Wheat and Barley Susceptibility and Tolerance to Multiple Isolates ofWheat streak mosaic virus

Lehnhoff, E., Miller, Z., Menalled, F., Ito, D., and Burrows, M. 2015. Wheat and barley susceptibility and tolerance to multiple isolates ofWheat streak mosaic virus. Plant Dis. 99:1383-1389. One of the greatest virus disease threats to wheat production in the Great Plains of the USA isWheat streak mosaic virus (WSMV). Breeding programs have developed wheat varieties that are resistant or tolerant to WSMV infection, but these characteristics are climate dependent, and may also vary by WSMV isolate. We tested 10 spring and nine winter wheat (Triticum aestivum) varieties and two barley (Hordeum vulgare) varieties for resistance and tolerance to one WSMV isolate over four years. In spring wheat and barley, there were year by cultivar interactions in terms of resistance and tolerance. However, in winter wheat, yield losses due to WSMV were relatively consistent across years and varieties. Additionally, we tested the impacts of three WSMV isolates individually and in a mixture on twelve, two, and twelve varieties of spring wheat, barley, and winter wheat, respectively. Resistance and tolerance varied by isolate and cultivar, but there were no isolate by cultivar interactions. For spring wheat and barley, yield impacts were greater for two of the three single isolates than for the isolate mixture, whereas in winter wheat, the isolate mixture caused greater yield losses than the individual isolates. Overall, the results indicate that resistance and tolerance phenotypes were influenced by environmental conditions and by WSMV isolate or combination of isolates, suggesting that cultivar screening should be conducted over multiple years and with multiple virus isolates. Wheat streak mosaic virus (WSMV) is a pathogen affecting wheat (Triticum aestivum L.), barley (Hordeum vulgare L.), and other cereal grains globally. In the Great Plains of the USA, this pathogen is one of the most problematic viral pests of cereal crop production, responsible for yield losses averaging up to 7% per year (Appel et al. 2014). The virus is transmitted by the wheat curl mite (WCM, Aceria tosichella Keifer) (Slykhuis et al. 1957), and through wheat seed at low rates (Jones et al. 2005). Both the virus and its vector require living plant hosts for survival and reproduction, so after crop harvest, an alternative host or infected wheat seed is needed until the next crop is planted. WCM and WSMV can infest a large variety of cereal crop and grassy species (Navia et al. 2013), with volunteer wheat being one of the most important alternative hosts between planted crops (Brey et al. 1998). The susceptibility (probability of infection following pathogen exposure) and tolerance (impacts of infection on growth and reproduction) of host plants to viruses is dependent upon many interacting abiotic and biotic factors including climate, vector, and plant genotype (Hull 2002). Understanding these relationships within the wheatWSMV-WCM disease complex can facilitate the development of disease management practices (Miller et al. 2014). For example, plant-virus interactions are often temperature-dependent (Kassanis 1957). Genes that confer resistance to WSMV do not function well at high temperatures (Seifers et al. 2007; Seifers et al. 2006; Fahim et al. 2012), and additionally, viral replication and movement within the plant are affected by temperature (Zaitlin and Hull 1987). Despite management practices based on knowledge of the seasonal dynamics of WCM movement from crops to alternative hosts and back to crops or through transmission in wheat seed (Coutts et al. 2008; Coutts et al. 2014), infection by WSMV is still common. Attempts have been made to control the wheat-WSMV-WCM disease complex through plant resistance to WCM (Carrera et al. 2012) and WSMV (Fahim et al. 2012); however, the utility of these genes is limited due to temperature sensitivity. Furthermore, vectors and viruses often rapidly evolve to overcome single-gene resistance (Harvey et al. 1997; Jones 2009). The potential of WSMV to overcome plant resistance depends, in part, on the diversity of viral strains within a population. Strain diversity in the field is also important to consider when screening wheat genotypes for WSMV resistance or tolerance. While little is known about the diversity of WSMV in the Northern Great Plains, there may be considerable genetic variation in WSMV populations. McNeil et al. (1996) reported that for five populations in Nebraska, there was as much variation within fields as among counties. Also, Robinson and Murray (2013) reported considerable diversity in the adjacent Pacific Northwest, with two distinct clades