The effects of Gibberella zeae, Barley Yellow Dwarf Virus, and co-infection on Rhopalosiphum padi olfactory preference and performance Rafaela Cristina dos Santos, Maria Fernanda Gomes Villalba Peñaflor, Patrícia Alessandra Sanches, Cristiane Nardi, et al. Phytoparasitica ISSN 0334-2123 Phytoparasitica DOI 10.1007/s12600-015-0493-y
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Author's personal copy Phytoparasitica DOI 10.1007/s12600-015-0493-y
The effects of Gibberella zeae, Barley Yellow Dwarf Virus, and co-infection on Rhopalosiphum padi olfactory preference and performance Rafaela Cristina dos Santos & Maria Fernanda Gomes Villalba Peñaflor & Patrícia Alessandra Sanches & Cristiane Nardi & José Mauricio Simões Bento
Received: 3 July 2015 / Accepted: 30 September 2015 # Springer Science+Business Media Dordrecht 2015
Abstract Insect-borne viruses promote several changes in plant phenotype, which can modify plant-vector interactions in favor of virus survival and dissemination. Although co-infections commonly occur in the field, little is known about their effects on interactions with the vector. The ecological interactions between Barley Yellow Dwarf Virus (BYDV) and its aphid vector, Rhopalosiphum padi, have been investigated extensively, but the vector’s behavior in more complex scenarios has yet to be examined. We assessed olfactory response and performance of R. padi to wheat singly and doubly infected by the pathogenic fungus Giberella zeae and BYDV. Non-viruliferous aphids preferred odors of BYDV-infected wheat over healthy wheat, as previously reported in the literature, and they were still
preferentially attracted to BYDV-infected plant during co-infection. However, around 35% more nonviruliferous aphids chose healthy wheat over G. zeaeinfected wheat. Viruliferous aphids did not show any preference to the treatments. BYDV-infected wheat was a superior host than healthy wheat for the aphids whose population increased in 25%. We observed a synergistic effect of the co-infected wheat, which was the best host for aphids, and promoted an elevation of 42% on population growth. Our results indicate that co-infection might be beneficial for virus spread as does not interfere with aphid olfactory preference and provides greater colony growth than in singly infected plants. Keywords head blight of wheat . persistently transmitted viruses . plant-vector interactions . Triticum aestivum
Electronic supplementary material The online version of this article (doi:10.1007/s12600-015-0493-y) contains supplementary material, which is available to authorized users. R. C. dos Santos : M. F. G. V. Peñaflor : P. A. Sanches : J. M. S. Bento Departament of Entomology and Acarology, Escola Superior de Agricultura BLuiz de Queiroz^, Universidade de São Paulo, Avenida Pádua Dias, 11, CP 09, Piracicaba, SP, Brazil R. C. dos Santos : C. Nardi Departament of Agronomy, Unicentro-Universidade Estadual do Centro Oeste, Rua Simeão Camargo Varela de Sá, 03, Guarapuava, PR, Brazil M. F. G. V. Peñaflor (*) Department of Entomology, Universidade Federal de Lavras, Câmpus Universitário, Caixa Postal 3037 Lavras, MG, Brazil e-mail:
[email protected]
Introduction Many plant viruses depend on insect vectors to spread in the field. Infection by insect-borne plant viruses can induce changes in the host phenotype that alter vector behavior (Hodge & Powell 2008; Fereres & Moreno 2009). These virus-induced plant traits usually promote novel interactions with insect vectors that favor pathogen acquisition and transmission (Mauck et al. 2010). Vectors must first be attracted to infected plants, but after acquiring virions, the movement of vectors to healthy plants is essential for virus dissemination (Mauck et al. 2012; Moreno-Delafuente et al. 2013).
