Glandular trichome heads confer cadmium tolerance in Nicotiana tabacum L. via the co-regulation of JA and ABA signaling

Cadmium (Cd) is a highly toxic heavy metal (HV) that poses significant threats to plant growth and development. Plant trichomes serve as critical sequestration organs for HVs; however, the different roles of glandular trichomes (GTs) and non-glandular trichomes (NGTs) in the process of detoxification remain elusive. In this study, two interacting proteins (NtHD9 and NtJAZ10) with opposite effects on glandular head formation in GTs were individually targeted for knockout in Nicotiana tabacum cv. K326: NtJAZ10 mutants (LK326) had dominant longstalk glandular trichomes (LGTs), whereas NtHD9 mutants (NK326) had dominant NGTs. Phytohormone content measurements and subsequent hormone supplementation assays in LK326 and NK326 suggested that the NtJAZ10-NtHD9 module regulated LGT head formation via jasmonate signaling. Both LGTs and NGTs were Cd sequestration sites, but showed different Cd detoxification mechanisms; NGTs compartmentalized Cd in the vacuole, whereas LGTs promoted the cytosol-to-cell wall translocation of Cd, facilitating Cd excretion. LK326 further exhibited strong Cd stress tolerance, which was confirmed by elevated abscisic acid (ABA) levels, strengthened antioxidant systems, and heightened photosynthetic abilities. To understand the molecular mechanisms underlying Cd detoxification in trichomes, LK326 and NK326 trichomes were used for comparative RNA sequencing analysis, which revealed 18 genes that may be involved in Cd absorption and transport. Our findings suggest that JAZ10 is an ideal candidate gene for enhancing Cd stress tolerance by promoting the development of LGT glandular heads and increasing ABA levels in plants. These findings provide novel insights into improving Cd tolerance in plants and exploring the mechanism of trichome-mediated Cd detoxification.