Plant galls are abnormal growing tissues induced by various parasitic organisms, exhibiting diverse and complex morphologies. Typically, these galls differ significantly in appearance from their host plants. Here, we report that larvae of a parasitic fly generate unique, rosette galls on Aster scaber, a perennial herb. These galls develop from vegetative organs after the larvae reprogram floral gene expression. To investigate the underlying mechanisms, we conducted whole-genome sequencing and transcriptome analysis. Our findings reveal that the larvae induce host organ dedifferentiation into an amorphous callus, activate floral genes, and selectively suppress genes associated with carpel development. As a result, the pseudoflowers consist solely of tepal-like leaflets and a specialized chamber, and the larvae influence pigment biosynthesis. Hijacking plants developmental gene networks by insects to sequentially mediate dedifferentiation, cytokinin regulation, and tepal-like leaflets formation provides a framework to study highly elaborate forms of parasitism and symbiosis between plants and insects.

AIT Austrian Institute of Technology Center for Health and Bioresources Bioresources Unit Donau Austria

Center for Nutraceutical and Pharmaceutical Materials Department of Bioscience and Bioinformatics Myongji University Yongin South Korea

Department of Adaptive Biotechnologies Global Change Research Institute CAS Brno Czech Republic

Department of Biochemistry and Biophysics Texas A and M University College Station Texas USA

Department of Biological Sciences college of Arts and Sciences University of North Texas Denton Texas USA

Department of Biotechnology College of Applied Life Sciences Jeju National University Jeju South Korea

Department of Biotechnology Sungshin University Seoul South Korea

Department of New Biology DGIST Daegu South Korea

Department of Plant and Environmental Sciences Faculty of Science University of Copenhagen Copenhagen Denmark

Department of Systems Biology College of Life Science and Biotechnology Yonsei University Seoul South Korea

Gregor Mendel Institute of Molecular Plant Biology GmbH Vienna Austria

Institute of Health and Environment Jeju South Korea

Institute of Research and Development Nareso Co Ltd Seoul National University Business Incubator Suwon South Korea

National Institute of Biological Resources Environmental Research Complex Incheon South Korea

School of Energy and Chemical Engineering UNIST UNIST gil 50 Ulsan South Korea

Subtropical Tropical Organism Gene Bank Jeju National University Jeju South Korea

Xenohelix Research Institute Incheon South Korea

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Alvarez‐Buylla, E. R. , Benítez M., Corvera‐Poiré A., et al. 2010. “Flower Development.” Arabidopsis Book 8: e0127. PubMed PMC

Aurin, M.‐B. , Haupt M., Görlach M., Rümpler F., and Theißen G.. 2020. “Structural Requirements of the Phytoplasma Effector Protein sap54 for Causing Homeotic Transformation of Floral Organs.” Molecular Plant‐Microbe Interactions® 33, no. 9: 1129–1141. PubMed

Bailey, S. , Percy D. M., Hefer C. A., and Cronk Q. C. B.. 2015. “The Transcriptional Landscape of Insect Galls: Psyllid (Hemiptera) Gall Formation in Hawaiian PubMed PMC

Bowman, J. L. , and Moyroud E.. 2024. “Reflections on the Abc Model of Flower Development.” Plant Cell 36, no. 5: 1334–1357. PubMed PMC

Chen, H. , Liu J., Cui K., et al. 2018. “Molecular Mechanisms of Tannin Accumulation in Rhus Galls and Genes Involved in Plant‐Insect Interactions.” Scientific Reports 8, no. 1: 9841. PubMed PMC

Chen, M.‐S. , Zhao H.‐X., Zhu Y. C., et al. 2008. “Analysis of Transcripts and Proteins Expressed in the Salivary Glands of Hessian Fly ( PubMed

Chen, X. , Yang Z., Chen H., et al. 2020. “A Complex Nutrient Exchange Between a Gall‐Forming Aphid and Its Plant Host.” Frontiers in Plant Science 11: 811. PubMed PMC

Cucinotta, M. , Cavalleri A., Chandler J. W., and Colombo L.. 2021. “Auxin and Flower Development: A Blossoming Field.” Cold Spring Harbor Perspectives in Biology 13, no. 2: a039974. PubMed PMC

Espinosa‐Soto, C. , Padilla‐Longoria P., and Alvarez‐Buylla E. R.. 2004. “A Gene Regulatory Network Model for Cell‐Fate Determination During PubMed PMC

Espírito‐Santo, M. M. , and Fernandes G. W.. 2007. “How Many Species of Gall‐Inducing Insects Are There on Earth, and Where Are They?” Annals of the Entomological Society of America 100, no. 2: 95–99.

