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, 21 (19), 5036-46

TRIPTYCHON and CAPRICE Mediate Lateral Inhibition During Trichome and Root Hair Patterning in Arabidopsis

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TRIPTYCHON and CAPRICE Mediate Lateral Inhibition During Trichome and Root Hair Patterning in Arabidopsis

S Schellmann et al. EMBO J.

Abstract

Trichome patterning in Arabidopsis is a model for the generation of a spacing pattern from initially equivalent cells. We show that the TRIPTYCHON gene that functions in lateral inhibition encodes a single-repeat MYB-related transcription factor that lacks a recognizable activation domain. It has high sequence similarity to the root hair patterning gene CAPRICE. Both genes are expressed in trichomes and act together during lateral inhibition. We further show that TRIPTYCHON and CAPRICE act redundantly in the position-dependent cell fate determination in the root epidermis. Thus, the same lateral inhibition mechanism seems to be involved in both de novo patterning and position-dependent cell determination. We propose a model explaining trichome and root hair patterning by a common mechanism.

Figures

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Fig. 1. Molecular characterization of the TRY gene. (A) Exon–intron structure of the TRY gene. The positions of mutations in the different try alleles are indicated. (B) Amino acid sequence comparison with the MYB-related proteins CPC, TRIPTYCHON HOMOLOG1 (TH1) and TRIPTYCHON HOMOLOG2 (TH2). (C) RT–PCR from total RNA extracts of different tissues. The minimal number of PCR cycles that allowed detection of TRY expression was used to enable a comparison of the expression levels between the tissues. RT–PCR amplification of ubiquitin was used as a control.
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Fig. 2. Overexpression phenotypes of 35S::TRY and 35S::CPC lines. (A) Rosette leaves of a try mutant plant rescued with the genomic 4.2 kb fragment. (B) Glabrous 35S::TRY plant. (C) Rosette leaves of a try mutant plant. (D) Scanning electron micrograph (SEM) of a 35S::GL1 cpc leaf trichome with two accessory cells transformed to trichomes. (E) Cotyledons of a 35S::GL1 cpc plant; many ectopic trichomes are formed. (F) SEM of a glabrous 35S::CPC leaf. (G) SEM of a 35S::CPC 35S::R-GR leaf after R gene induction with dexamethasone. Because in developing leaves only young cells at the base can respond to R gene-induced trichome induction, rescue is found only at the leaf base. (H) Inflorescence of a 35S::GL1 try cpc mutant plant. (I) Primary leaves of a 35S::GL1 try cpc mutant plant.
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Fig. 3. Expression analysis of TRY and CPC. (A) Young leaf of a TRY::GUS line showing ubiquitous expression. (B) Slightly older leaf of a TRY::GUS line. Ubiquitous expression is seen at the leaf base. Note that early developmental stages of trichome cells exhibit elevated expression levels. (C) Mature leaf of a TRY::GUS line. TRY expression is limited to mature trichome cells. (DIn situ hybridization of a wild-type leaf section with antisense TRY. Trichome cells display high expression of TRY. (E) Light microscopy micrograph of an in situ hybridization of a wild-type leaf section with antisense CPC. (F) Dark field micrograph of (E). (G) Young leaf of a CPC::GUS line showing ubiquitous expression. (H) Mature leaf of a CPC::GUS line; CPC expression is seen only in trichomes.
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Fig. 4. Comparison of trichome number in different mutants. (A and B) Trichome number counts on the fourth leaf at all developmental stages of leaf development. (C–G) Number of trichome initiation sites on the first leaf. (A) In wild-type (Ws-0), trichome number increases until the leaf reaches a length of 1 mm, after which trichome initiation ceases but leaf growth continues. (B) A cpc mutant. Compared with wild-type, cpc mutants produce more trichomes at all developmental stages. (C) Wild-type ecotype Ler. (D) Wild-type ecotype Ws-0. (E) A try mutant. (F) A cpc mutant. (G) A try cpc double mutant.
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Fig. 5. try cpc double mutant phenotype. (A) Rosette leaf of a try cpc double mutant plant showing trichome clusters. (B) Section through a try cpc trichome cluster. (C) SEMs of a large try cpc cluster. (D–H) SEMs of wax replicas of developing try cpc trichome clusters. (D) Overview of a young leaf. The square marks the initial stage of the developing trichome cluster shown below. Replicas of the developmental stages were taken at 8 h intervals. Note that the central trichome has been torn away. (E) One initial trichome has emerged from the epidermis. (F) At least three immediately neighbouring epidermal cells appear as bulges. (G) Additional neighbouring cells show trichome development. (H) Surrounding trichomes are elongated.
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Fig. 6. Analysis of root hair phenotypes. (A–G) Light microscopy micrographs of wild-type and mutant roots. (A) Wild-type. (B) A 35S::TRY root displaying extra root hairs. (C) A cpc mutant showing fewer root hairs. (D) A try cpc double mutant devoid of root hairs. (E) TRY:GUS expression in a cpc try background. (F) TRY:GUS expression in 35S:RGR induced roots. (G) TRY:GUS expression in 35S:RGR uninduced roots; expression is found in the tip region of the root. (H) Semi-quantitative RT–PCR of TRY and CPC. Note that CPC expression can be detected ∼5 amplification cycles earlier than TRY.
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Fig. 7. Genetic model of trichome and root hair patterning. It is postulated that both trichome (left) and root hair patterning (right) are based on a competition mechanism mediated by TRY and CPC. In both systems, this competition results in the activation of a set of positive regulators consisting of TTG1, and a MYB-related (GL1 or WER) and a bHLH-related (GL3 or an unknown factor in root hairs) transcription factor. The biased decision in the root system with respect to the underlying cortex cells is explained by a positive signal from the cortex cells (arrows) which is slightly weaker in epidermal cells overlying a cleft. For clarity, only those regulation events are indicated here that are immediately relevant for the proposed model. These activate the GL2 gene which in the leaf epidermis triggers trichome formation and in the root epidermis promotes non-root hair fate.

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