HOMEODOMAIN PROTEIN 1 is required for jasmonate‐mediated glandular trichome initiation in Artemisia annua

Abstract

Glandular trichomes are generally considered biofactories that produce valuable chemicals. Increasing glandular trichome density is a very suitable way to improve the productivity of these valuable metabolites, but little is known about the regulation of glandular trichome formation. Phytohormone jasmonate (JA) promotes glandular trichome initiation in various plants, but its mechanism is also unknown. By searching transcription factors regulated by JA in Artemisia annua, we identified a novel homeodomain-leucine zipper transcription factor, HOMEODOMAIN PROTEIN 1 (AaHD1), which positively controls both glandular and nonglandular trichome initiations. Overexpression of AaHD1 in A. annua significantly increased glandular trichome density without harming plant growth. Consequently, the artemisinin content was improved. AaHD1 interacts with A. annua jasmonate ZIM-domain 8 (AaJAZ8), which is a repressor of JA, thereby resulting in decreased transcriptional activity. AaHD1 knockdown lines show decreased sensitivity to JA on glandular trichome initiation, which indicates that AaHD1 plays an important role in JA-mediated glandular trichome initiation. We identified a new transcription factor that promotes A. annua glandular trichome initiation and revealed a novel molecular mechanism by which a homeodomain protein transduces JA signal to promote glandular trichome initiation. Our results also suggested a connection between glandular and nonglandular trichome formations.

Transcriptome Analysis of Genes Associated with the Artemisinin Biosynthesis by Jasmonic Acid Treatment under the Light in Artemisia annua

“…In recent years, there have been characterized several TFs which could directly bind to the promoters of the aretmisinin biosynthetic genes and regulate the artemisinin content in A. annua (Ma et al, 2009; Yu et al, 2012; Lu et al, 2013a; Shen et al, 2016). Furthermore, a novel TF, AaHD1 (HOMEODOMAIN PROTEIN 1), which belongs to the homeodomain-leucine zipper TF family was identified by our lab (Yan et al, 2016). The AaHD1 played an important role in promoting the JA-mediated glandular trichome initiation and thus improved the artemisinin content in A. annua (Yan et al, 2016).…”

“…Furthermore, a novel TF, AaHD1 (HOMEODOMAIN PROTEIN 1), which belongs to the homeodomain-leucine zipper TF family was identified by our lab (Yan et al, 2016). The AaHD1 played an important role in promoting the JA-mediated glandular trichome initiation and thus improved the artemisinin content in A. annua (Yan et al, 2016). For the ABA signaling to artemisinin accumulation in A. annua , the AabZIP1, a basic leucine zipper TF, was identified to activate the expression of AaADS and AaCYP71AV1 and promote artemisinin biosynthesis (Zhang et al, 2015).…”

“…The HD-ZIP TFs contain a homedomain with a leucine zipper motif and can be classified into four subfamilies (Ariel et al, 2007). AaHD1 belongs to the HD-ZIP IV subfamily and could promote glandular trichome initiation and improve the artemisinin content (Yan et al, 2016). In our study, the family of HD-ZIP, LSD and E2F/DP contains 39, 6 and 8 proteins, respectively, it is necessary to further analyze their function in A. annua .…”

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

“…In this respect, some phytohormones, especially jasmonate (JA) and possibly GAs, elicit glandular trichome development via signaling cascades and the activation of trichome-specific transcriptional regulators (Li et al, 2004;Koo and Howe, 2009;Bose et al, 2013;Bosch et al, 2014;Tian et al, 2014;Liu et al, 2017;Yan et al, 2017). In Mentha arvensis, exogenous application of GA resulted in a moderate increase in trichome density and diameter of the gland, suggesting a positive, although moderate, effect of GA on trichome initiation and development in mint (Bose et al, 2013).…”

The roles of AaMIXTA1 in regulating the initiation of glandular trichomes and cuticle biosynthesis in Artemisia annua

“…Increasing GST density could therefore be an effective approach to improve the artemisinin content. The previously characterized homeodomain regulator, AaHD1, also promotes glandular trichome initiation (Yan et al ., ) although the mechanism by which it regulates development of those trichomes has not yet been fully explored. In another recent study, overexpression of AaMYB1 was used to increase artemisinin content and like AaMIXTA1 this was through increasing the density of GSTs (Matias‐Hernandez et al ., ).…”