Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes
Plant breeding is used to develop crops with host resistance to aphids, however, virulent biotypes often develop that overcome host resistance genes. We tested whether the symbionts, Arsenophonus (A) and Wolbachia (W), affect virulence and fecundity in soybean aphid biotypes Bt1 and Bt3 cultured on...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1209595/full |
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| author | Rosanna Giordano Rosanna Giordano Everett P. Weber Ryan Mitacek Alejandra Flores Alonso Ledesma Arun K. De Theresa K. Herman Felipe N. Soto-Adames Minh Q. Nguyen Curtis B. Hill Glen L. Hartman |
| author_facet | Rosanna Giordano Rosanna Giordano Everett P. Weber Ryan Mitacek Alejandra Flores Alonso Ledesma Arun K. De Theresa K. Herman Felipe N. Soto-Adames Minh Q. Nguyen Curtis B. Hill Glen L. Hartman |
| author_sort | Rosanna Giordano |
| collection | DOAJ |
| description | Plant breeding is used to develop crops with host resistance to aphids, however, virulent biotypes often develop that overcome host resistance genes. We tested whether the symbionts, Arsenophonus (A) and Wolbachia (W), affect virulence and fecundity in soybean aphid biotypes Bt1 and Bt3 cultured on whole plants and detached leaves of three resistant, Rag1, Rag2 and Rag1 + 2, and one susceptible, W82, soybean genotypes. Whole plants and individual aphid experiments of A. glycines with and without Arsenophonus and Wolbachia did not show differences in overall fecundity. Differences were observed in peak fecundity, first day of deposition, and day of maximum nymph deposition of individual aphids on detached leaves. Bt3 had higher fecundity than Bt1 on detached leaves of all plant genotypes regardless of bacterial profile. Symbionts did not affect peak fecundity of Bt1 but increased it in Bt3 (A+W+) and all Bt3 strains began to deposit nymphs earlier than the Bt1 (A+W−). Arsenophonus in Bt1 delayed the first day of nymph deposition in comparison to aposymbiotic Bt1 except when reared on Rag1 + 2. For the Bt1 and Bt3 strains, symbionts did not result in a significant difference in the day they deposited the maximum number of nymphs nor was there a difference in survival or variability in number of nymphs deposited. Variability of number of aphids deposited was higher in aphids feeding on resistant plant genotypes. The impact of Arsenophonus on soybean aphid patterns of fecundity was dependent on the aphid biotype and plant genotype. Wolbachia alone had no detectable impact but may have contributed to the increased fecundity of Bt3 (A+W+). An individual based model, using data from the detached leaves experiment and with intraspecific competition removed, found patterns similar to those observed in the greenhouse and growth chamber experiments including a significant interaction between soybean genotype and aphid strain. Combining individual data with the individual based model of population growth isolated the impact of fecundity and host resistance from intraspecific competition and host health. Changes to patterns of fecundity, influenced by the composition and concentration of symbionts, may contribute to competitive interactions among aphid genotypes and influence selection on virulent aphid populations. |
| first_indexed | 2024-03-08T17:36:01Z |
| format | Article |
| id | doaj.art-9119b9eea1c146008f82ddb363c2033c |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-08T17:36:01Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-9119b9eea1c146008f82ddb363c2033c2024-01-02T12:19:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-08-011410.3389/fmicb.2023.12095951209595Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypesRosanna Giordano0Rosanna Giordano1Everett P. Weber2Ryan Mitacek3Alejandra Flores4Alonso Ledesma5Arun K. De6Theresa K. Herman7Felipe N. Soto-Adames8Minh Q. Nguyen9Curtis B. Hill10Glen L. Hartman11Institute of Environment, Florida International University, Miami, FL, United StatesPuerto Rico Science Technology and Research Trust, San Juan, Puerto RicoOffice of Institutional Research, Dartmouth College, Hanover, NH, United StatesDepartment of Crop Sciences, University of Illinois Urbana-Champaign, Urbana, IL, United StatesDepartment of Physiology and Biophysics, School of Medicine, Case Western Reserve University, Cleveland, OH, United StatesCollege of