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Visual symptoms of viral infection, such as yellowing leaves, were once thought to mediate the attractiveness of infected plants to insect vectors, particularly aphids (Ajayi & Dewar 1983; Eckel & Lampert 1996). Nevertheless, most recent studies have revealed that changes in plant volatile profiles seem to be a common plant virus strategy for attracting insect vectors to infected plants (Eigenbrode et al. 2002; JiménezMartínez et al. 2004a; Mauck et al. 2010). Similarly, plant nutritional quality can also change in response to viral infection, modifying vector feeding and settlement on infected plants (Colvin et al. 2006). One of the best studied systems is the Barley yellow dwarf virus (BYDV) (Luteoviridae), which is a serious wheat pathogen that is transmitted by the bird cherry-oat aphid, Rhopalosiphum padi L. (Hemiptera: Aphididae), a global wheat pest (Irwin & Thresh 1990; Miller & Rasochova 1997), among other species such as Sitobion avenae (F.) or Schizaphis graminum (Rondani). Because BYDV is persistently transmitted by aphids, the virus circulates in the phloem, and aphids only acquire viral particles if they sustainably feed on plant sap (Gray & Gildow 2003). BYDV circulates in the aphid body but does not replicate within it and is retained in the aphid’s salivary glands (Jing‐Quan et al. 1997; Gray et al. 2014). Therefore, BYDV can be carried by aphids for a long time but is only transmitted during phloem feeding (Brault et al. 2010). The ecological interactions between BYDV and the bird cherry-oat aphid have been studied extensively over the last ten years (Jiménez-Martinez & Bosque-Pérez 2004; Jiménez-Martínez et al. 2004a, b; Medina-Ortega et al. 2009; Bosque-Pérez & Eigenbrode 2011; Ingwell et al. 2012). BYDV-infected plants release volatiles that are attractive to the bird cherry-oat aphid (MedinaOrtega et al. 2009), and are of greater nutritional value relative to healthy plants possibly stimulating aphid feeding (Ajayi 1986; Mauck et al. 2012). However, the host preference of the bird cherry-oat aphid changes when it is carrying BYDV, and it is attracted to healthy wheat over BYDV-infected plants (Ingwell et al. 2012). BYDV infection has been reported to incur great yield losses, particularly when associated with other fungal plant pathogens (Potter 1980; Sward & Kollmorgen 1986) such as Gibberella zeae (Schwein.) Petch., the causal agent of the head blight of wheat (Smith 1962). In wheat-producing countries, head blight of wheat is highly destructive and results in large yield losses due to reduced grain weight (McMullen et al.
1997; Casa et al. 2004). Because this fungus produces mycotoxins (e.g., vomitoxin) when colonizing grains, consuming wheat-derived products can also pose a health risk to humans and animals (Simpson et al. 2001; Bhat et al. 2010). Although co-infections in plants regularly occur in natural and managed ecosystems, few studies have focused on the effects of co-infections on plant-insect interactions. Most studies have focused on double infection by insect-borne viruses, which often interact either synergistically or antagonistically (Syller 2012). Viral titer levels (Karyeija et al. 2000), symptoms (Wintermantel 2005), plant defenses (Mahuku et al. 1996) and volatile emissions (Salvaudon et al. 2013) can be altered by co-infections, suggesting that vector behavior (Srinivasan & Alvarez 2007) and transmission (Pinto et al. 2008) can also change. In this study, we investigated the effects of single and double infections with BYDV and G. zeae on the interactions between the aphid vector R. padi and wheat. We specifically address the following questions: (i) Do G. zeae-infected wheat volatiles attract R. padi? (ii) Does double infection alter R. padi olfactory preference for wheat? (iii) Does the R. padi olfactory preference for infected wheat differ among viruliferous aphids? (iv) Does feeding on singly or doubly infected wheat alter the performance of R. padi? Although direct and indirect effects of BYDV on R. padi behavior and biology have been well documented (Bosque-Pérez & Eigenbrode 2011; Ingwell et al. 2012), the current study provides insights into the ecological interactions among wheat, BYDV and the vector R. padi in more complex scenarios, such as co-infection with G. zeae. Furthermore, this is the first study to examine the effect of co-infection by a vector-borne virus and a non-insect vectored fungal pathogen on vector-plant interactions.
