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Jang and Lee: A Review and Perspective on Soybean (Glycine max L.) Breeding for the Resistance to Phytophthora sojae in Korea

Abstract

Phytophthora root and stem rot (PRR) of soybean is a severe disease that causes significant economic losses in soybean-growing countries. The causal agent, Phytophthora sojae, is a soil-borne oomycete that causes pre- and post-emergence damping-off of soybean in poorly drained soils. PRR has not been a severe problem in South Korea; however, as the cultivation of soybean in paddy fields recently increased, there is a growing interest because the incidence of PRR can be extensively expanded. R-gene mediated resistance is known as the main strategy for the management of this disease. On the other hand, partial resistance has also been known to provide more effective disease management than the Rps (Resistance to Phytophthora sojae) resistance. Responses of domestic soybean cultivars to a few P. sojae isolates were recently reported, while phenotypic distribution of numerous germplasms is mostly unknown. The objectives of this review are to summarize published studies conducted on PRR, to suggest future directions of genetic researches and breeding to the target pathogen. This review will discuss the followings; i) a brief introduction to PRR and the causal agent P. sojae, ii) types of genetic resistance to P. sojae and findings of genes/QTL conditioning to resistance, iii) changes in virulence pathotype of P. sojae populations, and iv) current status and perspective of genetic/genomic researches on the interaction of soybean and P. sojae in the South Korea.

INTRODUCTION

Phytophthora root and stem rot (PRR), caused by Phytophthora sojae Kauffmann and Gerdemann, is one of many soil-borne oomycete pathogens that can infect soybean. Over the last 60 years, many studies have reported the identification and the distribution of this pathogen over the world (Kaufmann and Gerdemann 1958; Ryley et al. 1998; Dorrance et al. 2003; Grau et al. 2004; Sugimoto et al. 2006; Dorrance and Grünwald 2009; Zhang et al. 2010). Due to PRR, a total loss of nearly 20.5 million tons was reported from 1996 to 2014, with an average annual loss of over 1.1 million tones (Wrather et al. 2001; Wrather and Koenning 2006, 2009; Koenning and Wrather 2010; Allen et al. 2017).
PRR was first identified in 1996 in Chungnam province in South Korea (Jee et al. 1998). In recent years, incidences of soybean diseases caused by soil-borne pathogens, including PRR, have been more frequently reported in South Korea (Kang et al. 2019; Kang et al. 2020; Ko et al. 2020). It is considered that as paddy-fields begin to be utilized in the soybean production, root rot diseases tends to occur more in such poorly drained soils. Consequently, attention for such soybean diseases is steadily increasing. The objectives of this review are to introduce soybean genetic researches and breeding efforts for resistance to PRR, and to suggest future directions of researches and breeding programs in South Korea to protect soybean production against the PRR.

Phytophthora root and stem rot (PRR) in soybeans

P. sojae is known to be host-specific, but it can also infect the lupine species (Lupinus spp.) (Dorrance and Grünwald 2009). This pathogen predominantly infects soybean pre-emergence, but as oospores germinate throughout the growing season, soybean plants can be attacked by P. sojae during any stage of the plant development (Dorrance 2018). When it infects susceptible soybean at the early stage of growth, consequently, seed decay and seedling damping-off would be the critical disease symptoms (Schmitthenner 1985). Root rot and brown stem lesions typically develop in susceptible plants during the later stage of growth, along with leaf yellowing, wilting, and finally, plant death, which subsequently results in reduced plant vigor and decreases in the seed yield (Schmitthenner 1985).
It is a monocyclic disease, and P. sojae can withstand freezing and cold temperatures as oospores in both soil and plant debris for several years (Schmitthenner 1985). In warm and highly wet soils, oospores of P. sojae germinate to form mycelia, and then the mycelia produce sporangia and zoospores under those wet conditions. Zoospores are the primary infectious agents of this process. They are attached to soybean roots via chemotaxis, which is done by isoflavones, such as genistein and daidzein (Morris and Ward 1992). Zoospores encyst, germinate, and penetrate the cell wall of soybean roots within a few hours after the inoculation (Morris and Ward 1992). Afterward, P. sojae colonizes the root and stem tissues as reproducing oospores (Schmitthenner 1985).

