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Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta

Wolbachia is a genus of maternally inherited endosymbionts that can affect reproduction of their hosts and influence metabolic processes. The pollinator, Valisia javana, is common in the male syconium of the dioecious fig Ficus hirta. Based on a high-quality chromosome-level V. javana genome with Pa...

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Autores principales: Liu, Wanzhen, Xia, Xue, Hoffmann, Ary A., Ding, Yamei, Fang, Ji-Chao, Yu, Hui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10621080/
https://www.ncbi.nlm.nih.gov/pubmed/37914998
http://dx.doi.org/10.1186/s12864-023-09726-2
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author Liu, Wanzhen
Xia, Xue
Hoffmann, Ary A.
Ding, Yamei
Fang, Ji-Chao
Yu, Hui
author_facet Liu, Wanzhen
Xia, Xue
Hoffmann, Ary A.
Ding, Yamei
Fang, Ji-Chao
Yu, Hui
author_sort Liu, Wanzhen
collection PubMed
description Wolbachia is a genus of maternally inherited endosymbionts that can affect reproduction of their hosts and influence metabolic processes. The pollinator, Valisia javana, is common in the male syconium of the dioecious fig Ficus hirta. Based on a high-quality chromosome-level V. javana genome with PacBio long-read and Illumina short-read sequencing, we discovered a sizeable proportion of Wolbachia sequences and used these to assemble two novel Wolbachia strains belonging to supergroup A. We explored its phylogenetic relationship with described Wolbachia strains based on MLST sequences and the possibility of induction of CI (cytoplasmic incompatibility) in this strain by examining the presence of cif genes known to be responsible for CI in other insects. We also identified mobile genetic elements including prophages and insertion sequences, genes related to biotin synthesis and metabolism. A total of two prophages and 256 insertion sequences were found. The prophage WOjav1 is cryptic (structure incomplete) and WOjav2 is relatively intact. IS5 is the dominant transposon family. At least three pairs of type I cif genes with three copies were found which may cause strong CI although this needs experimental verification; we also considered possible nutritional effects of the Wolbachia by identifying genes related to biotin production, absorption and metabolism. This study provides a resource for further studies of Wolbachia-pollinator-host plant interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09726-2.
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spelling pubmed-106210802023-11-03 Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta Liu, Wanzhen Xia, Xue Hoffmann, Ary A. Ding, Yamei Fang, Ji-Chao Yu, Hui BMC Genomics Research Wolbachia is a genus of maternally inherited endosymbionts that can affect reproduction of their hosts and influence metabolic processes. The pollinator, Valisia javana, is common in the male syconium of the dioecious fig Ficus hirta. Based on a high-quality chromosome-level V. javana genome with PacBio long-read and Illumina short-read sequencing, we discovered a sizeable proportion of Wolbachia sequences and used these to assemble two novel Wolbachia strains belonging to supergroup A. We explored its phylogenetic relationship with described Wolbachia strains based on MLST sequences and the possibility of induction of CI (cytoplasmic incompatibility) in this strain by examining the presence of cif genes known to be responsible for CI in other insects. We also identified mobile genetic elements including prophages and insertion sequences, genes related to biotin synthesis and metabolism. A total of two prophages and 256 insertion sequences were found. The prophage WOjav1 is cryptic (structure incomplete) and WOjav2 is relatively intact. IS5 is the dominant transposon family. At least three pairs of type I cif genes with three copies were found which may cause strong CI although this needs experimental verification; we also considered possible nutritional effects of the Wolbachia by identifying genes related to biotin production, absorption and metabolism. This study provides a resource for further studies of Wolbachia-pollinator-host plant interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09726-2. BioMed Central 2023-11-01 /pmc/articles/PMC10621080/ /pubmed/37914998 http://dx.doi.org/10.1186/s12864-023-09726-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Wanzhen
Xia, Xue
Hoffmann, Ary A.
Ding, Yamei
Fang, Ji-Chao
Yu, Hui
Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta
title Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta
title_full Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta
title_fullStr Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta
title_full_unstemmed Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta
title_short Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta
title_sort evolution of wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious ficus hirta
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10621080/
https://www.ncbi.nlm.nih.gov/pubmed/37914998
http://dx.doi.org/10.1186/s12864-023-09726-2
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