TEMPRANILLO Reveals the Mesophyll as Crucial for Epidermal Trichome Formation

Abstract

Plant trichomes are defensive specialized epidermal cells. In all accepted models, the epidermis is the layer involved in trichome formation, a process controlled by gibberellins (GAs) in Arabidopsis rosette leaves. Indeed, GA activates a genetic cascade in the epidermis for trichome initiation. Here we report that TEMPRANILLO (TEM) genes negatively control trichome initiation not only from the epidermis but also from the leaf layer underneath the epidermis, the mesophyll. Plants over-expressing or reducing TEM specifically in the mesophyll, display lower or higher trichome numbers, respectively. We surprisingly found that fluorescently labeled GA 3 accumulates exclusively in the mesophyll of leaves, but not in the epidermis, and that TEM reduces its accumulation and the expression of several newly identified GA transporters. This strongly suggests that TEM plays an essential role, not only in GA biosynthesis, but also in regulating GA distribution in the mesophyll, which in turn directs epidermal trichome formation. Moreover, we show that TEM also acts as a link between GA and cytokinin signaling in the epidermis by negatively regulating downstream genes of both trichome formation pathways. Overall, these results call for a reevaluation of the present theories of trichome formation as they reveal mesophyll essential during epidermal trichome initiation.

TEMPRANILLO is a direct repressor of the microRNA miR172

“…Under this condition, 35S::TEM1 plants also showed a substantially long juvenile phase, an unexpectedly short adult phase (Figures i,j and S1k,l, Table S2i,j) and flowered later than the wild‐type (Figures i,j and S2k,l, Table S3i,j). Most 35S::TEM1 plants did not produce leaves with abaxial trichomes, probably due to the fact that these plants, in addition to having a late juvenile‐to‐adult transition, produce very few leaf trichomes (Matías‐Hernández et al ., ). Due to the similar results obtained with all genotypes under both photoperiods we therefore used LD conditions for all subsequent experiments.…”

“…Unexpectedly, when TEM1 is overexpressed, instead of an extension of the adult phase we observed a dramatic lengthening of the juvenile phase under both LDs and SDs, together with an extreme shortening or even suppression of the adult phase under LDs (Figure 1i,j). However, 35S:: TEM1 plants show a dramatically reduced trichome density (Mat ıas-Hern andez et al, 2016). Therefore, it is possible that the alteration of the number of leaves without and with abaxial trichomes in these plants is a combination of the effects on the juvenile-to-adult transition and on trichome density.…”

Brassica napusGLABRA3‐1 promotes anthocyanin biosynthesis and trichome formation in true leaves when expressed in Arabidopsis thaliana

“…), while AtTEM2 represses trichome formation (Matias‐Hernandez et al . ), and the loss of AtCML42 expression results in trichomes with abnormal structures and increased branching (Dobney et al . ).…”

Trichome Formation: Gibberellins on the Move

“…In this issue, Matías-Hernández et al (2016) reported that two transcription factors, TEMPRANILLO1 (TEM1) and TEM2, inhibit trichome initiation from the underneath layer of the epidermis, the mesophyll. Matías-Hernández et al (2016) found that TEM genes expressed in the mesophyll cells can still affect epidermal trichome formation, suggesting the existence of a non-cell-autonomous regulation. Surprisingly, bioactive fluorescently labeled GA 3 , which was applied on top of leaves, accumulated exclusively in the mesophyll cells, but not in the epidermis, suggesting that the distribution of GA is under active regulation.…”

“…Indeed, TEMs suppress the expression of these newly identified GA transporters, and also suppress GA biosynthesis, to regulate GA distribution (Matías-Hernández et al, 2016). In fact, TEMs can reduce the mesophyll-specific accumulation of fluorescently labeled GA 3 .…”