Diversity of P. sojae population and its effect on the disease management

PRR is managed predominantly through the development of cultivars with one or two dominant resistance genes (Rps). Although the Rps genes are useful, such resistance is race-specific and, thus, they would be effective in limited numbers of P. sojae isolates. Each of the Rps genes have been often effective for less than 15 years as new P. sojae isolates that can evade Rps-mediated defense emerge (Schmitthenner 1985; Dorrance et al. 2003). Some of the Rps genes (Rps1a, 1b, 1c, 1k, 3a, and 6), individually or in combinations of two Rps, have been deployed into cultivars (Dorrance and Schmitthenner 2000; Slaminko et al. 2010). Other Rps genes (1d, 2, 3b, 3c, 4, 5, and 7) have not been commercially deployed because P. sojae populations that can overcome these R genes already existed in fields (Abney et al. 1997). Therefore, understanding the regional distribution of pathotypes of P. sojae is vital for managing the PRR by deploying a few Rps genes into new soybean cultivars.
The diversity of the P. sojae population has been widely studied since the late 1960s in North America, including the United States and Canada (Dorrance 2018). In these locations, the virulence pathotypes of P. sojae isolates were determined based on the responses following the hypocotyl inoculation on 15 differential varieties (Dorrance et al. 2004). The differentials consisted of universal susceptible “Williams” and near-isogenic lines carrying a single Rps gene in the Williams background (Dorrance et al. 2004). Rps1a, 1d, and 1k allele had been widely used in controlling PRR during the 1980s, and subsequently, new races with Rps1d and 1k virulence emerged during the 1990s (Schmitthenner 1985; Abney et al. 1997). Subsequently, the virulence prevalence of Rps1a, 1b, 1c, and 1k has continued to increase in the majority of north-central states in the United States, resulting in that 30-100% of the collected isolates were virulent toward Rps1a, 1b, 1c, and 1k (Dorrance et al. 2016). Until 2000, there were 55 races reported based on the reactions of eight soybean differentials for the Rps1a, 1b, 1c, 1d, 1k, 2, 3a, 6, and 7 genes, which were virulent to a few numbers of Rps genes (Grau et al. 2004). In the early 2000s, the pathotypes of P. sojae isolates were observed to be more complex and diverse (Kaitany et al. 2001; Dorrance et al. 2003; Jackson et al. 2004; Malvick and Grunden 2004; Nelson et al. 2008). In a study conducted during 2012-2013, over 200 unique virulence pathotypes were identified from more than 800 isolates, which were collected in the north-central region of the United States (Dorrance et al. 2016).
Diversity or changes in pathogenecity of P. sojae were also studied in other countries. In China, for instance, P. sojae was first identified in Heilongjiang in 1991 (Su and Shen 1993), and multiple races were subsequently identified until the early 2000s (Ma et al. 2005). Until 2015, the incidence of the pathogen has been reported in the Inner Mongolia Autonomous Region, Fujian Province, Xinjiang Uygur Autonomous Region (Wen and Chen 2002; Zhu et al. 2003; Chen et al. 2004; Liu et al. 2006; Wang et al. 2006; Xiao et al. 2011). Between 2005 and 2007, a total of 96 isolates were collected and investigated for their virulence pathotypes in Heilongjiang Province (Zhang et al. 2010). Of the 8 races identified, 4 races had new pathotypes and some known races were not discovered, implying that P. sojae population in Heilongjiang Province became more diverse during a decade. None of the P. sojae isolates found in Heilongjiang Province was virulent to Rps1c until race 4 and race 5 were found, which can overcome Rps1c (Zhang et al. 2010).
In Japan, the first PRR was reported in 1977 in Hokkaido (Tsuchiya et al. 1990). The virulence of 49 Japanese isolates was determined into 10 pathotypes based on 6 Japanese differential cultivars (Tsuchiya et al. 1990), which revealed distinguished pathotypes from the known 55 American P. sojae races (Grau 2004). This result indicates that genetic differences exist among American and Japanese isolates. Sugimoto et al. (2010) identified that pathotype E is most dominant in P. sojae populations in Japan from screening of 164 isolates collected between 2002 and 2006. Later, more than 100 P. sojae isolates identified from 14 regions were assessed using differential cultivars for 14 Rps genes (Moriwaki 2010). Rps1a, 1b, 1c, 1d, 1k, 3b, 7, and 8 were found to provide resistance against 47-81% of the assessed isolates. Rps1d and 1k were the most effective resistance genes (Moriwaki 2010).
In Brazil, the P. sojae population presents a different origin. Of 37 isolates collected in six Brazilian states, 17 pathotypes were determined and, surprisingly, all the Brazilian pathotypes differ from previously known pathotypes (Costamilan et al. 2013). It probably has been under different selection pressure by Rps genes that unknowingly exist in Brazilian soybean cultivars (Costamilan et al. 2013). The isolates in the Brazilian population were highly variable for their virulence to seven different Rps genes of the 14 Rps. Consequently, Rps1a, 1c, and 1k were highly recommended to utilize in breeding programs in Brazil, while Rps1a and 1c are not effective in the United States (Costamilan et al. 2013).

R-gene mediated resistance to P. sojae in soybean

Soybean genotypes have different reactions to different isolates of P. sojae (Kaufmann and Gerdemann 1958). With regards to fungicide application to the seeds, genetic resistance of soybeans has taken the roles in the disease management. Mainly, two types of genetic resistance are described in soybean–P. sojae system; R-gene mediated resistance and partial resistance (Schmitthenner 1985).
R-gene mediated resistance, conditioned by single dominant Rps genes, generally provides race-specific and complete resistance. Exceptionally, the Rps2 gene was known to provide root-specific and incomplete resistance that limits the colonization of infection on the soybeans (Mideros et al. 2007). As a result, Rps-mediated resistance has provided effective protection against the majority of P. sojae populations in the United States (Dorrance et al. 2018). Table 1 summarizes all the Rps alleles that were reported to date, their genomic positions, and flanking molecular markers used in the genetic mapping. The first Rps gene was identified in the 1950s (Bernard et al. 1957). More than 30 Rps alleles have been identified and mapped to nine chromosomes as follow: Rps1a, 1b, 1c, 1d, 1k, 7, 9, UN1, YU25, YD29, HN, Q, WY, HC18, X, and Waseshiroge on chromosome 3; Rps3a, 3b, 3c, 8, and SN10 on chromosome 13; Rps4, 5, 6, 12, and JS on chromosome 18; Rps2 and UN2 on chromosome 16; Rps10 on chromosome 17; Rps11 on chromosome 7; RpsZS18 on chromosome 2; RpsSu on chromosome 10; and RpsYB30 on chromosome 19 (Table 1) (Demirbas et al. 2001; Weng et al. 2001; Burnham et al. 2003a; Sandhu et al. 2004; Gordon et al. 2007; Sugimoto et al. 2007; Yu et al. 2010; Sugimoto et al. 2011; Sun et al. 2011; Lin et al. 2013; Sun et al. 2014; Cheng et al. 2017; Li et al. 2017; Niu et al. 2017; Sahoo et al. 2017; Zhong et al. 2017).
A few genomic regions have been repeatedly detected in multiple genetic mapping using bi-parent populations. Especially, a genomic region of ∼1.5 Mb on chromosome 3 is a hot spot, where resistance was identified in over ten previous studies using different resistance sources (Fig. 1). Many copies of R-gene type sequences were predicted in a recent genome annotation Wm82.a2.v1 (Glyma2.0) (available at http://soybase.org). Li et al. (2016) fine-mapped RpsUN1 in a 151-kb interval on chromosome 3 and RpsUN2 in a 36-kb interval on chromosome 16, where multiple copies of R-gene type annotation are found. Relative abundance of transcripts of selected candidate genes for RpsUN1 and UN2 (i.e. Glyma.03g034400 and Glyma.16g214900) also varied between the two parents (i.e. Williams and PI 567139B). Nucleotide-binding site leucine-rich repeat (NBS-LRR) proteins are typically encoded by the majority of disease resistance genes in plants (McHale et al. 2006). Thus, many studies highlighted the NBS-LRR containing genes in their candidate regions for R genes. Cheng et al. (2017) mapped RpsWY in a 35 kb-region of chromosome 3 through a high-resolution genetic mapping with ∼200 F7:8 recombinant inbred lines (RIL) and suggest four genes (Glyma03g04350, Glyma03g04360, Glyma03g04370, and Glyma03g04380) as candidates. Unlike Li et al. (2016), non-NBS-LRR types of genes have also been proposed as candidates for another Rps allele on chromosome 3 in this study (Cheng et al. 2017). Of the published Rps loci, Rps1 was most characterized and known to contain a cluster of coiled-coil (CC)-NBS-LRR type R genes (Bhattacharyya et al. 2005). Four copies of closely related CC-NBS-LRR gene isolated from the Rps1k genotype indicated that at least two of these copies (Rps1k-1 and Rps1k-2) function in steric resistance. Similarly, the Rps4-Rps6 locus contains multiple copies of the NBS-LRR gene, and the deletion of the NBS-LRR sequence in Rps4 locus was associated with loss of resistance to P. sojae (Sandhu et al. 2004). These studies imply that specificities of certain Rps might be regulated by haplotypes or copy number variations, rather than single genes.
Rps-mediated resistance is known to follow gene-for-gene interaction (Flor 1955). Individual isolates of P. sojae may possess one or more avirulence (Avr) genes corresponding to each of the existing Rps genes of soybean in their genome (Tyler 2007). Soybean Rps genes are thought to activate an effector-triggered immune response, like the well-characterized R-gene in other pathosystems (Jones and Dangl 2006; Dong et al. 2011). In P. sojae-infected plants, the expression of defense responses was determined based on the interaction between the proteins encoded by the Rps genes and the effector proteins encoded by the Avr genes. Direct or indirect interaction between such resistance proteins and cognate Avr proteins of pathogens leads to hypersensitive responses in the form of programmed cell death in infected cells; subsequently, the spread of the pathogen becomes limited locally (Bent and Mackey 2007; Tyler 2007).

