Co-Infection of Beet Mosaic Virus with Beet Yellowing Viruses Leads to Increased Symptom Expression on Sugar Beet
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Co-infection of Beet mosaic virus with Beet Yellowing Viruses Leads to Increased Symptom Expression on Sugar Beet William M. Wintermantel, United States Department of Agriculture, Agricultural Research Service, 1636 E. Alisal Street, Salinas, CA 93905 (5,13,32). Seed yields may be decreased ABSTRACT by up to 70% as a result of virus yellows Wintermantel, W. M. 2005. Co-infection of Beet mosaic virus with beet yellowing viruses leads infection (6). Each virus in the yellows to increased symptom expression on sugar beet. Plant Dis. 89:325-331. complex differs in its effect on yield in single infections. BYV infection results in Three distinct aphid-transmitted viruses associated with a yellowing disease on sugar beet were decreased leaf area and losses in both root examined in single and mixed infections for the effects of virus interactions on plant weight, rate weight and sugar yield (13). Yield losses of symptom development, and virus concentration. Sugar beet lines exhibiting different degrees associated with BWYV infection are much of susceptibility to the virus yellows complex were inoculated with either one, two, or all three less than those resulting from infection by viruses. Severe stunting, as measured by fresh plant biomass, was observed with mixed infec- tions with Beet yellows virus (BYV) and Beet mosaic virus (BtMV), compared to single infec- BYV (13). BtMV infections result in less tions of these viruses. In addition, the overall rate of appearance of Beet western yellows virus than 10% yield loss even when plants are (BWYV) symptoms increased during co-infection with BtMV. Synergistic effects on stunting infected early (13). severity, as measured by plant biomass, were more pronounced in susceptible beet lines, but Members of all three virus genera (rep- similar patterns also were observed in lines exhibiting tolerance to virus yellows. Relative con- resented here by BYV, BWYV, and BtMV) centrations of viruses were compared among single and mixed infections using dot-blot hybridi- can be present in plants at the same time. zation with virus specific probes, and quantified by phosphorimage analysis. Titers of all three Although BtMV is widespread in sugar viruses increased as a result of co-infection compared with single infections. beet production worldwide, it was not clear what effect interactions between Additional keywords: closterovirus, polerovirus, potyvirus, resistance, synergism BtMV and yellowing viruses could have on disease development. Furthermore, no studies had been conducted on the effects of mixed infections of these viruses on the “Virus yellows” is a term frequently are transmitted by the green peach aphid rate of disease development or on virus used by the sugar beet industry, and refers (Myzus persicae Sulzer) (Table 1). Other concentration in sugar beet plants. Possible to a disease resulting from a complex of aphids, such as Aphis fabae Scopoli (a effects of mixed infections were suggested viruses causing beet leaves to yellow pre- highly efficient vector of BYV), can by field studies demonstrating that yield maturely. Virus yellows has contributed to transmit some members of the complex; and sugar content reductions were more disease-related yield losses in California but M. persicae is the only vector known severe during field infection with combina- sugar beet production for many years (7). to efficiently transmit all yellowing viruses tions of these viruses (30). Studies by Different individual viruses or virus com- of sugar beet (13). Shepherd et al. (30) indicated additive binations are responsible for the disease in Symptoms on sugar beet resulting from effects on yield (tons/acre), and in some the many sugar beet production regions of BYV infection begin with light vein- cases sugar content, during co-infection by the world. Beet yellows virus (BYV; family clearing visible on leaves early in infec- BYV, BWYV, or BtMV. In addition, stud- Closteroviridae, genus Closterovirus), Beet tion, followed later by development of ies on other virus synergisms have identi- western yellows virus (BWYV; family interveinal yellowing on subsequent leaves fied interactions between potyviruses and Luteoviridae, genus Polerovirus), and Beet (Table 1). Infection by BWYV produces an members of both the Closteroviridae chlorosis virus (BChV; family Luteoviri- interveinal yellowing symptom difficult to (11,16) and Luteoviridae (3,4). Studies dae, genus Polerovirus) contribute to the distinguish from that caused by BYV. In conducted in the 1980s with a close rela- disease in the United States (Table 1) contrast to BYV, however, infection by tive of BWYV, Potato leafroll virus (13,14,20). In Europe, Beet mild yellowing BWYV or other beet-infecting polerovi- (PLRV; family Luteoviridae, genus Polero- virus (BMYV; family Luteoviridae, genus ruses does not produce the initial vein- virus), found that PLRV accumulation Polerovirus) is the predominant virus asso- clearing symptom (Table 1). A third type increased dramatically, and the ability of ciated with