Wolbachia enhances ovarian development in the rice planthopper Laodelphax striatellus through elevated energy production
AbstractThe endosymbiont Wolbachia can both benefit host nutrition and manipulate host reproduction to its own advantage. However, the mechanisms of its nutritional benefits remain unclear. We show that Wolbachia enhances ovarian development in the small brown planthopper Laodelphax striatellus by boosting energy production. Wolbachia-infected females have increased fecundity, accelerated ovarian development, and prolonged oviposition. Enhanced activity of mitochondrial complex I is linked to increased ATP production and the expression of energy metabolism-related genes. We further identify that Wolbachia-synthesized riboflavin is crucial for ATP production and ovarian development. A riboflavin transporter, slc52a3a, positively correlates with Wolbachia density and is required for normal ovarian maturation. Our findings demonstrate that Wolbachia-produced riboflavin drives energy production and accelerates ovarian maturation, thus improving host fecundity. This research reveals insights into symbiont-host metabolic interactions and underscores the role of nutrient delivery in symbiosis.
Data availability
The RNA-seq data generated in this study have been deposited in the NCBI GenBank database under accession code PRJNA1195149, PRJNA1195150, and PRJNA1195152. Source data are provided with this paper.
ReferencesPodsiadło, E., Michalik, K., Michalik, A. & Szklarzewicz, T. Yeast-like microorganisms in the scale insect Kermes quercus (Insecta, Hemiptera, Coccomorpha: Kermesidae). Newly acquired symbionts?. Arthropod Struct. Dev. 47, 56–63 (2018).
Google Scholar
Mathé-Hubert, H., Kaech, H., Ganesanandamoorthy, P. & Vorburger, C. Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids. Evolution 73, 1466–1481 (2019).
Google Scholar
Paniagua Voirol, L. R., Frago, E., Kaltenpoth, M., Hilker, M. & Fatouros, N. E. Bacterial symbionts in Lepidoptera: their diversity, transmission, and impact on the host. Front. Microbiol. 9, 556 (2018).
Google Scholar
Pina, T. et al. Molecular characterization of Cardinium, Rickettsia, Spiroplasma and Wolbachia in mite species from citrus orchards. Exp. Appl. Acarol. 81, 335–355 (2020).
Google Scholar
Porter, J. & Sullivan, W. The cellular lives of Wolbachia. Nat. Rev. Microbiol. 21, 750–766 (2023).
Google Scholar
Serbus, L. R., Casper-Lindley, C., Landmann, F. & Sullivan, W. The genetics and cell biology of Wolbachia-host interactions. Annu. Rev. Genet. 42, 683–707 (2008).
Google Scholar
Newton, I. L. G. & Rice, D. W. The Jekyll and Hyde symbiont: could Wolbachia be a nutritional mutualist? J. Bacteriol. 202, e00589–19 (2020).
Google Scholar
Zug, R. & Hammerstein, P. Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol. Rev. 90, 89–111 (2015).
Google Scholar
Brownlie, J. C. et al. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5, e1000368 (2009).
Google Scholar
Unckless, R. L. & Jaenike, J. Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution 66, 678–689 (2012).
Google Scholar
Dedeine, F. et al. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci. USA. 98, 6247–6252 (2001).
Google Scholar
Pannebakker, B. A., Loppin, B., Elemans, C. P. H., Humblot, L. & Vavre, F. Parasitic inhibition of cell death facilitates symbiosis. Proc. Natl. Acad. Sci. USA. 104, 213–215 (2007).
Google Scholar
Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.-Y. & Fukatsu, T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl. Acad. Sci. USA. 107, 769–774 (2010).
Google Scholar
Ju, J.-F. et al. Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. ISME J. 14, 676–687 (2020).
Google Scholar
Moriyama, M., Nikoh, N., Hosokawa, T. & Fukatsu, T. Riboflavin provisioning underlies Wolbachia’s fitness contribution to its insect host. mBio 6, e01732–01715 (2015).
Google Scholar
Depeint, F., Bruce, W. R., Shangari, N., Mehta, R. & O’Brien, P. J. Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem. Biol. Interact. 163, 94–112 (2006).
Google Scholar
Zhao, R.-Z., Jiang, S., Zhang, L. & Yu, Z.-B. Mitochondrial electron transport chain, ROS generation and uncoupling (Review). Int. J. Mol. Med. 44, 3–15 (2019).
Google Scholar
Noda, H., Koizumi, Y., Zhang, Q. & Deng, K. Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem. Mol. Biol. 31, 727–737 (2001).
Google Scholar
Huang, H.-J., Cui, J.-R., Chen, J., Bing, X.-L. & Hong, X.-Y. Proteomic analysis of Laodelphax striatellus gonads reveals proteins that may manipulate host reproduction by Wolbachia. Insect Biochem. Mol. Biol. 113, 103211 (2019).
Google Scholar
Bing, X.-L., Zhao, D.-S., Peng, C.-W., Huang, H.-J. & Hong, X.-Y. Similarities and spatial variations of bacterial and fungal communities in field rice planthopper (Hemiptera: Delphacidae) populations. Insect Sci 27, 947–963 (2020).
Google Scholar
Duan, X.-Z. et al. Recent infection by Wolbachia alters microbial communities in wild Laodelphax striatellus populations. Microbiome 8, 104 (2020).
Google Scholar
Hu, Q.-L. et al. Chromosome-level assembly, dosage compensation and sex-biased gene expression in the small brown planthopper, Laodelphax striatellus. Genome Biol. Evol. 14, evac160 (2022).