Partial resistance to P. sojae in soybean

Partial resistance is an alternative form of genetic resistance that has been used in soybean fields against P. sojae, which is quantitatively inherited by multiple genes, and effective against a wide range of P. sojae races (Schmitthenner 1985). It is also known as rate-limiting resistance, field tolerance, incomplete resistance, or non-race specific resistance (Tooley and Grau 1984; Walker and Schmitthenner 1984). This type of genetic resistance can be expressed in the form of reduced infection efficiency, reduced lesion size, and fewer oospores produced within the infected tissues (Mideros et al. 2007). This resistance has been shown to reduce yield loss in the presence of P. sojae, but not to negatively impact on yield even in the absence of the disease (St. Martin et al. 1994).
Partial resistance had moderate to high heritability, thus can be improved through the selection of resistance. Typically, the levels of partial resistance are determined using lesion length measurement, tray test, root rot score, inoculum layer test, or field evaluation (Tooley and Grau 1984; Dorrance et al. 2008). The soybean cultivar ‘Conrad’ was extensively studied for the resistance through the quantitative trait locus (QTL) analysis with several biparental populations, because it does not have Rps genes but exhibits high partial resistance (Burnham et al. 2003b; Han et al. 2008; Li et al. 2010; Wang et al. 2010; Stasko et al. 2016). Some common QTLs were identified against three isolates of P. sojae in a ‘Conrad’ × ‘Sloan’ population, indicating that common defense responses may occur in responsive to the individual isolates inoculated (Stasko et al. 2016). Two loci on chromosome 19 were highlighted in Wang et al. (2010) and Stasko et al. (2016), which were highly significant and effective to multiple isolates.
Hundreds of germplasm with high levels of partial resistance to P. sojae have been identified (Dorrance and Schmitthenner 2000) and some of them were used for identification of QTL for the target trait as listed in Table 2 (Burnham et al. 2003b; Tucker et al. 2010; Wang et al. 2010; Nguyen et al. 2012; Lee et al. 2013a, 2013b, 2014; Abeysekara et al. 2016). The majority of QTL were found to have minor effects, while some were responsible for more than 20% of phenotypic variation (Tucker et al. 2010; Lee et al. 2014). Several QTLs were repeatedly identified in multiple populations with different resistance sources, suggesting that those genomic regions are more likely to contain some key genes conditioning the partial resistance (Table 2).
Although the mechanisms of partial resistance are largely unknown, there is evidence that several studies provided evidences to support different mechanisms for partial resistance. Much higher levels of suberin were formed in the roots of Conrad and growth of hyphae of P. sojae was retarded in Conrad in comparison of a susceptible line, suggesting that colonization of P. sojae may be suppressed by pre-formed suberin (Thomas et al. 2007; Ranathunge et al. 2008). Expression of genes underlying the identified QTL revealed that signal transduction, hormone-associated defense pathway, and defeated Rps genes might be associated with high partial resistance in Conrad (Wang et al. 2012). High levels of sequence variation were identified in the upstream, intron, and downstream regulatory regions of the genes within the QTL on chromosome 19 (Wang et al. 2012). In two plant introductions (PIs) 398841 and 407861A, with high levels of partial resistance to P. sojae, a few of QTL for the partial resistance were mapped near known Rps loci; for instance, a region of Rps1 and Rps7 on chromosome 3 and a region of Rps3 and Rps8 on chromosome 13 (Lee et al. 2013a, 2013b). These results support that weak or defeated form of Rps genes may contribute to high levels of partial resistance to P. sojae because the two PIs did not have any Rps gene effective to the inoculated isolates.

