NCERA200: Management Strategies to Control Major Soybean Virus Diseases in the North Central Region
Statement of Issues and Justification
On initiation of the NCERA 200 committee, little was known about the incidence or impact of soybean-infecting viruses in the North Central (NC) region. Since then, research coordinated by this project has revealed that viruses cause recurring disease problems with significant impacts on soybean production in the NC region, the principal soybean producing area of the United States. In multiple years, soybean virus diseases were found at near epidemic levels in NC states causing significant yield reductions, decreased pod and seed set, reductions in oil content of seeds, and seed discoloration. Disease outbreaks were paralleled by abundant insect vector populations associated with these viruses. For example, mild winters allowed bean leaf beetles, which efficiently transmit Bean pod mottle virus (BPMV), to overwinter and immigrate into soybean fields at unprecedented levels, which resulted in very high incidences of BPMV early in the growing season when soybean plants are most sensitive. The spatial and temporal distributions of populations of the introduced soybean aphid, which transmits Alfalfa mosaic virus (AMV), Soybean dwarf virus (SbDV), Soybean mosaic virus (SMV) and several other viruses, also varied greatly from year to year. Emergence of unsuspected viruses in NC soybean fields, such as SbDV, Tobacco streak virus (TSV) and newly discovered viruses including Soybean vein necrosis virus (SVNV) and Soybean yellow mottle mosaic virus have also complicated this situation. While single-gene resistance has been identified for at least some strains of AMV, SMV, and TSV, effective control options for the other viruses remain to be elaborated. This project will coordinate research on soybean-infecting viruses among concerned scientists with the goal of identifying management options that reduce losses to soybean producers.Soybean virus incidence, distribution and disease etiology
Bean pod mottle virus: BPMV is the most common and widespread viral pathogen of soybean in the NC region (11,13,41,50,54) and has been detected as far north as Ontario, Canada (60). BPMV is transmitted by leaf-feeding beetles (primarily bean leaf beetles (Cerotoma trifurcata)). Sources of BPMV infection include rare alternative weed hosts, and very infrequent transmission through seed and by overwintering beetles (6,25,48). Incidences of BPMV infection in soybean fields can be very high in years when overwintering bean leaf beetle populations are high. For example, in 2001 when bean leaf beetle populations were high, 70% of randomly collected soybean leaf samples from 32 Nebraska counties were positive for BPMV (26). Even though the severity of BPMV-induced symptoms declines as plants mature (a phenomenon sometimes called masking), yield losses of up to 52% have been reported from BPMV infected plants. No genes for resistance to BPMV have been identified in cultivated soybean (90,99), but BPMV resistance was detected in a closely related wild soybean species, Glycine soja (61,99). Some soybean lines have been shown to suffer significantly less yield loss when infected with BPMV than others and have been called tolerant to BPMV infection (38,59,71,74,100). Multiple experiments have evaluated management of bean leaf beetle populations to reduce or delay BPMV infections. While insecticide treatments reduced bean leaf beetle populations, they did not consistently reduce the incidence of BPMV infections (9,47,66). Similarly, alteration of planting date has not been consistently successful for disease control (48).
Soybean mosaic virus: SMV is transmitted through seed at rates ranging from 0 to 5% in most commercial varieties and by multiple species of aphids, including soybean aphids, following short feeding periods (13,18,34). However, the efficiency of aphid transmission of SMV by soybean aphids declines dramatically following longer feedings (86). No widely dispersed perennial alternative hosts have been identified for SMV in North America. Consequently, transmission of SMV through seed likely constitutes the primary inoculum source of the virus in the U.S. Incidences of SMV infection in the NC region have been much lower than those for BPMV. For example, in Indiana during 2001, 6% of soybean plants with virus-like symptoms tested positive for SMV compared to 60% positive for BPMV (13). In counties in Iowa, the incidence of SMV infections ranged from 1.5% to 58% in 2005, 2006, and 2007 (53). From 2006 - 2009, SMV was detected in 13% of Illinois counties surveyed (41). Yield losses from SMV infection have been reported as high as 94%. When soybean plants are infected with both BPMV and SMV, symptoms are more severe than infection by either virus alone and usually results in complete loss of yield. Three resistance genes have been identified in soybean germplasm lines to SMV. Soybean lines have been produced carrying all three genes and shown to provide broad-spectrum resistance to all strains of SMV (56,76). However, these genes are not widely used in northern soybean cultivars. Consistent with previous studies, insecticide treatments did not significantly reduce SMV incidence (10,66).
