The loss-of-function GLABROUS 3 mutation in cucumber is due to LTR-retrotransposon insertion in a class IV HD-ZIP transcription factor gene CsGL3 that is epistatic over CsGL1.

Yupeng Pan,Zhihui Cheng,Yiqun Weng,Kailiang Bo

doi:10.1186/s12870-015-0693-0

Abstract

BackgroundTrichomes, developed from the protodermal cells (the outermost cell layer of the embryo), are hair-like structures covering the aerial parts of plants. The genetic network regulating trichome development has been extensively studied and well understood in the model species Arabidopsis thaliana, which bears unicellular, non-glandular and branched trichomes. However, little is known about the genetic and molecular basis of organogenesis of multi-cellular trichomes in plant species like cucumber (Cucumis sativus L.), which are likely different from Arabidopsis.ResultsWe identified a new trichome mutant in cucumber which exhibited a completely glabrous phenotype on all aerial organs. Genetic analysis indicated that the glabrous phenotype was inherited as a single recessive gene, csgl3. Fine genetic mapping delimited the csgl3 locus into a 68.4 kb region with 12 predicted genes. Genetic analysis, sequence alignment and allelic variation survey in natural populations identified Csa6G514870 encoding a class IV homeodomain-associated leucine zipper (HD-ZIP) transcription factor as the only candidate for CsGL3, which was 5188 bp in length with 10 predicted exons. Gene expression analysis revealed the loss-of-function of CsGL3 in the mutant due to the insertion of a 5-kb long terminal repeat (LTR) retrotransposon in the 4th exon of CsGL3. Linkage analysis in a segregating population and gene expression analysis of the CsGL1 and CsGL3 genes in csgl1, csgl3, and csgl1 + 3 genetic backgrounds uncovered interactions between the two genes. Phylogenetic analysis among 28 class IV HD-ZIP protein sequences from five species placed cucumber CsGL3 into the same clade with 7 other members that play important roles in trichome initiation.ConclusionsThe new glabrous mutation in cucumber was controlled by a single recessive locus csgl3, which was phenotypically and genetically distinct from two previously reported glabrous mutants csgl1 and csgl2. The glabrous phenotype in csgl3 was due to insertion of an autonomous, active, class I transposable element in CsGL3, a class IV HD-ZIP transcription factor. CsGL3 was epistatic to CsGL1. CsGL3 seemed to play important roles in cucumber trichome initiation whereas CsGL1 may act downstream in the trichome development pathway(s). Findings from the present study provide new insights into genetic control of trichome development in cucumber.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0693-0) contains supplementary material, which is available to authorized users.

Highlights

Trichomes, developed from the protodermal cells, are hairlike structures covering the aerial parts of plants
The unicellular, nonglandular trichome of Arabidopsis thaliana has been used as a model system to study the molecular genetic mechanisms of trichome organogenesis, which involves a transcriptional network consisting of three groups of transcription factors: R2R3 MYBs, the basic helix-loophelix factors and the WD40 repeat (WDR) proteins
To eliminate the possibility that the glabrous allele was introduced from other pollen sources, we genotyped Recombinant inbred line (RIL)-46 M and RIL-46 W with 238 highly polymorphic Simple sequence repeat (SSR) that were used in polymorphic screening in genetic mapping of this gene, and no polymorphism was found between the two sibling lines

Summary

Introduction

Trichomes, developed from the protodermal cells (the outermost cell layer of the embryo), are hairlike structures covering the aerial parts of plants. The genetic network regulating trichome development has been extensively studied and well understood in the model species Arabidopsis thaliana, which bears unicellular, nonglandular and branched trichomes. Trichomes, developed from the protodermal cells (the outermost cell layer of the embryo), are hair-like structures covering the aerial parts of plants such as leaves, stems, petioles, sepals, petals, ovaries, fruits and seeds. The unicellular, nonglandular trichome of Arabidopsis thaliana has been used as a model system to study the molecular genetic mechanisms of trichome organogenesis, which involves a transcriptional network consisting of three groups of transcription factors: R2R3 MYBs, the basic helix-loophelix (bHLH) factors and the WD40 repeat (WDR) proteins (reviewed by [3,4,5]). There is functional redundancy between GL2 and HDG11, and GL2 transcript levels are maintained through a positive feedback loop involving GL2 activation of MYB23 [11]

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