Perspective on genetic researches and breeding for resistance to P. sojae in South Korea

Kang et al. (2019) reported the presence or absence of Rps-mediated resistance in major soybean cultivars grown in S. Korea against 4 isolates, where the resistance reactions were observed only in ∼5 of the accessed 21 cultivars per isolate. Ten of the assessed cultivars were susceptible to all the inoculated isolates, which implies that major soybean cultivars are potentially under threat of this pathogen (Kang et al. 2019). Genetic resistance is a desirable and effective method in crop protection from various biotic stresses; thus, it is important for researchers/breeders to research soybean–P. sojae interaction via various approaches for successes in disease management of PRR. Fig. 2 highlights collaborative future researches to support better protection from PRR, which consists of two parts, i.e. soybean genetics/breedng and pathology.
Genetic diversity provides an essential key in plant breeding (Carter et al. 2004). A vast number of soybean germplasm are available in South Korea, as an origin of soybean, and a wide range of genetic diversity exists among them (Jeong et al. 2019). The germplasm have not been evaluated for Rps or partial resistance to P. sojae to date. Thus, it should be the first priority to identify soybean germplasm from continuous phenotypic screenings against many P. sojae isolates. A core collection of Korean cultivated soybean germplasm was recently defined and used to evaluate phenotypic variations and to dissect genetic architectures of multiple traits such as seed composition, seed size/color, and agronomic traits (Jeong et al. 2019). Since the core collection represents genetic diversity with minimal repeatability across the Korean soybean germplasm collection, it will be reasonable to conduct initial phenotypic screening with this representative of Korean cultivated soybean germplasm. Subsequently, the discovered resistant germplasm will need to be characterized to identify R-genes/QTL associated with resistance to P. sojae. This process can be conducted using a collection of hundreds of germplasm or bi-parental populations developed from segregating parents for the target traits. In addition to the core collection, the Korean soybean nested association mapping (NAM) population, which consisted of 27 F6-derived RIL population, is another valuable resource for dissecting genetic architecture of complex traits. These plant materials were genotyped with hundred thousands of single nucleotide polymorphism (SNP) markers, which will facilitate high resolution of genetic analyses after disease phenotypes are obtained. Identificaiton of resistance genes/QTL will be followed by further omic-based characterization for soybean-P. sojae molecular interactions as genetic research purposes. As well, fine mapping of the target gene and marker development for selection will lead to development of new Phytophthora-resistant cultivars.
Deploying Rps genes is a primary way to genetically improve existing susceptible varieties in a viewpoint of soybean breeding. Intense use of a few resistance varieties, however, has led selective pressures on the pathogen for changes in its ability to overcome the defenses (Abney et al. 1997). The utilization of various Rps genes will benefit to attenuate selective pressure on P. sojae populations caused by respective deployed Rps genes; consequently, increased occurrence of new virulence pathotypes is possibly delayed (Schmitthenner 1985). The selection of partial resistance combined with a few Rps genes is also recommended for the long-term management of PRR by avoiding boom and bust cycles in a single Rps locus (Buzzell and Anderson 1992). A recent study demonstrated genetic gains from selections for a major QTL for partial resistance to P. sojae (Karhoff et al. 2019). The introgressions of a resistance allele from the respective PI 427105B and PI 427106 improved the levels of resistance to P. sojae by ∼20% and ∼40%, respectively, and the yield by 13-29% under diseased condition (Karhoff et al. 2019).
On the other hand, understanding of the pathogen contributing valuable information for disease management because the pathogen also co-evolves as plant defense responses develop, a.k.a an evolutionary arm-race (Anderson et al. 2010). Kang et al. (2019) reported that although a small number of isolates were tested, the variability of virulence pathotypes also existed among the isolates, suggesting that dominant virulence pathotypes may differ across geographical regions. Therefore, it is highly requried to continue to collect P. sojae isolates as many as possible from fields, and to evaluate them with the designated differential varieties. Monitoring the changes in pathotypes among P. sojae populations overtimes will be a greatly valuable study because pathotype changes in P. sojae populations have been one of the significant hurdles in combating against P. sojae in several countries as stated above. Such tracking research will also assist to select a few effective Rps genes based on the dominant pathotypes of P. sojae observed in soybean fields. For this, at the same time, the addition of new differentials is strongly recommended as new Rps genes were discovered. The differential varieties for 14 Rps genes, developed in the United States, have been used to characterize P. sojae isolates in the majority of recent studies. Some recent studies have identified novel Rps genes (i.e. Rps10 and Rps11) in genomic locations distinct from the previously known Rps loci (Table 1). These additional differentials will improve the ability of diagnoses for the variability of pathotypes in P. sojae populations for current and future characterization.

CONCLUDING REMARKS

The study on the interaction between soybean and soil-borne oomycete pathogen P. sojae has relatively long histories in the United States, China, Japan, and other countries. This review provided a general introduction to PRR and its causal agent and summarized the results of published researches regarding Rps genes and QTL analysis to understand the resistance and pathotype diversity of P. sojae population. It is evident that PRR and other possible soil-borne diseases threaten the soybean production in South Korea. In this circumstance, proposed genetic researches should be conducted to provide a framework for effective management of newly-emerging diseases and to develop disease-resistant soybean varieties, which will be helpful to reduce yield losses caused by P. sojae in the future.

ACKNOWLEDGEMENTS

This research was funded by a grant from Chungnam National University.

Notes

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest.

