Effects of thrips feeding on tospovirus transmission in chrysanthemum
The introduction and rapid spread of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in Western Europe since the 1980s led to a considerable increase of losses in different, mainly ornamental crops due to tomato spotted wilt tospovirus (TSWV) infections. Besides the losses inflicted by TSWV, F. occidentalis itself is also an important pest on many of these crops. Chrysanthemum is one of those crops which is affected by both TSWV and its vector. Breeding and selection of this plant species has resulted in the identification of a few chrysanthemum cultivars with some partial resistance to thrips. However, resistant cultivars to TSWV have not been successfully developed yet, meaning that the control of TSWV has to rely on other strategies. Besides sanitation programs, other successful strategies to control TSWV or F. occidentalis are currently not available.To develop durable and effective control measures and integrated pest management strategies, more detailed knowledge of the precise interactions between the virus, its vector and the threatened crop is required. Since transmission of TSWV is associated with ingestion of food, the feeding behaviour of thrips is one of the most determining factors in virus transmission. This study was therefore aimed to analyse the interactions between virus, vector and (chrysanthemum) plant in relation to thrips feeding.Tospovirus is acquired by larvae and transmitted by old second instar larvae and adults after their emergence. As a first feature, the ability of larvae to acquire TSWV was analysed in relation to their age. The results obtained in a study with several F. occidentalis populations showed that the ability to acquire virus (defined as ingestion of virus by larvae, subsequently developing in viruliferous adults), dropped with the age of larvae. A notable result was obtained with one of the populations (NL3), which could only acquire TSWV when larvae were in their first larval (L1) stage.Besides the age of the larvae at which they acquire virus, other parameters such as the F. occidentalis population involved, the feeding behaviour by the amount of food ingested, the virus species acquired and the host plant involved were studied for their effect on virus acquisition and transmission. Large and significant differences were found in TSWV transmission competencies between fourteen F. occidentalis populations which originated from different countries all over the world. These differences were not affected by the amount of virus ingested or the host used as virus source. However, the use of another tospovirus species, impatiens necrotic spot virus (INSV), influenced the transmission differences between populations. The transmission efficiencies found appeared to be rather constant, supporting the view that the competence of a population to transmit TSWV is a stable, and, therefore, inherited property.The efficiency at which the F. occidentalis populations transmitted INSV was higher than that of TSWV. This observation confirms earlier reports that the different tospovirus species are transmitted at distinct rates by the same thrips population. It is likely that various isolates of TSWV will also be transmitted at different rates by one and the same F. occidentalis population as has been shown for some Thrips tabaci populations. In contrast to TSWV, INSV is acquired by L1s as well as second larval instars (L2s) of the NL3 population.Further studies revealed that males of F. occidentalis are more efficient TSWV transmitters than females. This feature was found for all fourteen F. occidentalis populations tested. The differences in virus transmission competencies between both sexes can be explained by differences in their feeding behaviour. Males produce less silvery scars and make more frequent inoculation punctures than females. These punctures may represent the event during which the virus is successfully transmitted, as cells remain viable allowing virus to be replicated after virus-containing saliva injection. In addition, cells which are pierced and drained in the feeding process (resulting in silvery scars) are probably so destroyed that they will not support virus replication.The different efficiencies by which males and females transmit virus may have an impact on the spread of the virus in a crop. Males may infect more plants than females as they show a higher mobility and the sex ratios in flights are male-biased. However, the contribution of males to the spread may be compensated or outweighed by the greater life expectation of females. Quantification of the development of an epidemic in terms of which part is caused by males and which by females, will be extremely difficult as the ratio between males and females will change continuously and their age can not accurately be determined.To analyse whether thrips resistant chrysanthemum cultivars could effectively be used to control TSWV spread in this crop, fifteen cultivars were assessed for their susceptibility for this virus. All cultivars were susceptible, irrespective their degree of thrips resistance. However, the number of plants that attracted an infection varied for each cultivar. lt appeared in this study that the infection proceeds poorly in the infected plants and that the virus became unevenly distributed over the plant. A consequence of these observations is that in the chrysanthemum crop the virus will disperse slowly from primary infected plants. No L1s emerging on such plants, or only a small proportion of them, will