Genetic variability in soybean with resistance to cyst nematode and powdery mildew: impact of multi-parent crosses on recombination and genetic diversityAbstract
The objective of this study was to analyze the genetic variability generated from two-way, four-way, and eight-way hybridizations in soybean, derived from parental lines contrasting in resistance to cyst nematode and powdery mildew. We assessed F2 populations using Simple Sequence Repeat (SSR) molecular markers located within the 50 cM region surrounding the Rmd (powdery mildew) and Rhg1 (cyst nematode) resistance genes. All markers were nonsignificant by chi-square test (P > 0.05), indicating that observed values align with the expected genotypic inheritance ratio in F2 populations (1:2:1). Lower polymorphism observed among parents explained the reduced recombination frequency in these populations. A higher mean crossover rate was observed in G4 (4.00) within linkage group G, and J8 (2.91) within linkage group J. In terms of the number of generations needed to form each population, crossover rates of 2.02 and 0.97 were found for G2 and J8, respectively. Recombination between alleles was present in some populations. Crosses involving a greater number of parents exhibited a higher frequency of crossovers, which positively impacts genetic variability. Therefore, the inclusion of more than two parents in hybridizations is recommended to enhance crossover frequency and genetic diversity. These findings provide valuable insights for breeding programs aiming to improve resistance in soybean, indicating that multi-parental crosses can be a strategic approach to increase genetic diversity and resilience against pathogens.
Keywords:
Glycine max; crossing-over; multiple crosses; SSR; genetic variability
Resumo
O objetivo deste estudo foi analisar a variabilidade genética gerada a partir de hibridizações de soja em cruzamentos de duas, quatro e oito vias, derivadas de cruzamentos parentais contrastantes quanto à resistência ao nematoide de cisto e ao oídio. Avaliamos populações F2 utilizando marcadores moleculares de sequência simples repetida (SSR) localizados na região de 50 cM ao redor dos genes de resistência Rmd (oídio) e Rhg1 (nematoide de cisto). Todos os marcadores foram não significativos pelo teste qui-quadrado (P > 0,05), indicando que os valores observados corroboram a proporção esperada de herança genotípica na população F2 (1:2:1). O menor polimorfismo observado entre os pais justificou a menor frequência de recombinação nas populações. Observou-se uma maior média de recombinações para G4 (4,00) no grupo de ligação G, e J8 (2,91) no grupo de ligação J. Quanto ao número de gerações necessárias para formar cada população, as taxas de recombinação foram de 2,02 para G2 e 0,97 para J8. A recombinação entre alelos ocorreu em algumas populações. Os cruzamentos com maior número de pais apresentaram uma frequência mais alta de recombinações, o que impacta positivamente a variabilidade genética. Portanto, recomenda-se a inclusão de mais de dois pais nas hibridizações para aumentar a frequência de recombinação e a diversidade genética. Esses achados fornecem insights valiosos para programas de melhoramento visando à melhoria da resistência em soja, indicando que cruzamentos multi-parentais podem ser uma estratégia eficaz para aumentar a diversidade genética e a resiliência contra patógenos.
Palavras-chave:
Glycine max; cruzamento; cruzamentos múltiplos; SSR; variabilidade genética
1. Introduction
Many pathogens are present in the soybean (Glycine max) cultural cycle, with the cyst nematode being one of the most economically damaging to the crop worldwide (McCarville et al., 2023). Being a soil pathogen, it infects soybean roots, making it more difficult to identify than aerial pathogens (Masonbrink et al., 2021). The symptoms caused can also be confused with those from herbicide injury (Jiang et al., 2021). Among the eight major soybean-producing countries, over 91% of the yield loss of 7.2 million tons caused by SCN occurs here (Lian et al., 2023). Due to the persistence of this pathogen and the cost, non-target toxicity, or low efficacy of available nematicides, SCN management primarily depends on crop rotation and host resistance (McCarville et al., 2023). Therefore, it is necessary to search for sources of soybean resistance to these pathogens. Greater genetic variability of soybean populations is needed.
The variability among progenies is increased by mutation, chromosome segregation, the independent assortment of genes, and intra-chromosomal genetic recombination during meiosis (Zhou et al., 2021). Studies have found that Brazilian and American soybean germplasm have narrow genetic bases, both derived from a few common ancestors (Vuong et al., 2021). This situation has resulted from the reduced number of parents used in developing segregant populations from which new cultivars are extracted (Lian et al., 2022). Additionally, methods that induce mutations have shown success in enhancing genetic diversity and yield stability under varied conditions, which supports the effectiveness of mutation-based strategies in expanding genetic bases (Bhuiyan et al., 2022).