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Fig. 1
A genomic region on chromosome 3 where several resistance genes to Phytophthora sojae were mapped. Lines between the two black points present the marker interval of each Rps gene/allele as reported in the publications. The dashed part of the interval presents outside of 2.0-6.0 Mbp.
PBB-8-114-f1.tif
Fig. 2
Schematic diagram of interdisciplinary researches suggested for soybean resistance to Phytophthora sojae in South Korea.
PBB-8-114-f2.tif
Table 1
A list of Rps genes/alleles and associated SNP/SSR markers reported in the previous studies.
Chr.z) (LG) Rpsy) Position1 (Mbp)x) Position2 (Mbp)x) Flanking marker 1y) Flanking marker 2y) Reference
1 (D1a) - 44.4 44.6 ss715579469 ss715579474 Niu et al. 2018
2 (D1b) RpsZS18 46.6* 44.3 Sat_069 (BARCSOYSSR_02_1540) Sat_183 (BARCSOYSSR_02_1602) Yao et al. 2010
3 (N) Rps1a 3.2 3.9 Satt159 (BARCSOYSSR_03_0180) Satt009 (BARCSOYSSR_03_0226) Weng et al. 2001
3 (N) Rps1b 3.4 5.7 Satt152 (BARCSOYSSR_03_0192) Satt530 Demirbas et al. 2001
3 (N) Rps1c 3.4 9.2 Satt152 (BARCSOYSSR_03_0192) Satt584 (BARCSOYSSR_03_0442) Demirbas et al. 2001
3 (N) Rps1d 3.4 3.5* Satt152 (BARCSOYSSR_03_0192) Sat_186 (BARCSOYSSR_03_0204) Sugimoto et al. 2007
3 (N) Rps7 3.9 18.4 Satt009 (BARCSOYSSR_03_0226) Satt125 (BARCSOYSSR_03_0564) Weng et al. 2001
3 (N) Rps9 2.9 3.5* Satt631 (BARCSOYSSR_03_0162) Sat_186 (BARCSOYSSR_03_0204) Wu et al. 2011a
3 (N) RpsUN1 3.2 4.3 Satt159 (BARCSOYSSR_03_0180) BARCSOYSSR_03_0250 Lin et al. 2013
3 (N) RpsYU25 3.5* 5.7 Sat_186 (BARCSOYSSR_03_0204) Satt530 Sun et al. 2011
3 (N) RpsYD29 3.9 4.1 SattWM82-50 Satt1k4b Zhang et al. 2013b
3 (N) RpsHN 4.2 4.5 SSRSOYN-25 SSRSOYN-44 Niu et al. 2017
3 (N) RpsQ 3.0 3.1 BARCSOYSSR_03_0165 InDel281 Li et al. 2017
3 (N) - 3.9 4.5 Satt009 (BARCSOYSSR_03_0226) T0003044871 Sugimoto et al. 2011
3 (N) RpsWY 2.9 3.4 Satt631 (BARCSOYSSR_03_0162) Satt152 (BARCSOYSSR_03_0192) Cheng et al. 2017
3 (N) RpsHC18 4.5 4.6 BARCSOYSSR_03_0269 BARCSOYSSR_03_0272 Zhong et al. 2017
3 (N) RpsX 2.9 3.2 InDelxz6 BARCSOYSSR_03_0175 Zhong et al. 2019
7 (M) Rps11 5.1 5.2 BARCSOYSSR_07_0266 BARCSOYSSR_07_0278 Ping et al. 2015
10 (O) RpsSu 1.0 39.4 Satt358 Sat_242 (BARCSOYSSR_10_1104) Wu et al. 2011b
13 (F) Rps3 31.8 32.7 Satt510 (BARCSOYSSR_13_1219) Satt335 (BARCSOYSSR_13_1271) Gordon et al. 2007
13 (F) Rps8 24.3 28.9 Satt425 (BARCSOYSSR_13_0784) Satt114 (BARCSOYSSR_13_1055) Gordon et al. 2006
13 (F) RpsSN10 16.6 16.9 Satt423 (BARCSOYSSR_13_0264) Satt149 (BARCSOYSSR_13_0245) Yu et al. 2010
16 (J) Rps2 1.6 34 Satt287 (BARCSOYSSR_16_0090) Satt547 (BARCSOYSSR_16_1165) Demirbas et al. 2001
16 (J) RpsUN2 36.9 37.3 BARCSOYSSR_16_1275 Sat_144 (BARCSOYSSR_16_1294) Lin et al. 2013
16 (J) - 4.0* - BARC-014467-01559 - Huang et al. 2016
17 (D2) Rps10 30.8 31.1 Sattwd15-24 Sattwd15-47 Zhang et al. 2013a
18 (G) Rps4 54.5 56.3 Satt191 (BARCSOYSSR_18_1750) Sat_064 (BARCSOYSSR_18_1858) Sandhu et al. 2004
18 (G) Rps5 - 53.9 - Satt472 (BARCSOYSSR_18_1708) Sahoo et al. 2017
18 (G) Rps6 54.5 - Satt191 (BARCSOYSSR_18_1750) Sat_372 Gordon et al. 2007
18 (G) Rps12 56 56.3 BARCSOYSSR_18_1840 Sat_064 (BARCSOYSSR_18_1858) Sahoo et al. 2017
18 (G) RpsJS 56.3 56.6 BARCSOYSSR_18_1859 BARCSOYSSR_18_1864 Sun et al. 2014
19 (L) RpsYB30 33.9 34.8 Satt497 (BARCSOYSSR_19_0760) Satt313 (BARCSOYSSR_19_0788) Zhu et al. 2007
20 (I) - 46.6* - BARC-013645-01207 - Huang et al. 2016

z)Chr., Chromosome; LG, Linkage group.

y)Indicated with a hyphen (-), if the Rps gene name or marker position is not available.

x)Approximate physical positions with an asterisk (*) are based on genome assembly Glyma.Wm82.a1, while others based on Glyma.Wm82.a2.

