Genome-Wide Identification of the TCP Gene Family in Tetraploid Potato and Analysis of Their Potential Roles in Tuber Development

Abstract

Potato tuber formation is a complex developmental process regulated by coordinated interactions among multiple phytohormones and genes. TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) transcription factors play important roles in plant growth, development and responses to environmental stimuli; however, their specific functions in tuber development in tetraploid potato remain poorly understood. In this study, we performed genome-wide identification and systematic characterization of the TCP gene family in tetraploid potato, integrated transcriptome profiling, quantitative real-time PCR (qRT-PCR), protein–protein interaction prediction and weighted gene co-expression network analysis (WGCNA) to identify candidate genes potentially associated with tuber development. A total of 57 StTCP genes were identified across 29 chromosomes and classified into eight subfamilies. Members within the same subfamily generally shared similar gene structures, conserved motifs and protein domains, whereas their promoter regions contained abundant cis-acting elements associated with light and phytohormone responses, growth and development, and stress responses. Expression profiling revealed distinct StTCP expression patterns under temperature stress and across tuber developmental stages. Eight StTCP genes exhibited pronounced stage-specific expression across the four developmental stages, and their expression trends were broadly supported by quantitative real-time PCR (qRT-PCR). In particular, StTCP42, StTCP55, and StTCP57 showed significantly higher expression at the stolon hook stage than at the other stages (p < 0.05), whereas StTCP20 was significantly upregulated at the subapical swelling stage (p < 0.05). Weighted gene co-expression network analysis (WGCNA) of RNA-seq data from the four developmental stages identified 27 co-expression modules. The turquoise, dark red, pink, and green modules were significantly and positively associated with the stolon hook, subapical swelling, initial tuber formation, and tuber formation stages, respectively; the turquoise module showed the strongest positive correlation with the stolon hook stage (r = 0.997, false discovery rate (FDR) = 2.77 × 10−10). Notably, StTCP42 and StTCP57 were both highly expressed at the stolon hook stage and were assigned to the turquoise module. StTCP42 further exhibited high module membership (kME = 0.930) and gene significance (GS = 0.937, p = 6.79 × 10−6), providing convergent evidence for its association with early tuber development by the transcriptomic, qRT-PCR, and co-expression evidence. This study systematically characterised the TCP gene family in tetraploid potato and identified several candidate genes potentially associated with tuber development, particularly StTCP42 and StTCP57. These findings provide a foundation for future functional studies aimed at elucidating the roles of TCP transcription factors in potato tuber formation and development.