Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106

Abstract

Leaf hairs (trichomes) of Arabidopsis (Arabidopsis thaliana) have been extensively used as a model to address general questions in cell and developmental biology. Here, we lay the foundation for a systems-level understanding of the biology of this model cell type by performing genome-wide gene expression analyses. We have identified 3,231 genes that are up-regulated in mature trichomes relative to leaves without trichomes, and we compared wild-type trichomes with two mutants, glabra3 and triptychon, that affect trichome morphology and physiology in contrasting ways. We found that cell wall-related transcripts were particularly overrepresented in trichomes, consistent with their highly elaborated structure. In addition, trichome expression maps revealed high activities of anthocyanin, flavonoid, and glucosinolate pathways, indicative of the roles of trichomes in the biosynthesis of secondary compounds and defense. Interspecies comparisons revealed that Arabidopsis trichomes share many expressed genes with cotton (Gossypium hirsutum) fibers, making them an attractive model to study industrially important fibers. In addition to identifying physiological processes involved in the development of a specific cell type, we also demonstrated the utility of transcript profiling for identifying and analyzing regulatory gene function. One of the genes that are differentially expressed in fibers is the MYB transcription factor GhMYB25. A combination of transcript profiling and map-based cloning revealed that the NOECK gene of Arabidopsis encodes AtMYB106, a MIXTA-like transcription factor and homolog of cotton GhMYB25. However, in contrast to Antirrhinum, in which MIXTA promotes epidermal cell outgrowth, AtMYB106 appears to function as a repressor of cell outgrowth in Arabidopsis.

Figure 1.

GO analysis of genes that are 2-fold more highly expressed in trichomes than in leaves without trichomes. The size of a node within the network is proportional to the number of genes in the respective GO category. The level of significance of an overrepresented GO category is indicated by the shift from yellow to orange, corresponding to a P value from 5.00E-2 to <5.00E-7. Statistical testing was as described by Maere et al. (2005). [See online article for color version of this figure.]

Figure 2.

Comparison of expression profiles between trichomes and atrichoblasts. A, GO analysis of genes expressed in both trichomes and atrichoblasts. For annotation, see Figure 1. B, Venn diagram showing the overlap of expression of genes in trichomes and different cell types of the root. Please note that the overlap between the different root cell types cannot be presented here. [See online article for color version of this figure.]

Figure 3.

GUS staining of promoter reporter lines of identified trichome-specific genes. A fusion of the promoter of a putative protein kinase (At1g66460) to GUS showed expression in trichomes (A) and patches of epidermal cells at the root tip (C). Expression of a PRO_WRKY8:GUS fusion was detected in trichomes (B) and the vascular tissue of the root (D).

Figure 4.

Phenotypic characterization and cloning of the NOK gene. In the nok-gb mutant (B), the number of trichome branches is increased in comparison with the Col-0 wild type (A). The papillae normally seen on the surface of the wild-type trichomes (C) are completely missing in the nok-gb mutant (D). Bars = 50 μm. NOK was mapped to the upper arm of chromosome 3 (E), distal to marker F4P13. The numbers given for the markers indicate the amount of recombinant chromosomes. Four alleles of nok were isolated, and the positions of the mutations are indicated (F). In addition to the general staining of emerging leaves and mature trichomes (G), GUS activity was also found in carpels, petals, and stamens of a PRO_MYB106:GUS fusion (H).