AaPDF2 promotes glandular trichome formation in Artemisia annua through jasmonic acid signaling

Abstract

Artemisia annua L., recognized as the sole plant species possessing the biosynthetic capacity to produce the antimalarial agent artemisinin, exhibits considerable medicinal importance. Biosynthetic production and storage of this sesquiterpene lactone occur exclusively within the glandular secretory trichomes (GSTs) of A. annua specimens. Therefore, investigating the developmental mechanisms of GSTs holds significant promise for enhancing both the artemisinin production and GST density. Although several regulators, such as AaHD1 and AaHD8, have been identified, the mechanism of multicellular glandular trichomes formation remains unclear. This study revealed the homeodomain leucine zipper (HD-ZIP IV) transcription factor AaPDF2, which promoted GST density. Meanwhile, AaPDF2 is induced by jasmonic acid and predominantly expressed in GSTs. Overexpression of AaPDF2 enhanced GST density and artemisinin production, in contrast to the reductions caused by RNAi silencing. Furthermore, AaPDF2 was positively regulated by AaHD1, and AaGSW2 acted downstream of AaPDF2. Furthermore, AaPDF2 engages in reciprocal inhibition with AaMYB5, a suppressor of glandular trichome development. Collectively, these findings establish AaPDF2 as a jasmonic acid-responsive activation factor that triggers GST morphogenesis in A. annua. This study elucidates the molecular basis of GST morphogenesis regulation mediated by the AaHD1-AaPDF2-AaGSW2 module in A. annua. Furthermore, this study clarifies the distinct roles of three HD-ZIP IV family members (AaHD8, AaHD1, and AaPDF2) in GST development, thereby refining and enriching the regulatory network underlying GST formation in A. annua. These findings provide a crucial theoretical foundation for germplasm innovation and cultivar improvement in this medicinal plant.