Arabidopsis thalianazinc accumulation in leaf trichomes is correlated with zinc concentration in leaves

Abstract

Zinc (Zn) is a key micronutrient. In humans, Zn deficiency is a common nutritional disorder, and most people acquire dietary Zn from eating plants. In plants, Zn deficiency can decrease plant growth and yield. Understanding Zn homeostasis in plants can improve agriculture and human health. While root Zn transporters in plat model species have been characterized in detail, comparatively little is known about shoot processes controlling Zn concentrations and spatial distribution. Previous work showed that Zn hyperaccumulator species such as Arabidopsis halleri accumulate Zn and other metals in leaf trichomes. The model species Arabidopsis thaliana is a non-accumulating plant, and to date there is no systematic study regarding Zn accumulation in A. thaliana trichomes. Here, we used Synchrotron X-Ray Fluorescence mapping to show that Zn accumulates at the base of trichomes of A. thaliana, as had seen previously for hyperaccumulators. Using transgenic and natural accessions of A. thaliana that vary in bulk leaf Zn concentration, we demonstrated that higher leaf Zn increases total Zn found at the base of trichome cells. Furthermore, our data suggests that Zn accumulates in the trichome apoplast, likely associated with the cell wall. Our data indicates that Zn accumulation in trichomes is a function of the Zn status of the plant, and provides the basis for future studies on a genetically tractable plant species aiming at understanding the molecular steps involved in Zn spatial distribution in leaves.

Interplay of EXO70 and MLO proteins modulates trichome cell wall composition and powdery mildew susceptibility

“…A. thaliana trichomes contain two distinct PM domains, with EXO70H4 and specific phospholipids being enriched in the apical one (Kubátová et al, 2019). We, thus, believe that the basal localization of zinc in trichomes as described before (Ricachenevsky et al, 2021;Kulich et al, 2015) represents part of the basal domain defined by the absence of EXO70H4 and the presence of EXO70A1 (Kulich et al, 2018;Kubátová et al, 2019). Our HM staining experiments as well as EXO70H4 localization data further support this notion.…”

“…A. thaliana trichomes contain two distinct PM domains, with EXO70H4 and specific phospholipids being enriched in the apical one (Kubátová et al, 2019). We, thus, believe that the basal localization of zinc in trichomes as described before (Ricachenevsky et al, 2021;Kulich et al, 2015) . CC-BY-NC-ND 4.0 International license perpetuity.…”

“…The zinc ZIP transporters are highly expressed in trichomes (Jakoby et al, 2008), and a copper transporter (COPT5, At5g20650) was found to be the most enriched protein in a comprehensive trichome proteome analysis (Huebbers et al, 2022). Recent studies reported that zinc accumulates at the basal part of the trichome (Kulich et al, 2015; Ricachenevsky et al, 2021), roughly corresponding to the region of the OR. Therefore, zinc and other heavy metal transporters can be considered additional candidates for the EXO70H4-MLO secretory pathway.…”

The overlooked functions of trichomes: Water absorption and metal detoxication

“…We have identified 37 studies examining metal accumulation in trichomes (Table 2). These studies have been conducted for a wide range of purposes, including for examining plant metal tolerance and detoxication mechanisms (Choi et al, 2001; Čiamporová et al, 2021; Iwasaki & Matsumura, 1999), observing metal distribution in plant leaves (Ager et al, 2003; Lei et al, 2008) and for examining the specific roles of trichomes in plant metal hyperaccumulation (W. Li et al, 2005; Mcnear & Kupper, 2014; Ricachenevsky et al, 2021). In addition, a variety of analytical approaches have been used to investigate the accumulation of metals in the trichomes, including scanning electron microscopy coupled with energy dispersive spectroscopy (SEM‐EDS), synchrotron‐based X‐ray fluorescence microspectroscopy (XFM), nuclear microprobe analysis and confocal microscopy with specific fluorescence dyes (Ager et al, 2003; Broadhurst, Chaney, Angle, Erbe, et al, 2004; Kozhevnikova et al, 2014).…”

Functional aspects of solanaceae trichomes in heavy metal detoxification

“…This is an effective exclusion mechanism adopted by plants to avoid interference of metals in metabolic activities of the mesophyll cells. Moreover, Zn accumulation in the trichome apoplast is associated with the cell wall (Ricachenevsky et al 2020). Similar sequestration of metals in trichomes are reported from Brassica juncea for Cd (Salt et al 1995), Helianthus annus for Zn (Li et al 2019) and Alyssum lesbiacum for Ni (Krämer et al 1997).…”