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Pollination Type Recognition from a Distance by the Ovary Is Revealed Through a Global Transcriptomic Analysis.

ABSTRACT: Sexual reproduction in flowering plants involves intimate contact and continuous interactions between the growing pollen tube and the female reproductive structures. These interactions can trigger responses in distal regions of the flower well ahead of fertilization. While pollination-induced petal senescence has been studied extensively, less is known about how pollination is perceived at a distance in the ovary, and how specific this response is to various pollen genotypes. To address this question, we performed a global transcriptomic analysis in the ovary of a wild potato species, Solanum chacoense, at various time points following compatible, incompatible, and heterospecific pollinations. In all cases, pollen tube penetration in the stigma was initially perceived as a wounding aggression. Then, as the pollen tubes grew in the style, a growing number of genes became specific to each pollen genotype. Functional classification analyses revealed sharp differences in the response to compatible and heterospecific pollinations. For instance, the former induced reactive oxygen species (ROS)-related genes while the latter affected genes associated to ethylene signaling. In contrast, incompatible pollination remained more akin to a wound response. Our analysis reveals that every pollination type produces a specific molecular signature generating diversified and specific responses at a distance in the ovary in preparation for fertilization.

SUBMITTER: Joly V

PROVIDER: S-EPMC6630372 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Pollination Type Recognition from a Distance by the Ovary Is Revealed Through a Global Transcriptomic Analysis.

Joly Valentin V Tebbji Faïza F Nantel André A Matton Daniel P DP

Plants (Basel, Switzerland) 20190624 6

Sexual reproduction in flowering plants involves intimate contact and continuous interactions between the growing pollen tube and the female reproductive structures. These interactions can trigger responses in distal regions of the flower well ahead of fertilization. While pollination-induced petal senescence has been studied extensively, less is known about how pollination is perceived at a distance in the ovary, and how specific this response is to various pollen genotypes. To address this que ...[more]

PMID: 31238522

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Project description:Sexual reproduction in flowering plants involves intimate interactions between the growing pollen tube and the female reproductive structure. These interactions start immediately after pollen landing on the stigma and continue during the pollen tube journey through the style and the ovary. Thus, well before fertilization, genes in the gynoecium are affected by the growing pollen tubes. Genes activated at a distance in the ovary before pollen tubes arrival represent one class of such genes. Using a global transcriptomic approach, expression profiles obtained from compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations revealed that these pollinations are perceived differently from a distance in the ovary. As the pollen tubes grew along the style, more and more genes became specific for each pollination type, although even early on when no difference could be observed in pollen tube growth rates, each pollination type already displayed its specific signature. Wounding experiments as well as methyl jasmonate treatment were also conducted to determine if transmitting tissue cell death caused by pollen tube growth in the style could also activate gene expression at distance in the ovary. Our data suggest that pollen tube growth in the style is at least partially perceived as a wounding aggression, and that a SI pollination is more akin to a wound response than the other pollination type tested, suggesting similarities in the signaling pathways controlling pollen recognition and stress responses. More importantly, our transcriptomic analysis reveals a highly specific recognition of various pollination types that is relayed from a distance to the ovary ahead of fertilization. To determine on a more global scale if interorgan communication during pollen-pistil interactions is a widespread phenomenon and does not only involve few specialized genes, we used a 7.7K cDNA microarray comprising ~6500 ovule-derived unigenes in duplicata from Solanum chacoense, a self-incompatible wild potato species (Germain et al., 2005), to conduct gene expression analyses through cDNA microarray hybridizations. Profiles obtained from compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations as well as from wounding treatments were all analyzed using the same minimal expression level critera (p < 0.05, fold change ≥± 1.5). Four independent biological replicates were produced from each time points. Ovules were collected at 6, 24 and 48 hours after each treatment and used for RNA extraction and probe preparation . compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations as well as from wounding treatments mRNA preparations were individually hybridized against unpollinated ovule mRNAs . All data was substracted from the touch control. Althought Methanol treated ovules RNA were hybridized against unpollinated ovule mRNAs from plant in closed chamber. To estimate reproducibility and to produce control data for statistical analysis, a large number of unfertilized ovules were isolated and separated between seven independent control groups. RNA from randomly selected pairs of control was hybridized on six microarrays.

Dataset Information

Pollination Type Recognition from a Distance by the Ovary Is Revealed Through a Global Transcriptomic Analysis.

Publications

Pollination Type Recognition from a Distance by the Ovary Is Revealed Through a Global Transcriptomic Analysis.

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