Soybean Mosaic Virus: a Successful Potyvirus with a Wide Distribution but Restricted Natural Host Range M

Plant Pathology and Microbiology Publications Plant Pathology and Microbiology

2017 Soybean mosaic virus: A successful potyvirus with a wide distribution but restricted natural host range M. R. Hajimorad University of Tennessee, Knoxville

L. L. Domier U.S. Department of Agriculture

S. A. Tolin Virginia Tech

S. A. Whitham Iowa State University, [email protected]

M. A. Saghai Maroof Virginia Tech Follow this and additional works at: http://lib.dr.iastate.edu/plantpath_pubs Part of the Agricultural Science Commons, Agriculture Commons, Plant Breeding and Genetics Commons, and the Plant Pathology Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ plantpath_pubs/206. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html.

This Article is brought to you for free and open access by the Plant Pathology and Microbiology at Iowa State University Digital Repository. It has been accepted for inclusion in Plant Pathology and Microbiology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Soybean mosaic virus: A successful potyvirus with a wide distribution but restricted natural host range

Abstract Taxonomy. Soybean mosaic virus (SMV) is a species within the genus Potyvirus, family Potyviridae that includes almost a quarter of all known plant RNA viruses affecting agriculturally important plants. The Potyvirus genus is the largest of all genera of plant RNA viruses with 160 species.

Particle. The filamentous particles of SMV, typical of potyviruses, are about 7,500 Å long and 120 Å in diameter with a central hole of about 15 Å in diameter. Coat protein residues are arranged in helice of about 34 Å pitch having slightly less than 9 subunits per turn.

Genome. The MVS genome consists of a single-stranded positive-sense polyadenylated RNA of approximately 9.6 kb with a virus-encoded protein (VPg) linked at the 5' terminus. The eg nomic RNA contains a single large open reading frame (ORF). The polypeptide produced from the large ORF is processed proteolytically by three viral-encoded proteinases to yield about 10 functional proteins. A small ORF, partially overlapping the P3 cistron, pipo, is encoded as a fusion protein in the N-terminus of P3 (P3N+PIPO).

Biological properties. SMV’s host range is restricted mostly to two plant species of a single genus; Glycine max (cultivated soybean) and G. soja (wild soybean). SMV is transmitted by aphids non-persistently and by seeds. Variability of SMV is recognized by reactions on cultivars with dominant resistance (R) genes. Recessive resistance genes are not known.

Geographical distribution and economic importance. As a consequence of its seed transmissibility, SMV is present in all soybean growing areas of the world. SMV infections can reduce significantly seed quantity and quality (e.g., mottled seed coats, reduced seed size and viability, and altered chemical composition).

Control. The most effective means of managing losses from SMV are planting virus-free seeds and cultivars containing single or multiple R genes.

Key attractions. The interactions of SMV with soybean genotypes containing different dominant R genes and understanding functional role(s) of SMV-encoded proteins in virulence, transmission and pathogenicity have been intensively investigated. The MVS -soybean pathosystem has become an excellent model for examining the genetics and genomics of uniquely complex gene-for-gene resistance model in a crop of worldwide importance.

Disciplines Agricultural Science | Agriculture | Plant Breeding and Genetics | Plant Pathology

Comments This is a manuscript of an article published as Hajimorad, M.R., Domier, L.L., Tolin, S.A., Whitham, S.A. and Saghai Maroof, M.A. (2017), Soybean mosaic virus: A successful potyvirus with a wide distribution but restricted natural host range. Molecular Plant Pathology. doi: 10.1111/mpp.12644.

This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/plantpath_pubs/206 Rights Works produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The onc tent of this document is not copyrighted.

This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/plantpath_pubs/206 Soybean mosaic virus: A successful potyvirus with a wide distribution but restricted natural host range

M.R. Hajimorad1*#, L.L. Domier2#, S.A. Tolin3, S.A. Whitham4, and M.A. Saghai Maroof5

1Department of Entomology and Plant Pathology, The University of Tennessee, Knoxville, TN 37996, USA 2United States Department of Agriculture-Agricultural Research Service and Department of Crop Sciences, University of Illinois, Urbana, IL 61801, USA 3Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA 24061, USA 4Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA 50011, USA 5Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, VA 24061 USA

Running title: Soybean mosaic virus

Keywords: Potyviridae, RNA viruses, virus-host interactions, R-genes, avirulence/virulence proteins, signaling, host responses

Total words: Running title (3); Summary (349); Text (6995); Figures (5 including 3 colored); Table (1)

*Correspondence: Email: [email protected] #These authors equally contributed to this work.

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an ‘Accepted Article’, doi: 10.1111/mpp.12644

This article is protected by copyright. All rights reserved. SUMMARY Taxonomy. Soybean mosaic virus (SMV) is a species within the genus Potyvirus, family Potyviridae that includes almost a quarter of all known plant RNA viruses affecting agriculturally important plants. The Potyvirus genus is the largest of all genera of plant RNA viruses with 160 species.

Genome. The SMV genome consists of a single-stranded positive-sense polyadenylated RNA of approximately 9.6 kb with a virus-encoded protein (VPg) linked at the 5' terminus. The genomic RNA contains a single large open reading frame (ORF). The polypeptide produced from the large ORF is processed proteolytically by three viral-encoded proteinases to yield about 10 functional proteins. A small ORF, partially overlapping the P3 cistron, pipo, is encoded as a fusion protein in the N-terminus of P3 (P3N+PIPO).

Control. The most effective means of managing losses from SMV are planting virus-free seeds and cultivars containing single or multiple R genes.

This article is protected by copyright. All rights reserved. pathosystem has become an excellent model for examining the genetics and genomics of uniquely complex gene-for-gene resistance model in a crop of worldwide importance.

INTRODUCTION Soybean mosaic virus (SMV) is one of 39 viruses in the Bean common mosaic virus (BCMV) lineage of potyviruses, most of which originated in South and East Asia (Gibbs, 2008). SMV can cause significant damage in soybean and is present worldwide. SMV has a very narrow host range and apart from soybean, natural infection has been documented only in Passiflora spp., Pinellia ternate, Senna occidentalis and Vigna angularis (Almeida et al., 2002; Chen et al., 2004; Benscher et al., 1996; Sun et al., 2008; Yoon et al., 2017). The SMV determinants for host specificity have not been mapped; however, it appears HC-Pro does not play a major role (Hajimorad et al., 2016). A role for P1 in adaptation of SMV to Pinellia ternata has been hypothsized (Chen et al., 2004; Valli et al., 2007); however, direct experimental evidence is lacking. Experimentally, SMV infects plant species belonging to the genera of Lespedeza, Phaseolus, Pisum, Nicotiana, Vigna, and Zantedeschia (Gao et al., 2015b; Hunst and Tolin, 1982; Ross, 1969). SMV is naturally transmitted by aphid species in a non-persistent manner and via infected seeds. Foliar symptoms vary from moderate to severe leaf mottling, distortion of leaves, necrosis and overall stunting and occasionally death of the infected plants. Seeds derived from the infected plants often exhibit mottling (Fig. 1). Yield losses as high as 86% were reported in uniformly infected field plots (Goodman and Oard, 1980; Hill et al., 1987; Pfeiffer et al., 2003; Ren et al., 1997a,b; Song et al., 2016a; Tu, 1989). The extent of damage to the crop is dependent on the host genotype, predominant virus strain, infection incidence, and the developmental stage at which soybean plants become infected. (Goodman et al., 1979; Goodman and Oard, 1980; Hill et al., 1980; Zhang et al., 1986). Infections that occur after flowering and infection incidences less than 25% usually have little impact on yields or seed quality (Bowers and Goodman, 1979; Ren et al., 1997a; Song et al., 2016a). Current reviews on various aspects of SMV are available (Cui et al., 2011; Hill and Whitham, 2014; Liu et al., 2016; Saghai Maroof et al., 2008a; Whitham et al., 2016).

TRANSMISSION

This article is protected by copyright. All rights reserved. Aphid transmission. SMV has been experimentally transmitted in a non-persistent manner by more than 35 species of aphids (Irwin and Goodman, 1981). However, a much smaller number of aphid species have been found to transmit SMV in the field. In the north central United States, Aphis craccivora, Macrosiphum euphorbiae, Myzus persicae, Rhopalosiphum maidis, and R. padi, were responsible for more than 90% of the transmissions in the field (Halbert et al., 1981). In Thailand, M. persicae, and A. gossypii were the most significant vectors of SMV (Banziger and Hengsawad, 1985). Even though A. glycines is capable of transmitting SMV experimentally (Clark and Perry, 2002; Hill et al., 2001), it is a poor vector in the field (Wang and Ghabrial, 2002). The growth rates of A. glycines on SMV-infected plants often are significantly lower than on healthy soybean plants (Cassone et al., 2015; Donaldson and Gratton, 2007; Penaflor et al., 2016). SMV isolates can differ significantly in their rates of transmission by a single aphid species (Domier et al., 2003; Lucas and Hill, 1980; O'Connell-Ziegler et al., 1986).

Aphid Transmission Determinants. Interactions between helper-component proteinase (Fig. 2) (HC-Pro) and coat protein (CP) are important for aphid transmission of SMV (Jossey et al., 2013; Kang et al., 2006; Seo et al., 2010). HC-Pro acts as a bridge between aphid stylets and virus particles (Ng and Falk, 2006). Within HC-Pro, the KITC (KLSC in SMV) motif is thought to be involved in binding aphid stylets. The PTK motif in HC-Pro is thought to interact with the DAG motif near the exposed amino terminus of the CP (Atreya et al., 1990; Blanc et al., 1997, 1998; Kendall et al., 2008; Shukla, et al., 1988). The KLSC and PTK motifs in HC-Pro, and the DAG motif in CP, have been confirmed to be involved in SMV aphid transmission (Jossey et al., 2013; Seo et al., 2010). Additional amino acid sequences near the carboxyl terminus of HC-Pro and the putatively exposed carboxyl terminus of CP have been implicated in aphid transmissibility of SMV (Jossey et al., 2013; Kang et al., 2006;; Seo et al., 2010).

Seed transmission. Transmission through seed is an important factor in the epidemiology of SMV in China and North America (Goodman et al., 1979; Goodman and Oard, 1980; Hill et al., 1980; Zhang et al., 1986). Rates of seed transmission vary from 0% to 64% depending on the genotype of virus and soybean (Bowers and Goodman, 1991; Domier et al., 2007; Porto and Hagedorn, 1975). The SMV protein 1 (P1), HC-Pro and CP cistrons are determinants for seed transmission (Jossey et al., 2013). Within the CP, the DAG motif and an amino acid substitution

This article is protected by copyright. All rights reserved. near the putatively exposed carboxyl terminus of CP were important for seed transmission and virus-induced seed-coat mottling. The findings that SMV HC-Pro and CP are involved in both aphid and seed transmission is supported by observations that SMV field isolates poorly transmitted by A. glycines also were poorly transmitted through seed (Domier et al., 2007). RNA silencing is suggested to play an important role in both seed transmission and virus- induced seed-coat mottling. Regions on soybean chromosomes 4 and 6 containing homologues of Arabidopsis genes DICER-LIKE 3 (DCL3) and RNA DEPENDENT RNA POLYMERASE 6 (RDR6) encoding enzymes involved in RNA silencing are associated with both seed transmission of SMV and SMV-induced seed-coat mottling (Domier et al., 2011). Infection of soybean by SMV, and by other viruses that express strong suppressors of RNA silencing, often induce mottling of soybean seed coats in a host and virus strain-specific manner (Bowers and Goodman, 1991; Domier et al., 2007; Hobbs et al., 2003). The mottling of soybean seed coats in plants infected with SMV results from partial suppression of RNA silencing of chalcone synthase mRNAs by SMV HC-Pro (Senda et al., 2004).

VARIABILITY Diversity among SMV isolates was first recognized when some resistant soybean lines became infected by SMV isolates (Ross, 1969, 1975). Isolates also varied in symptomatology, seed transmission, aphid transmission, ultrastructural effects, and to some extent experimental host range. Cho and Goodman (1979) developed a system to categorize SMV isolates in the US into seven strain groups (G1-G7) based on phenotypic responses of a set of susceptible and resistant soybean cultivars. This system is also used in Brazil, Iran, Korea, and Ukraine (Ahangaran et al., 2013; Almeida, 1981; Anjos et al., 1985; Choi et al., 2005; Cho et al., 1977; Sherepitko et al., 2011). In Japan and China alternative strain classification systems were reported. The Japanese system classifies SMV isolates into strains A, B, C, D, and E and considers both biological and sequence data (Saruta et al., 2005). The Chinese system uses several soybean differential lines to classify SMV strains SC1-21 (Li et al., 2010b; Ma et al., 2016; Wang et al., 2003). Complete genome sequences were first reported for SMV strains G2 and G7 (Jain et al., 1992; Jayaram et al., 1991, 1992). Since then, a rapidly increasing number of complete genome sequences of isolates from China, Iran, Japan, Korea and North America have been determined, enableing studies of virus evolution in relation to inoculum source and deployed resistance genes

This article is protected by copyright. All rights reserved. (Ahangaran et al., 2013; Chen et al., 2017b; Chowda-Reddy et al., 2011a; Domier et al., 2011; Hajimorad et al., 2003; Saruta et al., 2005; Seo et al., 2009a; Zhou et al., 2015; ). Analyses showed that SMV cistrons were subject to different selection pressures (Seo et al., 2009b; Zhou et al., 2015). For example, changes in pathotype prevalence in Korea since the early 1970s was correlated with changes in cytoplasmic inclusion (CI) and HC-Pro sequences (Cho et al., 1977; Kim et al., 2003; Choi et al., 2005; Li et al., 2014). Phylogenies constructed from non- recombinant full-length SMV sequences show four distinct clades and significant genetic differences among SMV isolates from China and from both Korea and the US (Chen et al., 2017b; Zhou et al., 2015). Intra- and interspecific recombination was common in China, including recombinants with BCMV suggesting that overcoming host resistance may involve recombination, as well as mutational events in the diversification of SMV populations (Seo et al., 2009b; Yang et al., 2014; Zhou et al., 2014).

