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LsAP2 regulates leaf morphology by inhibiting CIN-like TCP transcription factors and repressing LsKAN2 in lettuce.

ABSTRACT: Leaf size and flatness directly affect photosynthesis and are closely related to agricultural yield. The final leaf size and shape are coordinately determined by cell proliferation, differentiation, and expansion during leaf development. Lettuce (Lactuca sativa L.) is one of the most important leafy vegetables worldwide, and lettuce leaves vary in shape and size. However, the molecular mechanisms of leaf development in lettuce are largely unknown. In this study, we showed that the lettuce APETALA2 (LsAP2) gene regulates leaf morphology. LsAP2 encodes a transcriptional repressor that contains the conserved EAR motif, which mediates interactions with the TOPLESS/TOPLESS-RELATED (TPL/TPR) corepressors. Overexpression of LsAP2 led to small and crinkly leaves, and many bulges were seen on the surface of the leaf blade. LsAP2 physically interacted with the CINCINNATA (CIN)-like TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) transcription factors and inhibited their transcriptional activation activity. RNA sequencing analysis showed that LsAP2 affected the expression of auxin- and polarity-related genes. In addition, LsAP2 directly repressed the abaxial identity gene KANADI2 (LsKAN2). Together, these results indicate that LsAP2 regulates leaf morphology by inhibiting CIN-like TCP transcription factors and repressing LsKAN2, and our work provides insights into the regulatory mechanisms of leaf development in lettuce.

SUBMITTER: Luo C

PROVIDER: S-EPMC8408249 | biostudies-literature |

REPOSITORIES: biostudies-literature

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LsAP2 regulates leaf morphology by inhibiting CIN-like TCP transcription factors and repressing LsKAN2 in lettuce

Project description:Leaf size and flatness directly affect photosynthesis and are closely related to agricultural yield. The final leaf size and shape are coordinately determined by cell proliferation, differentiation, and expansion during leaf development. Lettuce (Lactuca sativa L.) is one of the most important leafy vegetables worldwide, and lettuce leaves vary in shape and size. However, the molecular mechanisms of leaf development in lettuce are largely unknown. In this study, we showed that the lettuce APETALA2 (LsAP2) gene regulates leaf morphology. LsAP2 encodes a transcriptional repressor that contains the conserved EAR motif, which mediates interactions with the TOPLESS/TOPLESS-RELATED (TPL/TPR) corepressors. Overexpression of LsAP2 led to small and crinkly leaves, and many bulges were seen on the surface of the leaf blade. LsAP2 physically interacted with the CINCINNATA (CIN)-like TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) transcription factors and inhibited their transcriptional activation activity. RNA sequencing analysis showed that LsAP2 affected the expression of auxin- and polarity-related genes. In addition, LsAP2 directly repressed the abaxial identity gene KANADI2 (LsKAN2). Together, these results indicate that LsAP2 regulates leaf morphology by inhibiting CIN-like TCP transcription factors and repressing LsKAN2, and our work provides insights into the regulatory mechanisms of leaf development in lettuce.

2021-03-29 | GSE168886 | GEO

LsAP2 regulates leaf morphology by inhibiting CIN-like TCP transcription factors and repressing LsKAN2 in lettuce

Project description:LsAP2 regulates leaf morphology by inhibiting CIN-like TCP transcription factors and repressing LsKAN2 in lettuce

| PRJNA714420 | ENA

The CIN-TCP transcription factors promote commitment to differentiation in Arabidopsis leaf pavement cells via both auxin-dependent and independent pathways.

Project description:Cells in organ primordia undergo active proliferation at an early stage to generate sufficient number, before exiting proliferation and entering differentiation. However, how the actively proliferating cells are developmentally reprogrammed to acquire differentiation potential during organ maturation is unclear. Here, we induced a microRNA-resistant form of TCP4 at various developmental stages of Arabidopsis leaf primordium that lacked the activity of TCP4 and its homologues and followed its effect on growth kinematics. By combining this with spatio-temporal gene expression analysis, we show that TCP4 commits leaf cells within the transition zone to exit proliferation and enter differentiation. A 24-hour pulse of TCP4 activity was sufficient to impart irreversible differentiation competence to the actively dividing cells. A combination of biochemical and genetic analyses revealed that TCP4 imparts differentiation competence by promoting auxin response as well as by directly activating HAT2, a HD-ZIP II transcription factor-encoding gene that also acts downstream to auxin response. Our study offers a molecular link between the two major organ maturation factors, CIN-like TCPs and HD-ZIP II transcription factors and explains how TCP activity restricts the cell number and final size in a leaf.

| S-EPMC6386416 | biostudies-literature

Inhibition of Arabidopsis thaliana CIN-like TCP transcription factors by Agrobacterium T-DNA-encoded 6B proteins.