Flynn, J. M. , Hubley R., Goubert C., et al. 2020. “Repeatmodeler2 for Automated Genomic Discovery of Transposable Element Families.” Proceedings of the National Academy of Sciences 117, no. 17: 9451–9457. PubMed PMC

Gätjens‐Boniche, O. , Jiménez‐Madrigal J. P., Whetten R. W., et al. 2023. “Microbiome and Plant Cell Transformation Trigger Insect Gall Induction in Cassava.” Frontiers in Plant Science 14: 1237966. PubMed PMC

Gautheret, R. 1939. “Sur la possibilité de réaliser la culture indéfinie des tissus de tubercules de carotte.” CR Hebd Seances Acad Sc 208: 118–120.

Grabherr, M. G. , Haas B. J., Yassour M., et al. 2011. “Full‐Length Transcriptome Assembly From RNA‐Seq Data Without a Reference Genome.” Nature Biotechnology 29, no. 7: 644–652. PubMed PMC

Großkinsky, D. K. , Albacete A., Jammer A., et al. 2014. “A Rapid Phytohormone and Phytoalexin Screening Method for Physiological Phenotyping.” Molecular Plant 7, no. 6: 1053–1056. PubMed

Großkinsky, D. K. , and Petrášek J.. 2019. “Auxins and Cytokinins–The Dynamic Duo of Growth‐Regulating Phytohormones Heading for New Shores.” New Phytologist 221, no. 3: 1187–1190. PubMed

Hammer, T. J. , De Clerck‐Floate R., Tooker J. F., Price P. W., Miller D. G., and Connor E. F.. 2021. “Are Bacterial Symbionts Associated With Gall Induction In Insects?” Arthropod‐Plant Interactions 15: 1–12.

Hardy, N. B. , and Cook L. G.. 2010. “Gall‐Induction in Insects: Evolutionary Dead‐End or Speciation Driver?” BMC Evolutionary Biology 10: 257. PubMed PMC

Hu, J. , Fan J., Sun Z., and Liu S.. 2020. “Nextpolish: A Fast and Efficient Genome Polishing Tool for Long‐Read Assembly.” Bioinformatics 36, no. 7: 2253–2255. PubMed

Huang, N. , and Li H.. 2023. “Compleasm: A Faster and More Accurate Reimplementation of Busco.” Bioinformatics 39, no. 10: btad595. PubMed PMC

Keilwagen, J. , Hartung F., and Grau J.. 2019. “Gemoma: Homology‐Based Gene Prediction Utilizing Intron Position Conservation and RNA‐Seq Data.” Gene Prediction: Methods in Molecular Biology (Clifton, N.J.) 1962: 161–177. PubMed

Kitazawa, Y. , Iwabuchi N., Himeno M., et al. 2017. “Phytoplasma‐Conserved Phyllogen Proteins Induce Phyllody Across the Plantae by Degrading Floral Mads Domain Proteins.” Journal of Experimental Botany 68, no. 11: 2799–2811. PubMed PMC

Kokot, M. , Długosz M., and Deorowicz S.. 2017. “Kmc 3: Counting and Manipulating K‐Mer Statistics.” Bioinformatics 33, no. 17: 2759–2761. PubMed

Korgaonkar, A. , Han C., Lemire A. L., et al. 2021. “A Novel Family of Secreted Insect Proteins Linked to Plant Gall Development.” Current Biology 31, no. 9: 1836–1849.e12. PubMed PMC

Labandeira, C. C. , and Phillips T. L.. 1996. “A Carboniferous Insect Gall: Insight Into Early Ecologic History of the Holometabola.” Proceedings of the National Academy of Sciences 93, no. 16: 8470–8474. PubMed PMC

Li, W. P. , Yang F. S., Jivkova T., and Yin G. S.. 2012. “Phylogenetic Relationships and Generic Delimitation of Eurasian Aster (Asteraceae: Astereae) Inferred From its, ets and trnl‐f Sequence Data.” Annals of Botany 109, no. 7: 1341–1357. PubMed PMC

Liu, H. , Wu S., Li A., and Ruan J.. 2021. “Smartdenovo: A De Novo Assembler Using Long Noisy Reads.” Gigabyte 2021: gigabyte15. PubMed PMC