GENOME ORGANIZATION AND EXPRESSION The SMV genome consists of a single-stranded positive-sense RNA of approximately 9,600 nucleotides harboring a single large open reading frame (ORF) (Jayaram et al., 1992). The genome is polyadenylated at the 3' end and has a virus-genome linked protein (VPg) covalently attached at the 5' end. The translated polyprotein is processed by three SMV encoded proteinases to produce a series of multifunctional proteins which include P1, HC-Pro, protein 3 (P3), 6K1, CI, 6K2, nuclear inclusion a (NIa), nuclear inclusion b (NIb), and CP. Self-cleavage of NIa yields two additional proteins, VPg and the protease domain (Fig. 2). The SMV genome also harbors pipo (Chung et al., 2008; Wen and Hajimorad, 2010). The pipo of SMV, the first to be described in potyviruses movement, is expressed as a fusion protein (P3N+PIPO) as a consequence of transcriptional slippage (Chung et al., 2008; Cui et al., 2017; Olspert et al., 2015; Rodamilans et al., 2015; Vijayapalani et al., 2012; Wen and Hajimorad, 2010; White, 2015). SMV particles have served as model to study symmetry of flexuous viruses by a combination of cryo-electron microscopy, X-ray fiber diffraction, and scanning transmission electron microscopy (Kendall et al., 2008). The mechanism of SMV replication, the genome organization and strategy for expression have been extrapolated largely based on studies conducted on other model potyviruses such as Tobacco etch virus (Eggenberger et al., 1989;

This article is protected by copyright. All rights reserved. Ghabrial et al., 1990; Vance and Beachy, 1984a,b). Excellent review articles describe these aspects of potyviruses (Ivanov et al., 2014; Lopez-Moyo et al., 2009; Revers and Garcia, 2015).

FUNCTIONS OF ENCODED PROTEINS SMV-encoded proteins have been subjects of limited studies. Host-specific interaction of SMV P1 with a mature Rieske Fe/S protein suggested that P1 is involved in symptom development and host adaptation (Shi et al., 2007). SMV HC-Pro has a role in aphid transmission and in suppression of gene silencing (Li et al., 2014; Lim et al., 2005, 2011; Jossey et al., 2013; Senda et al., 2004). Interactions between P3 and P3N+PIPO with small subunit of RubisCO have been associated with symptom development (Lin et al., 2011). Furthermore, interaction of P3 with soybean actin-depolymerizing factor 2 suggests a role in virus movement (Lu et al., 2015). Interaction of SMV P3N-PIPO with Golgi SNARE 12 may play a role in plasmodesmata targeting (Song et al., 2016b). The roles of HC-Pro and P3 in virulence (i.e. ability to overcome resistance mediated by a defined R gene) and pathogenicity (i.e. the ability to induce severe symptoms and enhanced virus accumulation in susceptible soybeans) have been demonstrated (Ahangaran et al., 2013; Chowda-Reddy et al., 2011a; Eggenberger et al., 2008; Hajimorad et al., 2003, 2005, 2006, 2008, 2011; Khatabi et al., 2012, 2013; Lim et al., 2007; Seo et al., 2011; Wang et al., 2015; Wang and Hajimorad, 2016; Wen et al., 2013). SMV pipo is involved in movement, but not in virulence on Rsv1-genotype soybeans (Wen and Hajimorad, 2010; Wen et al., 2011). The SMV 6K1 protein localizes to the periphery of infected cells suggesting a possible involvement in cell-to-cell movement (Hong et al., 2007). Involvement of CI in virulence and pathogenicity is well known (Seo et al., 2009a; Zhang et al., 2009). Protease activity of NIa was demonstrated and its consensus proteinase cleavage sequences identified (Ghabrial et al., 1990). CP is involved in cell-to-cell and long-distance movement as well as aphid and seed transmission (Jayaram et al., 1991, 1998; Jossey et al., 2013; Seo et al., 2010, 2013). As SMV represents a typical potyvirus, the role(s) of its encoded proteins in the infection cycle are expected to be analogous to those of model potyviruses where function(s) have been established experimentally. Reviews on potyviral encoded proteins and their roles have been published recently (Revers and Garcia, 2015; Rohozkova and Navratil, 2011; Sorel et al., 2014; Vali et al., 2017).

Extensive research has been conducted on the SMV-soybean pathosystem to identify and characterize genes conferring resistance to and interacting with various SMV strains. These efforts have been facilitated by the availability of genetics, virology and genomics resources including SMV strains, differential soybean cultivars, near isogenic lines, recombinant inbred lines, and high density linkage maps. The soybean genome sequence and affordable resequencing and RNA-sequencing have accelerated the progress leading to the identification of candidate genes for Rsv and Rsc (Table 1).

Dominant genes Rsv1, Rsv3, Rsv4, and Rsv5 confer resistance to the US SMV strains and have been mapped to three chromosomes 2, 13, and 14 (Saghai Maroof et al.; 2008a; Klepadlo et al., 2017b) (Table 1). Genes conferring resistance to SC strains are designated as Rsc followed by a strain identifier used in the Chinese system (Li et al., 2010b). Many of the Rsc genes have been mapped to the same three chromosomes as Rsv genes (Table 1). One gene, Rsc15 conferring resistance to SMV strain SC15, maps uniquely to chromosome 6 (Yang and Gai, 2011). Allelic relationship between the Rsv and Rsc loci have not been examined. No recessive genes for resistance to SMV have been described. The Rsv1 locus was identified in PI96983 (Kiihl and Hartwig 1979). Any Rsv1 genotype soybean, displays extreme resistance (ER) to avirulent SMV strains that, by definition, are asymptomatic and remain undetectable in inoculated leaves (Fig. 3A). No significant changes in gene expression in response to inoculation with an avirulent SMV strain were observed (Zhang et al., 2012). Graft-mediated inoculation of Rsv1-genotype soybean with an avirulent SMV resulted in a limited hypersensitive response (HR) associated with resistance (Hajimorad and Hill, 2001). SMV strain G7 induces local HR and a lethal systemic HR (LSHR), possibly a consequence of “weak elicitor” function resulting in a delayed defense response (Hajimorad et al., 2003, 2005; Wen et al., 2013).

The Rsv1 (PI96983) locus has been found to be extremely complex, with at least ten Rsv1 alleles recognized, namely Rsv1-c (Corsica), Rsv1-d (FT-10), Rsv1-h (Suweon97), Rsv1-k (Kwangyyo), Rsv1-m (Marshall), Rsv1-n (PI507389), Rsv1-r (Raiden), Rsv1-s (LR1, PI486355), Rsv1-t (Ogden), and Rsv1-y (York) (Chen et al., 1991, 2001, 2002; Ma et al., 1995, 2003; Moon et al., 2009; Shakiba et al., 2013). Rsv1-y in York was recently renamed as a new gene, Rsv5,

This article is protected by copyright. All rights reserved. and mapped near Rsv1 (Chen et al., 1991; Klepadlo et al., 2017b). The resistance gene in Raiden was initially assigned to Rsv2 since it differed from the Rsv gene in PI96983 (Buzzell & Tu, 1984; Kiihl & Hartwig, 1979). Its gene assignment was changed to Rsv1-r once allelism with Rsv1 was demonstrated using OX670, which had Raiden in its ancestry (Chen et al., 2001; Gunduz et al. 2001).

The dominant Rsv1 gene has been mapped to chromosome 13 (MLG F). Rsv1 is highly complex and has been extensively studied as discussed above and exemplified by the citations in Table 1. Hayes et al. (2004) identified a cluster of nucleotide-binding-leucine rich repeat (NB- LRR)-type R-gene candidates in PI96983, and demonstrated multiple genes within this cluster interacted to condition unique responses to SMV strains. A coiled-coil NB-LRR (CC-NB-LRR)- type R-gene, 3gG2 (Glyma13g190800) was identified as a strong candidate for Rsv1. Yang et al. (2013) mapped Rsc-ps and Rsc-pm conditioning resistance to SC3, SC6, SC7, and SC17 to the same chromosomal region. Recently, Ma et al. (2016) mapped Rsv1-h, which confers resistance to G1-G7, SC-6N and SC-7N strains, to a 97.5 Kb region and identified two CC-NB-LRR type R-gene candidates in the Rsv1 chromosomal region. More detail on the Rsv1 chromosomal interval is provided in Table 1.

The dominant gene Rsv3 was first identified in OX686 (Buzzell and Tu, 1989). Later, it was also identified in L29, Harosoy (Rsv3-hs), Tousan140, Hourei, and OX670 (Buss et al., 1999; Gunduz et al., 2001, 2002). Soybean cultivars with Rsv3 are resistant to SMV strains G5-G7, but susceptible to strains G1-G4. Rsv3 alleles with differential responses to SMV strains have been identified in PI61947 (Rsv3-h) and PI399091 (Rsv3-c) (Shakiba et al., 2012a). Cervantes- Martinez et al. (2015) identified a new Rsv3 allele, Rsv3-n, in PI61944. Other soybean cultivars, PI91346, Tej-sen-da-aj-pi and Kolhida 4, contain new but as yet uncharacterized Rsv3 alleles (Li et al., 2010a).

Rsv3 was fine mapped to a region of 154 kb on Chromosome 14 (MLG B2) in a cluster of five similar CC-NB-LRR genes (Suh et al., 2011). Comprehensive sequence analysis of the five genes from susceptible and resistant lines suggested Glyma14g38533 as the most likely candidate gene for Rsv3 (Redekar et al., 2016). In China, Wang et al. (2011a) also fine mapped Rsc4 from cv. Dabaima to an interval of <100 kb on the same chromosomal region and identified three CC-NB-LRR candidate genes including Glyma14g38533. Li et al. (2016) silenced the three

The dominant Rsv4 locus was initially recognized in PI486355 in association with an Rsv1-s allele. It was subsequently isolated in a line among crosses with Essex, and released as V94-5152 germplasm (Buss et al., 1997; Ma et al., 1995). Unlike Rsv1 and Rsv3, the Rsv4 in V94-5152 soybean was resistant with no necrotic responses to G1-G7 strains (Buss et al., 1997; Ma et al., 1995). The Rsv4 gene was also identified in PI88788 in which local infection by SMV-G1 and SMV-G4 was detected (Gunduz et al., 2004). Thus, Rsv4 appears to permit limited replication in inoculated leaves (Fig. 3C), and to delay and restrict systemic movement (Chowda-Reddy et al., 2011a; Gunduz et al., 2004; Ilut et al., 2016; Khatabi et al., 2012; Wang et al., 2015). A number of US field isolates have been found to be virulent on PI88788 (Khatabi et al., 2012). Nevertheless, resistance mediated by Rsv4 in V94-5152 is robust and alteration in the corresponding SMV avirulence factor is required for gain of virulence (Fig. 4E). Alleles of Rsv4 with interactions different from G1 and G4 were identified in Beeson (Rsv4-b) and Shin2 (Shakiba et al., 2013; Li et al., 2010a). The Rsv4-v allele in PI438307 (Klepadlo et al., 2016) gives reactions distinct from those of V94-5152 and PI88788 (Gunduz et al., 2004). Two new Rsv4 sources in Haman and Ilpumgeomjeong accessions have been identified from Korea (Ilut et al., 2016).

Rsv4 was fine mapped to a region of 94 kb on chromosome 2 (MLG D1B) through a targeted association analysis using resequencing data from 19 accessions to identify eleven candidate genes (Ilut et al., 2016). Unlike the Rsv1 and Rsv3 loci, the Rsv4 region lacked genes similar to known R-genes, suggesting that Rsv4 functions via a potentially novel resistance mechanism (Ilut et al., 2016). Additional candidate SMV resistance genes on chromosome 2 have been identified for Rsv4 and for Rsc7, Rsc8, and Rsc18 (Klepadlo et al., 2017a; Li et al., 2015; Wang et al., 2011b; Yan et al., 2015; Zhao et al., 2016) (Table 1).

SMV DETERMINANTS CONFERRING AVIRULENCE/VIRULENCE SMV has evolved mechanism(s) to counter resistance mediated by the R-genes and naturally occurring virulent SMV strains have been identified. By taking advantage of these naturally evolved virulent SMV, as well as experimentally evolved virulent variants, combined with

This article is protected by copyright. All rights reserved. comparative genomics, construction of recombinant viruses and site-directed mutagenesis, the determinants of SMV conferring avirulence/virulence on soybean genotypes containing each of the Rsv loci have been identified as discussed in brief below.