SSRs (Simple Sequence Repeat) markers are extremely useful in genetic studies related to genotype similarities, as they are highly polymorphic and multi-allelic, which is very important for genome mapping, identification, and discrimination of genotypes and population genetics (Sang et al., 2023). The alleles differ due to variations in the number of random tandem repetitions, arising from crossover events during the meiosis cycle (Dong and Hudson, 2022).
Because the crossover site occurs at random, selection for polygenic traits will alter the number and position of chiasmas in the selected lines used to advance generations, while this does not occur in the entire population. Therefore, for quantitative traits, meiotic recombination has been, and will continue to be, a mechanism by which breeders can establish novel superior linkage blocks in these regions. The objective of this study was to analyze the genetic variability derived from crossovers in F2 soybean populations, derived from two-way, four-way, and eight-way crosses, diverging in their reaction to resistance to soybean cyst nematode (race 3) and powdery mildew.
2. Materials and Methods
2.1. Genetic material
This study was conducted at São Paulo State University (UNESP/FCAV), Jaboticabal campus. The populations were obtained through artificial crosses between two, four, and eight soybean parents (Table 1), which exhibited contrasting reactions to soybean cyst nematode - race 3 (SCN) and powdery mildew (PW). Polymorphic markers were selected around the resistance genes Rmd (PW) in linkage group J and Rhg1 (SCN) in linkage group G. For linkage group G, only the Hartwig cultivar was used as a resistance source to SCN, while for linkage group J, cultivars BRS 137, Tainung 3, Embrapa 59, and Conquista were used as sources of resistance to PW. In each linkage group, three types of crosses were performed: two-way (G2 and J2), four-way (G4 and J4), and eight-way (G8 and J8). The smaller number of crosses for PW compared to SCN was due to the difficulty of finding resistance sources for this disease.
Parents of the genealogy and reaction to soybean cist nematode-race 3 and powdery mildew disease.
2.2. F1 seed production and F2 population development
The F1 seeds were obtained through artificial hybridization at UNESP/FCAV, resulting in two-way (simple cross), four-way (between two-way F1s), and eight-way (between four-way F1s) crosses. The F1 plants were then self-fertilized in a greenhouse, and seeds from each cross were grown to obtain F2 genotypes, from which leaf samples were collected for DNA extraction. The number of plants analyzed in each cross was 53, except for J2, where 33 plants were analyzed (Table 2). The limited number of individuals analyzed per population can be explained by the difficulty of obtaining fertilized flowers in soybean crosses and the low seed production per fertilized flower, usually only two, in addition to the occurrence of cleistogamy (self-fertilization at the time of flower opening). The methodology was based on similar studies, such as Ferreira Júnior et al. (2015), which used 41 genotypes.
Chi-square values (x2) for the 1:2:1 genotypic segregation proportion in two-way crosses from linkage groups G and J for each SSR marker. Crossover occurrences within linkage groups G and J.
2.3. Molecular analysis
Molecular analyses were conducted at the Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA. Approximately 5 g of leaf material was collected from each plant and selected parent, and this material was stored frozen until desiccated in a lyophilizer. The DNA from the parents and F2 population was extracted using the CTAB method and quantified with a fluorometer, then diluted to a concentration of 10 ng µL−1. A 10 µL aliquot of the DNA suspension was run on a 1.5% (w/v) agarose gel to verify quality and concentration.
All parents were screened with 29 SSR markers from linkage group G and 25 from linkage group J to identify polymorphism. The SSR primer sequences were obtained from Soybase (2017). From this screening, six polymorphic markers were found in group G and seven in group J, which were used to obtain crossover data (Figure 1). These markers were located within a 55 cM distance around the resistance genes for SCN (group G) and PW (group J), according to Cregan et al. (1999). The polymerase chain reaction (PCR) was performed as specified in Soybase (2017). Amplified PCR fragments were separated by either metaphor agarose (3% w/v) or polyacrylamide gel electrophoresis, depending on the size of the polymorphism among the parents. Metaphor agarose electrophoresis was conducted for 4 hours at a constant 70 V, and polyacrylamide gel for 6 hours at a constant 200 V. Both were stained with ethidium bromide.
Schematic representation showing the relative positions (approximately 55 cM) of six SSR markers in linkage group G (Rhg1) and seven SSR markers in linkage group J (Rmd), used to identify crossovers in F2 genotypes from two-way, four-way, and eight-way crosses.