Liu, L.‐Y. D. , Tseng H.‐I., Lin C.‐P., et al. 2014. “High‐Throughput Transcriptome Analysis of the Leafy Flower Transition of PubMed

Liu, X. , Khajuria C., Li J., et al. 2013. “Wheat mds‐1 Encodes a Heat‐Shock Protein and Governs Susceptibility Towards the Hessian Fly Gall Midge.” Nature Communications 4, no. 1: 2070. PubMed

Maejima, K. , Iwai R., Himeno M., et al. 2014. “Recognition of Floral Homeotic Mads Domain Transcription Factors by a Phytoplasmal Effector, Phyllogen, Induces Phyllody.” Plant Journal 78, no. 4: 541–554. PubMed PMC

Maejima, K. , Kitazawa Y., Tomomitsu T., et al. 2015. “Degradation of Class E Mads‐Domain Transcription Factors in Arabidopsis by a Phytoplasmal Effector, Phyllogen.” Plant Signaling & Behavior 10, no. 8: e1042635. PubMed PMC

Markel, K. , Novak V., Bowen B. P., et al. 2024. “Cynipid Wasps Systematically Reprogram Host Metabolism and Restructure Cell Walls in Developing Galls.” Plant Physiology 195, no. 1: 698–712. PubMed PMC

Murakami, R. , Ushima R., Sugimoto R., et al. 2021. “A New Galling Insect Model Enhances Photosynthetic Activity In An Obligate Holoparasitic Plant.” Scientific Reports 11, no. 1: 13013. PubMed PMC

Nabity, P. D. , Haus M. J., Berenbaum M. R., and DeLucia E. H.. 2013. “Leaf‐Galling Phylloxera on Grapes Reprograms Host Metabolism and Morphology.” Proceedings of the National Academy of Sciences 110, no. 41: 16663–16668. PubMed PMC

Nesom, G. L. 1994. “A New Species of Lippia (Verbenaceae) From South‐Central Mexico, With Comments on Related and Peripheral Species.” Phytologia 77: 309–317.

Nobécourt, P. 1939. “Sur la pérennité et l'augmentation de volume des cultures de tissues végétaux.” CR Seances Soc Biol Ses Fil 130: 1270–1271.

Ó'Maoiléidigh, D. S. , Graciet E., and Wellmer F.. 2014. “Gene Networks Controlling a Rabidopsis Thaliana Flower Development.” New Phytologist 201, no. 1: 16–30. PubMed

Oates, C. , Denby K., Myburg A., Slippers B., and Naidoo S.. 2016. “Insect Gallers and Their Plant Hosts: From Omics Data to Systems Biology.” International Journal of Molecular Sciences 17, no. 11: 1891. PubMed PMC

Oliveira, D. C. , Isaias R. M. S., Fernandes G. W., Ferreira B. G., Carneiro R. G. S., and Fuzaro L.. 2016. “Manipulation of Host Plant Cells and Tissues by Gall‐Inducing Insects and Adaptive Strategies Used by Different Feeding Guilds.” Journal of Insect Physiology 84: 103–113. PubMed

Paik, J.‐C. , Yukawa J., Uechi N., Sato S., and Ganaha T.. 2004. “Gall‐Inducing Species of the Family Cecidomyiidae (Diptera) Recorded From the Korean Peninsula and Surrounding Islands, in Comparison With the Gall‐Midge Fauna of Japan.” ESAKIA 44: 57–66.

Patro, R. , Duggal G., Love M. I., Irizarry R. A., and Kingsford C.. 2017. “Salmon Provides Fast and Bias‐Aware Quantification of Transcript Expression.” Nature Methods 14, no. 4: 417–419. PubMed PMC

Price, P. W. , Fernandes G. W., and Waring G. L.. 1987. “Adaptive Nature of Insect Galls.” Environmental Entomology 16, no. 1: 15–24.

Ranallo‐Benavidez, T. R. , Jaron K. S., and Schatz M. C.. 2020. “Genomescope 2.0 and Smudgeplot for Reference‐Free Profiling of Polyploid Genomes.” Nature Communications 11: 1432. PubMed PMC

Roach, M. J. , Schmidt S. A., and Borneman A. R.. 2018. “Purge Haplotigs: Allelic Contig Reassignment for Third‐Gen Diploid Genome Assemblies.” BMC Bioinformatics 19: 460. PubMed PMC

Samach, A. , Klenz J. E., Kohalmi S. E., Risseeuw E., Haughn G. W., and Crosby W. L.. 1999. “The Unusual Floral Organs Gene of PubMed

