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The plant leaf epidermis constitutes a critical interface with the environment and consists of a single layer comprising three cell types: stomata, trichomes, and pavement cells. Stomata are pores that regulate gas exchange and transpiration. Trichomes are hair-like cells that can secrete metabolites and that protect against UV light, insects, and temperature variation. Pavement cells are unspecialized cells that ensure stomata and trichomes are optimally distributed.
The mechanisms giving rise to epidermal cell types have been well studied in Arabidopsis (Arabidopsis thaliana), but our understanding in other species is limited. To address this knowledge gap, Galdon-Armero and colleagues (2020) exploited the natural variation of leaf epidermis structure between domesticated tomato (Solanum lycopersicum cv M82) and its wild relative, the green-fruited Solanum pennellii accession LA716. They used introgression lines (ILs) that were obtained by repeated crossing of M82 with LA716. Each IL carries a single and distinct homozygous chromosomal fragment from LA716 in an otherwise M82 background (Eshed and Zamir, 1995). The ILs have been extensively curated, mapped by RNA sequencing (Chitwood et al., 2013), and used to identify quantitative trait loci underlying such key traits as pathogen resistance, abiotic stress, metabolism, and secreted metabolites.
Galdon-Armero and colleagues (2020) screened the first fully expanded leaf of each IL by scanning electron microscopy to obtain high-resolution images of the epidermis structure (see figure). Manual examination and quantification of this large data set led the team to identify novel quantitative trait loci underlying trichome and stomata density, trichome type distribution and morphology, but not stomatal density, suggesting that natural variation may be relatively unimportant in determining this trait.
The Transcription Factor SlMixta-like Is a Negative Regulator of Trichome Spacing in Tomato.
Trichome spacing along the leaf epidermis is actively controlled by both positive and negative factors to ensure optimal distribution (left). Natural variation (top right) and virus-induced gene silencing (VIGS)-mediated silencing analyses (bottom right) revealed that the tomato MYB transcription factor SlMixta-like is a negative regulator of trichome formation. (Adapted from Galdon-Armero et al. [2020], Figures 4 to 6.)
In two ILs, trichomes were unusually distributed in clusters of up to four trichomes (see figure). These ILs contained overlapping fragments of chromosome 2 from LA716. Searching for genes related to trichome development in this interval, Galdon-Armero and colleagues (2020) identified the transcription factor SlMixta-like, which belongs to a family of MYB transcription factors associated with petal and fruit epidermal differentiation. Gain- and loss-of function experiments further confirmed that SlMixta-like acts as a repressor of trichome formation in M82 (see figure), although Mixta-like transcription factors typically function as positive regulators (Lashbrooke et al., 2015). Furthermore, the authors identified a short motif in the 5′ untranslated region of the SlMixta-like M82 allele that is missing from the LA716 allele. This motif may underlie the relatively higher expression of the transcription factor in leaves of M82 compared with that of the ILs harboring the allele from LA716. Thus, Galdon-Armero and colleagues (2020) identified a novel negative regulator of trichome formation in tomato and provide a valuable image-based resource to further unravel factors underlying natural variation in plant epidermal structure.
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