Effect of Temperature on Wheat Streak Mosaic Disease Development in Winter Wheat

Temperature is one of the key factors that influence viral disease development in plants. In this study, temperature effect onWheat streak mosaic virus (WSMV) replication and in planta movement was determined using a green fluorescent protein (GFP)-tagged virus in twowinter wheat cultivars. Virus-inoculated plants were first incubated at 10, 15, 20, and 25°C for 21 days, followed by 27°C for 14 days; and, in a second experiment, virus-inoculated plants were initially incubated at 27°C for 3 days, followed by 10, 15, 20, and 25°C for 21 days. In the first experiment, WSMV-GFP in susceptible ‘Tomahawk’ wheat at 10°C was restricted at the point of inoculation whereas, at 15°C, the virus moved systemically, accompanied with mild symptoms, and, at 20 and 25°C,WSMV elicited severeWSMVsymptoms. In resistant ‘Mace’wheat (PI 651043),WSMV-GFP was restricted at the point of inoculation at 10 and 15°C but, at 20 and 25°C, the virus infected systemically with no visual symptoms. Some plants that were not systemically infected at low temperatures expressed WSMV-GFP in regrowth shoots when later held at 27°C. In the second experiment, Tomahawk plants (100%) expressed systemic WSMV-GFP after 21 days at all four temperature levels; however, systemic WSMV expression in Mace was delayed at the lower temperatures. These results indicate that temperature played an important role in WSMV replication, movement, and symptom development in resistant and susceptible wheat cultivars. This study also demonstrates that suboptimal temperatures impair WSMV movement but the virus rapidly begins to replicate and spread in planta under optimal temperatures. Wheat streak mosaic virus (WSMV; genus Tritimovirus, family Potyviridae) infects wheat worldwide (Brunt et al. 1996; Dwyer et al. 2007; Ellis et al. 2003; Sánchez-Sánchez et al. 2001; Stenger et al. 1998). It causes 2 to 3% annual yield loss in wheat in North America (Great Plains) (Appel et al. 2013). In severe epidemics, WSMV usually causes total crop loss in affected fields (Wegulo et al. 2008). WSMV is transmitted by Aceria tosichella Keifer (wheat curl mite) (Slykhuis 1955; Staples and Allington 1956). The mite also is a vector of two other wheat viruses, Wheat mosaic virus (WMoV), tentatively in the genus Emaravirus (Seifers et al. 1997; Tatineni et al. 2014a) and Triticum mosaic virus (TriMV; genus Poacevirus, family Potyviridae) (Seifers et al. 2009; Tatineni et al. 2009). These viruses are widespread in the Great Plains but WSMV is the most common (Burrows et al. 2008; Byamukama et al. 2013). Environmental factors are known to influence plant–pathogen interactions, affecting both pathogenicity and host defense responses (Browder 1985; Colhoun 1973). Disease resistance in plants to bacteria, fungi, viruses, and insects is known to vary depending on prevailing temperatures (Garrett et al. 2006). Disease severity can be intense at either low or high temperatures but, in culture, the pathogens may establish under a broad temperature range. This is because the effects of temperature on disease, like those of some other environmental factors, may be due to effects on the host, the pathogen, or an interaction between pathogen and host (Colhoun 1973; Wang et al. 2009). Temperature-sensitive resistance to plant viruses has been reported in various host–pathogen systems such as cassava and cassava mosaic geminiviruses (Chellappan et al. 2005), tobacco and Tobacco mosaic virus (TMV) (Király et al. 2008), Nicotiana spp. and Tobacco ringspot virus (Siddiqui et al. 2008), and Nicotiana benthamiana and Cymbidium ringspot virus (Szittya et al. 2003). In wheat, temperature-sensitive resistance that impedes WSMV infection and symptom expression has been identified in various germplasm that is either associated with alien chromatin (Wsm1 gene) (Seifers et al. 1995) or obtained entirely from wheat germplasm (Wsm2) (Fahim et al. 2012; Seifers et al. 2006, 2007). Wsm1 has been deployed into resistant ‘Mace’ wheat (PI 651043) (Graybosch et al. 2009), while Wsm2 has been incorporated into ‘RonL’ and ‘Snowmass’ (Lu et al. 2011, 2012). Recently, another resistance gene, designated Wsm3, was identified in wheat germplasm, and it prevents WSMV symptom expression at higher temperatures (up to 24°C) (Seifers et al. 2013). Temperature-sensitive resistance in wheat cultivars containing the Wsm1 or Wsm2 gene is effective at 18°C but allows infection and symptom expression when subjected to temperatures ranging between 20 and 28°C for sustained periods (Fahim et al. 2012; Seifers et al. 1995, 2006, 2007; Tatineni et al. 2010, 2014b). Recently,Wsm1 andWsm2 genes were found to confer resistance in wheat cultivars by temperaturedependent impairment of viral long-distance movement, with no significant effects on virus replication and cell-to-cell movement (Tatineni et al. 2016). The appearance of visible WSMV symptoms (mosaic or chlorosis) in systemically infected leaves normally indicates virus presence. However, symptomatology does not show the primary site of phloem unloading (Roberts et al. 1997). The introduction of the green fluorescent protein (GFP) gene (Oparka et al. 1996) into viral genomes has permitted the noninvasive monitoring of the progress of viral infections (Baulcombe et al. 1995; Folimonova et al. 2008; Tatineni et al. 2011). In infections by Potato virus X, Citrus tristeza virus, and WSMV, GFP expression was used to track virus movement and study the effect of specific gene deletions on cell-to-cell movement (Baulcombe et al. 1995; Cruz et al. 1996; Folimonova et al. 2008; Oparka et al. 1996; Tatineni et al. 2011). Factors contributing to the impact of WSMV infection on the plant include plant stage at the time of infection and temperature and other environmental stresses during infection (Hunger et al. 1992). In the Great Plains, WSMV damage is usually more severe in cases where winter wheat is planted early in the fall, when temperatures are warmer, or during seasons with warmer growing conditions; however, damage is less severe when wheat is planted late in the fall or during Corresponding author: E. N. Wosula; E-mail: [email protected] Accepted for publication 26 September 2016. © 2017 The American Phytopathological Society 324 Plant Disease /Vol. 101 No. 2 Plant Disease • 2017 • 101:324-330 • http://dx.doi.org/10.1094/PDIS-07-16-1053-RE