Schäfer, M. , Brütting C., Meza‐Canales I. D., et al. 2015. “The Role of Cis‐Zeatin‐Type Cytokinins in Plant Growth Regulation and Mediating Responses to Environmental Interactions.” Journal of Experimental Botany 66, no. 16: 4873–4884. PubMed PMC

Schultz, J. C. , Edger P. P., Body M. J. A., and Appel H. M.. 2019. “A Galling Insect Activates Plant Reproductive Programs During Gall Development.” Scientific Reports 9, no. 1: 1833. PubMed PMC

Shinji, O. 1944. Chuei to chuei konchu: Galls and Gall Making Insects, 580.

Sinha, D. K. , Nagaraju J., Tomar A., Bentur J. S., and Nair S.. 2012. “Pyrosequencing‐Based Transcriptome Analysis of the Asian Rice Gall Midge Reveals Differential Response During Compatible and Incompatible Interaction.” International Journal of Molecular Sciences 13, no. 10: 13079–13103. PubMed PMC

Skoog, F. , and Miller C. O.. 1957. “Chemical Regulation of Growth and Organ Formation in Plant Tissues Cultured In Vitro.” Symposia of the Society for Experimental Biology 11: 118–130. PubMed

Song, A. , Su J., Wang H., et al. 2023. “Analyses of a Chromosome‐Scale Genome Assembly Reveal the Origin and Evolution of Cultivated Chrysanthemum.” Nature Communications 14, no. 1: 2021. PubMed PMC

Stern, D. L. , and Han C.. 2022. “Gene Structure‐Based Homology Search Identifies Highly Divergent Putative Effector Gene Family.” Genome Biology and Evolution 14, no. 6: evac069. PubMed PMC

Stone, G. N. , and Schönrogge K.. 2003. “The Adaptive Significance of Insect Gall Morphology.” Trends in Ecology & Evolution 18, no. 10: 512–522.

Tokuda, M. , Yukawa J., Kuzntsov V. N., and Kozhevnikov A. E. 2003. Asteralobia Gall Midges (diptera: Cecidomyiidae) on Aster Species (asteraceae) in Japan and the Russian Far East.

Wei, H. Y. , Ye Y. X., Huang H. J., et al. 2022. “Chromosome‐Level Genome Assembly for the Horned‐Gall Aphid Provides Insights into Interactions Between Gall‐Making Insect and Its Host Plant.” Ecology and Evolution 12, no. 4: e8815. PubMed PMC

Wei, W. , Davis R. E., Nuss D. L., and Zhao Y.. 2013. “Phytoplasmal Infection Derails Genetically Preprogrammed Meristem Fate and Alters Plant Architecture.” Proceedings of the National Academy of Sciences 110, no. 47: 19149–19154. PubMed PMC

White, P. R. 1939. “Potentially Unlimited Growth of Excised Plant Callus in an Artificial Nutrient.” American Journal of Botany 26: 59–64.

Yamaguchi, H. , Tanaka H., Hasegawa M., Tokuda M., Asami T., and Suzuki Y.. 2012. “Phytohormones and Willow Gall Induction by a Gall‐Inducing Sawfly.” New Phytologist 196, no. 2: 586–595. PubMed

Ye, J. , Wang C., Liu Y., et al. 2024. “Cgd: A Multi‐Omics Database for Chrysanthemum Genomic and Biological Research.” Horticulture Research 11, no. 11: uhae238. PubMed PMC

Yukawa, J. , Tokuda M., and Yamagishi K.. 2014. “Host Plant Ranges and Distribution Records of Identified and Unidentified Species of the Genus Lasioptera (Diptera: Cecidomyiidae) In Japan.” ESAKIA 54: 1–15.

Zhang, Z. , Shi W., Gu J., et al. 2024. “Short Day Promotes Gall Swelling by a Constans‐Flowering Locus T Pathway in PubMed

Zhao, C. , Escalante L. N., Chen H., et al. 2015. “A Massive Expansion of Effector Genes Underlies Gall‐Formation in the Wheat Pest PubMed

Zhao, C. , Shukle R., Navarro‐Escalante L., Chen M., Richards S., and Stuart J. J.. 2016. “Avirulence Gene Mapping in the Hessian Fly ( PubMed

Zhao, J. , Wang J., Liu J., et al. 2024. “Spatially Distributed Cytokinins: Metabolism, Signaling, and Transport.” Plant Communications 5: 100936. PubMed PMC