the disease (Table 1), although of virus associated with virus yellows is PLRV to exit phloem was enhanced, dur- the other three are also present in some Beet mosaic virus (BtMV; family Potyviri- ing co-infection of Nicotiana clevelandii areas (13,14,20). It is not uncommon for dae, genus Potyvirus; Table 1). BtMV is and N. benthamiana with potyviruses multiple aphid-transmitted viruses to infect present in all beet-growing regions (3,4). The leader-proteinase (L-Pro) en- the same plant simultaneously. All viruses throughout the world (25,27) and is often coded by the closterovirus, BYV, interferes associated with the virus yellows complex found in fields with virus yellows (13), with accumulation and systemic movement although it is not considered a yellowing of another potyvirus, Tobacco etch virus, virus. Infection of sugar beet by BtMV in a host-specific manner (11), suggesting Corresponding author: W. M. Wintermantel results in a generalized leaf mottling or the possibility of interactions between E-mail: [email protected] mosaic (Table 1), but only a slight de- BtMV and BYV as well. Sweet potato Accepted for publication 1 November 2004. crease in overall plant growth. In areas chlorotic dwarf disease is the result of a where virus yellows is widespread, sugar virus disease complex involving interac- yield can be decreased by as much as 50% tions between a potyvirus and a crinivirus DOI: 10.1094/PD-89-0325 as a result of early infection. This effect is (family Closteroviridae) (16). In this syn- This article is in the public domain and not copy- rightable. It may be freely reprinted with custom- primarily attributed to BYV, although ergism, concentrations of the potyvirus, ary crediting of the source. The American Phyto- other yellowing viruses can impact sugar Sweet potato feathery mottle virus pathological Society, 2005. yield as well if infection occurs early (SPFMV), were markedly elevated as a Plant Disease / March 2005 325 result of co-infection by the crinivirus, house. The virus isolates BYV-OR and under standard greenhouse conditions for 8 Sweet potato chlorotic stunt virus BWYV-OR were obtained from sugar beet weeks, under natural lighting, with green- (SPCSV). Interestingly, both synergisms steckling nurseries near Medford, OR. house temperature fluctuations varying by involving a potyvirus and a member of the BtMV-WA was obtained from table beet season. Plants were watered once daily and Closteroviridae contrast with the tradi- collected in the state of Washington. All provided with liquid fertilizer every 2 tional view of potyvirus synergisms, in three isolates have been maintained by the weeks with watering. The number of which the potyvirus remains unaffected but Salinas Virology Lab for several years. symptomatic plants per line per treatment facilitates accumulation of the associated These isolates were increased on source was recorded weekly, and percent infection virus (34). plants prior to transmission to provide was calculated. Although all three viruses The purpose of the experiments de- inoculum for aphid feeding. BYV was are common in California and are present scribed herein was to determine the effect increased on New Zealand Spinach (Tetra- in Monterey County where experiments of infection by multiple viruses associated gonia expansa Murr.), BWYV on shep- were conducted, all plant material from with virus yellows of sugar beet on symp- herd’s purse (Capsella bursa-pastoris L.), tests was autoclaved prior to disposal as a tom expression and plant growth. Three and BtMV on sugar beet (Beta vulgaris matter of standard procedure. viruses associated with virus yellows L.). Aviruliferous GPAs were allowed to Dot-blot hybridizations. Total nucleic (BYV, BWYV, and BtMV) were intro- feed on source plants containing single acid samples were prepared from sympto- duced into sugar beet breeding lines vary- infections of either BYV, BWYV, or BtMV matic leaves at 8 weeks postinoculation ing in susceptibility to virus yellows, in for approximately 48 h. After this time, (wpi) using a modification of procedures order to examine virus interactions that leaf pieces containing approximately 10 described by Dellaporta et al. (10). To affect the rate of symptom development, aphids each were cut from source plants determine virus concentration, replicate fresh plant biomass, and virus nucleic acid and deposited onto the basal leaves of dot blots were performed for each virus in concentration in leaf tissue. sugar beet seedlings (approximately two- single, double, and triple infections, using leaf stage) growing in 10-cm (4-in) square nucleic acid probes specific for detection MATERIALS AND METHODS pots containing greenhouse potting mix. of each virus. The BYV probe was a 602- Plant varieties and aphid transmis- Insect cages were placed over each plant nucleotide portion of the coat protein gene sions. Two susceptible sugar beet breeding individually to contain aphids and prevent of BYV (nucleotides 13638 to 14240) lines and two lines with tolerance to virus movement between plants. Plants to be subcloned from a larger BYV clone kindly yellows (18,19) were selected for these inoculated with a single virus received provided by V.