being present. Furthermore, Robinson and Murray (2013) found recombination within many of the isolates from wheat samples tested, suggesting that collected plants contained a mixed infection of WSMV isolates. Such diversity of isolates has implications for WSMV resistance breeding programs, as variable virus populations could interact differently with virus-resistance genes (Robinson and Murray 2013). These complications illustrate the importance of utilizing disease-resistant or tolerant varieties as part of an integrated disease management program, rather than relying solely on the breeding of resistant varieties. Hundreds of wheat varieties are available to growers across the Northern Great Plains, and new varieties are released annually throughout the region. Many of these varieties have not been screened for their susceptibility and tolerance to WSMV. Nevertheless, a proactive and preventive approach for disease management includes the use of resistant varieties when other options such as delayed planting date, volunteer control, wheat seed testing, and management of alternative hosts do not provide definitive disease control. In addition, Seifers et al. (2003) showed that there was variation in the response of crops including maize, pearl millet, Corresponding author: Mary Burrows; E-mail: [email protected] *The e-Xtra logo stands for “electronic extra” and indicates that two supplementary figures are published online. Accepted for publication 6 April 2015. http://dx.doi.org/10.1094/PDIS-11-14-1205-RE © 2015 The American Phytopathological Society Plant Disease /October 2015 1383 sorghum, and wheat to 52WSMV isolates. Thus, given the genotypic diversity of WSMV, it is important to determine if cultivar resistance/ tolerance is specific to WSMV isolates or varies across isolates as, in the former case, screening for WSMV resistance using a single virus isolate may not provide adequate data on resistance/tolerance. In this multiyear research, we used 12 spring and 12 winter wheat and two barley varieties, to test (i) if there were cultivar differences in the impact of WSMV on host susceptibility (disease incidence rate) and tolerance (based on ability to maintain yield compared with controls), and (ii) if the effects of WSMV were consistent across years, a proxy for environmental variability. Additionally, we (iii) assessed if cultivar disease resistance or tolerance phenotypes were consistent across WSMV isolates or if they are isolate-specific. Materials and Methods Experimental design. Field experiments were conducted from 2008 to 2012 at the Montana State University (MSU) Arthur H. Post Research Farm, five miles west of Bozeman, MT. The soil is an Amsterdam-Quagle silt loam, pH 7.5. Crop species, crop varieties, and WSMV isolates varied by experiment (Table 1). With the exception of Mace which is a WSMV resistant winter wheat cultivar from Nebraska, all wheat and barley varieties are commonly planted in Table 1. Summary of experiments conducted to assess wheat and barley susceptibility and tolerance to multiple isolates of Wheat streak mosaic virus Year(s) Crop Cultivars Notes 2008-2011 Spring wheat Amidon, Choteau, Conan, Corbin, Ernest, Fortuna, Hank, McNeal, Reeder, and Scholar Assessed effects of WSMV (Conrad isolate) on 10 spring wheat varieties (Experiment 1). 2009-2011 Barley Haxby and Metcalfe Barley added in second year of previous experiment (Experiment 1). 2011 Spring wheat Amidon, Choteau, and Conan, Corbin, Ernest, Fortuna, Hank, McNeal, Reeder, Scholar + Duclair, and Vida Assessed effects of four WSMV isolates (Conrad, Huntley, Marias, and Mix) (Experiment 2). 2008-2011 Winter wheat CDC Falcon, Genou, Jagalene, Ledger, Morgan, Pryor, Rampart, Tiber, and Yellowstone Assessed effects of WSMV (Conrad isolate) on nine winter wheat varieties (Experiment 3). 2011 Winter wheat CDC Falcon, Decade, Genou, Jagalene, Jerry, Ledger, Mace, Morgan, Pryor, Rampart, Tiber, and Yellowstone Assessed effects of four WSMV isolates (Conrad, Huntley, Marias, and Mix) (Experment 4). Fig. 1.Mean monthly (A) temperature and (B) precipitation at the Arthur H. Post Research Farm, Bozeman, Montana. The long-term average is from 1966-2014. Error bars around the long-term temperature average are the mean monthly maximum and minimum temperatures, and error bars around the long-term precipitation average are the standard deviation. Data source: Bozeman 6 W Exp Farm weather station, Western Regional Climate Center. Table 2. Experiment 1: Mean Wheat streak mosaic virus (Conrad isolate) incidence and induced yields in spring wheat and barleyz Yield (MT/ha) Yield (MT/ha) Cultivar Incidence (%) Control 1WSMV Relative yield (%) Incidence (%) Control 1WSMV Relative yield (%)