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Cynipid wasps systematically reprogram host metabolism and restructure cell walls in developing galls

Kasey Markel, View ORCID ProfileVlastimil Novak, Benjamin P. Bowen, Yang Tian, Yi-Chun Chen, Sasilada Sirirungruang, Andy Zhou, Katherine B. Louie, Trent R. Northen, Aymerick Eudes, Henrik V. Scheller, Patrick M. Shih
doi: https://doi.org/10.1101/2023.05.22.540048
Kasey Markel
1Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Vlastimil Novak
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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  • ORCID record for Vlastimil Novak
Benjamin P. Bowen
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
4Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United States
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Yang Tian
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Yi-Chun Chen
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Sasilada Sirirungruang
1Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Andy Zhou
1Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Katherine B. Louie
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
4Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United States
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Trent R. Northen
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
4Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United States
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Aymerick Eudes
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Henrik V. Scheller
1Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Patrick M. Shih
1Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA
2Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
4Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United States
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  • For correspondence: pmshih@berkeley.edu
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Abstract

Many insects have evolved the ability to manipulate plant growth to generate extraordinary structures called galls in which insect larva can develop while being sheltered within and feeding on the plant. In particular, Cynipid (Hymenoptera: Cynipidae) wasps have evolved to form some of the most morphologically complex galls known and generate an astonishing array of gall shapes, colors, and sizes. However, the biochemical basis underlying these remarkable cellular and developmental transformations remains poorly understood. A key determinant in plant cellular development is the deposition of the cell wall to dictate the physical form and physiological function of newly developing cells, tissues, and organs. However, it is unclear to what degree cell walls are restructured to initiate and support the formation of new gall tissue. Here, we characterize the molecular alterations underlying gall development using a combination of metabolomic, histological, and biochemical techniques to elucidate how leaf cells are reprogrammed to form galls. Strikingly, gall development involves an exceptionally coordinated spatial deposition of lignin and xylan to form de novo gall vasculature. Our results highlight how Cynipid wasps can radically change the metabolite profile and restructure the cell wall to enable the formation of galls, providing new insights into the mechanism of gall induction and the extent to which plants can be entirely reprogrammed to form novel structures and organs.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 23, 2023.
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Cynipid wasps systematically reprogram host metabolism and restructure cell walls in developing galls
Kasey Markel, Vlastimil Novak, Benjamin P. Bowen, Yang Tian, Yi-Chun Chen, Sasilada Sirirungruang, Andy Zhou, Katherine B. Louie, Trent R. Northen, Aymerick Eudes, Henrik V. Scheller, Patrick M. Shih
bioRxiv 2023.05.22.540048; doi: https://doi.org/10.1101/2023.05.22.540048
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Cynipid wasps systematically reprogram host metabolism and restructure cell walls in developing galls
Kasey Markel, Vlastimil Novak, Benjamin P. Bowen, Yang Tian, Yi-Chun Chen, Sasilada Sirirungruang, Andy Zhou, Katherine B. Louie, Trent R. Northen, Aymerick Eudes, Henrik V. Scheller, Patrick M. Shih
bioRxiv 2023.05.22.540048; doi: https://doi.org/10.1101/2023.05.22.540048

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