2.4. Data analysis
The expected 1:2:1 segregation ratio for the inheritance of parental alleles per SSR marker in the F2 population from two-way crosses was tested by chi-square test (Table 3). Genetic variability was analyzed by measuring crossover occurrence as a function of allele frequency changes among the markers. Thus, crossovers were characterized by allele changes among the markers surrounding the SCN and PW resistance genes. All statistical procedures were performed according to the recommendations of Snedecor and Cochran (1956) and Steel and Torrie (1980).
Descriptive parameter, total mean (), standard deviation (σ), variance (σ2), and generation mean (’) for each scheme mating.
3. Results
Chi-square significance was analyzed exclusively for two-way crosses within linkage groups G and J (Table 2).
3.1. Crossover frequency and genotypic variation
The limited polymorphism among the parents, combined with using Hartwig as the sole source of SCN resistance, may explain the low frequency of confirmed crossovers. In linkage group G (Table 3; Figure 1), 107 crossovers were observed for the two-way cross (G2), 212 for the four-way cross (G4), and 72 for the eight-way cross (G8). The highest mean crossover rate per genotype was observed in G4 (4.0), with a standard deviation of 1.47 and a variance of 2.15. When considering the generation mean (based on the number of generations required to form each population), G2 exhibited the highest mean (2.02), followed by G4 (2.00) and G8 (0.45).
3.2. Marker position representation
See Figure 1.
3.3. Descriptive parameters of crosses
See Table 3.
3.4. Frequency distribution of crossovers by genotype
The frequency distribution of genotypes based on detected crossover events was estimated for each mating scheme. For G2, approximately 21% of genotypes displayed no crossover occurrence, while 18.87% displayed one crossover, 26.42% two, 16.98% three, 9.43% four, 5.66% five, and 1.89% six crossovers. In G4, more than 35% of genotypes exhibited five crossovers, with only 1.89% showing no crossover events. In G8, a majority of genotypes (56.60%) showed no allele changes among SSR markers (Figure 2).
Frequency distribution of genotypes by new allele’s recombination number (crossovers) occurred in the three populations in the study, at the linkage group G.
3.5. Analysis for linkage group J
In linkage group J, 53 genotypes were analyzed for J4 and J8, and 33 genotypes for J2 (Table 4). The J8 population exhibited significantly higher crossover rates (154) compared to J4 (62) and J2 (30). J8 also showed the highest total mean of standardized crossovers (2.91), with a standard deviation of 1.16 and a variance of 1.36. The generation mean, based on the number of crosses, was also highest for J8 (0.97), followed by J2 (0.91) and J4 (0.59). In the J2 genotypes, a single crossover event was observed in 60.61% of cases, while 49.09% of J4 genotypes showed one crossover.
Mating schemes with respective genealogy and genotypes number analyzed (#Gen), to each Molecular Linkage Group (MLG) G and J (Cregan et al., 1999).
3.6. Crossover distribution in linkage group J
The J8 population showed a broader distribution of crossover events among genotypes, with approximately 38% and 27% of genotypes exhibiting two and three crossovers, respectively (Figure 3).
Frequency distribution of genotypes by new allele’s recombination number (crossovers) occurred in the three populations in the study, at the linkage group J.
4. Discussion
Chi-square significance analysis was applied only to the two-way crosses in linkage groups G and J, as four-way and eight-way crosses are not expected to exhibit a 1:2:1 segregation ratio. In our study, all SSR markers in the two-way crosses showed nonsignificant chi-square values (P > 0.05), corroborating the expected 1:2:1 inheritance ratio for F2 populations. Similar chi-square patterns have been reported in recent studies, supporting consistent inheritance ratios in soybean genotypes (Liu et al., 2021).
The markers showed low polymorphism, ranging from two to four alleles. This result can be related to the narrow genetic base of soybean and the genealogy of the parents, which may have common ancestors, as indicated by recent studies showing the limited genetic base in Brazilian soybean cultivars (Santos et al., 2022; Zatybekov et al., 2023). A pedigree study found that Roanoke, S-100, CNS, and Tokyo contributed 55.3% of the Brazilian genetic base, emphasizing a shared ancestry with American germplasm (Zatybekov et al., 2023). Additionally, Brazilian and American soybean cultivars share six primary ancestors: CNS, S-100, Roanoke, Tokyo, PI 54,610, and PI 548318 (Saharia and Sarma, 2022). In linkage group G, the parental genotypes showed 30 alleles distributed across six loci, varying from two alleles in markers such as satt217, satt324, and satt115, to three alleles in markers such as sat_210, sat_315, and satt394 (Rani et al., 2023). For linkage group J, which is associated with powdery mildew resistance, the parental genotypes displayed 36 alleles across seven loci, with two alleles for markers like sat_366, satt215, satt380, and sat_165, three for sat_224 and satt547, and four for satt431 (Kumar et al., 2022).
