Establishing Physalis as a 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

Research output: Contribution to journalArticlepeer-review

Abstract

The highly diverse Solanaceae family contains several widely studied models 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 Physalis pruinosa and use these resources to study natural and engineered variations 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 paradigm in the search for factors driving ICS.

Original languageEnglish (US)
Pages (from-to)351-368
Number of pages18
JournalPlant Cell
Volume35
Issue number1
DOIs
StatePublished - Jan 2023
Externally publishedYes

ASJC Scopus subject areas

  • Plant Science

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