar] [CrossRef]
  123. Rusholme, R.L.; Higgins, E.E.; Walsh, J.A.; Lydiate, D.J. Genetic Control of Broad-Spectrum Resistance to Turnip Mosaic Virus in Brassica rapa (Chinese Cabbage). J. Gen. Virol. 2007, 88, 3177–3186. [Google Scholar] [CrossRef] [PubMed]
  124. Brown, J.; Brown, A.P.; Davis, J.B.; Erickson, D. Intergeneric Hybridization between Sinapis alba and Brassica napus. Euphytica 1997, 93, 163–168. [Google Scholar] [CrossRef]
  125. Sohn, S.-I.; Thamilarasan, S.K.; Pandian, S.; Oh, Y.-J.; Ryu, T.-H.; Lee, G.-S.; Shin, E.-K. Interspecific Hybridization of Transgenic Brassica napus and Brassica rapa—An Overview. Genes 2022, 13, 1442. [Google Scholar] [CrossRef] [PubMed]
  126. Declercq, B.; Van Buyten, E.; Claeys, S.; Cap, N.; De Nies, J.; Pollet, S.; Höfte, M. Molecular Characterization of Phytophthora Porri and Closely Related Species and Their Pathogenicity on Leek (Allium porrum). Eur. J. Plant Pathol. 2010, 127, 341–350. [Google Scholar] [CrossRef]
  127. Peterka, H.; Budahn, H.; Schrader, O.; Ahne, R.; Schütze, W. Transfer of Resistance against the Beet Cyst Nematode from Radish (Raphanus sativus) to Rape (Brassica napus) by Monosomic Chromosome Addition. Theor. Appl. Genet. 2004, 109, 30–41. [Google Scholar] [CrossRef] [PubMed]
  128. Kim, H.; Jo, E.J.; Choi, Y.H.; Jang, K.S.; Choi, G.J. Pathotype classification of Plasmodiophora brassicae isolates using clubroot-resistant cultivars of Chinese cabbage. Plant Pathol. J. 2016, 32, 423–430. [Google Scholar] [CrossRef]
  129. Laila, R.; Nou, I.-S.; Park, J.-I.; Vijayakumar, H.; Robin, A.H.K.; Shirasawa, K.; Isobe, S.; Natarajan, S.; Kim, H.-T. Mapping of a novel clubroot resistance QTL using ddRAD-seq in Chinese cabbage (Brassica rapa L.). BMC Plant Biol. 2019, 19, 93. [Google Scholar] [CrossRef]
  130. Alix, K.; Lariagon, C.; Delourme, R.; Manzanares-Dauleux, M.J. Exploiting Natural Genetic Diversity and Mutant Resources of Arabidopsis thaliana to Study the A. thaliana—Plasmodiophora brassicae Interaction. Plant Breed. 2007, 126, 218–221. [Google Scholar] [CrossRef]
  131. Ochoa, J.C.; Mukhopadhyay, S.; Bieluszewski, T.; Jędryczka, M.; Malinowski, R.; Truman, W. Natural Variation in Arabidopsis Responses to Plasmodiophora brassicae Reveals an Essential Role for Resistance to Plasmodiophora Brasssicae 1 (RPB1). Plant J. 2023, 116, 1421–1440. [Google Scholar] [CrossRef]
  132. Zhao, Y.; Bi, K.; Gao, Z.; Chen, T.; Liu, H.; Xie, J.; Cheng, J.; Fu, Y.; Jiang, D. Transcriptome Analysis of Arabidopsis thaliana in Response to Plasmodiophora brassicae during Early Infection. Front. Microbiol. 2017, 8, 673. [Google Scholar] [CrossRef]
  133. Chen, W.; Li, Y.; Yan, R.; Ren, L.; Liu, F.; Zeng, L.; Sun, S.; Yang, H.; Chen, K.; Xu, L.; et al. SnRK1.1-mediated Resistance of Arabidopsis thaliana to Clubroot Disease Is Inhibited by the Novel Plasmodiophora brassicae Effector PBZF1. Mol. Plant Pathol. 2021, 22, 1057–1069. [Google Scholar] [CrossRef] [PubMed]
  134. Gravot, A.; Grillet, L.; Wagner, G.; Jubault, M.; Lariagon, C.; Baron, C.; Deleu, C.; Delourme, R.; Bouchereau, A.; Manzanares-Dauleux, M.J. Genetic and Physiological Analysis of the Relationship between Partial Resistance to Clubroot and Tolerance to Trehalose in Arabidopsis thaliana. New Phytol. 2011, 191, 1083–1094. [Google Scholar] [CrossRef] [PubMed]