Google Scholar
Jin, C. et al. Riboflavin transporters RFVT/SLC52A mediate translocation of riboflavin, rather than FMN or FAD, across plasma membrane. Biol. Pharm. Bull. 40, 1990–1995 (2017).
Google Scholar
Gnainsky, Y. et al. Systemic regulation of host energy and oogenesis by microbiome-derived mitochondrial coenzymes. Cell Rep. 34, 108583 (2021).
Google Scholar
Li, T.-P. et al. Stable establishment of Cardinium spp. in the brown planthopper Nilaparvata lugens despite decreased host fitness. Appl. Environ. Microbiol. 86, e02509–19 (2020).
Google Scholar
Chen, Y. et al. SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. GigaScience 7, gix120 (2018).
Google Scholar
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
Google Scholar
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
Google Scholar
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15, 550 (2014).
Google Scholar
R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2024).Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008).
Google Scholar
Yu, G., Wang, L.-G., Han, Y. & He, Q.-Y. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics J. Integr. Biol. 16, 284–287 (2012).
Google Scholar
Golbach, J. L., Chalova, V. I., Woodward, C. L. & Ricke, S. C. Adaptation of Lactobacillus rhamnosus riboflavin assay to microtiter plates. J. Food Compos. Anal. 20, 568–574 (2007).
Google Scholar
Pan, X., Lu, K., Qi, S., Zhou, Q. & Zhou, Q. The content of amino acids in artificial diet influences the development and reproduction of brown planthopper, Nilaparvata lugens (STÅL). Arch. Insect Biochem. Physiol. 86, 75–84 (2014).
Google Scholar
Li, T.-P. et al. Two newly introduced Wolbachia endosymbionts induce cell host differences in competitiveness and metabolic responses. Appl. Environ. Microbiol. 87, e0147921 (2021).
Google Scholar
Jiang, W. & Zhu, T. F. Targeted isolation and cloning of 100-kb microbial genomic sequences by Cas9-assisted targeting of chromosome segments. Nat. Protoc. 11, 960–975 (2016).
Google Scholar
Mendiburu, F. D. & Simon, R. Agricolae – ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ Prepr. 3, e1404v1401 (2015).Download referencesAcknowledgementsWe thank Prof. Fei-Rong Ren from Henan University, Dr. Xiang Sun and Tianyu Wang from Shenyang Agricultural University for their technical and material support in riboflavin detection experiments. We also thank Hao Zhang from Nanjing Agricultural University for his help in preparing RNA-seq samples. This work was supported by the Key Research and Development Project of Hainan Province (ZDYF2024XDNY249 to X.Y.H.), the National Natural Science Foundation of China (32572809 to X.L.B. and 32020103011 to X.Y.H.), and the Young Elite Scientists Sponsorship Program by Jiangsu Association for Science and Technology (TJ-2023-038 to X.L.B.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Author informationAuthors and AffiliationsState Key Laboratory of Agricultural and Forestry Biosecurity, College of Plant Protection, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaYue-Di Niu, Qi-Hang Fan, Zi-Han Wang, Meng-Ke Wang, Dian-Shu Zhao, Meng-Ru Wang, Bing-Xuan Wu, Xiao-Yue Hong & Xiao-Li BingAuthorsYue-Di NiuView author publicationsSearch author on:PubMed Google ScholarQi-Hang FanView author publicationsSearch author on:PubMed Google ScholarZi-Han WangView author publicationsSearch author on:PubMed Google ScholarMeng-Ke WangView author publicationsSearch author on:PubMed Google ScholarDian-Shu ZhaoView author publicationsSearch author on:PubMed Google ScholarMeng-Ru WangView author publicationsSearch author on:PubMed Google ScholarBing-Xuan WuView author publicationsSearch author on:PubMed Google ScholarXiao-Yue HongView author publicationsSearch author on:PubMed Google ScholarXiao-Li BingView author publicationsSearch author on:PubMed Google ScholarContributionsThe authors contributed to the present study as follows: Y.D.N., X.L.B., and X.Y.H. designed the research; Y.D.N., Q.H.F., Z.H.W., M.K.W., D.S.Z., M.R.W., B.X.W., and X.L.B. performed the research and analyzed the data; Y.D.N., X.L.B., and X.Y.H. wrote and edited the manuscript; all authors read and approved the manuscript.Corresponding authorsCorrespondence to
Xiao-Yue Hong or Xiao-Li Bing.Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Communications thanks the anonymous, reviewer(s) for their contribution to the peer review of this work. A peer review file is available.
Additional informationPublisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Supplementary informationSupplementary InformationDescriptions of Additional Supplementary FilesSupplementary Data 1Supplementary Data 2Supplementary Data 3Supplementary Data 4Reporting SummaryTransparent Peer Review fileSource dataSource Data fileRights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, 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 you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. 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-nc-nd/4.0/.
Reprints and permissionsAbout this articleCite this articleNiu, YD., Fan, QH., Wang, ZH. et al. Wolbachia enhances ovarian development in the rice planthopper Laodelphax striatellus through elevated energy production.
Nat Commun (2025). https://doi.org/10.1038/s41467-025-67660-1Download citationReceived: 02 March 2025Accepted: 05 December 2025Published: 13 December 2025DOI: https://doi.org/10.1038/s41467-025-67660-1Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy shareable link to clipboard
Provided by the Springer Nature SharedIt content-sharing initiative More