Table 2
A list of QTL for partial resistance to Phytophthora sojae in the previous studies.
Chr. (LG)z) Position1 (bp)y,x) Position2 (bp)y,x) Flanking marker1 Flanking marker2 PVE (%)w) Plant materials (Mapping population) Reference
1 (D1a) 50164447 50295635 BARC_2.0_Gm01_50164447 BARC_2.0_Gm01_50295635 4.5 Conrad × Sloan Stasko et al. 2016
1 (D1a) 50206347 50287274 BARC_2.0_Gm01_50206347 BARC_2.0_Gm01_50287274 8.2 Conrad × Sloan Stasko et al. 2016
1 (D1a) 50560774 51398886* BARCSOYSSR_01_1400 BARC-020113-04470 4.6 OX20-8 × PI398841 Lee et al. 2013a
1 (D1a) 50560774 50157973* BARCSOYSSR_01_1400 BARC-054071-12319 5.6 Combined population Lee et al. 2014
1 (D1a) 50572171 50797061 BARC_2.0_Gm01_50572171 BARC_2.0_Gm01_50797061 7.6 Conrad × Sloan Stasko et al. 2016
2 (D1b) 4549894* 5455404* BARC-065787-19749 BARC-056237-14178 10.7-11.4 PI399036 × AR3 Abeysekara et al. 2016
2 (D1b) 653563* 4901498* BARC-041773-08087 BARC-016573-02145 2.3 OX20-8 × PI398841 Lee et al. 2013a
2 (D1b) 14288241 19688108 Satt266 (BARCSOYSSR_02_0727) Satt579 (BARCSOYSSR_02_0855) 15.9 Conrad × Harosoy Burnham et al. 2003b
2 (D1b) 19688108 29355267 Satt579 (BARCSOYSSR_02_0855) Satt600 (BARCSOYSSR_02_1048) 10.6 Conrad × Sloan Burnham et al. 2003b
2 (D1b) 19688108 29355267 Satt579 (BARCSOYSSR_02_0855) Satt600 (BARCSOYSSR_02_1048) 20.7 Conrad × Williams Burnham et al. 2003b
2 (D1b) 19688108 34875449 Satt579 (BARCSOYSSR_02_0855) Sat_089 (BARCSOYSSR_02_1152) 5-28 Conrad × Hefeng25 Li et al. 2010
2 (D1b) 27699285 29355267 Satt005 (BARCSOYSSR_02_0998) Satt600 (BARCSOYSSR_02_1048) 11-22 Conrad × Hefeng25 Li et al. 2010
2 (D1b) - 45267040 OPL18800 Satt274 (BARCSOYSSR_02_1663) 2-10 Conrad × OX760-6-1 Han et al. 2008
2 (D1b) 50529114* 51243188* BARC-042881-08448 BARC-019805-04379 12.1-14.6 PI399036 × AR2 Abeysekara et al. 2016
PI399036 × AR3
2 (D1b) 51243188* 51550018* BARC-019805-04379 BARC-906743-01012 5.6 PI399036 × AR2 Abeysekara et al. 2016
3 (N) 2993784* - BARC-028645-05979 BARC-010837-00763 2.8 OX20-8 × PI398841 Lee et al. 2013a
3 (N) 2993784* 5656713 BARC-028645-05979 BARCSOYSSR_03_0317 3.0 OX20-8 × PI407861A Lee et al. 2013b
3 (N) 3225968* - Gm03_3225968 - 21.1 Germplasm (n=169) Ludke et al. 2019
3 (N) 3852827 - ss715585712 - - Germplasm (n=797) Schneider et al. 2016
3 (N) 3865669 - ss715585728 - - Germplasm (n=797) Schneider et al. 2016
3 (N) 4276473 - ss715586320 - - Germplasm (n=797) Schneider et al. 2016
3 (N) 4277319 - ss715586321 - - Germplasm (n=797) Schneider et al. 2016
3 (N) 4315451 - ss715586376 - - Germplasm (n=797) Schneider et al. 2016
3 (N) 5217414* - Gm03_5217414 - 13.9 Germplasm (n=169) Ludke et al. 2019
3 (N) 37047526* 38032013* BARC-050433-09624 BARC-010179-00543 6.7-6.9 PI399036 × AR2 Abeysekara et al. 2016
3 (N) 38834669 44771010* Sat_091 (BARCSOYSSR_03_1348) Sat_125 (BARCSOYSSR_03_1546) 4.0 OX20-8 × PI407861A Lee et al. 2013b
3 (N) 41065116 41146728* Sat_241 (BARCSOYSSR_03_1469) BARC-020101-04452 3.9 Combined population Lee et al. 2014
4 (C1) 57542* 3930569* BARC-038359-10052 BARC-021219-04011 2.5 OX20-8 × PI398841 Lee et al. 2013a
4 (C1) 57542* 2069791* BARC-038359-10052 BARC-054289-12451 2.0 OX20-8 × PI407861A Lee et al. 2013b
4 (C1) 8061903* 38604410* BARC-024445-04886 BARC-061079-17031 2.0 OX20-8 × PI407861A Lee et al. 2013b
4 (C1) 38604410* 43684322* BARC-061079-17031 BARC-042189-08197 1.9 OX20-8 × PI398841 Lee et al. 2013a
4 (C1) 45977762 46204517 BARC_2.0_Gm04_45977762 BARC_2.0_Gm04_46204517 3.2 Conrad × Sloan Stasko et al. 2016
4 (C1) 46096228 46536196 BARC_2.0_Gm04_46096228 BARC_2.0_Gm04_46536196 3.2 Conrad × Sloan Stasko et al. 2016
5 (A1) 33679928* 34294649* BARC-031361-07059 BARC-018011-02495 7.9 PI399036 × AR3 Abeysekara et al. 2016
6 (C2) 17218677 - Satt277 (BARCSOYSSR_06_0920) Satt365 9-21 Conrad × Hefeng25 Li et al. 2010
6 (C2) 23848501 31490622 Satt489 (BARCSOYSSR_06_1129) Satt100 (BARCSOYSSR_06_1202) 5-21 Conrad × Hefeng25 Li et al. 2010
6 (C2) 44049891 46820673 Satt460 (BARCSOYSSR_06_1456) Satt307 (BARCSOYSSR_06_1581) 4-7 Conrad × Hefeng25 Li et al. 2010