Avirulence/virulence determinants on Rsv1. Virulent field isolates of SMV on Rsv1-genotype soybeans are infrequent, but have been reported in Korea (Ahangaran et al., 2013; Choi et al., 2005; Khatabi et al., 2012; Seo et al., 2009b; Viel et al., 2009). The determinant of SMV provoking Rsv1-mediated LSHR has been mapped to P3 with the residues identified (Hajimorad et al., 2003, 2005). Indirect evidence suggests HC-Pro is also capable of provoking Rsv1- mediated LSHR (Khatabi et al., 2013; Seo et al., 2011; Wen et al., 2013). Gain of virulence on soybeans containing the entire Rsv1 locus requires concurrent mutations in both HC-Pro and P3 (Fig. 4A-B). Many observations suggest both viral genetics and the soybean background expressing the Rsv1 locus influence selection of virulence mutations (Eggenberger et al., 2008; Hajimorad et al., 2003, 2008, 2011; Wen et al., 2013). This was not considered by Chowda- Reddy et al. (2011b) who used chimeric SMV to map the determinants and concluded CI, in addition to P3 and HC-Pro, also is involved. Recognition of both HC-Pro and P3 by Rsv1 is not a deviation from gene-for-gene theory as the Rsv1 locus contains multiple R genes recognizing independently HC-Pro and P3 (Hajimorad et al., 2011; Hayes et al., 2004; Wen et al., 2011, 2013). The R gene(s) recognizing HC-Pro allows limited replication of an avirulent SMV at inoculation site whereas the gene recognizing P3 confers ER (Hajimorad et al., 2011; Wen et al., 2011, 2013). These closely related R-genes within the Rsv1 locus remain to be identified and characterized, but it appears 3gG2 targets P3 for recognition (Wen et al., 2011, 2013). Gain of virulence on Rsv1-genotype soybeans is associated with fitness loss on susceptible soybeans mainly as a consequence of HC-Pro mutation(s) (Khatabi et al., 2013). The requirement for multiple mutations in HC-Pro or P3 for gain of virulence on Rsv1-genotype soybeans (Fig. 4A-C) combined with a consequential fitness penalties could explain a limited presence of resistance-breaking SMV isolates.

Avirulence/virulence determinant on Rsv3. The Rsv3 locus in soybean L29 produces ER (Fig. 3B) or allows for limited replication of avirulent SMV isolates (G5-G7) at the site of inoculation (Seo et al., 2009a; Zhang et al., 2009). Regardless, an avirulent SMV remains restricted to the

This article is protected by copyright. All rights reserved. inoculated leaves. SMV strains virulent on L29 induce either mosaic or LSHR (Seo et al., 2009a; Zhang et al., 2009). The avirulence determinant provoking Rsv3-mediated resistance has been mapped to CI where a single amino acid residue converts avirulence to virulence (Fig. 4D) (Seo et al., 2009a; Zhang et al., 2009). CI is also a pathogenicity factor (Seo et al., 2009a; Zhang et al., 2009). Despite its dual roles in virulence and pathogenicity, virulent SMV isolates on Rsv3 are frequent around the world (Ahangaran et al., 2013; Choi et al., 2005; Khatabi et al., 2012; Seo et al., 2009b; Viel et al., 2009). Interestingly, Rsv3-virulent SMV isolates, e.g., the G2 isolate SMV-N, are highly pathogenic on susceptible cultivars (Hajimorad and Hill, 2001; Khatabi et al., 2013; Wang and Hajimorad, 2016; Zhang et al., 2009). The widespread presence of Rsv3-breaking isolates is contradictory to the hypothesis proposed by Chowda-Reddy et al., (2011b) that multiple simultaneous mutations in multiple SMV-encoded proteins are required for gain of virulence. If multiple mutations in multiple SMV-encoded proteins are requirements for gain of virulence by avirulent SMV on Rsv3, one expects such an R genes remain durable (Harrison, 1982).

Avirulence/virulence determinants on Rsv4. Amino acids substitutions at three positions of P3 independently confer avirulence/virulence to SMV on Rsv4 soybeans (Fig. 4D). However, the genetic composition of P3 influences the selection of the amino acid (Ahangaran et al., 2013; Chowda-Reddy et al., 2011a; Khatabi et al., 2012; Wang et al., 2015). Using chimeric viruses, Chowda-Reddy et al., (2011b) hypothesized that multiple SMV-encoded proteins are involved in virulence of SMV on Rsv4 soybeans, but findings by others do not support this hypothesis (Ahangaran et al., 2013; Khatabi et al., 2012; Wang et al., 2015). Gain of virulence mutations in Rsv4-genotype soybean is associated with a fitness penalty on susceptible soybeans suggesting a positive influence on the durability of Rsv4 (Wang and Hajimorad, 2016).

SIGNALING AND HOST RESPONSES A variety of approaches have been used to identify changes in host gene expression that influence compatible and incompatible SMV-soybean interactions. In this section we highlight major conclusions from these studies.

This article is protected by copyright. All rights reserved. Signaling and host responses in compatible interactions. Microarray expression profiling of the responses of a susceptible soybean cultivar to SMV strain G2 provided evidence for induction of stress and defense-like responses and down-regulation of photosynthesis- and cell wall-related genes, among other changes (Babu et al., 2008). In addition, basal defense pathways that involve the signaling proteins ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) and PHYTOALEXIN DEFICIENT 4 (PAD4), which function upstream of salicylic acid (SA), appear to be involved in limiting SMV infection, even in compatible interactions (Wang et al., 2014). Virus-induced gene silencing (VIGS) of GmEDS1 or GmPAD4 allowed greater accumulation of SMV G5 in a susceptible cultivar. Silencing a nuclear-localized heat shock protein (HPS) 40 gene suppressed basal soybean defenses and enhanced susceptibility to SMV (Liu and Whitham, 2013). When SA-based defenses are constitutively activated in SMV- susceptible soybeans by silencing expression of MITOGEN-ACTIVATED PROTEIN KINASE 4 (GmMPK4) or GmMPK6, plants develop enhanced resistance to SMV (Liu et al., 2011, 2014). However, silencing of GmMPK4 and GmMPK6 negatively impacted soybean growth and development demonstrating that constitutive SA-based defenses are not likely to be an effective approach for disease control in soybean (Liu et al., 2011, 2014). Although SMV may activate and be partially limited by basal defenses, it induces changes in cellular physiology that favor virus accumulation. The SMV P3 protein interacts with eukaryotic elongation factor 1A (eEF1A), a GDP:GTP binding protein that delivers aminoacylated tRNAs to ribosomes (Luan et al., 2016). The guanine nucleotide exchange factor eEF1B recycles eEF1A to the active GTP-bound form. VIGS of both eEF1A and eEF1B reduces SMV virulence suggesting that these proteins are essential for virulence (Luan et al., 2016). In addition, VIGS of these genes prevents an endoplasmic reticulum stress response to SMV. Chemicals like dithiothreitol and tunicamycin induce the unfolded protein response and in doing so promote SMV infection. However, the endoplasmic reticulum stress response to these chemicals is impaired when eEF1A is silenced, and they cannot promote SMV infection. It was proposed that P3 targets eEF1A to elicit the unfolded protein response that promotes SMV accumulation. Chen et al. (2016) used RNA sequencing to investigate changes in soybean mRNA and small RNA accumulation, and the mRNA degradome at 14 days post inoculation in a susceptible cultivar in response to three different compatible SMV isolates. Their data suggested that SMV infection affected a variety of regulatory networks. Yin et al. (2013) found that 11 microRNAs

This article is protected by copyright. All rights reserved. (miRNAs) were upregulated and three miRNA families were down regulated in susceptible soybean at 4 hours post infection (hpi) with SMV strain SC7. More recently, Bao et al. (2017) showed that SMV infection upregulates miRNAs that regulate antiviral gene silencing components (AGO1, AGO2, DCL1, and DCL2) and genes encoding NBS-LRR proteins. SMV infection down regulated the expression of the miRNA target genes, and interestingly, when the activity of the miRNAs were inhibited, plant tissues became less susceptible to SMV. These data suggest that SMV may inhibit antiviral defenses, in part, through upregulation of miRNAs.

Signaling and host responses in incompatible interactions. A significant amount of research has focused on identifying factors that function in Rsv1 signaling. The Rsv1-mediated ER has been difficult to study directly. However, the Rsv1-mediated LSHR that occurs on the whole plant level has been exploited to investigate Rsv1-mediated defense responses. Silencing of soybean homologous of RAR1 and SGT1 enabled systemic movement of SMV G2 in Rsv1 plants (Fu et al., 2009), indicating that the encoded proteins are necessary for proper Rsv1 function. Silencing of soybean homologous of HSP90, which often function in complexes with RAR1 and SGT1 to control R protein stability and function, did not result in systemic SMV G2 movement (Fu et al., 2009). However, Zhang et al. (2012) showed that silencing GmHSP90 enabled local replication and movement of a GUS-tagged SMV-G2. The combined results suggest that Rsv1 requires the chaperone HSP90 and co-chaperones RAR1 and SGT1 for proper function and expression of ER in response to avirulent SMV isolates. A long-scale VIGS identified genes required for Rsv1 function. This screen employed a SMV G2 expressing the uida gene, which enabled identification of a loss-of-ER phenotype (Fig. 5A) (Zhang et al., 2012). Using this approach, 82 VIGS clones were screened, and GmEDS1, GmPAD4, GmHSP90, GmJAR1, GmEDR1, GmWRKY6, and GmWRKY30 were required for Rsv1 resistance. R proteins typically signal through either EDS1 and PAD4 or NDR1, and consistent with this GmNDR1 was not associated with Rsv1 signaling in two different studies (Selote and Kachroo, 2010, Zhang et al., 2012). Based on genes identified by Zhang et al. (2012) and Fu et al. (2009), a Rsv1 signaling network is proposed (Fig. 5B). RNA-sequencing of the Rsv1-mediated LSHR to SMV-G7 identified eukaryotic translation initiation factor 5A (elF5A) as strongly induced gene. VIGS of elF5A suppressed the LSHR and associated responses such as GmPR1 expression, reactive oxygen species, and cell death, while

This article is protected by copyright. All rights reserved. accumulation of SMV-G7 was increased. Therefore, elF5A appears to be required for Rsv1- mediated LSHR to SMV-G7. Small RNA profiling showed that miRNA 168 (miR168) is strongly induced during LSHR (Chen et al., 2015). miR168 directs cleavage of the ARGONAUTE 1 (AGO1) mRNA transcripts, and in accordance with this, more AGO1 mRNA cleavage products and less AGO1 proteins were detected during LSHR. Silencing SUPPRESSOR OF GENE SILENCING 3, which promotes accumulation of AGO1 mRNA and protein, suppressed LSHR, but did not dramatically affect SMV accumulation. These results suggest that AGO1 homeostasis is disrupted during LSHR, but the impact and precise mechanism of the response is not yet known. Rsv3-mediated resistance to SMV is not accompanied by obvious symptoms, and it has been referred to as ER (Fig. 3B) (Seo et al., 2014). However, Zhang et al. (2009) found using a GUS- tagged SMV strain that there may be limited viral replication and cell-to-cell movement without HR. Using time course RNA sequencing, members of the protein phosphatase 2C (GmPP2C) family were up-regulated at 8 hpi in response to an avirulent SMV isolate, SMV-G5H (Seo et al., 2014). The most up-regulated gene was GmPP2C3a, which is associated with abscisic acid (ABA)-mediated responses. Accordingly, ABA levels were induced at 8 and 24 hpi in response to SMV-G5H and not to the virulent G7H strain, and there was no induction of SA. Increased callose deposition occurred in Rsv3 plants after inoculation with SMV-G5H. Treatment of Rsv3 plants with a callose synthase inhibitor resulted in the formation of HR lesions in response to SMV-G5H suggesting that the virus was not effectively localized and suggesting a possible link between Rsv3-mediated resistance and a cell death defense response. Studies have also been conducted on other SMV resistance responses. Proteomic analysis of the Rsc8 resistance response implicated genes involved in cell wall reinforcement, active oxygen removal, defense signal transduction, and regulation of metabolism (Yang et al., 2011). However, more work is needed to firmly establish roles for these genes in SMV resistance. Resistance in cultivar Jidou 7 is characterized by the formation of necrotic local lesions that become apparent by 72 hpi with an avirulent SMV isolate. In SMV inoculated Jidou 7 plants, the deposition of callose in association with plasmodesmata was detected as early as 2 hpi in incompatible but not compatible interactions (Li et al., 2012). Application of a callose synthase inhibitor prevented callose deposition and resulted in spreading HR lesions, which did not

This article is protected by copyright. All rights reserved. contain the avirulent SMV isolate. These results indicate that callose deposition associated with cell walls and plasmodesmata is required for effective restriction of SMV in Jidou 7.

CONTROL Similar to other non-persistently transmitted viruses, insecticidal control of aphid vectors usually provides little reduction in SMV incidence (Burrows et al., 2005; Johnson et al., 2008; Nakano et al., 1987; Pedersen et al., 2007). However, soybean cultivars with extra-dense pubescence had significantly lower incidence of SMV infection than more glabrous cultivars (Gunasinghe et al., 1988; Pfeiffer et al., 2003; Ren et al., 2000). Regardless, the most efficient and environmentally- sound approach to control SMV, apart from planting virus-free seeds, is deployment of resistance soybeans containing pyramided R-genes (Saghai et al., 2008b; Shakiba et al., 2012b; Shi et al., 2009). High levels of resistance to SMV have also been produced in transgenic plants expressing genomic regions of the SMV from sense or inverted repeat constructs (Furutani et al., 2006, 2007; Gao et al., 2015a; Kim et al., 2013, 2016; Wang et al., 2001; Zhang et al., 2011). Even though transgenic plants significantly lower SMV incidence in the field (Steinlage et al. 2002), none have been incorporated into soybean breeding programs.

