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Ovary Signals for Pollen Tube Guidance in Chalazogamous Mangifera indica L.

ABSTRACT: Most flowering plants show porogamy in which the pollen tubes reach the egg apparatus through the micropyle. However, several species show chalazogamy, an unusual pollen tube growth, in which the pollen tubes reach the embryo sac through the chalaza. While ovary signals for pollen tube growth and guidance have been extensively studied in porogamous species, few studies have addressed the process in chalazogamous species such as mango (Mangifera indica L.), one of the five most important fruit crops worldwide in terms of production. In this study, we characterize pollen-pistil interaction in mango, paying special attention to three key players known to be involved in the directional pollen tube growth of porogamous species such as starch, arabinogalactan proteins (AGPs), and ?-aminobutyric acid (GABA). Starch grains were observed in the style and in the ponticulus at anthesis, but their number decreased 1 day after anthesis. AGPs, revealed by JIM8 and JIM13 antibodies, were homogenously observed in the style and ovary, but were more conspicuous in the nucellus around the egg apparatus. GABA, revealed by anti-GABA antibodies, was specifically observed in the transmitting tissue, including the ponticulus. Moreover, GABA was shown to stimulate in vitro mango pollen tube elongation. The results support the heterotrophic growth of mango pollen tubes in the style at the expense of starch, similarly to the observations in porogamous species. However, unlike porogamous species, the micropyle of mango does not show high levels of GABA and starch, although they were observed in the ponticulus and could play a role in supporting the unusual pollen tube growth in chalazogamous species.

SUBMITTER: Lora J

PROVIDER: S-EPMC7902493 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Ovary Signals for Pollen Tube Guidance in Chalazogamous <i>Mangifera indica</i> L.

Lora Jorge J Perez Veronica V Herrero Maria M Hormaza Jose I JI

Frontiers in plant science 20210210

Most flowering plants show porogamy in which the pollen tubes reach the egg apparatus through the micropyle. However, several species show chalazogamy, an unusual pollen tube growth, in which the pollen tubes reach the embryo sac through the chalaza. While ovary signals for pollen tube growth and guidance have been extensively studied in porogamous species, few studies have addressed the process in chalazogamous species such as mango (<i>Mangifera indica</i> L.), one of the five most important f ...[more]

PMID: 33643328

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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.

Dataset Information

Ovary Signals for Pollen Tube Guidance in Chalazogamous Mangifera indica L.

Publications

Ovary Signals for Pollen Tube Guidance in Chalazogamous <i>Mangifera indica</i> L.

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