6 (C2) 7023397* 20218893 Satt520 (BARCSOYSSR_06_0386) Satt557 (BARCSOYSSR_06_1041) 4.3 Su88-M21 × Xinyixiaoheidou Wu et al. 2011c
6 (C2) 21775764* 46063373* BARC-040475-07751 BARC-062515-17881 4.7-5.5 PI399036 × AR2 Abeysekara et al. 2016
7 (M) 2471949* 6404814* BARC-029825-06442 BARC-042815-08424 11.6-12.4 PI399036 × AR3 Abeysekara et al. 2016
7 (M) 5899427* 14931953* BARC-028455-05917 BARC-065353-19384 2.4 OX20-8 × PI398841 Lee et al. 2013a
8 (A2) 17232172 - Satt233 (BARCSOYSSR_08_0960) Satt437 4-17 Conrad × Hefeng25 Li et al. 2010
8 (A2) 9492376* 21435976* BARC-057257-14650 BARC-060405-16674 14.5-15.9 PI 399036 × AR3 Abeysekara et al. 2016
8 (A2) 24848378* 44053323* BARC-051883-11286 BARC-042715-08379 7.0 OX20-8 × PI407861A Lee et al. 2013b
9 (K) 15487393 - BARC_2.0_Gm09_15487393 - 4.5-7.4 Conrad × Sloan Stasko et al. 2016
9 (K) 1280743* 2330196* BARC-007972-00189 BARC-051275-11075 7.1 PI399036 × AR3 Abeysekara et al. 2016
9 (K) 37144807* 38300154* BARC-017625-02635 BARC-055533-13402 29.9 PI399036 × AR3 Abeysekara et al. 2016
9 (K) 38300154* 38383165* BARC-055533-13402 BARC-007999-00186 21 PI399036 × AR3 Abeysekara et al. 2016
10 (O) 10091607 43788256 Satt420 (BARCSOYSSR_10_0507) Sat_274 (BARCSOYSSR_10_1353) 7.7 Su88-M21 × Xinyixiaoheidou Wu et al. 2011c
10 (O) 39359642* 44753498* BARC-060257-16508 BARC-015925-02017 4.0 OX20-8 × PI407861A Lee et al. 2013b
11 (B1) 34173104 - Satt453 (BARCSOYSSR_11_1468) Satt484 5-14 Conrad × Hefeng25 Li et al. 2010
12 (H) 1687387 - Satt353 (BARCSOYSSR_12_0068) OSU31 4.6 Conrad × Sloan Wang et al. 2010
12 (H) 7494659* 9770096* BARC-019775-04370 BARC-025943-05179 5.7 PI399036 × AR2 Abeysekara et al. 2016
12 (H) 14578917* 33153095* BARC-061985-17608 BARC-018895-03034 4.0 Combined population Lee et al. 2014
13 (F) 6216988 13134055 Satt509 (BARCSOYSSR_11_0342) Satt030 (BARCSOYSSR_13_0445) 6-13 Conrad × OX760-6-1 Han et al. 2008
13 (F) 8587948 10392903 Satt325 (BARCSOYSSR_13_0639) Satt343 (BARCSOYSSR_13_0518) 9-10 Conrad × Hefeng25 Li et al. 2010
13 (F) 10392903 - Satt343 (BARCSOYSSR_13_0518) OPG16600 2-8 Conrad × OX760-6-1 Han et al. 2008
13 (F) 16454986 16855019 Satt252 (BARCSOYSSR_13_0272) Satt149 (BARCSOYSSR_13_0245) 32.4 Conrad × Sloan Burnham et al. 2003b
13 (F) 16454986 16600399 Satt252 (BARCSOYSSR_13_0272) Satt423 (BARCSOYSSR_13_0264) 35.0 Conrad × Harosoy Burnham et al. 2003b
13 (F) 16454986 16855019 Satt252 (BARCSOYSSR_13_0272) Satt149 (BARCSOYSSR_13_0245) 21.4 Conrad × Williams Burnham et al. 2003b
13 (F) 16855019 17875691 Satt149 (BARCSOYSSR_13_0245) Satt160 (BARCSOYSSR_13_0196) 2.0 Conrad × Sloan Wang et al. 2010
13 (F) 27656895 30236183 Sat_234 (BARCSOYSSR_13_0981) BARCSOYSSR_13_1131 16.1 OX20-8 × PI398841 Lee et al. 2013a
13 (F) 27656895 30236183 Sat_234 (BARCSOYSSR_13_0981) BARCSOYSSR_13_1131 8.0 OX20-8 × PI407861A Lee et al. 2013b
13 (F) 28506083 35072147 Sat_154 (BARCSOYSSR_13_1029) Sat_375(BARCSOYSSR_13_1385) 20.1-35.8 S99-2281 × PI408105A Nguyen et al. 2012
13 (F) 28912864 31802559 Satt114 (BARCSOYSSR_13_1055) Satt510 (BARCSOYSSR_13_1219) 7.0 V71-370 × PI407162 Tucker et al. 2010
13 (F) 29685828 29647017 BARCSOYSSR13_1106 BARCSOYSSR13_1103 10.6 Combined population Lee et al. 2014
13 (F) 30739608 30739608* Sct_033 (BARCSOYSSR_13_1230) Sct_033 (BARCSOYSSR_13_1230) 5.4 Conrad × Sloan Wang et al. 2010
13 (F) 30765997 - ss715615031 - - Germplasm (n=797) Schneider et al. 2016
13 (F) 38566546* - BARC-061571-17276 BARC-013325-00484 5.7 PI399036 × AR3 Abeysekara et al. 2016
14 (B2) 7132730* 8339923* BARC-050249-09527 BARC-064873-18956 5.9 PI399036 × AR3 Abeysekara et al. 2016
14 (B2) 8642719* 13086766 Satt416 (BARCSOYSSR_14_0485) Satt304 (BARCSOYSSR_14_0646) 4.7 Conrad × Sloan Wang et al. 2010
15 (E) 2740854* 2893732* BARC-055329-13210 BARC-062899-18147 4.6 PI399036 × AR3 Abeysekara et al. 2016
15 (E) 2740854* 3581354 BARC-055329-13210 BARCSOYSSR_15_0160 7.0 OX20-8 × PI407861A Lee et al. 2013b
15 (E) 3639988 3591774 BARC_2.0_Gm15_3639988 BARC_2.0_Gm15_3591774 2.0 Conrad × Sloan Stasko et al. 2016