BIOTECHNOLOGY APPLICATIONS Infectious cDNA clones of various SMV strains have been constructed (Chowda-Reddy et al., 2011a; Domier et al., 2011; Hajimorad et al., 2003; Seo et al., 2009c,d; Wang et al., 2006). Similar to other potyviruses, SMV genome expression strategy has made it suitable for expression of inserted transgene sequences. Wang et al. (2006) inserted cloning sites between the P1 and HC-Pro cistrons and downstream of a synthetic protease cleavage site in infectious cDNAs of strains SMV-N and SMV-G7. The SMV expression vectors stably expressed uidA, green and red fluorescent protein genes and were used to examine the function of avirulence genes of a bacterium, the role of CI in Rsv3-mediated resistance, regulation of pathogen defense pathways by mitogen-activated protein kinases, and elicitation of foliar disease symptoms by a fungus (Chang et al., 2016; Hajimorad et al., 2011; Liu et al., 2011; Wang et al., 2006; Zhang et al., 2009). Recently, Seo et al. (2016) modified an infectious clone of SMV to serve as a vector for bimolecular fluorescence complementation studies of protein-protein interactions. The

CONCLUSION AND FUTURE PROSPECTS The SMV-soybean pathosystem is a well-characterized, genetically tractable model system to study infection cycles of potyviruses including compatible and incompatible virus-host interactions, host range, vector transmission, and seed transmission. Resources that include infectious cDNA clones of a number of distinct SMV strains, SMV 3-D crystal structure, and the soybean genome sequence position this pathosystem to make important contributions to fundamental knowledge of plant-virus interactions (Chowda-Reddy et al., 2011a; Domier et al., 2011; Hajimorad et al., 2003; Kendall et al., 2008; Schmutz et al., 2010; Seo et al., 2009c,d; Wang et al., 2006). Of particular interest is understanding the underlying mechanism(s) of Rsv1- mediated ER and the restriction in movement of SMV by the Rsv4 locus, which may represent a new class of R-gene (Ilut et al., 2016). These may provide insights applicable to other virus-plant pathosystems. ER is an unusually effective form of resistance where the perception of an invading virus is rapid and robust preventing it from replicating and generating mutants capable of evading host defenses. Thus, it is hypothesized that R-genes conferring ER are more durable than R-genes that permit localized virus replication evident by the durability of Ry and Rx in potato (Bendahman et al., 1999; Mestre et al., 2000). Although SMV virulence determinants corresponding for each of the Rsv loci have been identified, the functional role(s) of these mutations in virulence and the mechanism of evasion remain to be understood. Molecular isolation of all SMV R-genes and 3D resolution of SMV avirulence/virulence factors would provide insights into the mechnisms of recognition and factors that drive evolution of SMV virulence genes, including whether the encoded R protein directly or indirectly mediates recognition of SMV avirulence proteins, and to resolve the role(s) of already identified mutations in such interactions. Molecular isolation of SMV R-genes would benefit from establishing the genic and allelic relationships among the Rsv and Rsc genes that map to the same soybean chromosome (Table 1). Additionally, establishing a standardized system for naming and classifying type strains, isolates, and naturally-occurring SMV strains in relation to R-genes, would clarify both the host and pathogen components of the pathosystem.

This article is protected by copyright. All rights reserved. Recessive genes for virus resistance often are broadly more durable than dominant genes for strain-specific resistance. In other potyvirus systems, mutations in eIF4E have been shown to impart durable recessive virus resistance by disrupting interactions with VPg required for translation initiation (Moury et al., 2014). It may be possible to impart resistance to SMV by site-specific mutagenesis of soybean eIF4E or other genes encoding proteins essential for virus infection using CRISPR-Cas9 technologies (Sun et al., 2015). Additional areas of interest are understanding the underlying molecular mechanism(s) of host specificity of SMV. While most potyviruses, including SMV, have narrow host ranges, some have broad host ranges (Adams et al., 2012). Because the barriers to SMV’s host range expansion likely are at the level of virus-plant interactions, comparative analyses of narrow versus broad host range legume-infecting potyviruses may provide new insights into the important question of host specificity.

REFERENCES Adams, M.J., Zerbini, F.M., French, R., Stenger, D.C. and Valkonen, J.P.T. (2012) Potyviridae. In: King, A.M.Q., Adams, M.J., Carstens, E.B. and Lefkowitz, E.J. (eds) Virus Taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. London, Elsevier/Academic Press. Ahangaran, A., Habibi, M.K., Mosahebi Mohammadi, G.-H., Winter, S. and Garcia- Arenal, F. (2013) Analysis of Soybean mosaic virus genetic diversity in Iran allows the characterization of a new mutation resulting in overcoming Rsv4-resistance. J. Gen. Virol. 94, 2557-2568. Almeida, A.M.R. (1981) Identification of strains of soybean common mosaic virus in Parana State. Fitopatol. Bras. 6, 131-136. Almeida, A.M.R., Sakai, J., Souto, E.R., Kitajima, E.W., Fukuji, T.S. and Hanada, K. (2002) Mosaic in Senna occidentalis in Southern Brazil induced by a new strain of Soybean mosaic virus. Fitopatol. Bras. 27, 151-156. Anjos, J.R.M., Lin, M.T. and Kitajima, E.W. (1985) Characterization of an isolate of soybean mosaic virus. Fitopatol. Bras. 10, 143-157. Atreya, C.D., Raccah, B. and Pirone, T.P. (1990) A point mutation in the coat protein abolishes aphid transmissibility of a potyvirus. Virology 178, 161-165.

This article is protected by copyright. All rights reserved. Babu, M., Gagarinova, A.G., Brandle, J.E. and Wang, A. (2008) Association of the transcriptional response of soybean plants with Soybean mosaic virus systemic infection. J. Gen. Virol. 89, 1069-1080. Banziger, H. and Hengsawad, V. (1985) Species spectrum abundance and potential importance of aphids caught by yellow pan traps in experimental soybean plots in northern Thailand. Thai J. Agri. Sci. 18, 123-136. Bao, D., Ganbaatar, O., Cui, X., Yu, R., Bao, W., Falk, B.W. and Wuriyanghan, H. (2017), Down-regulation of genes coding for core RNAi components and disease resistance proteins via corresponding microRNAs might be correlated with successful Soybean mosaic virus infection in soybean. Mol. Plant Pathol. doi:10.1111/mpp.12581. Bendahmane, A, Kanyuka, K. and Baulcombe, D.C. (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11, 781–92 Benscher, D., Pappu, S.S., Niblett, C.L., Varon de Agudelo, V., Morales, F., Hodson, E., Alvarez, E., Acosta, O. and Lee, R.F. (1996) A strain of soybean mosaic virus infecting Passiflora spp. in Colombia. Plant Dis. 80, 258-262. Blanc, S., Ammar, E.D., Garcia-Lampasona, S., Dolja, V.V., Llave, C., Baker, J. and Pirone, T.P. (1998) Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J. Gen. Virol. 79, 3119-3122. Blanc, S., Lopezmoya, J.J., Wang, R.Y., Garcialampasona, S., Thornbury, D.W. and Pirone, T.P. (1997) A specific interaction between coat protein and helper component correlates with aphid transmission of a potyvirus. Virology 231, 141-147. Bowers, G.R. and Goodman, R.M. (1991) Strain specificity of soybean mosaic virus seed transmission in soybean. Crop Sci. 31, 1171-1174. Bowers, G.R., Jr. and Goodman, R.M. (1979) Soybean mosaic virus: infection of soybean seed parts and seed transmission. Phytopathology 69, 569-572. Burrows, M.E.L., Boerboom, C.M., Gaska, J.M., Grau, C.R. (2005) The relationship between Aphis glycines and Soybean mosaic virus incidence in different pest management systems. Plant Dis. 89, 926-934. Buss, G., Ma, G., Kristipati, S., Chen, P. and Tolin, S. (1999) A new allele at the Rsv3 locus for resistance to soybean mosaic virus. In: Proc. World Soybean Res. Conf. VI, Chicago, IL. pp. 4-7.

This article is protected by copyright. All rights reserved. Buss, G.R., Ma, G., Chen, P. and Tolin, S.A. (1997) Registration of V94-5152 soybean germplasm resistant to soybean mosaic potyvirus. Crop Sci. 37, 1987-1988. Buzzell, R.I. and Tu, J.C. (1984) Inheritance of soybean resistance to soybean mosaic virus. J. Hered. 75, 82. Buzzell, R.I. and Tu, J.C. (1989) Inheritance of a soybean stem-tip necrosis reaction to soybean mosaic virus. J. Hered. 80, 400-401.

Cassone, B.J., Redinbaugh, M.G., Dorrance, A.E. and Michel, A.P. (2015) Shifts in Buchnera aphidicola density in soybean aphids (Aphis glycines) feeding on virus-infected soybean. Insect Mol. Biol. 24, 422-431. Cervantes-Martinez, I., Chen, P., Orazaly, M. and Klepadlo, M. (2015) Identification of a new allele at the Rsv3 locus for resistance to Soybean mosaic virus in PI 61944 soybean accession. Crop Sci. 55, 999-1005. Chang, H.X., Domier, L.L., Radwan, O., Yendrek, C.R., Hudson, M.E. and Hartman, G.L. (2016) Identification of multiple phytotoxins produced by Fusarium virguliforme including a phytotoxic effector (FvNIS1) associated with sudden death syndrome foliar symptoms. Molec. Plant-Microbe Interact. 29, 96-108. Chen, H., Arsovski, A.A., Yu, K. and Wang, A. (2017a) Deep sequencing leads to the identification of eukaryotic translation initiation factor 5A as a key element in Rsv1-mediated lethal systemic hypersensitive response to Soybean mosaic virus infection in soybean. Mol. Plant Pathol. 18, 391–404. Chen, H., Arsovski, A.A., Yu, K. and Wang, A. (2016) Genome-wide investigation using sRNA-seq, degradome-seq and transcriptome-seq reveals regulatory networks of microRNAs and their target genes in soybean during Soybean mosaic virus infection. PLoS One 11, e0150582. Chen, P., Buss, G. R., Roane, C. W. and Tolin, S. A. (1991) Allelism among genes for resistance to soybean mosaic virus in strain-differential soybean cultivars. Crop Sci. 31, 305- 309. Chen, P., Buss, G. and Tolin, S.A. (2002) Identification of a valuable gene in Suweon 97 for resistance to all strains of soybean mosaic virus. . Crop Sci. 42, 333-337.

This article is protected by copyright. All rights reserved. Chen, J., Zhang, H.-Y., Lin, L., Adams, M. J., Antoniw, J. F., Zhao, M.-F., Shang, Y.-F. and Chen, J.-P. (2004) A virus related to Soybean mosaic virus from Pinellia ternata in China and its comparison with local soybean SMV isolates. Arch. Virol. 149, 349-363. Chen, P., Ma, G., Buss, G.R., Gunduz, I., Roane, C.W. and Tolin, S.A. (2001) Inheritance and allelism tests of Raiden soybean for resistance to soybean mosaic virus. J. Hered. 92, 51- 55. Chen, H., Zhang, L., Yu, K. and Wang, A. (2015) Pathogenesis of Soybean mosaic virus in soybean carrying Rsv1 gene is associated with miRNA and siRNA pathways, and breakdown of AGO1 homeostasis. Virology 476, 395-404. Chen, Y.-X., Wu, M., Ma, F.-F., Chen, J.-Q. and Wang, B. (2017b) Complete nucleotide sequences of seven soybean mosaic viruses (SMV), isolated from wild soybeans (Glycine soja) in China. Arch. Virol. 162, 901-904. Cho, E.K., Chung, B.J. and Lee, S.H. (1977) Studies on identification and classification of soybean virus diseases in Korea. II. Etiology of a necrotic disease of Glycine max. Plant Dis. Report. 61, 313-317. Cho, E.-K. and Goodman, R.M. (1979) Strains of soybean mosaic virus: Classification based on virulence in resistant soybean cultivars. Phytopathology 69, 467-470. Choi, B.K., Koo, J.M., Ahn, H.J., Yum, H.J., Choi, C.W., Ryu, K.H., Chen, P. and Tolin, S.A. (2005) Emergence of Rsv-resistance breaking Soybean mosaic virus isolates from Korean soybean cultivars. Virus Res. 112, 42-51. Chowda-Reddy, R.V., Sun, H., Chen, H., Poysa, V., Ling, H., Gijzen, M. and Wang, A. (2011a) Mutations in the P3 protein of Soybean mosaic virus G2 isolates determine virulence on Rsv4-genotype soybean. Mol. Plant–Microbe Interact. 24, 37–43. Chowda-Reddy, R.V., Sun, H., Hill, J.H., Poysa, V. and Wang, A. (2011b) Simultaneous mutations in multi-viral proteins are required for Soybean mosaic virus to gain virulence on soybean genotypes carrying different R genes. PLoS ONE 6, e28342. Chung, B.Y., Miller, W.A., Atkins, J.F., Firth, A.E. (2008) An overlapping essential gene in the Potyviridae. Proc. Natl. Acad. Sci. U. S. A. 105, 5897−5902. Clark, A.J. and Perry, K.L. (2002) Transmissibility of field isolates of soybean viruses by Aphis glycines. Plant Dis. 86, 1219-1222.