Alfalfa mosaic virus: AMV is transmitted by aphids of multiple species, including the soybean aphid, and through seed at low levels (13,34,85,87). In yield trials in Wisconsin, AMV infections produced yield losses of up to 48% (62). AMV infections were detected at high levels in Nebraska (40% and 26% of fields in 2001 and 2002, respectively) and Wisconsin (28% and 13% of fields in 1999 and 2000, respectively) (26). AMV infection rates in Illinois and Indiana have been less than 1% (13,40,41). Because alfalfa and clover plants in the NC region are commonly infected with AMV, it is possible for the incidence of AMV in soybean to increase more rapidly than that of SMV. Yield loss estimates specific to AMV are 32 to 48% once the incidence of AMV-infected plants exceeds 30% in induced epidemics in Wisconsin (Mueller and Grau, 2007). Two soybean lines have been identified that are resistant to certain AMV isolates (1,46). Pyramiding genes for resistance from these two sources may provide resistance to multiple AMV isolates.
Soybean dwarf virus: SbDV, which causes severe soybean yield losses in Japan (79), is transmitted only by aphids that colonize soybean or other host plants. SbDV infects more than 40% of red clover plants in Illinois (31) and has been consistently detected in commercial soybean fields in both Illinois and Wisconsin at incidences ranging from 0.3 to 2%, often in association with heavy infestations of soybean aphids (67,80,81). From 2006 - 2009, SbDV was detected in 42% of Illinois counties surveyed (41). Multiple Midwestern isolates of SbDV have been shown to be transmitted among soybean plants with low efficiency by soybean aphids (15,80). However, SbDV incidences in Illinois and Wisconsin have not been correlated with annual aphid abundance as determined by the North Central Regional Soybean Aphid Suction Trap Network (41,72). Like BPMV, no sources of resistance for SbDV infection have been identified in cultivated soybean.
Soybean vein necrosis virus: SVNV is a new Tospovirus that was discovered in soybean in Tennessee in 2008, detected in soybean in Illinois and Kentucky in 2009 (84), and caused widespread, significant damage in soybean fields in Arkansas in 2010 (5). Infection by SVNV initially induces vein clearing that becomes necrotic as leaves mature, leading to large sections of leaves becoming necrotic. The incidence of SVNV in commercial soybean fields, and the economic impact of SVNV infections on soybean production have not been determined.
Tobacco streak virus: TSV is transmitted by thrips and very efficiently through seed. TSV was detected in 21% of plants tested in 1999, 18% of plants in 2000, and 45% of plants in 2001, but was not detected in 2002 in production trials in Wisconsin (69). TSV was not detected in Indiana during 2000 and was detected in only three samples in Illinois during 2001, 2007 and 2009 (13,41). In soybean, TSV titers decline significantly as plants mature and recover from infection. Consequently, TSV incidence, as determined by enzyme-linked immunosorbent assay (ELISA), can appear to increase and then decrease over time (69). Hence, the point during infections at which samples are analyzed for virus infection can affect the ability to detect viruses. Even though the severities of symptoms induced by AMV and TSV infections appear to decline over time, both viruses are still capable of being transmitted through seed and reducing yields (69). In yield trials, TSV can significantly reduce soybean yields, but the source of the virus and its impact on commercial soybean production are unknown. Almost all soybean varieties tested have been susceptible. Recently, Wang et al. (19) identified a soybean line that is resistant to Illinois and Kentucky isolates of TSV.
