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Korgaonkar A, Han C, Lemire AL, et al. A novel family of secreted insect proteins linked to plant gall development. Curr Biol. 2021;31(9):1836-1849.e12doi: 10.1016/j.cub.2021.01.104.
Korgaonkar, A., Han, C., Lemire, A. L., Siwanowicz, I., Bennouna, D., Kopec, R. E., Andolfatto, P., Shigenobu, S., & Stern, D. L. (2021). A novel family of secreted insect proteins linked to plant gall development. Current biology : CB, 31(9), 1836-1849.e12. https://doi.org/10.1016/j.cub.2021.01.104
Korgaonkar, Aishwarya, et al. "A novel family of secreted insect proteins linked to plant gall development." Current biology : CB vol. 31,9 (2021): 1836-1849.e12. doi: https://doi.org/10.1016/j.cub.2021.01.104
Korgaonkar A, Han C, Lemire AL, Siwanowicz I, Bennouna D, Kopec RE, Andolfatto P, Shigenobu S, Stern DL. A novel family of secreted insect proteins linked to plant gall development. Curr Biol. 2021 May 10;31(9):1836-1849.e12. doi: 10.1016/j.cub.2021.01.104. Epub 2021 Mar 02. PMID: 33657407; PMCID: PMC8119383.
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Curr Biol. 2021 May 10;31(9):1836-1849.e12. doi: 10.1016/j.cub.2021.01.104. Epub 2021 Mar 02.

A novel family of secreted insect proteins linked to plant gall development.

Current biology : CB

Aishwarya Korgaonkar, Clair Han, Andrew L Lemire, Igor Siwanowicz, Djawed Bennouna, Rachel E Kopec, Peter Andolfatto, Shuji Shigenobu, David L Stern

Affiliations

  1. Janelia Research Campus of the Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USA.
  2. Human Nutrition Program, Department of Human Sciences, The Ohio State University, 262G Campbell Hall, 1787 Neil Avenue, Columbus, OH 43210, USA.
  3. Human Nutrition Program, Department of Human Sciences, The Ohio State University, 262G Campbell Hall, 1787 Neil Avenue, Columbus, OH 43210, USA; Ohio State University's Foods for Health Discovery Theme, The Ohio State University, 262G Campbell Hall, 1787 Neil Avenue, Columbus, OH 43210, USA.
  4. Department of Biology, Columbia University, 600 Fairchild Center, New York, NY 10027, USA.
  5. Laboratory of Evolutionary Genomics, Center for the Development of New Model Organism, National Institute for Basic Biology, Okazaki 444-8585, Japan; NIBB Research Core Facilities, National Institute for Basic Biology, Okazaki 444-8585, Japan; Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka, Myodaiji, Okazaki 444-8585, Japan.
  6. Janelia Research Campus of the Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USA. Electronic address: [email protected].

PMID: 33657407 PMCID: PMC8119383 DOI: 10.1016/j.cub.2021.01.104

Abstract

In an elaborate form of inter-species exploitation, many insects hijack plant development to induce novel plant organs called galls that provide the insect with a source of nutrition and a temporary home. Galls result from dramatic reprogramming of plant cell biology driven by insect molecules, but the roles of specific insect molecules in gall development have not yet been determined. Here, we study the aphid Hormaphis cornu, which makes distinctive "cone" galls on leaves of witch hazel Hamamelis virginiana. We found that derived genetic variants in the aphid gene determinant of gall color (dgc) are associated with strong downregulation of dgc transcription in aphid salivary glands, upregulation in galls of seven genes involved in anthocyanin synthesis, and deposition of two red anthocyanins in galls. We hypothesize that aphids inject DGC protein into galls and that this results in differential expression of a small number of plant genes. dgc is a member of a large, diverse family of novel predicted secreted proteins characterized by a pair of widely spaced cysteine-tyrosine-cysteine (CYC) residues, which we named BICYCLE proteins. bicycle genes are most strongly expressed in the salivary glands specifically of galling aphid generations, suggesting that they may regulate many aspects of gall development. bicycle genes have experienced unusually frequent diversifying selection, consistent with their potential role controlling gall development in a molecular arms race between aphids and their host plants.

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Keywords: Hamamelis; Hormaphis; anthocyanins; aphid; bicycle genes; effector genes; high-performance liquid chromatography; mass spectrometry; novel genes; plant gall

Conflict of interest statement

Declaration of interests HHMI has filed a provisional patent, number 63/092,942, for the inventors A.K. and D.L.S., covering unique aphid polypeptides for use in modifying plants.

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