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Establishing Physalis as a new Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome

View ORCID ProfileJia He, View ORCID ProfileMichael Alonge, Srividya Ramakrishnan, View ORCID ProfileMatthias Benoit, View ORCID ProfileSebastian Soyk, Nathan T. Reem, Anat Hendelman, Joyce Van Eck, Michael C. Schatz, View ORCID ProfileZachary B. Lippman
doi: https://doi.org/10.1101/2022.07.29.502011
Jia He
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
2Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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  • ORCID record for Jia He
Michael Alonge
3Department of Computer Science, Johns Hopkins University, Baltimore, MD 21218, USA
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Srividya Ramakrishnan
3Department of Computer Science, Johns Hopkins University, Baltimore, MD 21218, USA
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Matthias Benoit
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
2Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Sebastian Soyk
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Nathan T. Reem
4Boyce Thompson Institute, Ithaca, NY 14853, USA
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Anat Hendelman
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Joyce Van Eck
4Boyce Thompson Institute, Ithaca, NY 14853, USA
5Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA
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Michael C. Schatz
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
3Department of Computer Science, Johns Hopkins University, Baltimore, MD 21218, USA
6Department of Biology, Johns Hopkins University, Baltimore, MD 21218, USA
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Zachary B. Lippman
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
2Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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  • ORCID record for Zachary B. Lippman
  • For correspondence: lippman@cshl.edu
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ABSTRACT

The highly diverse Solanaceae family contains several widely studied model and crop species. Fully exploring, appreciating, and exploiting this diversity requires additional model systems. Particularly promising are orphan fruit crops in the genus Physalis, which occupy a key evolutionary position in the Solanaceae and capture understudied variation in traits such as inflorescence complexity, fruit ripening and metabolites, disease and insect resistance, self-compatibility, and most notable, the striking Inflated Calyx Syndrome (ICS), an evolutionary novelty found across angiosperms where sepals grow exceptionally large to encapsulate fruits in a protective husk. We recently developed transformation and genome editing in Physalis grisea (groundcherry). However, to systematically explore and unlock the potential of this and related Physalis as genetic systems, high-quality genome assemblies are needed. Here, we present chromosome-scale references for P. grisea and its close relative P. pruinosa and use these resources to study natural and engineered variation in floral traits. We first rapidly identified a natural structural variant in a bHLH gene that causes petal color variation. Further, and against expectations, we found that CRISPR-Cas9 targeted mutagenesis of 11 MADS-box genes, including purported essential regulators of ICS, had no effect on inflation. In a forward genetics screen, we identified huskless, which lacks ICS due to mutation of an AP2-like gene that causes sepals and petals to merge into a single whorl of mixed identity. These resources and findings elevate Physalis to a new Solanaceae model system, and establish a new paradigm for the search of factors driving ICS.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 30, 2022.
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Establishing Physalis as a new Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome
Jia He, Michael Alonge, Srividya Ramakrishnan, Matthias Benoit, Sebastian Soyk, Nathan T. Reem, Anat Hendelman, Joyce Van Eck, Michael C. Schatz, Zachary B. Lippman
bioRxiv 2022.07.29.502011; doi: https://doi.org/10.1101/2022.07.29.502011
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Establishing Physalis as a new Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome
Jia He, Michael Alonge, Srividya Ramakrishnan, Matthias Benoit, Sebastian Soyk, Nathan T. Reem, Anat Hendelman, Joyce Van Eck, Michael C. Schatz, Zachary B. Lippman
bioRxiv 2022.07.29.502011; doi: https://doi.org/10.1101/2022.07.29.502011

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