This article is protected by copyright. All rights reserved. Cui, X., Chen, X. and Wang, A. (2011) Detection, understanding and control of soybean mosaic virus. In: Soybean-Molecular Aspects of Breeding (Rijeka, S.A. ed.), pp. 335-354. InTech, Croatia. Cui, X., Yaghmaiean, H., Wu, G., Wu, X., Chen, X., Thorn, G. and Wang, A. (2017) The C- terminal region of the Turnip mosaic virus P3 protein is essential for viral infection via targeting P3 to the viral replication complex. Virology 510, 147-155. Domier, L.L., Hobbs, H.A., McCoppin, N.K., Bowen, C.R., Steinlage, T.A., Chang, S., Wang, Y. and Hartman, G.L. (2011) Multiple loci condition seed transmission of Soybean mosaic virus (SMV) and SMV-induced seed coat mottling in soybean. Phytopathology 101, 750-756. Domier, L.L., Latorre, I.J., Steinlage, T.A., McCoppin, N. and Hartman, G.L. (2003) Variability and transmission by Aphis glycines of North American and Asian Soybean mosaic virus isolates. Arch. Virol. 148, 1925-1941. Domier, L.L., Steinlage, T.A., Hobbs, H.A., Wang, Y., Herrara-Rodriguez, G., Haudenshield, J.S., McCoppin, N.K. and Hartman, G.L. (2007) Similarities in seed and aphid transmission among Soybean mosaic virus isolates. Plant Dis. 91, 546-550. Donaldson, J.R. and Gratton, C. (2007) Antagonistic effects of soybean viruses on soybean aphid performance. Environ. Entomol. 36, 918-925. Eggenberger, A.L., Hajimorad, M.R. and Hill, J.H. (2008) Gain of virulence on Rsv1- genotype soybean by an avirulent Soybean mosaic virus requires concurrent mutations in both P3 and HC-Pro. Mol. Plant–Microbe Interact. 21, 931–936. Eggenberger, A.L., Stark, D.M. and Beachy, R.N. (1989) The nucleotide sequence of soybean mosaic virus coat protein-coding region and its expression in Escherichia coli, Agrobacterium tumefaciens and tobacco callus. J. Gen. Virol. 70, 1853-1860. Fu, D.Q., Ghabrial, S. and Kachroo, A. (2009) GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean. Mol. Plant Microbe Interact. 22, 86-95. Furutani, N., Hidaka, S., Kosaka, Y., Shizukawa, Y. and Kanematsu, S. (2006) Coat protein gene-mediated resistance to soybean mosaic virus in transgenic soybean. Breeding Sci. 56, 119-124.

This article is protected by copyright. All rights reserved. Furutani, N., Yamagishi, N., Hidaka, S., Shizukawa, Y., Kanemastu, S. and Kosaka, Y. (2007) Soybean Mosaic Virus Resistance in Transgenic Soybean Caused by Post- transcriptional Gene Silencing. Breeding Sci. 57, 123-128 Gao, L., Ding, X.N., Li, K., Liao, W.L., Zhong, Y., Ren, R., Liu, Z., Adhimoolam, K. and Zhi, H. (2015a) Characterization of Soybean mosaic virus resistance derived from inverted repeat-SMV-HC-Pro genes in multiple soybean cultivars. Theoret. Appl. Genet. 128, 1489- 1505. Gao, L., Zhai, R., Zhong, Y.K., Karthikeyan, A., Ren, R., Zhang, K., Li, K. and Zhi, H.J. (2015b) Screening isolates of Soybean mosaic virus for infectivity in a model plant, Nicotiana benthamiana. Plant Dis. 99, 442-446. Ghabrial, S.A., Smith, H.A., Parks, T.D. and Dougherty, W.G. (1990) Molecular genetic analyses of the soybean mosaic virus NIa proteinase. J. Gen. Virol. 71, 1921-1927. Gibbs, A.J., Trueman, J.W.H. and Gibbs, M.J. (2008) The bean common mosaic virus lineage of potyviruses: where did it arise and when? Arch. Virol. 153, 2177-2187. Goodman, R.M., Bowers, G.R., Jr. and Paschal, E.H., II (1979) Identification of soybean germplasm lines and cultivars with low incidence of soybean mosaic virus transmission through seed. Crop Sci. 19, 264-267. Goodman, R.M. and Oard, J.H. (1980) Seed transmission and yield losses in tropical soybeans infected by soybean mosaic virus. Plant Dis. 64, 913-914. Gunasinghe, U.B., Irwin, M.E. and Kampmeier, G.E. (1988) Soybean leaf pubescence affects aphid vector transmission and field spread of soybean mosaic virus. Ann. Appl. Bio.l 112, 259-272. Gunduz, I., Buss, G.R., Chen, P. and Tolin, S.A. (2002) Characterization of SMV resistance genes in Tousan 140 and Hourei soybean. Crop Sci. 42, 90-95. Gunduz, I., Buss, G.R., Ma, G., Chen, P. and Tolin, S.A. (2001) Genetic analysis of resistance to Soybean mosaic virus in OX670 and Harosoy soybean. Crop Sci. 41, 1785-1791. Gunduz, I., Buss, G.R., Chen, P. and Tolin, S.A. (2004) Genetic and phenotypic analysis of Soybean mosaic virus resistance in PI88788 soybean. Phytopathology, 94, 687-692. Hajimorad, M.R. and Hill, J.H. (2001) Rsv1-mediated resistance against Soybean mosaic virus-N is hypersensitive response-independent at inoculation site, but has the potential to initiate a hypersensitive response-like mechanism. Mol. Plant-Microbe Interact. 14, 587-598.

This article is protected by copyright. All rights reserved. Hajimorad, M.R., Wang, Y., Abe, J. and Nakahara, K. (2016) Exchange of HC-Pro cistron between Soybean mosaic virus and Clover yellow vein virus: Impact on pathogenicity. Phytopathology 106, S4.154. Hajimorad, M.R., Eggenberger, A.L. and Hill, J.H. (2003) Evolution of Soybean mosaic virus-G7 molecularly cloned genome in Rsv1-genotype soybean results in emergence of a mutant capable of evading Rsv1- mediated recognition. Virology 314, 497-509. Hajimorad, M.R., Eggenberger, A.L. and Hill, J.H. (2005) Loss and gain of elicitor function of Soybean mosaic virus G7 provoking Rsv1-mediated lethal systemic hypersensitive response maps to P3. J. Virol. 79, 1215-1222. Hajimorad, M.R., Eggenberger, A.L. and Hill, J.H. (2006) Strain-specific P3 of Soybean mosaic virus elicits Rsv1-mediated extreme resistance, but absence of P3 elicitor function alone is insufficient for virulence on Rsv1-genotype soybean. Virology 345, 156-166. Hajimorad, M.R., Eggenberger, A.L. and Hill, J.H. (2008) Adaptation of Soybean mosaic virus avirulent chimeras containing P3 sequences from virulent strains to Rsv1-genotype soybeans is mediated by mutations in HC-Pro. Mol. Plant-Microbe Interact. 21, 937-946. Hajimorad, M.R., Wen, R.-H., Eggenberger, A.L., Hill, J. H. and Saghai Maroof, M.A. (2011) Experimental adaptation of an RNA virus mimics natural evolution. J. Virol. 85, 2557–2564. Halbert, S.E., Irwin, M.E. and Goodman, R.M. (1981). Alate aphid (Homoptera: Aphididae) species and their relative importance as field vectors of soybean mosaic virus. Ann. Appl. Biol. 97, 1-10. Harrison, B.D. (2002) Virus variation in relation to resistance-breaking in plants. Euphytica 124, 181-192. Hayes, A.J., Jeong, S.C., Gore, M.A., Yu, Y.G., Buss, G.R., Tolin, S.A. and Saghai Maroof, M.A. (2004) Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics 166, 493-503. Hill, J.H., Alleman, R., Hogg, D.B. and Grau, C.R. (2001) First report of transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the new world. Plant Dis. 85, 561.

This article is protected by copyright. All rights reserved. Hill, J.H., Bailey, T.B., Benner, H.I., Tachibana, H. and Durand, D.P. (1987) Soybean mosaic-virus - effects of primary disease incidence on yield and seed quality. Plant Dis. 71, 237-239. Hill, J.H., Lucas, B.S., Benner, H.I., Tachibana, H., Hammond, R.B. and Pedigo, L.P. (1980) Factors associated with the epidemiology of soybean mosaic virus in Iowa. Phytopathology 70, 536-540. Hill, J.H. and Whitham, S.A. (2014) Control of virus diseases in soybeans. Adv. Virus. Res. 90, 355–390. Hobbs, H.A., Hartman, G.L., Wang, Y., Bernard, R.L., Pederson, W.I. and Domier, L.L. (2003) Occurrence of seed coat mottling in soybean plants inoculated with Bean pod mottle virus and Soybean mosaic virus. Plant Dis. 87, 1333-1336. Hong, X.-Y., Chen, J., Shi, Y.-H. and Chen, J.-P. (2007) The ‘6K1’ protein of a strain of Soybean mosaic virus localizes to cell periphery. Arch Virol. 152, 1547-1551. Hunst, P.L. and Tolin, S.A. (1982) Isolation and comparison of two strains of soybean mosaic virus. Phytopathology 72, 710-713. Ilut, D.C., Lipka, A.E., Jeong, N., bae, D.N., Kim, D.H., Kim, J.H., Redekar, N., Yang, K., Park, W., Kang, S.-T., Kim, N., Moon, J.-K., Saghai Maroof, M.A., Gore, M.A. and Jeong, S.-C. (2016) Identification of haplotypes at the Rsv4 genomic region in soybean associated with durable resistance to soybean mosaic virus. Theor. Appl. Genet. 129, 453- 468. Irwin, M.E. and Goodman, R.M. (1981) Ecology and control of soybean mosaic virus, in: Maramorosch, K., Harris, K.F. (Eds.), Plant Diseases and Vectors: Ecology and Epldemiology. Academic Press, New York, pp. 181-229. Ivanov, K.I., Eskelin, K., Lohmus, A. and Makinen, K. (2014) Molecular and cellular mechanisms underlying potyvirus infection. J. Gen. Virol. 95, 1415-1429. Jain, R.K., McKern, N.M., Tolin, S.A., Hill, J.H., Barnett, O.W., Tosic, M., Ford, R.E., Beachy, R.N., Yu, M.H., Ward, C.W. and Shukla, D.D. (1992) Conformation that fourteen potyvirus isolates from soybean are strains of one virus by comparing coat protein peptide profiles. Phytopathology 82, 294-299.

This article is protected by copyright. All rights reserved. Jayaram, C.H., Hill, J.H. and Miller, W.A. (1991) Nucleotide sequence of the coat protein genes of two aphid-transmissible strains of soybean mosaic virus. J. Gen. Virol. 72, 1001- 1003. Jayaram, C.H., Hill, J.H. and Miller, W.A. (1992) Complete nucleotide sequences of two soybean mosaic virus strains differentiated by response of soybean containing the Rsv resistance gene. J. Gen. Virol. 73, 2067-2077. Jayaram, C.H., Van Deusen, R.A., Eggenberger, A.L., Schwabacher, A.W. and Hill, J.H. (1998) Characterization of a monoclonal antibody recognizing a DAG-containing epitope conserved in aphid transmissible potyviruses: evidence that the DAG motif is in a defined conformation. Virus Res. 58, 1-11. Jeong, S.C. and Maroof, M.A.S. (2004) Detection and genotyping of SNPs tightly linked to two disease resistance loci, Rsv1 and Rsv3, of soybean. Plant Breeding 123, 305-310. Johnson, K.D., O'Neal, M.E., Bradshaw, J.D. and Rice, M.E. (2008) Is preventative, concurrent management of the soybean aphid (Hemiptera : aphididae) and bean leaf beetle (Coleoptera : chrysomelidae) possible? J. Econ. Entomol. 101, 801-809. Jossey, S., Hobbs, H.A. and Domier, L.L. (2013) Role of Soybean mosaic virus-encoded proteins in seed and aphid transmission in soybean. Phytopathology 103, 801-809. Kang, S.H., Lim, W.S., Hwang, S.H., Park, J.W., Choi, H.S. and Kim, K.H. (2006) Importance of the C-terminal domain of soybean mosaic virus coat protein for subunit interactions. J Gen Virol. 87, 225-229. Kendall, A., McDonald, M., Bian, W., Bowless, T., Baumgarten, S.C., Shi, J., Stewart, P.L., Bullitt, S., Gore, D., Irving, T.C., Havens, W.M., Ghabrial, S.A., Wall, J.S. and Stubbs, G. (2008) Structure of flexible filamentous plant viruses. J. Virol. 82, 9546-9554. Khatabi, B., Fajolu, O.L., Wen, R.-H. and Hajimorad, M.R. (2012) Evaluation of North American isolates of Soybean mosaic virus for gain of virulence on Rsv-genotype soybeans with special emphasis on resistance-breaking determinants on Rsv4. Mol. Plant Pathol. 13, 1077-1088. Khatabi, B., Wen, R.-H. and Hajimorad, M.R. (2013) Fitness penalty in susceptible host is associated with virulence of Soybean mosaic virus on Rsv1-genotype soybean: a consequence of perturbation of HC-Pro and not P3. Mol. Plant Pathol. 14, 885-897.

