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Soybean cyst nematode ( Ichinohe) (SCN) is the most destructive pest affecting soybeans [ (L.) Merr.] in the U.S. To date, only two major SCN resistance alleles, and , identified in PI 88788 ( ) and Peking ( ), residing on chromosomes (Chr) 18 and 8, respectively, have been widely used to develop SCN resistant cultivars in the U.S. Thus, some SCN populations have evolved to overcome the PI 88788 and Peking derived resistance, making it a priority for breeders to identify new alleles and sources of SCN resistance. Toward that end, 461 soybean accessions from various origins were screened using a greenhouse SCN bioassay and genotyped with Illumina SoySNP50K iSelect BeadChips and three KASP SNP markers developed at the and loci to perform a genome-wide association study (GWAS) and a haplotype analysis at the and loci. In total, 35,820 SNPs were used for GWAS, which identified 12 SNPs at four genomic regions on Chrs 7, 8, 10, and 18 that were significantly associated with SCN resistance ( < 0.001). Of those, three SNPs were located at and , and 24 predicted genes were found near the significant SNPs on Chrs 7 and 10. KASP SNP genotyping results of the 462 accessions at the and loci identified 30 that carried PI 88788-type resistance, 50 that carried Peking-type resistance, and 58 that carried neither the Peking-type nor the PI 88788-type resistance alleles, indicating they may possess novel SCN resistance alleles. By using two subsets of SNPs near the and loci obtained from SoySNP iSelect BeadChips, a haplotype analysis of 461 accessions grouped those 58 accessions differently from the accessions carrying Peking or PI 88788 derived resistance, thereby validating the genotyping results at and . The significant SNPs, candidate genes, and newly characterized SCN resistant accessions will be beneficial for the development of DNA markers to be used for marker-assisted breeding and developing soybean cultivars carrying novel sources of SCN resistance.

Soybean cyst nematode (SCN) is a destructive pathogen of soybeans responsible for annual yield loss exceeding $1.5 billion in the United States. Here, we conducted a series of genome-wide association studies (GWASs) to understand the genetic landscape of SCN resistance in the University of Missouri soybean breeding programs (Missouri panel), as well as germplasm and cultivars within the United States Department of Agriculture (USDA) Uniform Soybean Tests—Northern Region (NUST). For the Missouri panel, we evaluated the resistance of breeding lines to SCN populations HG 2.5.7 (Race 1), HG 1.2.5.7 (Race 2), HG 0 (Race 3), HG 2.5.7 (Race 5), and HG 1.3.6.7 (Race 14) and identified seven quantitative trait nucleotides (QTNs) associated with SCN resistance on chromosomes 2, 8, 11, 14, 17, and 18. Additionally, we evaluated breeding lines in the NUST panel for resistance to SCN populations HG 2.5.7 (Race 1) and HG 0 (Race 3), and we found three SCN resistance-associated QTNs on chromosomes 7 and 18. Through these analyses, we were able to decipher the impact of seven major genetic loci, including three novel loci, on resistance to several SCN populations and identified candidate genes within each locus. Further, we identified favorable allelic combinations for resistance to individual SCN HG types and provided a list of available germplasm for integration of these unique alleles into soybean breeding programs. Overall, this study offers valuable insight into the landscape of SCN resistance loci in U.S. public soybean breeding programs and provides a framework to develop new and improved soybean cultivars with diverse plant genetic modes of SCN resistance.

Disease resistance is one of the most successful strategies in crop protection. For example, the implementation of PI 88788 type resistance, which contains high copy numbers of Resistance to Heterodera glycines 1 (rhg1) loci, into the commercial soybean varieties of the United States has significantly reduced the yield losses caused by soybean cyst nematode (SCN, H. glycines). Vegetable soybean, or edamame, has become a major exporting agricultural product in Taiwan with an annual revenue over $80 million USD since 2017. Several local varieties have been developed to fulfill the market needs such as the traits of flavor and sweetness. However, it remains unclear if the historical breeding programs ever incorporated rhg1 resistance into the varieties of Taiwan. This study applied the TaqMan qPCR method to measure the fluorescent signals specific to the rhg1 locus on the chromosome 18 of soybean, and the ratio of VIC and FAM signals were analyzed to predict the rhg1 copy number in the 21 soybean varieties of Taiwan. The results indicated the copy number and the single nucleotide polymorphisms of the 21 soybean varieties were identical to the susceptible soybean variety ‘Williams 82’. As importation of soybean will be continuously needed to fulfill the market and because SCN is absent in the soybean fields of Taiwan, lacking rhg1 resistance in the local soybean varieties may put the edamame industry at risk and early implementation of SCN resistance in the breeding program, alongside the application of quarantine regulations, will be the key to maintain the SCN-free status and to sustain the edamame industry in Taiwan.