  135. Wang, Y.; Zafar, N.; Ali, Q.; Manghwar, H.; Wang, G.; Yu, L.; Ding, X.; Ding, F.; Hong, N.; Wang, G.; et al. CRISPR/Cas Genome Editing Technologies for Plant Improvement against Biotic and Abiotic Stresses: Advances, Limitations, and Future Perspectives. Cells 2022, 11, 3928. [Google Scholar] [CrossRef] [PubMed]
  136. Zhang, H.; Ma, X.; Liu, X.; Zhang, S.; Li, F.; Li, G.; Sun, R.; Zhang, S. Identification and Fine-Mapping of Clubroot (Plasmodiophora brassicae) Resistant QTL in Brassica rapa. Horticulturae 2022, 8, 66. [Google Scholar] [CrossRef]
  137. Suwabe, K.; Tsukazaki, H.; Iketani, H.; Hatakeyama, K.; Kondo, M.; Fujimura, M.; Nunome, T.; Fukuoka, H.; Hirai, M.; Matsumoto, S. Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: The genetic origin of clubroot resistance. Genetics 2006, 173, 309–319. [Google Scholar] [CrossRef]
  138. Schaart, J.G.; Smulders, M.J.M.; Van de Wiel, C.C.M. Genome editing of polyploid crops: Prospects, achievements and bottlenecks. Transgenic Res. 2021, 30, 337–351. [Google Scholar] [CrossRef]
  139. Hussin, S.H.; Iqbal, M.A.; Liu, X.; Diaby, M.; Jatoi, G.H.; Li, C.; Imran, M.; Ahmed, R. An updated overview on insights into sugarcane genome editing via CRISPR/Cas9 for sustainable production. Sustainability 2022, 14, 12285. [Google Scholar] [CrossRef]
  140. Gao, W.; Long, L.; Tian, X.; Xu, F.; Liu, J.; Singh, P.K.; Botella, J.R.; Song, C. Genome editing in cotton with the CRISPR/Cas9 system. Front. Plant Sci. 2017, 8, 1364. [Google Scholar] [CrossRef]
  141. Ryder, P.; Spillane, C.; McHale, M.; Fort, A. Generation of stable nulliplex autopolyploid lines of Arabidopsis thaliana using CRISPR/Cas9 genome editing. Plant Cell Rep. 2017, 36, 1005–1008. [Google Scholar] [CrossRef]
  142. Laforest, L.C.; Nadakuduti, S.S. Advances in delivery mechanisms of CRISPR gene-editing reagents in plants. Front. Genome Ed. 2022, 4, 830178. [Google Scholar] [CrossRef]
  143. Ahmad, S.; Wei, X.; Sheng, Z.; Hu, P.; Tang, S. CRISPR/Cas9 for Development of Disease Resistance in Plants: Recent Progress, Limitations and Future Prospects. Brief. Funct. Genom. 2020, 19, 26–39. [Google Scholar] [CrossRef] [PubMed]
  144. Erdoğan, İ.; Cevher-Keskin, B.; Bilir, Ö.; Hong, Y.; Tör, M. Recent Developments in CRISPR/Cas9 Genome-Editing Technology Related to Plant Disease Resistance and Abiotic Stress Tolerance. Biology 2023, 12, 1037. [Google Scholar] [CrossRef]
  145. Dong, G.; Fan, Z. CRISPR/Cas-Mediated Germplasm Improvement and New Strategies for Crop Protection. Crop Health 2024, 2, 2. [Google Scholar] [CrossRef]
  146. Chen, K.; Wang, Y.; Zhang, R.; Zhang, H.; Gao, C. CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture. Annu. Rev. Plant Biol. 2019, 70, 667–697. [Google Scholar] [CrossRef]
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Design and Testing of a Vision-Based, Electrically Actuated, Row-Guided Inter-Row Cultivator
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