Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host
Tomato spotted wilt orthotospovirus (TSWV) is one of the most successful pandemic agricultural pathogens transmitted by several species of thrips in a persistent propagative manner. Current management strategies for TSWV heavily rely on growing single-gene resistant cultivars of tomato (“Sw-5b” gene...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1257724/full |
| _version_ | 1797670015861784576 |
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| author | Senthilraja Chinnaiah Senthilraja Chinnaiah Saurabh Gautam Saurabh Gautam Benjamin Herron Benjamin Herron Fekede Workneh Fekede Workneh Charles M. Rush Charles M. Rush Kiran R. Gadhave Kiran R. Gadhave |
| author_facet | Senthilraja Chinnaiah Senthilraja Chinnaiah Saurabh Gautam Saurabh Gautam Benjamin Herron Benjamin Herron Fekede Workneh Fekede Workneh Charles M. Rush Charles M. Rush Kiran R. Gadhave Kiran R. Gadhave |
| author_sort | Senthilraja Chinnaiah |
| collection | DOAJ |
| description | Tomato spotted wilt orthotospovirus (TSWV) is one of the most successful pandemic agricultural pathogens transmitted by several species of thrips in a persistent propagative manner. Current management strategies for TSWV heavily rely on growing single-gene resistant cultivars of tomato (“Sw-5b” gene) and pepper (“Tsw” gene) deployed worldwide. However, the emergence of resistance-breaking strains (RB) in recent years has compounded the threat of TSWV to agricultural production worldwide. Despite this, an extensive study on the thrips transmission biology of RB strains is currently lacking. It is also unclear whether mutualistic TSWV-thrips interactions vary across different novel strains with disparate geographical origins. To address both critical questions, we studied whether and how four novel RB strains of TSWV (two sympatric and two allopatric), along with a non-RB strain, impact western flower thrips (WFT) fitness and whether this leads to differences in TSWV incidence, symptom severity (virulence), and virus accumulation in two differentially resistant tomato cultivars. Our findings show that all RB strains increased WFT fitness by prolonging the adult period and increasing fecundity compared to non-RB and non-viruliferous controls, regardless of the geographical origin of strains or the TSWV titers in individual thrips, which were substantially low in allopatric strains. TSWV accumulation in thrips varied at different developmental stages and was unrelated to the infected tissues from which thrips acquired the virus. However, it was significantly positively correlated to that in WFT-inoculated susceptible plants, but not the resistant ones. The TSW incidences were high in tomato plants infected with all RB strains, ranging from 80% to 90% and 100% in resistant and susceptible plants, respectively. However, TSW incidence in the non-RB-infected susceptible tomato plants was 80%. Our findings provide new insights into how novel strains of TSWV, by selectively offering substantial fitness benefits to vectors, modulate transmission and gain a potential epidemiological advantage over non-RB strains. This study presents the first direct evidence of how vector-imposed selection pressure, besides the one imposed by resistant cultivars, may contribute to the worldwide emergence of RB strains. |
| first_indexed | 2024-03-11T20:53:24Z |
| format | Article |
| id | doaj.art-24bb6c67f4c34e7586da57cca9a08ceb |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-11T20:53:24Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-24bb6c67f4c34e7586da57cca9a08ceb2023-09-30T21:48:49ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12577241257724Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant hostSenthilraja Chinnaiah0Senthilraja Chinnaiah1Saurabh Gautam2Saurabh Gautam3Benjamin Herron4Benjamin Herron5Fekede Workneh6Fekede Workneh7Charles M. Rush8Charles M. Rush9Kiran R. Gadhave10Kiran R. Gadhave11Texas A&M AgriLife Research, Amarillo, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesTexas A&M AgriLife Research, Amarillo, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesTexas A&M AgriLife Research, Amarillo, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesTexas A&M AgriLife Research, Amarillo, TX, United StatesDepartment of Plant Pathology, Texas A&M University, College Station, TX, United StatesTexas A&M AgriLife Research, Amarillo, TX, United StatesDepartment of Plant Pathology, Texas A&M University, College Station, TX, United StatesTexas A&M AgriLife Research, Amarillo, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesTomato spotted wilt orthotospovirus (TSWV) is one of the most successful pandemic agricultural pathogens transmitted by several species of thrips in a persistent propagative manner. Current management strategies for TSWV heavily rely on growing single-gene resistant cultivars of tomato (“Sw-5b” gene) and pepper (“Tsw” gene) deployed worldwide. However, the emergence of resistance-breaking strains (RB) in recent years has compounded the threat of TSWV to agricultural production worldwide. Despite this, an extensive study on the thrips transmission biology of RB strains is currently lacking. It is also unclear whether mutualistic TSWV-thrips interactions vary across different novel strains with disparate geographical origins. To address both critical questions, we studied whether and how four novel RB strains of TSWV (two sympatric and two allopatric), along with a non-RB strain, impact western flower thrips (WFT) fitness and whether this leads to differences in TSWV incidence, symptom severity (virulence), and virus accumulation in two differentially resistant tomato cultivars. Our findings show that all RB strains increased WFT fitness by prolonging the adult period and increasing fecundity compared to non-RB and non-viruliferous controls, regardless of the geographical origin of strains or the TSWV titers in individual thrips, which were substantially low in allopatric strains. TSWV accumulation in thrips varied at different developmental stages and was unrelated to the infected tissues from which thrips acquired the virus. However, it was significantly positively correlated to that in WFT-inoculated susceptible plants, but not the resistant ones. The TSW incidences were high in tomato plants infected with all RB strains, ranging from 80% to 90% and 100% in resistant and susceptible plants, respectively. However, TSW incidence in the non-RB-infected susceptible tomato plants was 80%. Our findings provide new insights into how novel strains of TSWV, by selectively offering substantial fitness benefits to vectors, modulate transmission and gain a potential epidemiological advantage over non-RB strains. This study presents the first direct evidence of how vector-imposed selection pressure, besides the one imposed by resistant cultivars, may contribute to the worldwide emergence of RB strains.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1257724/fullresistance-breaking strainswestern flower thripsOrthotospovirus tomatomaculaeinsect vector biologyvector-virus interactions |
| spellingShingle | Senthilraja Chinnaiah Senthilraja Chinnaiah Saurabh Gautam Saurabh Gautam Benjamin Herron Benjamin Herron Fekede Workneh Fekede Workneh Charles M. Rush Charles M. Rush Kiran R. Gadhave Kiran R. Gadhave Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host Frontiers in Microbiology resistance-breaking strains western flower thrips Orthotospovirus tomatomaculae insect vector biology vector-virus interactions |
| title | Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host |
| title_full | Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host |
| title_fullStr | Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host |
| title_full_unstemmed | Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host |
| title_short | Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host |
| title_sort | novel strains of a pandemic plant virus tomato spotted wilt orthotospovirus increase vector fitness and modulate virus transmission in a resistant host |
| topic | resistance-breaking strains western flower thrips Orthotospovirus tomatomaculae insect vector biology vector-virus interactions |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1257724/full |
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