This article is protected by copyright. All rights reserved. Kiihl, R.A.S. and Hartwig, E.E. (1979) Inheritance of reaction to soybean mosaic virus in soybeans. Crop Sci. 19, 372-375. Kim, Y.-H., Kim, O.-S., Moon, J.-K., Lee, S.-C. and Lee, J.-Y. (2003) G7H, a new Soybean mosaic virus strain: its virulence and nucleotide sequence of CI gene. Plant Dis. 87, 1372- 1373. Kim, H.J., Kim, M.J., Pak, J.H., Im, H.H., Lee, D.H., Kim, K.-H., Lee, J.-H., Kim, D.-H., Choi, H.K., Jung, H.W. and Chung, Y.-S. (2016) RNAi-mediated Soybean mosaic virus (SMV) resistance of a Korean soybean cultivar. Plant Biotechnol. Rep. 10, 257-267. Kim, H.J., Kim, M.J., Pak, J.H., Jung, H.W., Cjoi, H.K., Lee, Y.-H., Back, I.-Y., Ko, J.-M., Jeong, S.-C., Pack, I.S., Ryu, K.H. and Chung, Y.-S. (2013) Characterization of SMV resistance of soybean produced by genetic transformation of SMV-CP gene in RNAi. Plant Biotechnol. Rep. 7, 425-433. Klepadlo, M., Chen, P., Shi, A., Mason, R.E., Korth, K.L. and Srivastava, V. (2017a) Single nucleotide polymorphism markers for rapid detection of the Rsv4 locus for soybean mosaic virus resistance in diverse germplasm. Mol. Breeding, 37, 10. Klepadlo, M., Chen, P., Shi, A., Mason, R.E., Korth, K.L., Srivastava, V. and Wu, C. (2017b) Two tightly linked genes for Soybean mosaic virus resistance in soybean. Crop Sci. 57, 1-10. Klepadlo, M., Chen, P. and Wu, C. (2016) Genetic analysis of resistance to Soybean mosaic virus in PI 438307 soybean accessions. Crop Sci. 56, 3016-3023. Li, C., Adhimoolam, K., Yuan, Y., Yin, J., Ren, R., Yang, Y. and Zhi, H. (2017) Identification of candidate genes for resistance to Soybean mosaic virus strain SC3 by using fine mapping and transcriptome analyses. Crop Pasture Sci. 68, 156-166. Li, D., Chen, P., Alloatti, J., Shi, A. and Chen, Y.F. (2010a) Identification of new alleles for resistance to Soybean mosaic virus in soybean. Crop Sci. 50, 649-655. Li, H.-C., Zhi, H.-J., Gai, J.-Y., Guo, D.-Q., Wang, Y.-W., Li, K. Bai, L. and Yang, H. (2006) Inheritance and gene mapping of resistance to Soybean mosaic virus strain SC14 in soybean. J. Integr. Plant Biol. 48, 1466-1472. Li, K., Ren, R., Adhimoolam, K., Gao, L., Yuan, Y., Liu, Z., Zhong, Y. and Zhi, H. (2015) Genetic analysis and identification of two soybean mosaic virus resistance genes in soybean [Glycine max (L.) Merr.]. Plant Breeding 134, 684-695.

This article is protected by copyright. All rights reserved. Li, K., Yang, Q., Zhi, H. and Gai, J. (2010b) Identification and distribution of Soybean mosaic virus strains in southern China. Plant Dis. 94, 351-357. Li, M.-J., Kim, J.-K., Seo, E.-Y., Hong, S. M., Hwang, E.-I., Moon, J.-K., Domier, L. L., Hammond, J., Youn, Y.-N. and Lim, H.-S. (2014) Sequence variability in the HC-Pro coding regions of Korean soybean mosaic virus isolates is associated with differences in RNA silencing suppression. Arch Virol. 159, 1373-1383. Li, W., Zhao, Y., Liu, C., Yao, G., Wu, S., Hou, C., Zhang, M. and Wang, D. (2012) Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cell movement of Soybean mosaic virus. Plant Cell Rep. 31, 905-916. Li, N., Yin, J.L., Li, C., Wang, D.G., Yang, Y.Q., Karthikeyan, A., Luan, H.K. and Zhi,

H.J. (2016) NB-LRR gene family required for Rsc4-mediated resistance to Soybean mosaic virus. Crop Pasture Sci. 67, 541-552. Lim, H.-S., Jang, C. Y., Bae, H., Kim, J. K., Lee, C.-H., Hong, J.-S., Ju, H.-J., Kim, H. G. and Domier, L. L. (2011) Soybean mosaic virus infection and helper component-protease enhance accumulation of Bean pod mottle virus-specific SiRNAs. Plant Pathol. J. 27, 315- 323. Lim, H.S., Ko, T.S., Hobbs, H.A., Lambert, K.N., Yu, J.M., McCoppin, N.K., Korban, S.S., Hartman, G.L. and Domier, L.L. (2007) Soybean mosaic virus helper component-protease alters leaf morphology and reduces seed production in transgenic soybean plants. Phytopathology 97, 336-372. Lim, H.-S., Ko, T.-S., Lambert, K. N., Kim, H.-G., Korban, S.S., Hartman, G.L. and Domier, L.L. (2005) Soybean mosaic virus helper component-protease enhances somatic embryo production and stabilizes transgene expression in soybean. Plant Physiol. Biochem. 43, 1014-1021. Lin, L., Luo, Z., Yan, F., Lu, Y., Zheng, H. and Chen, J. (2011) Interaction between potyvirus P3 and ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) of host plant. Virus Genes 43, 90-92. Liu, J. Z., Braun, E., Qiu, W. L., Shi, Y. F., Marcelino-Guimarães, F. C., Navarre, D., Hill, J. H. and Whitham, S. A. (2014) Positive and negative roles for soybean MPK6 in regulating defense responses. Mol. Plant Microbe Interact. 27, 824-834.

This article is protected by copyright. All rights reserved. Liu, J.-Z., Fang. Y. and Pang, H. (2016) The current status of the soybean-Soybean mosaic virus (SMV) pathosystem. Front. Microbiol. 7, 1906. doi: 10.3389/fmicb.2016.01906. Liu, J. Z., Horstman, H. D., Braun, E., Graham, M. A., Zhang, C., Navarre, D., Qiu, W. L., Lee, Y., Nettleton, D., Hill, J. H. and Whitham, S.A. (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol. 157, 1363-1378. Liu, J.Z. and Whitham, S.A. (2013) Overexpression of a soybean nuclear localized type III DnaJ domain-containing HSP40 reveals its roles in cell death and disease resistance. Plant J. 74, 110-121. Lopez-Moya, J.J., Valli, A. and Garcia, J.A. (2009) Potyviridae. In: Encyclopedia of Life Sciences (ELS). John Willey & Sons, Ltd: Chichester. doi: 10.1002/9780470015902.a0000755.pub2. Lu, L., Wu, G., Xu, X., Luan, H., Zhi, H., Cui, J., Cui, X. and Chen, X. (2015) Soybean actin-depolymerizing factor 2 interacts with Soybean mosaic virus-encoded P3 protein. Virus Genes 50, 333-339. Luan, H., Shine, M.B., Cui, X., Chen, X., Ma, N., Kachroo, P., Zhi, H. and Kachroo, A. (2016) The potyviral P3 protein targets eukaryotic elongation factor 1A to promote the unfolded protein response and viral pathogenesis. Plant Physiol. 172, 221-234. Lucas, B.S. and Hill, J.H. (1980) Characteristics of the transmission of three soybean mosaic virus isolates by Myzus persicae and Rhopalosiphum maidis. J. Phytopath. 99, 47-53. Ma, F.-F., Wu, X.-Y., Chen, Y.-X., Liu, Y.-N., Shao, Z.-Q., Wu, P., Wu, M., Liu, C.-C., Wu, W.-P., Yang, Y.-Y., Li, D.-X., Chen, J.-Q. and Wang, B. (2016) Fine mapping of the Rsv1- h gene in the soybean cultivar Suweon 97 that confers resistance to two Chinese strains of the soybean mosaic virus. Theor. Appl. Genet. 129, 2227-2236. Ma, G., Chen, P., Buss, G.R. and Tolin, S.A. (1995) Genetic characteristics of two genes for resistance to soybean mosaic virus in PI486355 soybean. Theor. Appl. Genet. 91, 907–914. Ma, G., Chen, P., Buss, G.R. and Tolin, S.A. (2003) Genetic study of a lethal necrosis to Soybean mosaic virus in PI 507389 soybean. J. Hered. 94, 205-211. Ma, Y., Li, H., Wang, D., Liu, N. and Zhi, H. (2010) Molecular mapping and marker assisted

selection of Soybean mosaic virus resistance gene RSC-12 in soybean. Legume Genom. Genet. 1, 41-46.

Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus in soybean. Euphytica 181, 127-135. Mestre, P, Brigneti, G. and Baulcombe, D.C. (2000) An Ry-mediated resistance response in potato requires the intact active site of the NIa proteinase from potato virus Y. Plant J. 23, 653–61. Moon, J.-K., Jeong, S.-C., Van, K., Maroof, M. A. S. and Lee, S.-H. (2009) Marker-assisted identification of resistance genes to soybean mosaic virus in soybean lines. Euphytica, 169, 375-385. Moury B, Charron C, Janzac B, Simon V, Gallois JL, Palloix A, Caranta C. (2014) Evolution of plant eukaryotic initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg): A game of mirrors impacting resistance spectrum and durability. Infect. Genet. Evol. 27, 472-480. Nakano, M., Usugi, T. and Shinkai, A. (1987) Effects of the application of chemicals on the spread of soybean mosaic virus. Proc. Assoc. Pl. Prot. Kyushu 33, 33-35. Ng, J.C. and Falk, B.W. (2006) Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annu. Rev. Phytopathol. 44, 183-212. O'Connell Ziegler, P., Benner, H.I. and Hill, J.H. (1986) Soybean mosaic virus: vector specificity and coat protein properties. J. Phytopathol. 115, 29-36. Olspert, A., Chung, B.Y.-W., Atkins, J.F. and Carr, J.P. (2015) Transcriptional slippage in the positive-sense RNA virus family Potyviridae. EMBO Rep. 16, 995-1004. Pedersen, P., Gran, C., Cullen, E. and Hill, J.H. (2007) Potential for integrated management of soybean virus disease. Plant Dis. 91, 1255-1259. Penaflor, M., Mauck, K.E., Alves, K.J., De Moraes, C.M. and Mescher, M.C. (2016) Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host- plant chemistry and host-vector interactions. Funct. Ecol. 30, 1648-1659. Pfeiffer, T.W., Peyyala, R., Ren, Q.X. and Ghabrial, S.A. (2003) Increased soybean pubescence density: Yield and soybean mosaic virus resistance effects. Crop Sci. 43, 2071- 2076. Porto, M.D.M. and Hagedorn, D.J. (1975) Seed transmission of a Brazilian isolate of soybean mosaic virus. Phytopathology 65, 713-716.

This article is protected by copyright. All rights reserved. Redekar, N.R., Clevinger, E.M., Laskar, M.A., Biyashev, R.M., Ashfield, T., Jensen, R.V., Jeong, S.C., Tolin, S.A. and Saghai Maroof, M.A. (2016) Candidate gene sequence analyses toward identifying Rsv3-type resistance to Soybean mosaic virus. Plant Genome 9. 12. Ren, Q., Pfeiffer, T.W. and Ghabrial, S.A. (1997a) Soybean mosaic virus incidence level and infection time - interaction effects on soybean. Crop Sci. 37, 1706-1711. Ren, Q., Pfeiffer, T.W. and Ghabrial, S.A. (1997b) Soybean mosaic virus resistance improves productivity of double-cropped soybean. Crop Sci. 37, 1712-1718. Ren, Q., Pfeiffer, T.W. and Ghabrial, S.A. (2000) Relationship between soybean pubescence density and soybean mosaic virus field spread. Euphytica 111, 191-198. Revers, F. and Garcia, J.M. (2015) Molecular biology of potyviruses. Adv. Virus Res. 92, 101- 199. Rodamilans, B., Valli, A., Mingot, A., Leon, D.S., Baulcombe, D., Lopez-Moya, J.J. and Garcia, J.A. (2015) RNA polymerase slippage as a mechanism for the production of frameshift gene products in plant viruses of the Potyviridae family. J. Virol. 89, 6965-6967. Rohozkova, J. and Navratil, M. (2011) P1 peptidase-a mysterious protein of family Potyviridae. J. Biosci. 36, 189-200. Ross, J. P. (1969) Pathogenic variation among isolates of soybean mosaic virus. Phytopathology, 59, 829-832. Ross, J. P. (1975) A newly recognized strain of soybean mosaic virus. Plant Dis. Rep. 59, 806- 808. Saghai Maroof, M.A., Tucker, D.M. and Tolin, S.A. (2008a) Genomics of viral-soybean interactions. In: Genetics and genomics of soybean (Stacey, G., ed.). New York: Springer pp. 295–321. Saghai Maroof, M.A., Jeong, S.C., Gunduz, I., Tucker, D.M., Buss, G.R. and Tolin, S.A. (2008b) Pyramiding of soybean mosaic virus resistance genes by marker-assisted selection. Crop Sci. 48, 517-526. Saruta, M., Kikuchi, A., Okabe, A. and Sasaya, T. (2005) Molecular characterization of A2 and D strains of Soybean mosaic virus, which caused a recent virus outbreak in soybean cultivar Sachiyutaka in Chugoku and Shikoku regions of Japan. J. Gen. Plant Pathol. 71, 431-435.

This article is protected by copyright. All rights reserved. Schmutz, J.S,B., Cannon, J., Schlueter, J., Ma, T., Mitros, W., nelson, D.L., Hyten, Q., Song, J.J., Thelen, J., Cheng, D., et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183. Selote, D. and Kachroo, A. (2010) RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol. 153, 1199- 1211. Senda, M., Masuta, C., Ohnishi, S., Goto, K., Kasai, A., Sano, T., Hong, J.-S. and MacFarlane, S. (2004) Patterning of virus-infected Glycine max seed coat is associated with suppression of endogenous silencing of chalcone synthase genes. Plant Cell 16, 807-818. Seo, J.-K., Lee, H.-G., Choi, H.-S., Lee, S.-H. and Kim, K.-H. (2009c) Infectious in vivo transcripts from a full-length clone of Soybean mosaic virus strain G5H. Plant Pathol. J. 25, 54-61. Seo, J.-K., Lee, H.-G. and Kim, K.-H. (2009d) Systemic gene delivery into soybean by simple rub-inoculation with plasmid DNA of a Soybean mosaic virus-based vector. Arch. Virol. 154, 87-99. Seo, J.K., Choi, H.S. and Kim, K.H. (2016) Engineering of soybean mosaic virus as a versatile tool for studying protein-protein interactions in soybean. Sci Rep-Uk 6, 22436. Seo, J.-K., Kang, S.-H., Seo, B. Y., Jung, J.K. and Kim, K.-H. (2010) Mutational analysis of interaction between coat protein and helper component-proteinase of Soybean mosaic virus involved in aphid transmission. Mol. Plant Pathol. 11, 265-276. Seo, J.K., Kwon, S.J., Cho, W.K., Choi, H.S. and Kim, K.H. (2014) Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Sci. Rep. 4, 5905. Seo, J.-K., Lee, S.-H. and Kim, K.-H. (2009a) Strain-specific cylindrical inclusion protein of Soybean mosaic virus elicits extreme resistance and a lethal systemic hypersensitive response in two resistant soybean cultivars. Mol. Plant-Microbe. Interact. 22, 1151.1159. Seo, J.-K., Ohshima, K., Lee, H.-G., Son, M., Choi, H.-S., Lee, S.-H., Sohn, S.-H. and Kim, K.-H. (2009b) Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. Virology 393, 91-103.

