# Multi-omics analysis of somatic mutants reveals TCP7 allelically regulates multiple carotenogenic genes in citrus

## TL;DR

This study identifies TCP7 as a key regulator of carotenoid-related genes in citrus fruits, explaining color variation in pomelo varieties.

## Contribution

The study reveals TCP7 as a novel allelic regulator of multiple carotenogenic genes in citrus through multi-omics analysis.

## Key findings

- TCP transcription factors are enriched in chromatin open regions associated with fruit color mutants.
- CgTCP7 is under positive selection and differentially regulates carotenoid accumulation in pomelo.
- TCP7 alleles modulate expression of key carotenogenic genes like ZDS, BCH, and NCED2.

## Abstract

Somatic mutations are widespread in all organisms and cause abundant phenotypic changes, constituting an important source of variation especially for clonally propagated plants. Somatic mutants can serve as a mutation-introducing method for exploring the regulatory mechanism of mutated trait formation in clonally propagated plants. Red-fleshed and orange-fleshed pomelo varieties derive from independent mutations of the wild-type white-fleshed Guanxi honey pomelo (Citrus grandis), offering an ideal system for dissecting core regulatory transcription factors behind the fruit color trait. Here, we performed a meta-analysis comprising genome, transcriptome, DNA methylome and chromatin accessibility assays of the two color mutants and their wild type, resulting in haplotype-scaled pan-genome. The chromatin openness analysis suggested that binding sites for TEOSINTE BRANCHED 1/CYCLOIDEA/PCF (TCP) transcription factors are significantly enriched in the differentially open regions, with different footprint patterns in the mutants and wild type. We identified CgTCP3, CgTCP7, and CgTCP20 as regulators of key carotenogenic genes including ZDS, BCH, and NCED2. Furthermore, CgTCP7 underwent positive selection in pomelo germplasm, with various alleles differentially affecting carotenogenic gene expression and modulating carotenoid accumulation. We therefore identified the core transcription factor genes responsible for color trait formation, providing resources for breeding varieties with diversified phenotypes.

The online version contains supplementary material available at 10.1186/s43897-025-00193-9.