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Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor.

ABSTRACT: BACKGROUND AND AIMS: During sexual reproduction in higher angiosperms, the pollen tubes are directed to the ovules in the pistil to deliver sperm cells. This pollen tube attraction is highly species specific, and a group of small secreted proteins, TfCRPs, are necessary for this process in Torenia fournieri. METHODS: A candidate pollen tube attractant protein in Torenia concolor, a related species of T. fournieri, was isolated and the attractant abilities between them were compared. KEY RESULTS: TcCRP1, an orthologous gene of TfCRP1 from T. concolor, is expressed predominantly in the synergid cell. The gene product attracted pollen tubes in a concentration-dependent manner, but attracted fewer pollen tubes from the other species. CONCLUSIONS: The results indicated that this class of CRP proteins is a common pollen tube attractant in Torenia species. The sequence diversity of these proteins is important for species-specific pollen tube attraction.

SUBMITTER: Kanaoka MM

PROVIDER: S-EPMC3170153 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor.

Kanaoka Masahiro M MM Kawano Nao N Matsubara Yoshiyuki Y Susaki Daichi D Okuda Satohiro S Sasaki Narie N Higashiyama Tetsuya T

Annals of botany 20110505 4

<h4>Background and aims</h4>During sexual reproduction in higher angiosperms, the pollen tubes are directed to the ovules in the pistil to deliver sperm cells. This pollen tube attraction is highly species specific, and a group of small secreted proteins, TfCRPs, are necessary for this process in Torenia fournieri.<h4>Methods</h4>A candidate pollen tube attractant protein in Torenia concolor, a related species of T. fournieri, was isolated and the attractant abilities between them were compared. ...[more]

PMID: 21546430

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Project description:BackgroundAs in animals, cell-cell communication plays a pivotal role in male-female recognition during plant sexual reproduction. Prelaid peptides secreted from the female reproductive tissues guide pollen tubes towards ovules for fertilization. However, the elaborate mechanisms for this dialogue have remained elusive, particularly from the male perspective.ResultsWe performed genome-wide quantitative liquid chromatography-tandem mass spectrometry analysis of a pistil-stimulated pollen tube secretome and identified 801 pollen tube-secreted proteins. Interestingly, in silico analysis reveals that the pollen tube secretome is dominated by proteins that are secreted unconventionally, representing 57 % of the total secretome. In support, we show that an unconventionally secreted protein, translationally controlled tumor protein, is secreted to the apoplast. Remarkably, we discovered that this protein could be secreted by infiltrating through the initial phases of the conventional secretory pathway and could reach the apoplast via exosomes, as demonstrated by co-localization with Oleisin1 exosome marker. We demonstrate that translationally controlled tumor protein-knockdown Arabidopsis thaliana plants produce pollen tubes that navigate poorly to the target ovule and that the mutant allele is poorly transmitted through the male. Further, we show that regulators of the endoplasmic reticulum-trans-Golgi network protein secretory pathway control secretion of Nicotiana tabacum Pollen tube-secreted cysteine-rich protein 2 and Lorelei-like GPI-anchor protein 3 and that a regulator of endoplasmic reticulum-trans-Golgi protein translocation is essential for pollen tube growth, pollen tube guidance and ovule-targeting competence.ConclusionsThis work, the first study on the pollen tube secretome, identifies novel genome-wide pollen tube-secreted proteins with potential functions in pollen tube guidance towards ovules for sexual reproduction. Functional analysis highlights a potential mechanism for unconventional secretion of pollen tube proteins and reveals likely regulators of conventional pollen tube protein secretion. The association of pollen tube-secreted proteins with marker proteins shown to be secreted via exosomes in other species suggests exosome secretion is a possible mechanism for cell-cell communication between the pollen tube and female reproductive cells.

Project description:BackgroundTorenia (Torenia fournieri Lind.) is a model plant increasingly exploited in studies in various disciplines, including plant engineering, biochemistry, physiology, and ecology. Additionally, cultivars with different flower colors have been bred and made commercially available. Flower color in torenia is mainly attributed to the accumulation of anthocyanins, but the molecular mechanisms inducing flower color mutations in torenia have not been well elucidated. In this study, we therefore attempted to identify the cause of white coloration in torenia by comparing the white-flowered cultivar Crown White (CrW) with Crown Violet (CrV), a violet-flowered variety.ResultsIn an expression analysis, no flavanone 3-hydroxylase (TfF3H) transcript accumulation was detected in CrW petals. Sequence analyses revealed that a novel long terminal repeat (LTR)-type retrotransposable element, designated as TORE1 (Torenia retrotransposon 1), is inserted into the 5'-upstream region of the TfF3H gene in CrW. A transient expression assay using torenia F3H promoters with or without TORE1 insertion showed that the TORE1 insertion substantially suppressed F3H promoter activity, suggesting that this insertion is responsible for the absence of F3H transcripts in white petals. Furthermore, a transformation experiment demonstrated that the introduction of a foreign gentian F3H cDNA, GtF3H, into CrW was able to recover pink-flower pigmentation, indicating that F3H deficiency is indeed the cause of the colorless flower phenotype in CrW. Detailed sequence analysis also identified deletion mutations in flavonoid 3'-hydroxylase (TfF3'H) and flavonoid 3',5'- hydroxylase (TfF3'5'H) genes, but these were not directly responsible for white coloration in this cultivar.ConclusionsTaken together, a novel retrotransposable element, TORE1, inserted into the F3H 5'-upstream region is the cause of deficient F3H transcripts in white-flowered torenia, thereby leading to reduced petal anthocyanin levels. This is the first report of a retrotransposable element involved in flower color mutation in the genus Torenia.

Project description:Background and aimsAn unusual form of pollen tube growth was observed for several Conospermum species (family Proteaceae). The rate of pollen tube growth, the number of tubes to emerge and the ultrastructure of these tubes are given here.MethodsPollen was germinated in vitro in different sucrose concentrations and in the presence of calcium channel blockers, and tube emergence and growth were recorded on a VCR. Measurements were taken of the number of tubes to emerge and rate of tube emergence. Pollen behaviour in vivo was also observed. The ultrastructure of germinated and ungerminated pollen was observed using TEM.ResultsAfter 10 s to 3 min in germination medium, up to three pollen tubes emerged and grew at rates of up to 55 micro m s(-1); the rate then slowed to around 2 micro m s(-1), 30 s after the initial growth spurt. Tubes were observed to grow in pulses, and the pulsed growth continued in the presence of calcium channel blockers. Optimal sugar concentration for pollen germination was 300 g L(-1), in which up to 81 % of pollen grains showed fast germination. Germination and emergence of multiple tubes were observed in sucrose concentrations of 100-800 g L(-1). The vegetative and generative nuclei moved into one of the tubes. Multiple tubes from a single grain were observed on the stigma. Under light microscopy, the cytoplasm in the tube showed a clear region at the tip. The ultrastructure of C. amoenum pollen showed a bilayered exine, with the intine being very thick at the pores, and elsewhere having large intrusions into the plasma membrane. The cytoplasm was dense with vesicles packed with inner tube cell wall material. Golgi apparatus producing secretory vesicles, and mitochondria were found throughout the tube. The tube wall was bilayered; both layers being fibrous and loosely packed.ConclusionsIt is proposed that, for Conospermum, initial pollen tube wall constituents are manufactured and stored prior to pollen germination, and that tube extension occurs as described in the literature for other species, but at an exceptionally fast rate.

Dataset Information

Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor.

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Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor.

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