Project description:Agrobacterium T-DNA-encoded 6B proteins cause remarkable growth effects in plants. Nicotiana otophora carries two cellular T-DNAs with three slightly divergent 6b genes (TE-1-6b-L, TE-1-6b-R and TE-2-6b) originating from a natural transformation event. In Arabidopsis thaliana, expression of 2×35S:TE-2-6b, but not 2×35S:TE-1-6b-L or 2×35S:TE-1-6b-R, led to plants with crinkly leaves, which strongly resembled mutants of the miR319a/TCP module. This module is composed of MIR319A and five CIN-like TCP (TEOSINTHE BRANCHED1, CYCLOIDEA and PROLIFERATING CELL NUCLEAR ANTIGEN BINDING FACTOR) genes (TCP2, TCP3, TCP4, TCP10 and TCP24) targeted by miR319a. The CIN-like TCP genes encode transcription factors and are required for cell division arrest at leaf margins during development. MIR319A overexpression causes excessive growth and crinkly leaves. TE-2-6b plants did not show increased miR319a levels, but the mRNA levels of the TCP4 target gene LOX2 were decreased, as in jaw-D plants. Co-expression of green fluorescent protein (GFP)-tagged TCPs with native or red fluorescent protein (RFP)-tagged TE-6B proteins led to an increase in TCP protein levels and formation of numerous cytoplasmic dots containing 6B and TCP proteins. Yeast double-hybrid experiments confirmed 6B/TCP binding and showed that TE-1-6B-L and TE-1-6B-R bind a smaller set of TCP proteins than TE-2-6B. A single nucleotide mutation in TE-1-6B-R enlarged its TCP-binding repertoire to that of TE-2-6B and caused a crinkly phenotype in Arabidopsis. Deletion analysis showed that TE-2-6B targets the TCP4 DNA-binding domain and directly interferes with transcriptional activation. Taken together, these results provide detailed insights into the mechanism of action of the N. otophora TE-encoded 6b genes.

| S-EPMC7187390 | biostudies-literature

Genome-Wide Identification of TCP Transcription Factors Family in Sweet Potato Reveals Significant Roles of miR319-Targeted TCPs in Leaf Anatomical Morphology.

Project description:Plant-specific TCP transcription factors play vital roles in the controlling of growth, development, and the stress response processes. Extensive researches have been carried out in numerous species, however, there hasn't been any information available about TCP genes in sweet potato (Ipomoea batatas L.). In this study, a genome-wide analysis of TCP genes was carried out to explore the evolution and function in sweet potato. Altogether, 18 IbTCPs were identified and cloned. The expression profiles of the IbTCPs differed dramatically in different organs or different stages of leaf development. Furthermore, four CIN-clade IbTCP genes contained miR319-binding sites. Blocking IbmiR319 significantly increased the expression level of IbTCP11/17 and resulted in a decreased photosynthetic rate due to the change in leaf submicroscopic structure, indicating the significance of IbmiR319-targeted IbTCPs in leaf anatomical morphology. A systematic analyzation on the characterization of the IbTCPs together with the primary functions in leaf anatomical morphology were conducted to afford a basis for further study of the IbmiR319/IbTCP module in association with leaf anatomical morphology in sweet potato.

| S-EPMC8379018 | biostudies-literature

Knockdown and overexpression of CIN-TCP genes

Project description:Leaf development has been monitored chiefly by following anatomical markers. Analysis of transcriptome dynamics during leaf maturation revealed multiple expression patterns that rise or fall with age or that display age specific peaks. These were used to formulate a digital differentiation index (DDI), based on a set of selected markers with informative expression during leaf ontogeny. The leaf-based DDI reliably predicted the developmental state of leaf samples from diverse sources and was independent of mitotic cell division transcripts or propensity of the specific cell type. When calibrated by informative root markers, the same algorithm accurately diagnosed dissected root samples. We used the DDI to characterize plants with reduced activities of multiple CINCINNATA (CIN)-TCP growth regulators. These plants had giant curled leaves made up of small cells with abnormal shape, low DDI scores and low expression of mitosis markers, depicting the primary role of CIN-TCPs as promoters of differentiation. Delayed activity of several CIN-TCPs resulted in abnormally large but flat leaves with regular cells. The application of DDI has therefore portrayed the CIN-TCPs as heterochronic regulators that permit the development of a flexible and robust leaf form through an ordered and protracted maturation schedule.

2008-09-17 | GSE12691 | GEO

A CIN-like TCP transcription factor (LsTCP4) having retrotransposon insertion associates with a shift from Salinas type to Empire type in crisphead lettuce (Lactuca sativa L.).