15 (E) 4415019* 5522858* BARC-054257-12408 BARC-028907-06042 6.7-7.3 PI399036 × AR2 Abeysekara et al. 2016
15 (E) 6823519 13653981 Satt651 (BARCSOYSSR_15_0306) Satt598 (BARCSOYSSR_15_0645) 15.9 Su88-M21 × Xinyixiaoheidou Wu et al. 2011
15 (E) 1541381* 5522858* BARC-018923-03037 BARC-028907-06042 2.6 OX20-8 × PI398841 Lee et al. 2013a
15 (E) 18422604* - Gm15_18422604 - 18.4 Germplasm (n=169) Ludke et al. 2019
16 (J) 486741 807114 BARC_2.0_Gm16_486741 BARC_2.0_Gm16_807114 5.1 Conrad × Sloan Stasko et al. 2016
16 (J) 3124736 3362395 BARC_2.0_Gm16_3124736 BARC_2.0_Gm16_3362395 3.5-5.4 Conrad × Sloan Stasko et al. 2016
16 (J) 8909747 23417256 Satt414 Satt529 (BARCSOYSSR_16_0703) 22-32 V71-370 × PI407162 Tucker et al. 2010
16 (J) 8909747 14155157 Satt414 Satt596 13-21 Conrad × OX760-6-1 Weng et al. 2007
16 (J) 36544070* 36732606* BARC-011625-00310 BARC-048135-10500 3.9 Combined population Lee et al. 2014
17 (D2) 7756014* 8360833* BARC-058841-15463 BARC-052295-11407 7.6-12.7 PI 399036 × AR3 Abeysekara et al. 2016
17 (D2) 18425834 31915278* Satt514 (BARCSOYSSR_17_0930) Satt574 (BARCSOYSSR_17_1164) 7.1 Conrad × Sloan Wang et al. 2010
17 (D2) 20378955 20352435* Sat_300 (BARCSOYSSR_17_0988) BARC-023721-03465 7.5-8.8 S99-2281 × PI408105A Nguyen et al. 2012
18 (G) 2296656* 2833147* BARC-025777-05064 BARC-047665-10370 19.4 Combined population Lee et al. 2014
18 (G) 2419864 - Sat_163 (BARCSOYSSR_18_0143) SLP142 10-11 V71-370 × PI407162 Tucker et al. 2010
18 (G) 56710850 56876857 BARC_2.0_Gm18_56710850 BARC_2.0_Gm18_56876857 13.6 Conrad × Sloan Stasko et al. 2016
18 (G) 56710850 56766936 BARC_2.0_Gm18_56710850 BARC_2.0_Gm18_56766936 5.3 Conrad × Sloan Stasko et al. 2016
18 (G) 54810869* 57797198* BARC-040163-07672 BARC-041331-07965 3.0 OX20-8 × PI407861A Lee et al. 2013b
18 (G) 57797198* 60488428* BARC-041331-07965 BARC-044363-08678 3.6 OX20-8 × PI398841 Lee et al. 2013a
19 (L) 42821735* 46116996 BARC-047496-12943 BARC_2.0_Gm19_46116996 4.6 Conrad × Sloan Stasko et al. 2016
19 (L) 43036918 - Satt527 (BARCSOYSSR_19_1214) OSU10 4.6 Conrad × Sloan Wang et al. 2010
19 (L) 43533689 44370710 BARCSOYSSR_19_1243 BARCSOYSSR_19_1286 3.1 Conrad × Sloan Stasko et al. 2016
19 (L) 44370710 46116996 BARCSOYSSR_19_1286 ss715635553 9.1 Conrad × Sloan Stasko et al. 2016
19 (L) 47528116 47787869 BARCSOYSSR_19_1452 Glyma.19G226100 4.1-7.8 Conrad × Sloan Stasko et al. 2016
19 (L) 47114567* 48609875* BARC-064609-18739 BARC-039977-07624 8.5-8.9 PI399036 × AR2 Abeysekara et al. 2016
19 (L) 49121197 - ss715635897 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 49461521 - ss715635934 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50305134 50222676* BARC_2.0_Gm19_50305134 BARC-014385-01342 6.6 Conrad × Sloan Stasko et al. 2016
19 (L) 50544302 - ss715636056 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50555372 - ss715636059 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50604872 - ss715636064 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50663405 - ss715636073 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50666502 - ss715636076 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50668601 - ss715636077 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50680353 - ss715636083 - - Germplasm (n=797) Schneider et al. 2016
19 (L) 50681202 - ss715636084 - - Germplasm (n=797) Schneider et al. 2016
20 (I) 343168* 1747664* BARC-042281-08231 BARC-057033-14543 6.8-7.4 PI 399036 × AR3 Abeysekara et al. 2016
20 (I) 25275083 - Satt239 (BARCSOYSSR_20_0543) Sat_105 7-12 V71-370 × PI407162 Tucker et al. 2010
20 (I) 26484795* 35176184* BARC-046570-12662 Sat_268 (BARCSOYSSR_20_0855) 1.9 OX20-8 × PI398841 Lee et al. 2013a

z)Chr., Chromosome; LG, Linkage group.

y)Indicated with a hyphen (-) if the information is not available.

x)Approximate physical positions with an asterisk (*) are based on genome assembly Glyma.Wm82.a1, while others based on Glyma.Wm82.a2.

w)Phenotypic variance (%) explained by the identified QTL.

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