Micro‐trichome as a class I homeodomain‐leucine zipper gene regulates multicellular trichome development in Cucumis sativus

Abstract

Plant trichomes serve as a highly suitable model for investigating cell differentiation at the single-cell level. The regulatory genes involved in unicellular trichome development in Arabidopsis thaliana have been intensively studied, but genes regulating multicellular trichome development in plants remain unclear. Here, we characterized Cucumis sativus (cucumber) trichomes as representative multicellular and unbranched structures, and identified Micro-trichome (Mict), using map-based cloning in an F 2 segregating population of 7,936 individuals generated from a spontaneous mict mutant. In mict plants, trichomes in both leaves and fruits, are small, poorly developed, and denser than in the wild type. Sequence analysis revealed that a 2,649-bp genomic deletion, spanning the first and second exons, occurred in a plant-specific class I homeodomain-leucine zipper gene. Tissue-specific expression analysis indicated that Mict is strongly expressed in the trichome cells. Transcriptome profiling identified potential targets of Mict including putative homologs of genes known in other systems to regulate trichome development, meristem determinacy, and hormone responsiveness. Phylogenic analysis charted the relationships among putative homologs in angiosperms. Our paper represents initial steps toward understanding the development of multicellular trichomes.

A fragment substitution in the promoter of CsHDZIV11/CsGL3 is responsible for fruit spine density in cucumber (Cucumis sativus L.)

“…This hypothesis was supported by data from the present study, with no observed difference in leaf trichome density but a significant difference in fruit spine density between fs1 and WT (Fig. Neighbor-joining phylogenetic tree was generated after a complete protein sequence alignment with Clustal X (1.81) Table 3 of trichomes on foliage or fruit were mapped on chromosomes 2, 3 and 6, respectively (Yang et al 2011;Li et al 2015;Pan et al 2015;Wang et al 2016;Zhao et al 2015;Cui et al 2016). In cucumber, a number of genes related to fruit spines have been identified: B for black spine, ns for numerous spines, ss for small spines, s or s1 for spine size and frequency, s2 and s3 for dense and small spines, and gl (glabrous) and tril (trichome-less) for trichomes formation (Call and Wehner 2010;Wang et al 2016).…”

“…Moreover, the existence of cucumber fruit spines is a precondition for the formation of fruit tubercules, as genetic analysis indicated that cucumber glabrous 1 (csgl1), a gene controlling fruit spine formation, was epistatic to the Tuberculate fruit (Tu) (Cao and Guo 1999;Cao et al 2001;Yang et al 2014;Li et al 2015). Genes gl-2, csgl1 and tril/ csgl3 controlling presence or absence of trichomes on the foliage or fruit were mapped in chromosomes 2, 3 and 6, respectively; and csgl1, tril and csgl3 were recently cloned, and both Tril and CsGL3 were found to be the same gene, Csa6M514870, in three different labs (Yang et al 2011;Li et al 2015;Pan et al 2015;Wang et al 2016;Zhao et al 2015;Cui et al 2016). Several genes related to fruit spine size and density have been identified through genetic analysis (Tkachenko 1935;Hutchins 1940;Poole 1944;Caruth 1975;Fanourakis and Simon 1987).…”

“…Existing results demonstrated that members of the HD-Zip IV subfamily play pivotal roles in trichome formation of several plants: AtGL2, AtML1, AtPDF2, AtHDG1, AtHDG2, AtHDG11 and AtHDG12 in Arabidopsis (Rerie et al 1994;Abe et al 2003;Nakamura et al 2006;Khosla et al 2014); Woolly (Wo) in tomato (Solanum lycopersicum) (Yang et al 2011); GhHD-1, GbML1 and HOX1, 2 and 3 in cotton (Wang et al 2004;Guan et al 2008;Zhang et al 2010a, b;Walford et al 2012;Shan et al 2014); and OUTER CELL LAYER4 (OCL4) in maize (Zea mays) (Vernoud et al 2009). A new discovery indicated that a HD-Zip I protein, CsGL1, is a key factor in cucumber trichome development (Li et al 2015;Zhao et al 2015). However, it remains unknown whether fruit spine density in cucumber is also regulated by HD-Zip IV proteins.…”

Molecular mapping and candidate gene analysis for fruit epidermal structure in cucumber

“…The genetic mapping of several cucumber genes was finished. These genes included fruit dull gene ( D ) (Yang et al., ), heavy netting of mature cucumber gene ( H ) (Miao et al., ), uniform colour gene ( u ) (Yang, Yue et al., ; Yang, Zhang et al., ), fruit tumour gene ( Tu ) (Yang, Yue et al., ; Yang, Zhang et al., ; Zhang et al., ), black spine ( B ) (Li, Wen, & Weng, ), yellow fruit ( yf ) (Lu et al., ), white rind gene ( w ) (Liu et al., ), fruit bitter (Zhang et al., ), glabrous (Gl) (Cui et al., ; Zhao et al., ), fruit spine density (Zhang, Liu et al., ; Zhang, Wang et al., ). However, chromosomal mapping of palisade epidermis has not been reported so far.…”

CsTTG1 Encodes a WD-repeat Protein That Regulates Fruit Wart Formation in Cucumis sativus through Interaction with the Homeodomain-leucine Zipper I Protein Mict

“…It has been shown that the phenotype of the csgl cucumber mutant is controlled by a single recessive nuclear gene and that csgl1 is epistatic to the Tuberculate fruit (Tu) gene (Cao et al, 2001;Yang et al, 2014). Tu and Mict/CsGL1 were both identified, and Mict/CsGL1 was shown to be required for further differentiation of cucumber trichomes in all aerial parts of the plant, including leaves, stems, tendrils, floral organs, and fruits, but not for their initiation (Li et al, 2015;Zhao et al, 2015). Recently, a homeodomainleucine zipper gene, Tril, involved in multicellular trichome initiation in cucumber, was identified (Wang et al, 2016).…”