Materials and Methods Plants, insects and pathogens Wheat plants (Triticum aestivum L. cv Tbio Mestre) were cultivated in plastic tubes (300 mL capacity) filled with a commercial substrate composed of coconut fiber (Golden Mix, Piracicaba, SP, Brazil) and fertilized with Osmocote® (10N: 10P: 10K). Plants were cultivated in insect-free greenhouses with no temperature or light controls. Experiments were conducted between August
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and November 2013 in Piracicaba, SP, Brazil (the mean temperature and humidity during this period were 22 ± 8°C and 80± 10% r.h.). Colonies of R. padi were maintained on wheat plants in cages under laboratory conditions (22 ± 2°C, 60 ± 10% r.h. and 12 L:12 D photoperiod). Aphid colonies were reared on either healthy or BYDV-infected wheat (T. aestivum cv Tbio Mestre) to obtain non-viruliferous and viruliferous aphids, respectively. Plants were replaced each week or when aphid colonies became overcrowded. The isolate BYDV-PAV was provided by Embrapa Trigo (Passo Fundo, RS, Brazil) and originally obtained from black oat (Avena strigosa Schreb.) plantations in Passo Fundo, RS, Brazil. The virus was maintained in wheat plants and aviruliferous R. padi aphids were used to acquire and transmit BYDV to healthy plants as described in Parizoto et al. (2013). The inoculum of G. zeae was provided by the Laboratory of Phytopathology (Fundação de Pesquisas Agropecuárias da Cooperativa Agrária, FAPA, Guarapuava, PR, Brazil). Colonies of G. zeae were cultivated in potato dextrose agar (PDA) medium in growth chambers (25 ± 1°C and 12 L:12 D photoperiod) for one week to permit mycelial growth and fungal sporulation (Alfenas & Mafia 2007). G. zeae colonies were subsequently stored in the refrigerator until use. Just prior to sowing, wheat seeds were immersed for 5 min in a G. zeae mycelial suspension prepared from a fully colonized Petri dish and 10 mL of distilled and sterile water. Simultaneously, control (non-infected) wheat seeds were immersed in distilled water using the same procedure for infection with G. zeae in the absence of mycelia. To check if inoculation was successful, the leaf mid vein of inoculated plants was transversally cut and observed under stereoscope. Translucent sap indicated that the plant was infected, while greenish color indicated that the plant was healthy (Alfenas & Mafia 2007). We confirmed G. zeae infection by cutting the basis of plant stems and leaving in the humid chamber for 48h. We observed growth of white mycelia (Online Resource 1), from which we were able to isolate it in PDA medium. Wheat at code number one (principal growth stage established by Zadoks et al. 1974) was infected with BYDV using ten viruliferous R. padi aphids in clipcages for 72 h (Jiménez-Martinez & Bosque-Pérez 2004) when they were removed from plants. Fifteen days later, the wheat plants showing BYDV
characteristic symptoms (Online Resource 1) were used in experiments when they reached Zadocks code number 2. According to Jiménez-Martínez et al. (2004a) and Medina-Ortega et al. (2009), behavioral response of R. padi in the controls, non-viruliferous-aphid-induced wheat and undamaged wheat, is similar, and volatile emission of these controls also does not differ. Therefore, we used only undamaged and healthy wheat plants as controls for the BYDV inoculation. Dual Choice Assays Leaves containing non-viruliferous and viruliferous R. padi aphids were harvested 24 h prior to assays and enclosed in plastic pots. The aphids were crawling the next day, allowing them to be collected without harm. Dual choice assays were adapted from the method of Jiménez-Martínez et al. (2004a). The arena consisted of a Petri dish (15 cm diameter) with two rectangular holes in the bottom covered with voile fabric to prevent the aphids from inserting their stylets into the plant tissue. Without