Abstract
The fruits of Physalis (Solanaceae) have a unique structure, a lantern-like fruiting calyx known as inflated calyx syndrome (ICS) or the Chinese lantern, and are rich in steroid-related compounds. However, the genetic variations underlying the origin of these characteristic traits and diversity in Physalis remain largely unknown. Here, we present a high-quality chromosome-level reference genome assembly of Physalis floridana (~1.40 Gb in size) with a contig N50 of ~4.87 Mb. Through evolutionary genomics and experimental approaches, we found that the loss of the SEP-like MADS-box gene MBP21 subclade is likely a key mutation that, together with the previously revealed mutation affecting floral MPF2 expression, might have contributed to the origination of ICS in Physaleae, suggesting that the origination of a morphological novelty may have resulted from an evolutionary scenario in which one mutation compensated for another deleterious mutation. Moreover, the significant expansion of squalene epoxidase genes is potentially associated with the natural variation of steroid-related compounds in Physalis fruits. The results reveal the importance of gene gains (duplication) and/or subsequent losses as genetic bases of the evolution of distinct fruit traits, and the data serve as a valuable resource for the evolutionary genetics and breeding of solanaceous crops.
Highlights
Introduction The familySolanaceae is an important source of nutritional and culinary diversity
To understand the whole-genome duplication (WGD) history of P. floridana, we investigated the distribution of the synonymous substitution rate (Ks) between syntenic gene pairs based on comparisons among P. floridana, C. annuum, S. lycopersicum, and Vitis vinifera
Based on the novel genomic data, we pinpointed another key genetic mutation involved in the loss of a SEP-like MADS-box gene, in addition to the previously known MPF2 and MPF3 genes[5,14], which apparently contributed to the origin of the morphological novelty of inflated calyx syndrome (ICS), or Chinese lantern
Summary
Introduction The familySolanaceae is an important source of nutritional and culinary diversity. Physalis is one of the largest genera within Solanaceae, with 70–90 species[4] Species in this genus have emerged as a new class of solanaceous horticultural crops as well as new model plants for studies in ecology, evolution, and development[3,5], as the genus is characterized by novel morphological traits and biochemical diversity in fruits. Understanding how such complex traits originated during evolutionary history is a fundamental question, since fruit evolution has long been considered a key contributor to the success of angiosperms[6]. The origin of these evolutionary novelties is a fascinating subject in itself, and the processes giving rise to them are largely unresolved evolutionary mysteries
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