Project description:To improve several agronomic traits in crisphead lettuce (Lactuca sativa L.) under high-temperature growth conditions, we investigated the correlation among those traits in multiple cultivars and performed genetic mapping of their causal genes. In a field cultivation test of Empire type (serrated leaf) and Salinas type (wavy leaf) cultivars, Empire type cultivars showed increased tipburn susceptibility and late bolting compared with Salinas type cultivars. We attempted genetic mapping of leaf shape and bolting time by ddRAD-seq using the F2 population derived from a cross between 'VI185' (Empire type) and 'ShinanoGreen' (Salinas type). These analyses suggested that both traits are controlled by a single locus in LG5. Genotyping of 51 commercial lettuce cultivars with a tightly linked marker (LG5_v8_252.743Mbp) at this locus showed an association between its genotype and the serrated leaf phenotype. By further fine mapping and transcriptome analysis, a gene encoding putative CIN-like TCP transcription factor was determined to be a candidate gene at this locus and was designated as LsTCP4. An insertion of retrotransposable element was found in the allele of 'VI185', and its transcript level in the leaves was lower than that in 'ShinanoGreen'. Because shapes of leaf epidermal cells in 'VI185' were similar to those in the TCP family mutant of Arabidopsis thaliana, the leaf shape phenotype was likely caused by reduced expression of LsTCP4. Furthermore, because it is known that the TCP family protein also controls flowering time via interaction with FT in A. thaliana, it was highly possible that LsTCP4 gave pleiotropic effects on both leaf shape and bolting time in lettuce.

| S-EPMC6994696 | biostudies-literature

Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development

Project description:The characteristic leaf shapes we see in all plants are in good part outcome of the combined action of several transcription factor networks that translate into cell division activity during the early development of the organ. We show here that wild-type leaves have distinct transcriptomic profiles in center and marginal regions. Certain transcripts are enriched in margins, including those of CINCINNATA-like TCPs, and members of the NGATHA (NGA) and STYLISH (STY) gene families. We study in detail the contribution of miR319 regulated TCP (Teosinte branched, Cycloidea, PCF1/2) transcription factors to the development of the center and marginal regions of Arabidopsis leaves. We compare in molecular analyses wildtype, a tcp2 tcp4 mutant that has enlarged flat leaves and a tcp2 tcp3 tcp4 tcp10 mutant with strongly crinkled leaves. The different leaf domains of the tcp mutants show changed expression patterns for many photosynthesis related genes, indicating delayed differentiation, especially in the marginal parts of the organ. At the same time, we found an upregulation of cyclin genes and other genes that are known to participate in cell division, specifically in the marginal regions of tcp2 tcp3 tcp4 tcp10. Using GUS reporter constructs we confirmed extended mitotic activity in the tcp2 tcp3 tcp4 tcp10 leaf which persisted in small defined foci in the margins when the mitotic activity had already ceased in wild-type leaves. Our results describe the role of miR319-regulated TCP transcription factors in the coordination of activities in different leaf domains during the organs development.

2017-11-20 | GSE99854 | GEO

Genome-wide Identification of TCP Family Transcription Factors from Populus euphratica and Their Involvement in Leaf Shape Regulation.

Project description:Higher plants have been shown to experience a juvenile vegetative phase, an adult vegetative phase, and a reproductive phase during its postembryonic development and distinct lateral organ morphologies have been observed at the different development stages. Populus euphratica, commonly known as a desert poplar, has developed heteromorphic leaves during its development. The TCP family genes encode a group of plant-specific transcription factors involved in several aspects of plant development. In particular, TCPs have been shown to influence leaf size and shape in many herbaceous plants. However, whether these functions are conserved in woody plants remains unknown. In the present study, we carried out genome-wide identification of TCP genes in P. euphratica and P. trichocarpa, and 33 and 36 genes encoding putative TCP proteins were found, respectively. Phylogenetic analysis of the poplar TCPs together with Arabidopsis TCPs indicated a biased expansion of the TCP gene family via segmental duplications. In addition, our results have also shown a correlation between different expression patterns of several P. euphratica TCP genes and leaf shape variations, indicating their involvement in the regulation of leaf shape development.

| S-EPMC5015053 | biostudies-literature

Identification of GROWTH-REGULATING FACTOR transcription factors in lettuce (Lactuca sativa) genome and functional analysis of LsaGRF5 in leaf size regulation.

Project description:BackgroundGROWTH-REGULATING FACTORs (GRFs), a type of plant-specific transcription factors, play important roles in regulating plant growth and development. Although GRF gene family has been identified in various plant species, a genome-wide analysis of this family in lettuce (Lactuca sativa L.) has not been reported yet.ResultsHere we identified 15 GRF genes in lettuce and performed comprehensive analysis of them, including chromosomal locations, gene structures, and conserved motifs. Through phylogenic analysis, we divided LsaGRFs into six groups. Transactivation assays and subcellular localization of LsaGRF5 showed that this protein is likely to act as a transcriptional factor in the cell nucleus. Furthermore, transgenic lettuce lines overexpressing LsaGRF5 exhibited larger leaves, while smaller leaves were observed in LsaMIR396a overexpression lines, in which LsaGRF5 was down-regulated.ConclusionsThese results in lettuce provide insight into the molecular mechanism of GRF gene family in regulating leaf growth and development and foundational information for genetic improvement of the lettuce variations specialized in leaf character.

| S-EPMC8539887 | biostudies-literature

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