Comparative transcriptomics from multiple environments reveals robustly developmentally-regulated genes by fertilization in Physalis and differentially expressed genes with Solanum

Fertilization is an important biological process, which triggers the fruit development and morphology variation. The Chinese lantern, a morphological novelty derived from the calyx, is started to be formed upon fertilization in Physalis, but it is not observed in Solanum. The underlying genetic variations are largely unknown, while differentially expressed genes (DEGs) might act. Here, we documented developmental and morphological differences in the flower and fruit between Physalis floridana and Solanum pimpinellifolium, and then evaluated both sequence variation and gene expression at the transcriptomic level around fertilization between the two species. Sequencing the Physalis transcriptome revealed 147,118 unigenes, and 468 unigenes were identified to be DEGs robustly regulated by fertilization under multiple environments. When aligned to the tomato genome, we estimated that around 33,125 genes were expressed in the Physalis floral-fruit transcriptome, and 14,536 strict single-copy orthologous gene pairs were identified between P. floridana and S. pimpinellifolium. Principal component analyses revealed that DEGs around fertilization could well distinguish Solanum and Physalis. Nine distinct types of gene variation patterns with distinct GO-enriched patterns were identified, and they covered 58.82% orthologous gene pairs that were differentially expressed in either trend or dosage at floral-fruit transition between the two species, whereas only 9 non-regulatory genes were detected to be positively selected, thus implying that cis-regulatory variation leading to differential gene expression, including transcription factor genes (TFs), around fertilization might be a predominant event during the Solanum-Physalis divergence and fruit evolution. Virus-induced gene silencing analyses revealed various developmental roles of some TFs in fertility, Chinese lantern development, or fruit weight control in Physalis. Our work sheds light on the genetic variations accounting for the evolution of Physalis fruit early development in comparison to Solanum.