being excised, a pair of leaves from each tested plant were positioned below the Petri dish bottom and between the holes and a cardboard support (Online Resource 2). Assays were conducted in a dark room in the laboratory under controlled conditions (23 ± 2°C; 50 ± 10% r.h.). Twenty aphids were released in the center of the Petri dish, which was then closed, and the dish was observed under red light. The number of aphids on the voile fabric above the leaves was recorded at 10 and 60 min (short and long time points). We conducted at least 12 replicates for non-viruliferous and viruliferous wingless aphids in the following combinations: (i) healthy wheat vs. G. zeae-infected wheat, (ii) healthy wheat vs. BYDV-infected wheat; and (iii) healthy wheat vs. G. zeae + BYDV-infected wheat. Aphid Performance Assays Aphid performance was assessed on the basis of colony growth in healthy, G. zeae-infected, BYDV-infected and G. zeae + BYDV-infected wheat. Each colony was initiated with 20 non-viruliferous first-instar aphids, selected based on their size from R. padi laboratory rearing, and transferred to a wheat plant, which was covered by a voile fabric bag (20 cm × 30 cm) attached to the pot with an elastic band. Twelve replicates were established in a climate-controlled room (25º ± 1ºC,
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60% ± 10% r.h. and 12 L:12 D photoperiod). Total number of aphids, including alate, was counted 12 days later. Statistical analysis The numbers of aphids in the preference choice tests were analyzed using general log-linear models (GLM) and assuming a quasi-poisson distribution. The effect of treatment, time interval (10 and 60 min) and the interaction was analyzed by chi-square tests. Tests were conducted separately for viruliferous and nonviruliferous aphids. The Anderson-Darling normality test was employed to determine the normality of the data for aphid performance, as measured in terms of colony growth or number of wingless and winged aphids at day 12, which were analyzed using a GLM followed by Tukey’s post hoc test to assess differences among treatments (P < 0.05). Statistical tests were performed using the software package R (www.R-project. org) version 3.2.2 or Minitab® release 14.1 (Minitab Inc., State College, PA, USA).
Results
Fig. 1 Olfactory preference of non-viruliferous R. padi for healthy and infected wheat plants in dual choice assays. The bars indicate the mean percentage of aphids ± SE. On the right side of the graph, 10’ and 60’ are the times of the aphid counts. (a) Nonviruliferous aphids preferred healthy plant odors over G. zeaeinfected wheat. (b) Non-viruliferous aphids preferred BYDVinfected plant odors over healthy wheat. (c) Non-viruliferous aphids preferred G. zeae + BYDV-infected plant odors over healthy wheat
Dual Choice Bioassays
Aphid Performance
About 35% more non-viruliferous wingless aphids oriented to the odors of healthy wheat over G. zeae-infected wheat (Figure 1 (a), chi-square test, treatment effect P < 0.05, for more statistical details see Online Resource 3). However, 47% more non-viruliferous R. padi preferred BYDV-infected wheat over healthy plants at 10 min (Figure 1 (b) and Online Resource 3, chisquare test, treatment effect P < 0.05). When aphids were exposed to odors of healthy and doubly infected wheat (G. zeae + BYDV), 30% more aphids preferred the odors of doubly infected wheat (Figure 1 (c) and Online Resource 3, chi-square test, treatment effect P < 0.05). By contrast, viruliferous R. padi aphids did not differentiate between the odors of healthy plants and G. zeae-infected (Figure 2 (a) and Online Resource 3, chi-square test, treatment effect P > 0.05), BYDVinfected (Figure 2 (b) and Online Resource 3, chisquare test, treatment effect P > 0.05) or G. zeae + BYDV-infected wheat (Figure 2 (c) and Online Resource 3, chi-square test, treatment effect P > 0.05).
