A lineage‐specific arginine in POS1 is required for fruit size control in Physaleae (Solanaceae) via gene co‐option

Abstract

SUMMARY Solanaceae have important economic value mainly due to their edible fruits. Physalis organ size 1/cytokinin response factor 3 (POS1/CRF3), a unique gene in Solanaceae, is involved in fruit size variation in Physalis but not in Solanum. However, the underlying mechanisms remain elusive. Here, we found that POS1/CRF3 was likely created via the fusion of CRF7 and CRF8 duplicates. Multiple genetic manipulations revealed that only POS1 and Capsicum POS1 (CaPOS1) functioned in fruit size control via the positive regulation of cell expansion. Comparative studies in a phylogenetic framework showed the directional enhancement of POS1‐like expression in the flowers and fruits of Physaleae and the specific gain of certain interacting proteins associated with cell expansion by POS1 and CaPOS1. A lineage‐specific single nucleotide polymorphism (SNP) caused the 68th amino acid histidine in the POS1 orthologs of non‐Physaleae (Nicotiana and Solanum) to change to arginine in Physaleae (Physalis and Capsicum). Substituting the arginine in Physaleae POS1‐like by histidine completely abolished their function in the fruits and the protein–protein interaction (PPI) with calreticulin‐3. Transcriptomic comparison revealed the potential downstream pathways of POS1, including the brassinosteroid biosynthesis pathway. However, POS1‐like may have functioned ancestrally in abiotic stress within Solanaceae. Our work demonstrated that heterometric expression and a SNP caused a single amino acid change to establish new PPIs, which contributed to the co‐option of POS1 in multiple regulatory pathways to regulate cell expansion and thus fruit size in Physaleae. These results provide new insights into fruit morphological evolution and fruit yield control.

Advances in Physalis molecular research: applications in authentication, genetic diversity, phylogenetics, functional genes, and omics

“…In P. philadelphica , the expression level of Physalis Organ Size 1 ( POS1 ) gene is positively associated with variations in fruit size ( Wang et al., 2014 ). POS1 plays a crucial role in regulating fruit size by controlling cell wall expansion in Physaleae ( Wang et al., 2022 ). In P. floridana , the Cell Number Regulator 1 (CNR1) gene encodes a cell membrane-anchored modulator that negatively regulates fruit size through its interaction with an AGAMOUS-like ovary identity protein (PfAG2) ( Li and He, 2015 ).…”

Comparative Transcriptome Analysis Identified Genes Associated with Fruit Size in Pepper (Capsicum annuum L.)

“…Similarly, Chunthawodtiporn et al identified candidate genes (Big Brother, Ovate, and KLUH/CYP78A5) in chromosomes 1, 2, and 3 of pepper that control the fruit shape [37]. CaPOS1 in pepper, a direct homolog of trichomes POS1, has been shown to control fruit size, and this function is achieved by positively regulating cell size [38]. However, fewer genes have been identified in pepper than in other crops to control fruit size, and there are many genes whose functions have been shown in other crops but have yet to be reported in pepper, as well as there being no transparent molecular regulatory network.…”