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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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Autores principales: Giordano, Rosanna, Weber, Everett P., Mitacek, Ryan, Flores, Alejandra, Ledesma, Alonso, De, Arun K., Herman, Theresa K., Soto-Adames, Felipe N., Nguyen, Minh Q., Hill, Curtis B., Hartman, Glen L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10501154/
https://www.ncbi.nlm.nih.gov/pubmed/37720159
http://dx.doi.org/10.3389/fmicb.2023.1209595
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author Giordano, Rosanna
Weber, Everett P.
Mitacek, Ryan
Flores, Alejandra
Ledesma, Alonso
De, Arun K.
Herman, Theresa K.
Soto-Adames, Felipe N.
Nguyen, Minh Q.
Hill, Curtis B.
Hartman, Glen L.
author_facet Giordano, Rosanna
Weber, Everett P.
Mitacek, Ryan
Flores, Alejandra
Ledesma, Alonso
De, Arun K.
Herman, Theresa K.
Soto-Adames, Felipe N.
Nguyen, Minh Q.
Hill, Curtis B.
Hartman, Glen L.
author_sort Giordano, Rosanna
collection PubMed
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.
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spelling pubmed-105011542023-09-15 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 Giordano, Rosanna Weber, Everett P. Mitacek, Ryan Flores, Alejandra Ledesma, Alonso De, Arun K. Herman, Theresa K. Soto-Adames, Felipe N. Nguyen, Minh Q. Hill, Curtis B. Hartman, Glen L. Front Microbiol Microbiology 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. Frontiers Media S.A. 2023-08-31 /pmc/articles/PMC10501154/ /pubmed/37720159 http://dx.doi.org/10.3389/fmicb.2023.1209595 Text en Copyright © 2023 Giordano, Weber, Mitacek, Flores, Ledesma, De, Herman, Soto-Adames, Nguyen, Hill and Hartman. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Giordano, Rosanna
Weber, Everett P.
Mitacek, Ryan
Flores, Alejandra
Ledesma, Alonso
De, Arun K.
Herman, Theresa K.
Soto-Adames, Felipe N.
Nguyen, Minh Q.
Hill, Curtis B.
Hartman, Glen L.
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 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 Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10501154/
https://www.ncbi.nlm.nih.gov/pubmed/37720159
http://dx.doi.org/10.3389/fmicb.2023.1209595
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