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The HD-ZIP IV transcription factor GL2-LIKE regulates male flowering time and fertility in cucumber.

ABSTRACT: Cucumber is dioecious by nature, having both male and female flowers, and is a model system for unisexual flower development. Knowledge related to male flowering is limited, but it is reported to be regulated by transcription factors and hormone signals. Here, we report functional characterization of the cucumber (Cucumis sativus) GL2-LIKE gene, which encodes a homeodomain leucine zipper (HD-ZIP) IV transcription factor that plays an important role in regulating male flower development. Spatial-temporal expression analyses revealed high-level expression of CsGL2-LIKE in the male flower buds and anthers. CsGL2-LIKE is closely related to AtGL2, which is known to play a key role in trichome development. However, ectopic expression of CsGL2-LIKE in Arabidopsis gl2-8 mutant was unable to rescue the gl2-8 phenotype. Interestingly, the silencing of CsGL2-LIKE delayed male flowering by inhibiting the expression of the florigen gene FT and reduced pollen vigor and seed viability. Protein-protein interaction assays showed that CsGL2-LIKE interacts with the jasmonate ZIM domain protein CsJAZ1 to form a HD-ZIP IV-CsJAZ1 complex. Collectively, our study indicates that CsGL2-LIKE regulates male flowering in cucumber, and reveals a novel function of a HD-ZIP IV transcription factor in regulating male flower development of cucumber.

SUBMITTER: Cai Y

PROVIDER: S-EPMC7501822 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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The HD-ZIP IV transcription factor GL2-LIKE regulates male flowering time and fertility in cucumber.

Cai Yanling Y Bartholomew Ezra S ES Dong Mingming M Zhai Xuling X Yin Shuai S Zhang Yaqi Y Feng Zhongxuan Z Wu Licai L Liu Wan W Shan Nan N Zhang Xiao X Ren Huazhong H Liu Xingwang X

Journal of experimental botany 20200901 18

Cucumber is dioecious by nature, having both male and female flowers, and is a model system for unisexual flower development. Knowledge related to male flowering is limited, but it is reported to be regulated by transcription factors and hormone signals. Here, we report functional characterization of the cucumber (Cucumis sativus) GL2-LIKE gene, which encodes a homeodomain leucine zipper (HD-ZIP) IV transcription factor that plays an important role in regulating male flower development. Spatial- ...[more]

PMID: 32490515

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Project description:BACKGROUND: Plant HD-Zip transcription factors are modular proteins in which a homeodomain is associated to a leucine zipper. Of the four subfamilies in which they are divided, the tested members from subfamily I bind in vitro the same pseudopalindromic sequence CAAT(A/T)ATTG and among them, several exhibit similar expression patterns. However, most experiments in which HD-Zip I proteins were over or ectopically expressed under the control of the constitutive promoter 35S CaMV resulted in transgenic plants with clearly different phenotypes. Aiming to elucidate the structural mechanisms underlying such observation and taking advantage of the increasing information in databases of sequences from diverse plant species, an in silico analysis was performed. In addition, some of the results were also experimentally supported. RESULTS: A phylogenetic tree of 178 HD-Zip I proteins together with the sequence conservation presented outside the HD-Zip domains allowed the distinction of six groups of proteins. A motif-discovery approach enabled the recognition of an activation domain in the carboxy-terminal regions (CTRs) and some putative regulatory mechanisms acting in the amino-terminal regions (NTRs) and CTRs involving sumoylation and phosphorylation. A yeast one-hybrid experiment demonstrated that the activation activity of ATHB1, a member of one of the groups, is located in its CTR. Chimerical constructs were performed combining the HD-Zip domain of one member with the CTR of another and transgenic plants were obtained with these constructs. The phenotype of the chimerical transgenic plants was similar to the observed in transgenic plants bearing the CTR of the donor protein, revealing the importance of this module inside the whole protein. CONCLUSIONS: The bioinformatical results and the experiments conducted in yeast and transgenic plants strongly suggest that the previously poorly analyzed NTRs and CTRs of HD-Zip I proteins play an important role in their function, hence potentially constituting a major source of functional diversity among members of this subfamily.

Project description: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.

Dataset Information

The HD-ZIP IV transcription factor GL2-LIKE regulates male flowering time and fertility in cucumber.

Publications

The HD-ZIP IV transcription factor GL2-LIKE regulates male flowering time and fertility in cucumber.

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