The amplification allele size of a simple locus depends on the motif and tandem sequence repeat (Ramzan and Anwar, 2021). SSR markers have been widely used in genetic studies because they allow detailed detection of genetic variation at the individual, population, and species levels (Rani et al., 2023). The number of alleles per locus can also be influenced by the degree of dissimilarity between parents, as demonstrated in previous work on polymorphism in soybean (Kumar et al., 2022). Additionally, the variability of microsatellite loci is influenced by their relative distance from the centromere and the recombination frequencies observed in specific populations (Saharia and Sarma, 2022). SSR markers are thus highly effective for detecting crossover increments in F2 populations by identifying broken gene blocks and new allelic combinations (Liu et al., 2021). These markers are among the most reliable for detecting polymorphism between parents and are widely used in genetic diversity studies across soybean cultivars in Brazil, the United States, and China (Liu et al., 2021; Rani et al., 2023). Notably, SSRs demonstrate a high rate of polymorphism and efficiently identify unique alleles in elite soybean germplasm compared to other marker systems, further enhancing their value in genetic studies (Kumar et al., 2022; Zatybekov et al., 2023). SSR markers have proven particularly useful in studies identifying associations between cyst nematode resistance loci and soybean productivity, as shown by Ramzan and Anwar (2021).
In our study, the presence of monomorphic markers in the segregant populations was observed for satt217 in G4 and G8, and satt380 in J8. This monomorphism may result from genetic similarity among parents or the limited number of F1 seeds used to establish the populations, which reduces genetic variation and crossover frequency (Santos et al., 2022). Low crossover frequency in these groups maintains existing linkage blocks and preserves epistatic interactions, which has implications for breeding strategies focused on maximizing recombination (Sedivy et al., 2017). The higher recombination level detected in the four-way and eight-way crosses, compared to the two-way scheme, suggests that a substantial amount of additive genetic variance can be exploited in advanced generations. The larger number of parents involved in multiple mating schemes is known to increase crossover occurrences, as seen in (Table 4). The lower generation mean in G4 (2.00) and G8 (0.45) compared to G2 (2.02) can be attributed to the low polymorphism among parentals detected by the markers, which reduces crossover detection capability. This low polymorphism was also observed in linkage group J, though higher values were found for J8 (0.97), J2 (0.91), and J4 (0.56) (Liu et al., 2021).
The high level of allele recombination detected in crosses involving four and eight parents supports the efficiency of multiple crosses in creating genetic variability, as suggested by Kumar et al. (2022). Hybridization strategies like this increase genetic diversity and enhance germplasm banks, a necessity emphasized in soybean breeding research (Stebbins, 1959; Suarez-Gonzalez et al., 2018; Marques et al., 2019; Schley et al., 2022). Depending on the crop’s reproductive cycle, molecular markers like SSRs can significantly shorten selection cycles, thus accelerating selection gains compared to conventional methods (Heffner et al., 2010; Heslot et al., 2015).
While increasing recombination through inter-mating has been proposed as a breeding strategy (Hanson, 1959), previous soybean breeding programs have not always supported maximal recombination for genetic gain. For instance, Piper and Fehr (1987) demonstrated reduced genetic gain when mating schemes were designed solely to increase recombination. In our experiment, however, we could not measure the impact of all crossovers because detecting crossover increments in populations derived from four or eight parents and determining precise recombination regions presented challenges. The allele recombination detected in populations derived from eight-way crosses in linkage group G was limited, likely due to low polymorphism among parents (Saharia and Sarma, 2022).
5. Conclusions
This study demonstrated that the likelihood of detecting crossovers is directly related to the degree of polymorphism among parents, as identified by the markers used. Recombination was observed to be more frequent in populations derived from crosses involving more than two parents. Although developing these populations require greater effort, this is offset by the release of increased genetic variability, which facilitates the selection process.
Acknowledgements
We would like to acknowledge the Coordination for the Improvement of higher Education Personnel (CAPES) for the financial support (code 0001).
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