Cell elongation and altered phytohormone levels play a role in establishing distyly in Averrhoa carambola

• Published in: Gene 2025-03, Vol.939, p.149167, Article 149167
• Main Authors: Lin, Wubaiyu, Qin, Si, Chen, Siyu, Xu, Lianhuan, Yang, Zirui, Lin, Xinyun, Zhai, Junwen, Ren, Hui, Zhang, Zehuang, Wu, Shasha
• Format: Article
• Language: English
• Subjects: Averrhoa carambola; Distyly; Heterostyly; Plant hormones; Transcriptome analysis
• ISSN: 0378-1119; 1879-0038; 1879-0038
• DOI: 10.1016/j.gene.2024.149167

•Difference in cell elongation is the main cause of the reciprocal herkogamy in the distyly of Averrhoa carambola.•Auxin and brassinolide influence pistil elongation, while gibberellin promotes both pistil and stamen elongation.•Hormone-related genes and cell development pattern-related genes promote distyly formation.•The homologs of the S-locus genes do not show hemizygous inheritance in Averrhoa carambola.•Four candidate genes possess conserved motifs characteristic of their respective families. The flowers of distylous plants exhibit two distinct morphologies that facilitate precise pollen transfer. Averrhoa carambola, a woody plant characterized by distyly, has an unclear molecular regulatory mechanism underlying this trait. Its prolonged flowering period and substantial flower production render it an excellent model for investigating the distylous syndrome. This study aims to elucidate the mechanism of distyly in A. carambola and to identify the regulatory genes. The long-style cultivar ‘Daguo Tianyangtao 1′ and the short-style cultivar ‘Daguo Tianyangtao 3′ were selected as models for this investigation. We examined phenotypic characteristics, anatomical structures, and endogenous hormone content associated with distyly. Transcriptomic data were utilized to pinpoint candidate genes involved in the regulation of distyly, followed by a bioinformatics analysis these genes. The results indicate that variations in cell elongation contribute to the differential heights of stigmas and anthers in A. carambola, thereby resulting in the distylous syndrome. Auxins, Gibberellin A3 (GA3), Gibberellin A4 (GA4), and brassinolide (BL) were found to influence elongation of styles, whereas Gibberellin A1 (GA1) and GA4 affected filament elongation. Transcriptome sequencing analysis identified 34 hormone-related differentially expressed genes (DEGs) and 16 cell development-related DEGs in different morphs of pistils, and 29 hormone-related DEGs and 22 cell development-related DEGs were identified in different morphs of stamens. Four candidate genes—AcaBRU1, AcaPRE1, AcaXTH2, and AcaEXPA11—were found to possess conserved motifs characteristic of their respective families. Consequently, various plant hormones modulate the expression of response genes, leading to differences in elongation of style and filament cells between different flower types of A. carambola, thereby promoting the distylous syndrome. This study provides a theoretical basis for understanding the mechan