This article is protected by copyright. All rights reserved. Seo, J.-K., Phan, M. S. V., Kang, S.-H., Choi, H.-S. and Kim, K.-H. (2013) The charged residues in the surface-exposed C-terminus of the Soybean mosaic virus coat protein are critical for cell-to-cell movement. Virology 446, 95-101. Seo, J.-K., Sohn, S.-H. and Kim, K.-H. (2011) A single amino acid change in HC-Pro of soybean mosaic virus alters symptom expression in a soybean cultivar carrying Rsv1 and Rsv3. Arch Virol 156, 135-141. Shakiba, E., Chen, P., Shi, A., Li, D., Dong, D. and Brye, K. (2012a) Two novel alleles at the Rsv 3 locus for resistance to Soybean mosaic virus in PI 399091 and PI 61947 soybeans. Crop Sci. 52, 2587-2594. Shakiba, E., Chen, P., Shi, A., Li, D., Dong, D. and Brye, K. (2013) Inheritance and allelic relationships of resistance genes for Soybean mosaic virus in ‘Corsica’ and ‘Beeson’ soybean. Crop Sci., 53, 1455-1463. Shakiba, E., Chen, P., Gergerich, R., Li, S., Dombek, D., Brye, K. and Shi, A. (2012b) Reactions of commercial cultivars from the mid south to Soybean mosaic virus. Crop Sci. 52, 1990-1997. Sherepitko, D.V., Budzanivska, I.G., Polischuk, V.P. and Boyko, A.L. (2011) Partial sequencing and phylogenetic analysis of soybean mosaic virus isolated in Ukraine. Biopolym. Cell. 27, 472-479. Shi, A., Chen, P., Li, D., Zheng, C., Zhang, B. and Hou, A. (2009) Pyramiding multiple genes for resistance to soybean mosaic virus in soybean using molecular markers. Mol. Breeding 23, 113-124. Shi, Y., Chen, J., Hong, X., Chen, J., and Adams, M.J. (2007) A potyvirus P1 protein interacts with the Rieske Fe/S protein of its host. Mol. Plant Pathol. 8, 785-790. Shukla, D.D., Strike, P.M., Tracy, S.L., Gough, K.H. and Ward, C.W. (1988) The N and C termini of the coat proteins of potyviruses are surface-located and the N terminus contains the major virus specific epitopes. J. Gen. Virol. 69, 1497–1508. Song, Y.P., Li, C., Zhao, L., Karthikeyan, A., Li, N., Li, K. and Zhi, H.J. (2016a) Disease spread of a popular soybean mosaic virus strain (SC7) in southern China and effects on two susceptible soybean cultivars. Philipp. Agric. Sci. 99, 355-364.

This article is protected by copyright. All rights reserved. Song, P., Zhi, H., Wu, B., Cui, X. and Chen, X. (2016b) Soybean Golgi SNARE 12 protein interacts with Soybean mosaic virus encoded P3N-PIPO protein. Biochem. Biophys. Res. Commun. 478, 1503-1508. Sorel, M., Garcia, J.A. and German-Retana, S. (2014) The Potyviridae cylindrical inclusion helicase: A key multipartner and multifunctional protein. Mol. Plant-Microbe. Interact. 27, 215.226. Steinlage, T.A., Hill, J.H. and Nutter, F.W., Jr. (2002) Temporal ans spatial spread of Soybean mosaic virus (SMV) in soybeans transformed with the coat protein gene of SMV. Phytopathology 92, 478-486. Suh, S. J., Bowman, B. C., Jeong, N., Yang, K., Kastl, C., Tolin, S. A., Saghai Maroof, M.A. and Jeong, S.-C. (2011) The Rsv3 locus conferring resistance to Soybean mosaic virus is associated with a cluster of coiled-coil nucleotide-binding leucine-rich repeat genes. Plant Genome 4, 55-64. Sun, H., Tu, S. S., Xue, F., Duns, G. and Che, J. (2008) Molecular characterization and evolutionary analysis of soybean mosaic virus infecting Pinellia ternata in China. Virus Genes 36, 177-190. Sun X, Hu Z, Chen R, Jiang Q, Song G, Zhang H, Xi Y. (2015) Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci. Rep. 5:10342. Tu, J.C. (1989) Effect of different strains of soybean mosaic virus on growth, maturity, yield, seed mottling and seed transmission in several soybean cultivars. J. Phytopathol. 126, 231- 236. Valli, A., López-Moya, J.J. and Antonio García, J. (2007) Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J. Gen. Virol. 88, 1016-1028. Valli, A.A., Gallo, A., Rodamilans, B., López-Moya, J.J. and Antonio García, J. (2017) The HCPro from the Potyviridae family: an enviable multitasking Helper Component that every virus would like to have. Mol. Plant Pathol. doi: 10.1111/mpp.12553. Vance, V.B. and Beachy, R.N. (1984a) Translation of soybean mosaic virus RNA in vitro: evidence of protein processing. Virology 132, 271-284. Vance, V.B. and Beachy, R.N. (1984b) Detection of genomic-length soybean mosaic virus RNA on polyribosomes of infected soybean leaves. Virology 138, 26-36.

This article is protected by copyright. All rights reserved. Viel, C., Ide, C., Cui, X., Wang, A., Farsi, M., Michelutti, R. and Stromvik, M. (2009) Isolation, partial sequencing, and phylogenetic analyses of Soybean mosaic virus (SMV) in Ontario and Quebec. Can. J. Plant Pathol. 31, 108-113. Vijayapalani, P., Maeshima, M., Nagasaki-Takekuchi, N. and Miller, W.A. (2012) Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitate potyvirus movement. PLOS Pathog. 8, e1002639. Wang, L., Eggenberger, A., Hill, J. and Bogdanove, A.J. (2006) Pseudomonas syringae effector avrB confers soybean cultivar-specific avirulence on Soybean mosaic virus adapted for transgene expression but effector avrPto does not. Molec. Plant-Microbe Interact. 19, 304-312. Wang, X.Y., Eggenberger, A.L., Nutter, F.W. and Hill, J.H. (2001) Pathogen-derived transgenic resistance to Soybean mosaic virus in soybean. Molec. Breed. 8, 119-127. Wang, X., Gai, J. and Zuo, Z. (2003) Classification and distribution of strain groups of soybean mosaic virus in middle and lower Huang-Huai and Changjiang valleys. Soybean Sci. 22, 102- 107. Wang, R.Y. and Ghabrial, S.A. (2002) Effect of aphid behavior on efficiency of transmission of Soybean mosaic virus by the soybean-colonizing aphid, Aphis glycines. Plant Dis. 86, 1260-1264. Wang, Y. and Hajimorad, M. R. (2016) Gain of virulence by Soybean mosaic virus on Rsv4- genotype soybeans is associated with a relative fitness loss in a susceptible host. Mol. Plant Pathol. 17, 1154-1159. Wang, Y., Khatabi, B. and Hajimorad, M.R. (2015) Amino acid substitution in P3 of Soybean mosaic virus to convert avirulence to virulence on Rsv4-genotype soybeans is influenced by the genetic composition of P3. Mol. Plant Pathol. 16, 301-307. Wang, D., Ma, Y., Liu, N., Yang, Z., Zheng, G. and Zhi, H. (2011a) Fine mapping and

identification of the soybean Rsc4 resistance candidate gene to soybean mosaic virus. Plant Breeding 130, 653-659. Wang, D., Ma, Y., Yang, Y., Liu, N., Li, C., Song, Y. and Zhi, H. (2011b) Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean. Theor. Appl. Genet. 122, 555-565.

This article is protected by copyright. All rights reserved. Wang, J., Shine, M.B., Gao, Q.M., Navarre, D., Jiang, W., Liu, C., Chen, Q., Hu, G. and Kachroo, A. (2014) Enhanced disease susceptibility 1 mediates pathogen resistance and virulence function of a bacterial effector in soybean. Plant Physiol. 165, 1269-1284. Wen, R.-H. and Hajimorad, M.R. (2010) Mutational analysis of the putative pipo of soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 400, 1-7. Wen, R.-H., Khatabi, B., Ashfield, T., Saghai Maroof, M.A. and Hajimorad, M.R. (2013) The HC-Pro and P3 cistrons of an avirulent Soybean mosaic virus are recognized by different genes at the complex Rsv1 locus. Mol. Plant-Microbe Interact. 26, 203-215. Wen, R.-H., Saghai Maroof, M.A. and Hajimorad, M.R. (2011) Amino acid changes in P3, and not the overlapping pipo-encoded protein, determine virulence of Soybean mosaic virus on functionally immune Rsv1-genotype soybean. Mol. Plant Pathol. 12, 799-807. White, A. (2015) The polymerase slips and PIPO exist. EMBO Rep. 16, 885-886. Whitham, S.A., Qi, M., Innes, R.W., Ma, W., Lopes-Caitar, V. and Hewezi, T. (2016) Molecular soybean-pathogen interactions. Annu. Rev. Phytopathol. 54, 19.1-19.26. Yan, H., Wang, H., Cheng, H., Hu, Z., Chu, S., Zhang, G. and Yu, D. (2015) Detection and fine-mapping of SC7 resistance genes via linkage and association analysis in soybean. J. Integr. Plant Biol. 57, 722-729. Yang, Q.H. and Gai, J.Y. (2011) Identification, inheritance and gene mapping of resistance to a virulent Soybean mosaic virus strain SC15 in soybean. Plant Breeding 130, 128-132. Yang, H., Huang, Y., Zhi, H. and Yu, D. (2011) Proteomics-based analysis of novel genes involved in response toward soybean mosaic virus infection. Mol. Biol. Rep. 38, 511-521. Yang, Y., Lin, J., Zheng, G., Zhang, M. and Zhi, H. (2014) Recombinant soybean mosaic virus is prevalent in Chinese soybean fields. Arch. Virol. 159, 1793-1796. Yang, Y., Zheng, G., Han, L., Dagang, W., Yang, X., Yuan, Y., Huang, S. and Zhi, H. (2013) Genetic analysis and mapping of genes for resistance to multiple strains of Soybean mosaic virus in a single resistant soybean accession PI 96983. Theor. Appl. Genet. 126, 1783-1791. Yin, X., Wang, J., Cheng, H., Wang, X. and Yu, D. (2013) Detection and evolutionary analysis of soybean miRNAs responsive to Soybean mosaic virus. Planta 237, 1213-1225.

This article is protected by copyright. All rights reserved. Yoon, Y., Lim, S., Jang, Y.W., Kim, B.-S., Bao, D.H., Maharjan, R., Yi, H., Bao, S. et al. (2017) First report of Soybean mosaic virus and Soybean yellow mottle mosaic virus in Vigna angularis. Plant Dis. doi.org.10.1094/PDIS-08-17-1284-PDN. Zhang, C., Grosic, S., Whitham, S.A. and Hill, J.H. (2012) The requirement of multiple defense genes in soybean Rsv1 mediated extreme resistance to Soybean mosaic virus. Mol. Plant-Microbe. Interact. 25, 1307-1313. Zhang, C., Hajimorad, M.R., Eggenberger, A.L., Tsang, S.,Whitham, S.A. and Hill, J.H. (2009) Cytoplasmic inclusion of Soybean mosaic virus serves as a virulence determinant on Rsv3-genotype soybean and a symptom determinant. Virology 391, 240–248. Zhang, M.H., Lu, W.Q., Zhong, Z.X., Wang, R.Y., Li, Y.H. (1986) The importance of the diseased seedlings from SMV infected seeds and the vector of the virus in the epidemic. Acta Phytopathol. Sin. 16, 151-158. Zhang, X.C., Sato, S., Ye, X.H., Dorrance, A.E., Morris, T.J. and Clemente, T.E., Qu, F. (2011) Robust RNAi-based resistance to mixed infection of three viruses in soybean plants expressing separate short hairpins from a single transgene. Phytopathology 101, 1264-1269. Zhao, L., Wang, D., Zhang, H., Shen, Y., Yang, Y., Li, K., Wang, L., Yang, Y. and Zhi, H. (2016) Fine mapping of the RSC8 locus and expression analysis of candidate SMV resistance genes in soybean. Plant Breeding 135, 701-706. Zheng, G.-j., Yang, Y.-q., Ma, Y., Yang, X.-f., Chen, S.-y., Ren, R., Wang, D.-g., Yang, Z.-l. and Zhi, H.-j. (2014) Fine mapping and candidate gene analysis of resistance gene RSC3Q to Soybean mosaic virus in Qihuang 1. J. Integrative Agri. 13, 2608-2615. Zhou, G.C., Shao, Z.Q., Ma, F.F., Wu, P., Wu, X.-Y., Xie, Z.-Y., Yu, D.-Y., Cheng, H., Liu, Z.-H., Jiang, Z.-F., Chen, Q.-S., Wang, B. and Chen, J.-Q. (2015) The evolution of soybean mosaic virus: An updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Res. 208, 189-198. Zhou, G.-C., Wu, X.-Y., Zhang, Y.-M., Wu, P., Wu, X.-Z., Liu, L.-W., Wang, Q., Hang, Y.- Y., Yang, J.-Y., Shao, Z.-Q., Wang, B. and Chen, J.-Q. (2014) A genomic survey of thirty soybean-infecting bean common mosaic virus (BCMV) isolates from China pointed BCMV as a potential threat to soybean production. Virus Res. 191, 125-133.

