Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii

Aphis gossypii Glover (Hemiptera: Aphididae) causes considerable damage to crop yields globally. Solanum nigrum (Solanales: Solanaceae), an annual malignant weed, serves as a crucial weed host for A. gossypii. However, the potential mechanisms by which A. gossypii adapts to different hosts during th...

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Main Authors: Peng Wang, Yu-Xi Jing, Ya-Jie Ma, Dan Wang, Yong-Pan Shan, Hongyan Hu, Changcai Wu, Xian-Peng Song, Xiangliang Ren, Yan Ma, Xiaoyan Ma
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Sustainable Food Systems
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Online Access:https://www.frontiersin.org/articles/10.3389/fsufs.2024.1523123/full
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author Peng Wang
Peng Wang
Yu-Xi Jing
Ya-Jie Ma
Ya-Jie Ma
Dan Wang
Yong-Pan Shan
Hongyan Hu
Changcai Wu
Xian-Peng Song
Xiangliang Ren
Xiangliang Ren
Xiangliang Ren
Yan Ma
Yan Ma
Yan Ma
Xiaoyan Ma
Xiaoyan Ma
Xiaoyan Ma
author_facet Peng Wang
Peng Wang
Yu-Xi Jing
Ya-Jie Ma
Ya-Jie Ma
Dan Wang
Yong-Pan Shan
Hongyan Hu
Changcai Wu
Xian-Peng Song
Xiangliang Ren
Xiangliang Ren
Xiangliang Ren
Yan Ma
Yan Ma
Yan Ma
Xiaoyan Ma
Xiaoyan Ma
Xiaoyan Ma
author_sort Peng Wang
collection DOAJ
description Aphis gossypii Glover (Hemiptera: Aphididae) causes considerable damage to crop yields globally. Solanum nigrum (Solanales: Solanaceae), an annual malignant weed, serves as a crucial weed host for A. gossypii. However, the potential mechanisms by which A. gossypii adapts to different hosts during the transition between crops, such as Gossypium hirsutum (Malvales: Malvaceae) and S. nigrum remain elusive. We calculated the life table parameters of A. gossypii after rearing on S. nigrum for ten generations. The fifth generation of A. gossypii (T5) exhibited the strongest adaptability to S. nigrum, demonstrating notably higher values of r (intrinsic rate of increase), λ (finite rate of increase), and fecundity compared to the first generation of A. gossypii (T1). Upon retransferring T1, T5, and the tenth generation of A. gossypii (T10) were retransferred to G. hirsutum (designated as T1-M, T5-M, and T10-M, respectively), the T5-M showed superior r, λ, and fecundity compared to both T1-M and T10-M. 16S rRNA sequencing and qPCR analyses indicated a significant decrease in the diversity of the symbiotic bacterial community in both T5 and T10. Notably, Buchnera and Arsenophonus were two dominant symbiotic bacteria related to metabolism and host adaptability in A. gossypii. The relative abundance of Buchnera in T5 and T10 significantly increased compared to M and T, while the relative abundance of Arsenophonus decreased markedly. KEGG (Kyoto Encyclopedia of Genes and Genomes) function prediction analysis suggested that the roles of symbiotic bacteria in A. gossypii are primarily linked to metabolic processes. Therefore, the adaptation of A. gossypii to S. nigrum enhances its population expansion on G. hirsutum, potentially involving the metabolic functions of Buchnera and Arsenophonus. These findings provide a theoretical foundation for the scientific management of A. gossypii and S. nigrum in the fields.
