The dual role of GoPGF reveals that the pigment glands are synthetic sites of gossypol in aerial parts of cotton

Abstract

Summary Gossypol and the related terpenoids are stored in the pigment gland to protect cotton plants from biotic stresses, but little is known about the synthetic sites of these metabolites. Here, we showed that GoPGF, a key gene regulating gland formation, was expressed in gland cells and roots. The chromatin immunoprecipitation sequencing (ChIP‐seq) analysis demonstrated that GoPGF targets GhJUB1 to regulate gland morphogenesis. RNA‐sequencing (RNA‐seq) showed high accumulation of gossypol biosynthetic genes in gland cells. Moreover, integrated analysis of the ChIP‐seq and RNA‐seq data revealed that GoPGF binds to the promoter of several gossypol biosynthetic genes. The cotton callus overexpressing GoPGF had dramatically increased the gossypol levels, indicating that GoPGF can directly activate the biosynthesis of gossypol. In addition, the gopgf mutant analysis revealed the existence of both GoPGF‐dependent and ‐independent regulation of gossypol production in cotton roots. Our study revealed that the pigment glands are synthetic sites of gossypol in aerial parts of cotton and that GoPGF plays a dual role in regulating gland morphogenesis and gossypol biosynthesis. The study provides new insights for exploring the complex relationship between glands and the metabolites they store in cotton and other plant species.

GhHAM regulates GoPGF‐dependent gland development and contributes to broad‐spectrum pest resistance in cotton

“…To analyze the relationship between GhHAM and GoPGF, we measured the expression of GhHAM and GoPGF in both gopgf (Zhang et al., 2024) and ghham mutants. As shown in Figure 4, the expression of GoPGF in the leaves, stems, and carpel walls of the gopgf mutants was dramatically reduced compared to the WT, possibly due to the lack of gland structure in gopgf .…”

“…Previous studies have suggested that terpenoids can inhibit the growth of pathogens and pests (Gao et al., 2013; Sharma et al., 2017; Tian et al., 2015). The presence of a large amount of terpenoids strongly suggests that terpenoid‐synthesizing glands in plants are evolutionarily considered an effective defense mechanism against adverse environments (Cheng et al., 2007; Zhang et al., 2024). In cotton breeding, the gossypol content is often evaluated as an indicator of the cotton's ability to defend itself against pests, although the specific role of the pigment glands remains to be fully understood.…”

“…GoPGF encodes a bHLH transcription factor, and the substitution of Ala to Val at residue 43 of GoPGF results in the dominant Gl 2 e allele. The gopgf mutants produced through CRISPR system also exhibit a whole‐plant glandless phenotype (Li et al., 2021; Zhang et al., 2024). The characterization of GoPGF has provided important insights into the molecular mechanisms underlying gland initiation.…”

“…Zhang et al. (2024) utilized chromatin immunoprecipitation sequencing (ChIP‐seq) to screen downstream targets of GoPGF, discovering that GoPGF directly activates the expression of GhJUB1 . Silencing GhJUB1 significantly reduces gland density and gossypol content, revealing the significant role of GoPGF‐GhJUB1 module in gland formation and terpene production.…”

Molecular regulation of oil gland development and biosynthesis of essential oils in Citrus spp.

“…Notably, the MpERF13 gene is required for oil body formation and terpenoid biosynthesis in M. polymorpha ( 36 ). Overall, CsMYC5 plays a role in promoting a secondary metabolism similar to that of its closest cotton homolog GoPGF, but its involvement in gland development was restricted to later stages unlike GoPGF, which controls the initiation of glandular trichomes ( 37 , 38 ). This observation suggests that distinct developmental programs are involved in governing secretory cavity formation and glandular trichome initiation.…”