Current status of soybean virus management:
Illustrating the need for continued research, there are currently no specific production practices recommended for the management of the most prevalent virus diseases of soybean in the NC region that can be implemented by soybean producers. For example, the Soybean Plant Health Initiative web site (http://www.planthealth.info) lists four management strategies for soybean-infecting viruses: 1) soybean variety selection, 2) planting virus-free seed, 3) control of insect vectors, and 4) crop management to avoid periods of peak insect activity. However, information about sensitivity to virus infection is available only for a very small number of commercial soybean cultivars, and commercial seed are not routinely assayed for seed transmission of viruses. Hence, growers have no means to select cultivars that, for example, are less sensitive to BPMV or have SMV-free seed. Additionally, research in the NC region has shown that insecticidal control of vector insects and altering planting date to avoid vector activity does not provide consistent reduction in the incidence of virus infections.
While the incidences of AMV, SbDV, SMV, SVNV and TSV are usually low, incidences of BPMV infections can exceed 80% in years when bean leaf beetle populations are high. Since vector management often is ineffective in reducing incidence of infection by non-persistently transmitted viruses, the most cost-effective and sustainable method for limiting losses caused by virus diseases of soybeans is the development of soybean cultivars that are resistant to or tolerant of virus infection. To date, resistance to infection by BPMV or SbDV has not been detected in cultivated soybean, and no information is yet available on possible sources of resistance for SVNV. Genes for resistance to infection by AMV, SMV, and TSV have been identified in soybean. In addition, transgenic soybean plants have been produced for resistance to BPMV, SbDV and SMV (70,82,88). However, none of these genes is widely used. For example, less than 2% of the commercial soybean varieties available in Illinois have resistance to SMV (http://www.vipsoybeans.org). This underutilization of available genetic resources likely results from masking of virus symptoms that leads to the perception that soybean viruses do not cause economically important yield losses - in spite of research dating back more than 40 years that has documented significant cultivar-specific yield losses from BPMV infections, e.g., (74). Thus, the need for incorporation of virus resistance/tolerance into northern soybean lines is critical.
Impacts and accomplishments during previous committee period: One of the most significant achievements of this project is the bringing together of scientists from different disciplines to work on soybean virus problems. The objectives during the previous five years were to 1) enhance interaction among scientists who are engaged in fundamental and applied soybean virus research and 2) establish media for effective dissemination and communication of information about the incidence, identification, and management of soybean virus diseases. Under the first objective, research coordinated by the committee has had a major beneficial impact to soybean producers in the North Central United States through coordination, promotion, and interaction of regional research sponsored by the North Central Soybean Research Program, state soybean research and promotion councils, USDA-ARS, and other funding agencies. At the time of inception of this project, virus diseases were epidemic in multiple areas of the region. Further, in contrast to previous supposition, green-stem disorder does not appear to be strongly associated with infection by viruses (32,42). Although, BPMV and SMV have historically been most important, surveys in various states coordinated by the project identified the presence of AMV, SbDV, SVNV, Tobacco ringspot virus, and TSV in the region (26,31,41,53,62,69,84). Distribution and incidence was dependent upon vector populations and geographic region (53). The committee coordinated the development of diagnostic reagents and methodologies, which have been shared among cooperators. Similarly, gene silencing systems based on BPMV were developed that have facilitated studies of gene function in disease resistance and fatty acid metabolism (44,58,63,92-94). Basic biology of soybean-infecting viruses was investigated, including the expression and function of SMV genes (51,52,91), the role of RNA-RNA recombination virus virulence (75,95), and the structure of SMV was determined (45).
Extensive efforts have been devoted to describing the ecology and phenology of insect vectors (especially related to bean leaf beetles and soybean aphids) and whether these could lead to disease control. Chemical and cultural practice were shown to significantly reduce damage from insect feeding, but impacts on virus incidence were more variable (6,9,10,43,48,71). Consequently, longer-term strategies for all viruses dictate the development of tolerance and/or resistance. For BPMV, no resistance genes are known to exist in cultivated soybean, but were discovered in closely related species. Research in several states has identified apparent tolerance to BPMV using varying techniques (38,59,71,74,100). Some currently available commercial cultivars were shown to possess tolerance to virus infection. In other cases, it is available in germplasm or breeding lines. This remains to be incorporated into commercial cultivars.