acquire virus. With the development of the infection in the plant and development of the thrips population, more larvae will be able to acquire virus and thus become transmitters. This means that the early developing population of thrips found on primary infected plants by incoming (dispersing) adults will hardly contribute to the (intercrop) spread of the virus an that, with time, the infection pressure may increase from these primary infected plants. Studies on assessing the development of viruliferous thrips in a population on a primary infected chrysanthemum plant should enhance our understanding of TSWV spread in chrysanthemum.In most cases, tospovirus infections have been attributed to virus introduction from sources located outside the crop, and less to secondary (intercrop) spread in the crop as reported for groundnut, tomato and pepper. The incidence of TSWV infections in the Dutch chrysanthemum crops is low, despite the fact that TSWV transmission to chrysanthemum occurs highly efficiently. Since the virus is not seed transmitted, the first infections may arise as a result from primary infections, subsequently followed by some secondary spread.Using plants in testing the susceptibility of chrysanthemum for TSWV and vector resistance is a time- and labour-consuming activity. An expeditious leaf disk assay was introduced to assess this susceptibility. This assay was also used to quantify TSWV transmission to a partially vector-resistant and a susceptible cultivar. It was shown that the inoculation access period in which 50% of the disks became infected (IAP 50 ) was shorter for a partially vector-resistant cultivar than for a susceptible cultivar, indicating that TSWV is more efficiently transmitted to the more vector resistant cultivar. This may be the result of a different feeding behaviour on the less preferred, partially resistant cultivar, resulting in a higher frequency of inoculation punctures in a unit of time, and subsequently in greater probability of successful transmission.The spread of TSWV will certainly be affected by the attractiveness of the plant as food source of the thrips. The lower development rate of viruliferous thrips and the shorter life expectancy on partially vector-resistant cultivars likely reduces secondary spread. On the contrary, the mobility and dispersal of thrips and subsequent TSWV transmission in enhanced on partially resistant vector plants, and hence, the use of vector-resistant cultivars may not under all circumstances lead to an effective control of TSWV spread.
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| Format: | Doctoral thesis biblioteca |
| Language: | English |
| Subjects: | chrysanthemum, disease transmission, disease vectors, feeding, plant diseases, plant viruses, thrips, plantenvirussen, plantenziekten, vectoren, ziekten, voedering, ziekteoverdracht, |
| Online Access: | https://research.wur.nl/en/publications/effects-of-thrips-feeding-on-tospovirus-transmission-in-chrysanth |
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| Summary: | The introduction and rapid spread of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in Western Europe since the 1980s led to a considerable increase of losses in different, mainly ornamental crops due to tomato spotted wilt tospovirus (TSWV) infections. Besides the losses inflicted by TSWV, F. occidentalis itself is also an important pest on many of these crops. Chrysanthemum is one of those crops which is affected by both TSWV and its vector. Breeding and selection of this plant species has resulted in the identification of a few chrysanthemum cultivars with some partial resistance to thrips. However, resistant cultivars to TSWV have not been successfully developed yet, meaning that the control of TSWV has to rely on other strategies. Besides sanitation programs, other successful strategies to control TSWV or F. occidentalis are currently not available.To develop durable and effective control measures and integrated pest management strategies, more detailed knowledge of the precise interactions between the virus, its vector and the threatened crop is required. Since transmission of TSWV is associated with ingestion of food, the feeding behaviour of thrips is one of the most determining factors in virus transmission. This study was therefore aimed to analyse the interactions between virus, vector and (chrysanthemum) plant in relation to thrips feeding.Tospovirus is acquired by larvae and transmitted by old second instar larvae and adults after their emergence. As a first feature, the ability of larvae to acquire TSWV was analysed in relation to their age. The results obtained in a study with several F. occidentalis populations showed that the ability to acquire virus (defined as ingestion of virus by larvae, subsequently developing in viruliferous adults), dropped with the age of larvae. A notable result was obtained with one of the populations (NL3), which could only acquire TSWV when larvae were in their first larval (L1) stage.Besides the age of the larvae at which they acquire virus, other parameters such as the F. occidentalis population involved, the feeding behaviour by the amount of food ingested, the virus species acquired and the host plant involved were studied for their effect on virus acquisition and transmission. Large and significant differences were found in TSWV transmission competencies between fourteen F. occidentalis populations which originated from different countries all over the world. These differences were not affected by the amount of virus ingested or the host used