Roots of soybean, Glycine max cv. Kent L. Merr., plants susceptible to the soybean cyst nematode (SCN), Heterodera glycines Ichinohe, were inoculated and allowed to develop feeding sites (syncytia) for 8 days. Root samples enriched in syncytial cells were collected using laser capture microdissection (LCM). RNA was extracted and used to make a cDNA library and expressed sequence tags (ESTs) were produced and used for a Gene Ontology (GO) analysis. RT-PCR results indicated enhanced expression of an aquaporin (GmPIP2,2), alpha-tubulin (GmTubA1), beta-tubulin (GmTubB4) and several other genes in syncytium-enriched samples as compared to samples extracted from whole roots. While RT-PCR data showed increased transcript levels of GmPIP2,2 from LCM tissue enriched in syncytial cells, in situ hybridization showed prominent GmPIP2,2 hybridization to RNA in the parenchymal cells tightly juxtaposed to the syncytium. Immunolocalization indicated stronger alpha-tubulin signal within the syncytium as compared to surrounding tissue. However, alpha-tubulin labeling appeared diffuse or clumped. Thus, LCM allowed for the isolation of tissue enriched for syncytial cells, providing material suitable for a variety of molecular analyses.

Key messageThis review provides a comprehensive atlas of QTLs, genes, and alleles conferring resistance to 28 important diseases in all major soybean production regions in the world.Breeding disease-resistant soybean [Glycine max (L.) Merr.] varieties is a common goal for soybean breeding programs to ensure the sustainability and growth of soybean production worldwide. However, due to global climate change, soybean breeders are facing strong challenges to defeat diseases. Marker-assisted selection and genomic selection have been demonstrated to be successful methods in quickly integrating vertical resistance or horizontal resistance into improved soybean varieties, where vertical resistance refers to R genes and major effect QTLs, and horizontal resistance is a combination of major and minor effect genes or QTLs. This review summarized more than 800 resistant loci/alleles and their tightly linked markers for 28 soybean diseases worldwide, caused by nematodes, oomycetes, fungi, bacteria, and viruses. The major breakthroughs in the discovery of disease resistance gene atlas of soybean were also emphasized which include: (1) identification and characterization of vertical resistance genes reside rhg1 and Rhg4 for soybean cyst nematode, and exploration of the underlying regulation mechanisms through copy number variation and (2) map-based cloning and characterization of Rps11 conferring resistance to 80% isolates of Phytophthora sojae across the USA. In this review, we also highlight the validated QTLs in overlapping genomic regions from at least two studies and applied a consistent naming nomenclature for these QTLs. Our review provides a comprehensive summary of important resistant genes/QTLs and can be used as a toolbox for soybean improvement. Finally, the summarized genetic knowledge sheds light on future directions of accelerated soybean breeding and translational genomics studies.

For broadening the narrow genetic base of modern soybean cultivars, 159 accessions were selected from the Chinese soybean collection which contained at least one of seven important agronomic traits: resistance to soybean cyst nematode (SCN) or soybean mosaic virus (SMV), tolerance to salt, cold, or drought, high seed oil content or high protein content. Genetic diversity evaluation using 55 microsatellite loci distributed across the genome indicated that a large amount of genetic diversity (0.806) and allelic variation (781) were conserved in this selected set, which captured 65.6% of the alleles present in Chinese soybean collection (1,863 accessions). On average, 9.4 rare alleles (frequency <5%) per locus were present, which were highly informative. Using model-based Bayesian clustering in STRUCTURE we distinguished four main clusters and a set of accessions with admixed ancestry. The four clusters reflected different geographic regions of origin of the accessions. Since the clusters were also clearly different with respect to the seven agronomic traits, the inferred population structure was introduced when association analysis was conducted. A total of 21 SSR markers on 16 chromosomes were identified as significantly ( P  < 0.01) associated with high oil content (6), high protein content (1), drought tolerance (5), SCN resistance (6) and SMV resistance (3). Twelve of these markers were located in or near previously identified quantitative trait loci (QTL). The results for both genetic relationship and trait-related markers will be useful for effective conservation and utilization of soybean germplasm.

Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396–GRF1/3 module is a master regulator of syncytium development in model cyst nematode H. schachtii infection of Arabidopsis. Here, we investigated whether this regulatory system operates similarly in soybean roots and is likewise important for H. glycines infection. We found that a network involving nine MIR396 and 23 GRF genes is important for normal development of soybean roots and that GRF function is specified in the root apical meristem by miR396. All MIR396 genes are down-regulated in the syncytium during its formation phase while, specifically, 11 different GRF genes are up-regulated. The switch to the syncytium maintenance phase coincides with up-regulation of MIR396 and down-regulation of the 11 GRF genes specifically via post-transcriptional regulation by miR396. Furthermore, interference with the miR396–GRF6/8–13/15–17/19 regulatory network, through either overexpression or knockdown experiments, does not affect the number of H. glycines juveniles that enter the vascular cylinder to initiate syncytia, but specifically inhibits efficient H. glycines development to adult females. Therefore, homeostasis in the miR396–GRF6/8–13/15–17/19 regulatory network is essential for productive H. glycines infections.

miR2118 triggers phased small interfering RNA (phasiRNA) biogenesis in plants and has multifaceted roles in plant development and disease resistance.Targeting the passenger strands (miR2118a/b-5p) of soybean miR2118a/b via clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas9) successfully created transgene-free amiR2118a/b mutants.Artificial miR2118a/b (amiR2118a/b) double mutants showed an altered secondary structure of pre-amiR2118a/b, and suppressed biogenesis of mature miR2118a/b and phasiRNAs; and upregulated expression of growth-related and defense-related genes under normal and Pseudomonas syringae pv. glycinea (Psg)-infected conditions, respectively.Two transgene-free amir2118a/b double mutants exhibited enhanced resistance to Pseudomonas syringae pv. glycinea, soybean cyst nematode, and root-knot nematode, and achieved increased yield under pathogen-free field conditions.A strategy is provided for generating artificial miRNAs (amiRNAs) to improve crops via the CRISPR/Cas system by mutating miRNAs* in crops. While regulatory functions of mature miRNAs are well established, the functions of miRNAs* and their potential for genetic engineering in crop improvement remain underexplored. Here, we used clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas9) to generate artificial miR2118a/b (amiR2118a/b) by editing miR2118a/b-5p and obtained several amir2118a/b mutants in soybean (Glycine max). miR2118a/b-5p modifications altered the secondary structure of precursor amiR2118a/b (pre-amiR2118a/b) and reduced mature miR2118a/b levels. These amir2118a/b mutants retained the ability to initiate biogenesis of phased small interfering RNAs (phasiRNAs), albeit with a reduced abundance compared with wild-type (WT) plants. Furthermore, these mutants upregulated the expression of genes related to growth and defense under normal and Pseudomonas syringae pv. glycinea (Psg)-infected conditions, respectively. Notably, two transgene-free amir2118 mutants exhibited enhanced resistance to Psg, soybean cyst nematode (SCN), and root-knot nematode (RKN), and achieved increased yield under pathogen-free field conditions. This study provides a strategy to generate artificial miRNAs (amiRNAs) for crop improvement through the CRISPR/Cas system by mutating miRNAs* in crops. [Display omitted] This work presents a convenient and reliable strategy to generate artificial miRNAs (amiRNAs) for soybean improvement through clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas9) system by mutating miRNAs* in soybean. The current technology readiness level (TRL) of the described technology is 4-5. At TRL 4, data from laboratory and controlled environments confirm core mechanisms, that is, amiR2118a/b mutants show altered pre-amiR2118a/b secondary structure, reduced mature miR2118a/b and phased small interfering RNAs (phasiRNAs) levels, upregulated expression of growth-related and defense-related genes under normal and Pseudomonas syringae pv. glycinea (Psg)-infected conditions, respectively, and enhanced resistance to Psg, soybean cyst nematode (SCN, races 3/5) and root-knot nematode (RKN) in greenhouses without growth inhibition. At TRL 5, field trials conducted in Beijing and Hanchuan from 2023 to 2024 show that the mutants achieved a consistent yield increase of 7.4–8.7%; pot experiments in greenhouses using naturally SCN-infested soil collected from Daqing confirmed that the SCN population density in the mutants decreased by 22.19–32.68% without yield loss, realizing the connection between laboratory and real agricultural scenarios. However, when this technology is applied on a large scale, it may face several challenges, including genotype dependence, mechanistic gaps, field-scale pathogen resistance verification, and integration of regulatory and breeding processes. These challenges need to be addressed by expanding genotype and crop testing, filling mechanistic gaps, conducting advanced field verification, and optimizing regulatory and breeding processes. This study uses clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas9) to mutate miR2118a/b-5p, generating amiR2118a/b mutants, altering pre-amiR2118a/b structures, reducing the levels of mature miR2118a/b and phased small interfering RNAs (phasiRNAs), upregulating growth/defense-related genes under normal and Pseudomonas syringae pv. glycinea (Psg)-infected conditions, and enhancing soybean field yield and broad-spectrum resistance, thus offering a novel crop improvement approach.