AMV, SbDV, SVNV and TSV previously were not commonly isolated from soybean in the NC states. The impacts these virus might have for producers is unclear. AMV was detected for the first time in soybean in Tennessee and shown to produce synergistic disease with SMV (21,55). A gene for AMV resistance was discovered and mapped in a soybean plant introduction (46). However, because the high variability of AMV isolates in soybean, the sustainability of this resistance needs to be evaluated. Also, the first reported resistance to TSV was discovered (90). Identification and characterization of new sources of virus resistance/tolerance were made possible through resistance screening (17,89,90,97,98).
Previously, three naturally occurring resistance genes to SMV were identified. However little information was available concerning how the genes might act, and how durable they would be in the field. Research in the last period showed that pyramiding the three resistance genes conferred broad-spectrum resistance to SMV (57,77), but also demonstrated that naturally occurring and artificially selected SMV isolates were capable of overcoming at least one of these resistance genes (12,20,22). The interactions between SMV and soybean genes leading to resistance, susceptibility and hypersensitive disease were characterized (27-30,83,96).
As previously suggested, the introduction of soybean aphids from Asia added additional complexity to the picture. Of major potential impact is the discovery of SbDV in soybeans in Illinois and Wisconsin, and the documentation of its transmission by the soybean aphid. Even though soybean aphids transmit AMV, SbDV, and SMV (15,80,87) and have been associated with devastating virus diseases in snap bean throughout the Great Lakes region, no evidence has been found for increased incidence of the three viruses in soybean. For the second objective, research results generated by this group have been disseminated to soybean growers and industry through extensive extension efforts ranging from meetings, fact sheets, multimedia productions, and web sites, including playing a major technical supporting role to the Plant Health Initiative web site (http://www.planthealth.info) developed by the North Central Soybean Research Program. In addition, websites are maintained by universities in Illinois (4), Iowa (64,65), Ohio (19), Nebraska (23,24), and Wisconsin (3,14) with information on virus diseases in those states. Educational materials for high school students that describe the impact of BPMV infections on soybean have been prepared for dissemination through the American Phytopathological Society (49). Press releases have been prepared describing new developments in soybean virus diseases, like that from the University of Arkansas describing the discovery, incidence and symptoms induced by SVNV (5). Presentations have been made at university field days, e.g., (16), and commodity board and growers group meetings. Preliminary data from field trials and virus surveys have been made available to the public on web pages (2,68,78), extension publications (7,8,33,35-37,39,73) and, as described above, the reactions of approximately 400 commercial soybean lines to infection by SMV are determined each year and posted on the web (http://www.vipsoybeans.org) where they are immediately available to producers. Summary Soybean virus diseases in the NC region result from dynamic interactions among viruses, associated arthropod vectors and susceptible soybean plants, and have the potential to cause severe economic losses for soybean producers. While globalization of trade has opened new markets to NC soybean producers, it has also resulted in the introduction of potential virus vector insects into the region, most notably the soybean aphid, that have become established and caused significant disease problems in soybean and related legume crops. Because of the constantly evolving nature of vector populations, it is critically important to monitor the incidence of virus disease in the NC region to try to anticipate future epidemics. It is also important to reduce losses to endemic and emerging soybean viral pathogens by taking advantage of resources currently available and identifying and improving sources of resistance/tolerance to virus infection. The committee therefore seeks to develop an understanding of these diseases and their epidemiology and pathology and to provide management strategies for these diseases through a multi-state, multi-disciplinary effort composed of virologists, plant pathologists, entomologists, and agronomists. Currently, annual meetings, sponsored by the North Central Soybean Research Program in coordination with this committee, have assisted in reviewing newly developed information, discussing what is still not known, and developing priorities for future research. Through continuation of its work, the committee will strive to minimize the risk from these diseases to NC soybean producers. An NCERA committee will provide the administrative, communication, and educational structures required for bringing leading researchers together to accomplish these goals and objectives.
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