This article is protected by copyright. All rights reserved. FIGURE LEGENDS Fig. 1 Properties of the Soybean mosaic virus (SMV)-soybean pathosystem. (A) Typical symptoms induced by SMV in a susceptible soybean. (B) Negatively stained filamentous SMV particles of about 750 nm in length. (C) Alate Rhopalosiphum padi that transmits SMV non- persistently. R. Padi is one of the most important aphid vectors of SMV in the Midwest of the United States. (D) Seed-coat mottling of soybean seeds induced by SMV.

This article is protected by copyright. All rights reserved. Fig. 2 Genome organization of Soybean mosaic virus (SMV) illustrating the proteases responsible for cleaving (arrows) the polyprotein precursor to produce mature proteins shown as rectangular boxes. The functions attributed to the SMV encoded proteins are indicated for each cistron. Single amino acid changes in HC-Pro and CP associated with seed and aphid transmission of SMV are indicated parenthetically.

Fig. 3 Phenotypes of SMV resistance in soybean isolines expressing resistant and susceptible alleles for each of the Rsv genes to inoculation with cDNA clones of avirulent SMV strains modified to express the uidA gene encoding the β-glucuronidase reporter enzyme. Unifoliate leaves were biolistically inoculated and stained for β-glucuronidase activity 14 days post inoculation. Note the expression of extreme resistance by (A) the Rsv1 allele in L78-379 against SMV-G2, (B) the Rsv3 in L29 against SMV-G7, and (C) restriction in movement by the Rsv4 allele in V94-5152 against SMV-G2.

Fig. 4 Avirulence/virulence determinants SMV shown on a schematic representation of the SMV genome on soybean genotypes containing (A, B) the entire Rsv1 locus from PI96983, (C) two soybean recombinant inbred lines (RILs) that contained a recombination event within the Rsv1 locus from PI96983 (Hayes et al., 2004) , (D) the Rsv3-locus in L29, and (E) the Rsv4-locus in V94-5152. The location of the mutation and the amino acid residues for each determinant is shown below the viral protein. Data are summarized from (A) (Eggenberger et al., 2008); (B) (Hajimorad et al., 2008, 2011; Wen et al., 2013); (C) (Hayes et al., 2004; Hajimorad et al., 2011; Wen et al., 2011, 2013); (D) (Seo et al., 2009a; Zhang et al., 2009); (E) (Ahangaran et al., 2013; Chowda-Reddy et al., 2011a; Khatabi et al., 2012; Wang et al., 2015).

Fig. 5 Proposed Rsv1 signaling pathway. (A) Example of Rsv1 loss-of-extreme resistance (ER) screen strategy via virus-induced gene silencing (VIGS). Inoculation of soybean plants previously infected with a Bean pod mottle virus-derived VIGS vector containing a fragment of the soybean homologue of PHYTOALEXIN DEFICENT 4 (PAD4) (Glyma08g00420) suppressed ER and allowed movement of SMV-G2 expressing the uida gene out of inoculation sites (detected by staining for the β-glucuronidase reporter enzyme). (B) A proposed signaling

This article is protected by copyright. All rights reserved. pathway incorporating gene silencing results from Fu et al. (2009) and Zhang et al. (2012). VIGS suggests that the signaling proteins listed are necessary for Rsv1 resistance. The hierarchy of the signaling pathway is inferred from genetic studies of defense signaling genes in other plant species. NB-LRR, nucleotide binding site leucine-rich repeat; HSP90, heat shock protein 90; SGT1, suppressor of the G2 allele of skp1; RAR1, required for Mla12 resistance 1; EDS1, enhanced disease susceptibility 1; JAR1, jasmonate resistant 1; EDR1, enhanced disease resistance 1; WRKY, WRKY transcription factor family member.

This article is protected by copyright. All rights reserved. Fig. 1 Properties of the Soybean mosaic virus (SMV)-soybean pathosystem. (A) Typical symptoms induced by SMV in a susceptible soybean. (B) Negatively stained filamentous SMV particles of about 750 nm in length. (C) Alate Rhopalosiphum padi that transmits SMV non-persistently. R. Padi is one of the most important aphid vectors of SMV in the Midwest of the United States. (D) Seed-coat mottling of soybean seeds induced by SMV.

60x52mm (600 x 600 DPI)

56x17mm (300 x 300 DPI)

This article is protected by copyright. All rights reserved. Fig. 3 Phenotypes of SMV resistance in soybean isolines expressing resistant and susceptible alleles for each of the Rsv genes to inoculation with cDNA clones of avirulent SMV strains modified to express the uidA gene encoding the βglucuronidase reporter enzyme. Unifoliate leaves were biolistically inoculated and stained for βglucuronidase activity 14 days post inoculation. Note the expression of extreme resistance by (A) the Rsv1 allele in L78379 against SMVG2, (B) the Rsv3 in L29 against SMVG7, and (C) restriction in movement by the Rsv4 allele in V945152 against SMVG2.

132x205mm (300 x 300 DPI)

This article is protected by copyright. All rights reserved. Fig. 4 Avirulence/virulence determinants SMV shown on a schematic representation of the SMV genome on soybean genotypes containing (A, B) the entire Rsv1 locus from PI9683, (C) two soybean recombinant inbred lines (RILs) that contained a recombination event within the Rsv1 locus from PI96983 (Hayes et al., 2004) , (D) the Rsv3-locus in L29, and (E) the Rsv4-locus in V94-5152. The location of the mutation and the amino acid residues for each determinant is shown below the viral protein. Data are summarized from (A) (Eggenberger et al., 2008); (B) (Hajimorad et al., 2008, 2011; Wen et al., 2013); (C) (Hayes et al., 2004; Hajimorad et al., 2011; Wen et al., 2011, 2013); (D) (Seo et al., 2009a; Zhang et al., 2009); (E) (Chowda-Reddy et al., 2011a; Khatabi et al., 2012; Wang et al., 2015; Ahangaran et al., 2013).

179x314mm (300 x 300 DPI)

This article is protected by copyright. All rights reserved. Fig. 5 Proposed Rsv1 signaling pathway. (A) Example of Rsv1 lossofextreme resistance (ER) screen strategy via virusinduced gene silencing (VIGS). Inoculation of soybean plants previously infected with a Bean pod mottle virusderived VIGS vector containing a fragment of the soybean homologue of PHYTOALEXIN DEFICENT 4 (PAD4) (Glyma08g00420) suppressed ER and allowed movement of SMVG2 expressing the uida gene out of inoculation sites (detected by staining for the βglucuronidase reporter enzyme). (B) A proposed signaling pathway incorporating gene silencing results from Fu et al. (2009) and Zhang et al. (2012). VIGS suggests that the signaling proteins listed are necessary for Rsv1 resistance. The hierarchy of the signaling pathway is inferred from genetic studies of defense signaling genes in other plant species. NBLRR, nucleotide binding site leucinerich repeat; HSP90, heat shock protein 90; SGT1, suppressor of the G2 allele of skp1; RAR1, required for Mla12 resistance 1; EDS1, enhanced disease susceptibility 1; JAR1, jasmonate resistant 1; EDR1, enhanced disease resistance 1; WRKY, WRKY transcription factor family member.

108x124mm (100 x 100 DPI)

This article is protected by copyright. All rights reserved. Table 1. Current status of research on soybean R gene loci conditioning resistance to Soybean mosaic virus (SMV). SMV strain- specific resistance conferred by genes on four chromosomal regions in the soybean genome is described in terms of resistant cultivars, SMV strains, flanking genetic markers, physical intervals, and candidate genes within the identified target regions.

R gene Host genomic locus information Candidate genes (SMV strains) CHROMOSOME NO. 2 (MLG D1B) Rsv4 (G1-G7) Cultivar: V94-5152 Candidate genes1: Glyma.02g121500, Glyma.02g121600, Glyma.02g121700, Glyma.02g121800, Interval: 94 kb (12,044,285–12,163,994) Glyma.02g121900, Glyma.02g122000, Glyma.02g122100, Glyma.02g122200, Glyma.02g122300, Flanking markers: Glyma.02g122400, Glyma.02g122500 Rat2 and S6ac Reference: (Ilut et al., 2016) Other reference: (Klepadlo et al., 2017a) Rsc8 (SC8) Cultivar: Kefeng No.1 Putative MADS-box protein encoding candidate genes1: Glyma.02G121500, Glyma.02G121600 Interval: 30.75 kb (12,060,477- Reference: (Zhao et al., 2016) 12,091,080) Other reference: (Wang et al., 2011b) Flanking markers: BARCSOYSSR_02_0614 and ZL-52 Rsc7 (SC7) Cultivar: Kefeng No.1 Reference: (Yan et al., 2015) Interval: 158 kb (12,156,250- 12,313,357) Flanking markers: BARCSOYSSR_02_0621 BARCSOYSSR_02_0632 Rsc18 (SC18) Cultivar: Kefeng No.1 Candidate genes1: Glyma.02G127800, Glyma.02G128200, Glyma.02G128300 (specific to Interval: 80 kb (13,026,964-13,104,653) Kefeng No.1) Flanking markers: Reference: (Li et al., 2015) BARCSOYSSR_02_0667 BARCSOYSSR_02_0670 CHROMOSOME NO. 6 (MLG C2) Rsc15 (SC15) Cultivar: RN-9 Reference: (Yang and Gai, 2011) Interval: 1.58 Mb (14,644,242-

16,221,141) Flanking markers: Sat213 and Satt286 CHROMOSOME NO. 13 (MLG F) Rsv1 (G1-G7) Cultivar: PI96983 (Rsv1) Cloned NBS-LRR-encoding Rsv1 gene candidates from PI969831: Glyma.13g190000 (5gG3), Interval: 75.3 kb (30,355,157-30,430,435) Glyma.13g190800 (3gG2) References: (Jeong and Saghai Maroof, 2004, Hayes et al., 2004) Rsv1-h Cultivar: Suweon97 (Rsv1-h) Suweon97 contains Rsv1-h that also confers resistance to SC6-N and SC7-N SMV strains. (G1-G7) Interval: 97.5 kb (29,815,342-29,912,454) Candidate NBS-LRR-encoding Rsv1-h genes1: Glyma.13g184800, Glyma.13g184900 (SC6-N, SC7-N) Flanking markers for Rsv1-h: Reference: (Ma et al., 2016) BARCSOYSSR_13_1114 BARCSOYSSR_13_1115 Rsc-ps (SC7) Cultivar: PI96983 Reference: (Yang et al., 2013) Interval: 378 kb (30,501,849-30,880,147) Flanking markers: BARCSOYSSR_13_1140 BARCSOYSSR_13_1155 Rsc-pm (SC3, Cultivar: PI96983 Reference: (Yang et al., 2013) SC6, SC17) Interval: 345 kb (30,119,784-30,464,941) Flanking markers: BARCSOYSSR_13_1128 BARCSOYSSR_13_1136 Rsc3Q (SC3) Cultivar: Qihuang1 Candidate NBS-LRR-encoding genes1: Glyma.13g190000 (Glyma13g25920), Glyma.13g190300 Interval: 181 kb (30,284,317-30,464,941) (Glyma13g25950), Glyma.13g190400 (Glyma13g25970), Glyma.13g190800 (Glyma13g26000) Flanking markers: Reference: (Li et al., 2017) S-110 and BARCSOYSSR_13_1136 Other reference: (Zheng et al., 2014) Rsc12 (SC12) Cultivar: Qihuang22 Reference: (Ma et al., 2010) Interval: (29,609,605--30,739,608) Flanking markers: Satt334 and Sct_033 Rsc14Q or Cultivar: Qihuang1, PI96983 References: (Li et al., 2006; Ma et al., 2011) Rsc14 (SC14) Interval: 3.1 Mb (27,656,933-30,739,608) Flanking markers:

Sat_234 and Sct_033

Rsc18Q (SC18) Cultivar: Qihuang22 Rsc18Q locus coincides with Rsv1, Rpv1 (Peanut mottle virus resistance), Rps3 (Phytophthora root rot (specific to Interval: 568 kb (29,041,580-29,609,652) resistance) Qihuang22) Flanking markers: Reference: (Li et al., 2015) SOYHSP176 and Satt334 CHROMOSOME NO. 14 (MLG B2) Rsv3 (G5-G7) Cultivar: L29 Candidate NBS-LRR encoding gene1: Glyma.14g204700 (Glyma14g38533) Interval: 153 kb (46,937,863- 47,091,090) Reference: (Suh et al., 2011) Flanking markers: Other reference: (Redekar et al., 2016) A519F/R and M3Satt Rsc4 (SC4) Cultivar: Dabaima Candidate NBS-LRR encoding gene1s: Glyma.14g204500 (Glyma14g38500), Glyma.14g204600 Interval: 63.3 kb (46,944,330-47,007,611) (Glyma14g38516), Glyma.14g204700 (Glyma14g38533) Flanking markers: Reference: (Wang et al., 2011a) BARCSOYSSR_14_1413 Other reference: (Li et al., 2016) BARCSOYSSR_14_1416 1 Annotations from Glycine max Wm82.a2.v1 genome sequence