Genome-Wide Identification and Analysis of Fruit Expression Patterns of the TCP Gene Family in Three Genera of Juglandaceae

TL;DR

This study identifies and analyzes TCP genes in three nut-producing tree species, revealing their roles in fruit development and offering insights for improving nut quality and resilience.

Contribution

The study provides the first genome-wide analysis of TCP genes in Juglandaceae species, highlighting their evolutionary patterns and potential roles in fruit development.

Findings

TCP genes, especially the CIN subfamily, show high activity in fruit tissues and may regulate fruit structure and maturation.

Synteny and gene duplication events suggest evolutionary conservation and functional divergence of TCP genes across species.

Specific genes like AsTCP23, CiTCP14, and JrTCP09 are highly expressed during fruit development, indicating their importance in fruit quality.

Abstract

Nut-producing trees such as pecan, beaked walnut, and walnut are valued for their high nutritional quality, but the genetic basis of their fruit development is still not well understood. Genes known as TCP genes play key roles in controlling plant growth, development, and responses to the environment. In this study, we carefully searched the entire genomes of pecan, beaked walnut, and walnut and identified the members of the TCP gene family in each species. We then examined their characteristics, positions on chromosomes, evolutionary relationships, and activity during fruit growth. Our results showed that many TCP genes are active in fruits, especially a group called the CIN type, which may be particularly important for shaping fruit structure and supporting fruit maturation. We also confirmed that some specific genes in each species are strongly expressed when the fruits are developing, suggesting they could be crucial for determining fruit quality. This research improves our understanding of how nut fruits develop at the genetic level and provides useful information that may support future breeding efforts to produce nut varieties with better yield, quality, and resilience to environmental stress.

The TCP gene family plays essential roles in plant growth, development, and stress responses, yet their evolutionary dynamics and functional characteristics remain poorly understood in Juglandaceae species. Here, we aimed to systematically identify, classify, and characterize TCP genes across three nut-producing Juglandaceae species—Carya illinoinensis, Annamocarya sinensis, and Juglans regia—to elucidate their evolutionary relationships and potential functions in fruit development. We identified 44, 35, and 36 TCP genes in C. illinoinensis, A. sinensis, and J. regia, respectively, and classified them into three subfamilies (PCF, CIN, and CYC/TB1). Physicochemical property analysis revealed that most proteins were hydrophilic but relatively unstable. Conserved motif and gene structure analyses showed strong similarity among closely related members, while promoter regions were enriched with cis-acting elements associated with development, hormone signaling, and stress responses. Chromosomal mapping demonstrated an uneven distribution of TCP genes, with frequent clustering, and synteny analysis indicated strong conservation and gene duplication within and across species. Transcriptome profiling revealed that approximately half of the TCP genes were expressed in fruit tissues, with CIN subfamily members showing preferential expression. qRT-PCR validation further highlighted AsTCP23, CiTCP14, and JrTCP09 as highly expressed during fruit development, suggesting potential regulatory roles in fruit maturation. These findings provide new insights into the evolutionary patterns and functional divergence of TCP genes in Juglandaceae and establish a valuable foundation for future studies on fruit development and genetic improvement. Collectively, these findings advance our understanding of TCP gene evolution and provide potential molecular targets for improving fruit development and nut quality in Juglandaceae crops.

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