as virus source. However, the use of another tospovirus species, impatiens necrotic spot virus (INSV), influenced the transmission differences between populations. The transmission efficiencies found appeared to be rather constant, supporting the view that the competence of a population to transmit TSWV is a stable, and, therefore, inherited property.The efficiency at which the F. occidentalis populations transmitted INSV was higher than that of TSWV. This observation confirms earlier reports that the different tospovirus species are transmitted at distinct rates by the same thrips population. It is likely that various isolates of TSWV will also be transmitted at different rates by one and the same F. occidentalis population as has been shown for some Thrips tabaci populations. In contrast to TSWV, INSV is acquired by L1s as well as second larval instars (L2s) of the NL3 population.Further studies revealed that males of F. occidentalis are more efficient TSWV transmitters than females. This feature was found for all fourteen F. occidentalis populations tested. The differences in virus transmission competencies between both sexes can be explained by differences in their feeding behaviour. Males produce less silvery scars and make more frequent inoculation punctures than females. These punctures may represent the event during which the virus is successfully transmitted, as cells remain viable allowing virus to be replicated after virus-containing saliva injection. In addition, cells which are pierced and drained in the feeding process (resulting in silvery scars) are probably so destroyed that they will not support virus replication.The different efficiencies by which males and females transmit virus may have an impact on the spread of the virus in a crop. Males may infect more plants than females as they show a higher mobility and the sex ratios in flights are male-biased. However, the contribution of males to the spread may be compensated or outweighed by the greater life expectation of females. Quantification of the development of an epidemic in terms of which part is caused by males and which by females, will be extremely difficult as the ratio between males and females will change continuously and their age can not accurately be determined.To analyse whether thrips resistant chrysanthemum cultivars could effectively be used to control TSWV spread in this crop, fifteen cultivars were assessed for their susceptibility for this virus. All cultivars were susceptible, irrespective their degree of thrips resistance. However, the number of plants that attracted an infection varied for each cultivar. lt appeared in this study that the infection proceeds poorly in the infected plants and that the virus became unevenly distributed over the plant. A consequence of these observations is that in the chrysanthemum crop the virus will disperse slowly from primary infected plants. No L1s emerging on such plants, or only a small proportion of them, will acquire virus. With the development of the infection in the plant and development of the thrips population, more larvae will be able to acquire virus and thus become transmitters. This means that the early developing population of thrips found on primary infected plants by incoming (dispersing) adults will hardly contribute to the (intercrop) spread of the virus an that, with time, the infection pressure may increase from these primary infected plants. Studies on assessing the development of viruliferous thrips in a population on a primary infected chrysanthemum plant should enhance our understanding of TSWV spread in chrysanthemum.In most cases, tospovirus infections have been attributed to virus introduction from sources located outside the crop, and less to secondary (intercrop) spread in the crop as reported for groundnut, tomato and pepper. The incidence of TSWV infections in the Dutch chrysanthemum crops is low, despite the fact that TSWV transmission to chrysanthemum occurs highly efficiently. Since the virus is not seed transmitted, the first infections may arise as a result from primary infections, subsequently followed by some secondary spread.Using plants in testing the susceptibility of chrysanthemum for TSWV and vector resistance is a time- and labour-consuming activity. An expeditious leaf disk assay was introduced to assess this susceptibility. This assay was also used to quantify TSWV transmission to a partially vector-resistant and a susceptible cultivar. It was shown that the inoculation access period in which 50% of the disks became infected (IAP 50 ) was shorter for a partially vector-resistant cultivar than for a susceptible cultivar, indicating that TSWV is more efficiently transmitted to the more vector resistant cultivar. This may be the result of a different feeding behaviour on the less preferred, partially resistant cultivar, resulting in a higher frequency of inoculation punctures in a unit of time, and subsequently in greater probability of successful transmission.The spread of TSWV will certainly be affected by the attractiveness of the plant as food source of the thrips. The lower development rate of viruliferous thrips and the shorter life expectancy on partially vector-resistant cultivars likely reduces secondary spread. On the contrary, the mobility and dispersal of thrips and subsequent TSWV transmission in enhanced on partially resistant vector plants, and hence, the use of vector-resistant cultivars may not under all circumstances lead to an effective control of TSWV spread. |
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