Agricultural, Consumer and Environmental Sciences, University of Illinois Urbana-Champaign, Urbana, IL, United StatesAnimal Sciences Division, ICAR-Central Island Agricultural Research Institute, Port Blair, IndiaUSDA-Agricultural Research Service, Urbana, IL, United StatesDivision of Plant Industry, Florida Department of Agriculture and Consumer Services, Gainesville, FL, United States0Neochromosome, Inc., Long Island City, NY, United States0Neochromosome, Inc., Long Island City, NY, United StatesDepartment of Crop Sciences, University of Illinois Urbana-Champaign, Urbana, IL, United StatesPlant breeding is used to develop crops with host resistance to aphids, however, virulent biotypes often develop that overcome host resistance genes. We tested whether the symbionts, Arsenophonus (A) and Wolbachia (W), affect virulence and fecundity in soybean aphid biotypes Bt1 and Bt3 cultured on whole plants and detached leaves of three resistant, Rag1, Rag2 and Rag1 + 2, and one susceptible, W82, soybean genotypes. Whole plants and individual aphid experiments of A. glycines with and without Arsenophonus and Wolbachia did not show differences in overall fecundity. Differences were observed in peak fecundity, first day of deposition, and day of maximum nymph deposition of individual aphids on detached leaves. Bt3 had higher fecundity than Bt1 on detached leaves of all plant genotypes regardless of bacterial profile. Symbionts did not affect peak fecundity of Bt1 but increased it in Bt3 (A+W+) and all Bt3 strains began to deposit nymphs earlier than the Bt1 (A+W−). Arsenophonus in Bt1 delayed the first day of nymph deposition in comparison to aposymbiotic Bt1 except when reared on Rag1 + 2. For the Bt1 and Bt3 strains, symbionts did not result in a significant difference in the day they deposited the maximum number of nymphs nor was there a difference in survival or variability in number of nymphs deposited. Variability of number of aphids deposited was higher in aphids feeding on resistant plant genotypes. The impact of Arsenophonus on soybean aphid patterns of fecundity was dependent on the aphid biotype and plant genotype. Wolbachia alone had no detectable impact but may have contributed to the increased fecundity of Bt3 (A+W+). An individual based model, using data from the detached leaves experiment and with intraspecific competition removed, found patterns similar to those observed in the greenhouse and growth chamber experiments including a significant interaction between soybean genotype and aphid strain. Combining individual data with the individual based model of population growth isolated the impact of fecundity and host resistance from intraspecific competition and host health. Changes to patterns of fecundity, influenced by the composition and concentration of symbionts, may contribute to competitive interactions among aphid genotypes and influence selection on virulent aphid populations.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1209595/fullsoybean aphidreproductionresistant soybean varietiessymbiontsWolbachiaArsenophonus |
| spellingShingle | Rosanna Giordano Rosanna Giordano Everett P. Weber Ryan Mitacek Alejandra Flores Alonso Ledesma Arun K. De Theresa K. Herman Felipe N. Soto-Adames Minh Q. Nguyen Curtis B. Hill Glen L. Hartman Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes Frontiers in Microbiology soybean aphid reproduction resistant soybean varieties symbionts Wolbachia Arsenophonus |
| title | Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes |
| title_full | Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes |
| title_fullStr | Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes |
| title_full_unstemmed | Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes |
| title_short | Patterns of asexual reproduction of the soybean aphid, Aphis glycines (Matsumura), with and without the secondary symbionts Wolbachia and Arsenophonus, on susceptible and resistant soybean genotypes |
| title_sort | patterns of asexual reproduction of the soybean aphid aphis glycines matsumura with and without the secondary symbionts wolbachia and arsenophonus on susceptible and resistant soybean genotypes |
| topic | soybean aphid reproduction resistant soybean varieties symbionts Wolbachia Arsenophonus |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1209595/full |
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