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spelling doaj-art-2f3d7f62f713401badaacc65579d03362025-01-17T06:50:33ZengFrontiers Media S.A.Frontiers in Sustainable Food Systems2571-581X2025-01-01810.3389/fsufs.2024.15231231523123Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypiiPeng Wang0Peng Wang1Yu-Xi Jing2Ya-Jie Ma3Ya-Jie Ma4Dan Wang5Yong-Pan Shan6Hongyan Hu7Changcai Wu8Xian-Peng Song9Xiangliang Ren10Xiangliang Ren11Xiangliang Ren12Yan Ma13Yan Ma14Yan Ma15Xiaoyan Ma16Xiaoyan Ma17Xiaoyan Ma18Research Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaState Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, ChinaState Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaWestern Agricultural Research Center, Chinese Academy of Agricultural Sciences, Changji, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaState Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, ChinaWestern Agricultural Research Center, Chinese Academy of Agricultural Sciences, Changji, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaState Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, ChinaWestern Agricultural Research Center, Chinese Academy of Agricultural Sciences, Changji, ChinaResearch Base of Zhengzhou University, State Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, ChinaState Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, ChinaWestern Agricultural Research Center, Chinese Academy of Agricultural Sciences, Changji, ChinaAphis gossypii Glover (Hemiptera: Aphididae) causes considerable damage to crop yields globally. Solanum nigrum (Solanales: Solanaceae), an annual malignant weed, serves as a crucial weed host for A. gossypii. However, the potential mechanisms by which A. gossypii adapts to different hosts during the transition between crops, such as Gossypium hirsutum (Malvales: Malvaceae) and S. nigrum remain elusive. We calculated the life table parameters of A. gossypii after rearing on S. nigrum for ten generations. The fifth generation of A. gossypii (T5) exhibited the strongest adaptability to S. nigrum, demonstrating notably higher values of r (intrinsic rate of increase), λ (finite rate of increase), and fecundity compared to the first generation of A. gossypii (T1). Upon retransferring T1, T5, and the tenth generation of A. gossypii (T10) were retransferred to G. hirsutum (designated as T1-M, T5-M, and T10-M, respectively), the T5-M showed superior r, λ, and fecundity compared to both T1-M and T10-M. 16S rRNA sequencing and qPCR analyses indicated a significant decrease in the diversity of the symbiotic bacterial community in both T5 and T10. Notably, Buchnera and Arsenophonus were two dominant symbiotic bacteria related to metabolism and host adaptability in A. gossypii. The relative abundance of Buchnera in T5 and T10 significantly increased compared to M and T, while the relative abundance of Arsenophonus decreased markedly. KEGG (Kyoto Encyclopedia of Genes and Genomes) function prediction analysis suggested that the roles of symbiotic bacteria in A. gossypii are primarily linked to metabolic processes. Therefore, the adaptation of A. gossypii to S. nigrum enhances its population expansion on G. hirsutum, potentially involving the metabolic functions of Buchnera and Arsenophonus. These findings provide a theoretical foundation for the scientific management of A. gossypii and S. nigrum in the fields.https://www.frontiersin.org/articles/10.3389/fsufs.2024.1523123/fullcotton aphid16S rRNAlife tablehost shiftsymbiotic bacterium
spellingShingle Peng Wang
Peng Wang
Yu-Xi Jing
Ya-Jie Ma
Ya-Jie Ma
Dan Wang
Yong-Pan Shan
Hongyan Hu
Changcai Wu
Xian-Peng Song
Xiangliang Ren
Xiangliang Ren
Xiangliang Ren
Yan Ma
Yan Ma
Yan Ma
Xiaoyan Ma
Xiaoyan Ma
Xiaoyan Ma
Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii
Frontiers in Sustainable Food Systems
cotton aphid
16S rRNA
life table
host shift
symbiotic bacterium
title Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii
title_full Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii
title_fullStr Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii
title_full_unstemmed Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii
title_short Multi-generational adaptation to Solanum nigrum increases reproduction and decreases microbial diversity of Aphis gossypii
title_sort multi generational adaptation to solanum nigrum increases reproduction and decreases microbial diversity of aphis gossypii
topic cotton aphid
16S rRNA
life table
host shift
symbiotic bacterium
url https://www.frontiersin.org/articles/10.3389/fsufs.2024.1523123/full
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