The performance of wingless aphids differed when feeding on infected and healthy plants (Figure 3, GLM F3,44 = 13.91, P < 0.001). Aphid colony growth increased in BYDV-infected in 25% compared to healthy wheat (Tukey’s test, P = 0.035); however, no difference in aphid colony growth was observed between healthy and G. zeae-infected wheat (Tukey’s test, P = 0.130). Aphids exhibited superior performance in doubly infected plants (G. zeae + BYDV) compared with singly infected and healthy wheat (Tukey’s test, P < 0.01 for all pairwise comparisons). Mean aphid population growth increased in doubly infected by 42% compared to healthy wheat and 23% compared to BYDV-infected wheat. However, equal numbers of winged aphids were produced on healthy and infected plants (Healthy = 5.7 ± 0.6, BYDV-infected = 6.2 ± 0.9, G. zeae-infected = 6.5 ± 1.0, G. zeae + BYDV-infected = 6.7 ± 1.0; GLM F3,44 = 0.22, P = 0.880). Even when number of winged aphids were normalized by wingless ones, there was no significance among treatments (Wingless/Winged proportions: Healthy = 0.019 ± 0.001, BYDV-infected =
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Discussion
Fig. 2 Olfactory preference of viruliferous R. padi for healthy and infected wheat plants in dual choice assays. The bars indicate the mean percentage of aphids ± SE. On the right side of the graph, 10’ and 60’ are the times of the aphid counts. (a) Viruliferous aphids did not distinguish between the odors of healthy and G. zeae-infected wheat plants. (b) Viruliferous aphids did not distinguish between the odors of healthy and BYDV-infected plants. (c) Viruliferous aphids did not distinguish between the odors of healthy and G. zeae + BYDV-infected plants
0.017 ± 0.002, G. zeae-infected = 0.016 ± 0.002, G. zeae + BYDV-infected = 0.013 ± 0.002; GLM F3,44 = 1.55, P = 0.215).
Fig. 3 Performance of Rhopalosiphum padi on healthy and infected wheat plants (infected by G. zeae, BYDV or G. zeae + BYDV) measured on the basis of aphid colony growth. The bars indicate the mean number of aphids ± SE. Different letters indicate significant differences between treatments according to Tukey’s test (P < 0.05)
Although co-infections often occur in the field (Malpica et al. 2006), little information is available on the influence of co-infections on the behavior of insect vectors. Previous studies have focused on mixed infections by two pathogens that both have insect vectors and, to our knowledge, this is the first study to examine the response of an insect vector to a naturally occurring coinfection by a vectored and persistently transmitted virus, BYDV, and an airborne and non-insect transmissible pathogen, G. zeae. In the present study, viruliferous bird cherry-oat aphids did not exhibit a preference for infected or healthy wheat in any of the assays. By contrast, non-viruliferous aphids preferred healthy wheat odors when exposed to volatiles of a healthy wheat plant and a G. zeae-infected plant. However, non-viruliferous aphids preferred single infection by BYDV and doubly infected (G. zeae + BYDV) wheat over healthy plants, indicating that the BYDV-induced volatiles prevail over changes in the volatile profile promoted by G. zeae infection. Because the preference assays were conducted in the dark with no access to gustatory or tactile cues, aphid choice was solely a result of volatile plant emissions, although these assays do not allow us to differentiate attractive and arrestant effects. Even though we did not use sham-inoculated plants (i.e., wheat plants damaged by non-viruliferous aphids) as controls and infection was not confirmed by molecular tests, our results confirm previous studies demonstrating that nonviruliferous R. padi prefers BYDV-infected plants over healthy wheat volatiles, while viruliferous aphids do not distinguish the odors of healthy and infected wheat (Jiménez-Martínez et al. 2004a; Medina-Ortega et al. 2009). A more recent study indicated that viruliferous R. padi with access to visual, olfactory and gustatory cues prefer to settle on healthy plants (Ingwell et al. 2012), clearly favoring virus spread. Co-infection by BYDV and G. zeae has been observed in wheat crops (Smith 1962; Stoetzer, A., personal communication); however, the frequency of coinfection has not been determined. We initially hypothesized that G. zeae infection occurs first based on the ability of the fungus G. zeae to be seed-transmitted, while BYDV is only transmitted by aphid vectors. Because viruliferous R. padi did not exhibit a preference for G. zeae-infected plants, aphid behavior is likely not the main factor responsible for the occurrence of co-