The rhg1-b allele of soybean is widely used for resistance against soybean cyst nematode (SCN), the most economically damaging pathogen of soybeans in the United States. Gene silencing showed that genes in a 31-kilobase segment at rhg1-b, encoding an amino add transporter, an α-SNAP protein, and a WI12 (wound-inducible domain) protein, each contribute to resistance. There is one copy of the 31-kilobase segment per haploid genome in susceptible varieties, but 10 tandem copies are present in an rhg1-b haplotype. Overexpression of the individual genes in roots was ineffective, but overexpression of the genes together conferred enhanced SCN resistance. Hence, SCN resistance mediated by the soybean quantitative trait locus Rhg1 is conferred by copy number variation that increases the expression of a set of dissimilar genes in a repeated multigene segment.

This study reports the identification of the first soybean gene that has a role in resistance to soybean cyst nematode; this finding should help to improve crop resistance to nematodes. New resistance gene in soya bean The soya bean cyst nematode is a constant threat to soya bean crops worldwide. Resistant cultivars are grown, but the mechanisms of resistance are not known. Shiming Liu et al . have now identified a gene that confers natural resistance to the nematode. It encodes a serine hydroxymethyltransferase, which is responsible for the interconversion of serine and glycine, and is essential for cellular one-carbon metabolism. Soybean ( Glycine max (L.) Merr.) is an important crop that provides a sustainable source of protein and oil worldwide. Soybean cyst nematode ( Heterodera glycines Ichinohe) is a microscopic roundworm that feeds on the roots of soybean and is a major constraint to soybean production. This nematode causes more than US$1 billion in yield losses annually in the United States alone 1 , making it the most economically important pathogen on soybean. Although planting of resistant cultivars forms the core management strategy for this pathogen, nothing is known about the nature of resistance. Moreover, the increase in virulent populations of this parasite on most known resistance sources necessitates the development of novel approaches for control. Here we report the map-based cloning of a gene at the Rhg4 (for resistance to Heterodera glycines 4) locus, a major quantitative trait locus contributing to resistance to this pathogen. Mutation analysis, gene silencing and transgenic complementation confirm that the gene confers resistance. The gene encodes a serine hydroxymethyltransferase, an enzyme that is ubiquitous in nature and structurally conserved across kingdoms. The enzyme is responsible for interconversion of serine and glycine and is essential for cellular one-carbon metabolism. Alleles of Rhg4 conferring resistance or susceptibility differ by two genetic polymorphisms that alter a key regulatory property of the enzyme. Our discovery reveals an unprecedented plant resistance mechanism against a pathogen. The mechanistic knowledge of the resistance gene can be readily exploited to improve nematode resistance of soybean, an increasingly important global crop.