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infection with G. zeae and BYDV in wheat crops. On the other hand, increased visits of aviruliferous aphids to co-infected plants can favor the spread of the head blight of wheat, together or not with BYDV, in the case aphids act as mechanical vectors of G. zeae. Therefore, the fungus would benefit from the co-occurrence with BYDV. In general, persistently transmitted plant viruses promote nutritional changes, increasing free amino acids and sugars in the phloem sap that are important nutrients for aphids (Mauck et al. 2012). BYDV-infected cereal plants are a superior host for R. padi, likely due to this increase in free amino acids in the phloem sap (Ajayi 1986; Araya & Foster 1987; Jiménez-Martínez et al. 2004b). The evaluation of aphid performance suggests that BYDV infection also improves the nutritional quality of a Brazilian cultivar (‘TBio Mestre’) for R. padi. Interestingly, infection of wheat by G. zeae did not induce any changes in the host quality for R. padi, while co-infection with G. zeae and BYDV had a synergistic effect, resulting in a nearly twofold increase in aphid colony growth compared to that on healthy plants. If BYDV titer is elevated or unaltered in co-infected wheat, virus spread would likely be enhanced as G. zeae does not negatively interfere in BYDV-induced plant traits that influence R. padi attraction and promotes greater R. padi colony growth. However, in the case BYDV titer is reduced, further studies can elucidate weather higher aphid population growth could compensate for low BYDV titer promoting virus spread. Alate production has been reported to increase in BYDVinfected plants (Gildow 1980), and alates are an important means of virus spread (Müller et al. 2001). We did not observe a difference in the number of R. padi alate forms on infected and healthy wheat. The number of alates was slightly lower in healthy plants than infected ones, and it is possible that a longer-term experiment might reveal differences in alate production. The results presented here indicate that the attractiveness and superior quality of BYDV-infected wheat to its vector R. padi are consistent. Even when BYDV shares the same host with the causal agent of head blight of wheat (G. zeae), aphid vector attraction is unaltered, and performance is synergistically enhanced. Further studies are required to determine whether co-infection with BYDV and G. zeae alters virus acquisition and transmission by R. padi. If BYDV is acquired and transmitted by R. padi at similar rates in singly and doubly infected wheat, co-infection may enhance virus dissemination by
permitting faster multiplication of aphids in co-infected hosts. The mechanism underlying the improved growth of aphids on co-infected hosts should be investigated, including characterizations of amino acid and sugar contents as well as plant defenses regulated by phytohormones such as jasmonic acid and salicylic acid. It would also be interesting to study the underlying mechanisms of the direct effect of BYDV on R. padi aphids; the different responses of viruliferous and nonviruliferous aphids suggest that viruliferous aphids lose the ability to discriminate between plant volatile blends. BYDV-induced plant traits influencing bird cherry-oat aphids are likely present in doubly infected wheat and they might explain some of the success of the virus in infecting wheat crops, which results in high yield losses. Acknowledgements We thank Alfred Stoetzer (Fundação Agrária de Pesquisa Agropecuária, Guarapuava, PR) for providing seeds and the G. zeae isolate. We also thank Dr. Paulo Roberto Valle da Silva Pereira and Dr. Douglas Lau (Embrapa Trigo, Passo Fundo, RS) for providing the BYDV-PAV isolate and aphids. Felipe Goulart gently provided the schematic diagram of the dual choice set-up. This work was supported by the National Institute of Science and Technology (INCT) Semiochemicals in Agriculture, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP). MFGVP and PAS are supported by FAPESP (Process 2012/12252-1 and 2013/11993-0).
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