PLC-Mediated Signaling Pathway in Pollen Tubes Regulates the Gametophytic Self-incompatibility of Pyrus Species

Qu, Haiyong; Guan, Yaqin; Wang, Yongzhang; Zhang, Shaolin

doi:10.3389/fpls.2017.01164

Cited by 26 publications

(21 citation statements)

References 90 publications

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“…Therefore, it is generally accepted that the S-RNase causes pollen tube lethality in Pyrus solely by degrading pollen tube RNA (McClure et al., 1990; Huang et al., 1994; DeFranceschi et al., 2012). However, increasing evidence indicates that the S-RNase may act as a trigger for biochemical processes that eventually lead up to pollen tube rejection instead of directly causing it via RNA degradation (Wang et al., 2010; Wang and Zhang, 2011; Qu et al., 2017). Several studies in Pyrus and related species showed that the S-RNase interacts with (1) F-actin (Liu et al., 2007), (2) phospholipase C (PLC) (Qu et al., 2017), and (3) pyrophosphatase (PPa) (Li et al., 2018).…”

Section: The Molecular Mechanisms Of Self-recognition and Rejection Imentioning

confidence: 99%

Finding a Compatible Partner: Self-Incompatibility in European Pear (Pyrus communis); Molecular Control, Genetic Determination, and Impact on Fertilization and Fruit Set

et al. 2019

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Pyrus species display a gametophytic self-incompatibility (GSI) system that actively prevents fertilization by self-pollen. The GSI mechanism in Pyrus is genetically controlled by a single locus, i.e., the S-locus, which includes at least two polymorphic and strongly linked S-determinant genes: a pistil-expressed S-RNase gene and a number of pollen-expressed SFBB genes (S-locus F-Box Brothers). Both the molecular basis of the SI mechanism and its functional expression have been widely studied in many Rosaceae fruit tree species with a particular focus on the characterization of the elusive SFBB genes and S-RNase alleles of economically important cultivars. Here, we discuss recent advances in the understanding of GSI in Pyrus and provide new insights into the mechanisms of GSI breakdown leading to self-fertilization and fruit set. Molecular analysis of S-genes in several self-compatible Pyrus cultivars has revealed mutations in both pistil- or pollen-specific parts that cause breakdown of self-incompatibility. This has significantly contributed to our understanding of the molecular and genetic mechanisms that underpin self-incompatibility. Moreover, the existence and development of self-compatible mutants open new perspectives for pear production and breeding. In this framework, possible consequences of self-fertilization on fruit set, development, and quality in pear are also reviewed.

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Section: The Molecular Mechanisms Of Self-recognition and Rejection Imentioning

confidence: 99%

Finding a Compatible Partner: Self-Incompatibility in European Pear (Pyrus communis); Molecular Control, Genetic Determination, and Impact on Fertilization and Fruit Set

et al. 2019

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“…According to the results of the RNA-Seq and quantitative PCR, once the compatible pollen and incompatible pollen had come into contact with the stigma, genes related to pollen tube growth regulation were significantly upregulated. We previously reported on calcium- and phospholipase C-related genes in the pollen tube that were also significantly differentially expressed in the early stage following pollination (Qu et al , 2017; Qu et al , 2016). All these factors indicate that the gametophytic self-incompatibility response of Pyrus has already been initiated after pollination, rather than when the pollen tube enters the style.…”

Section: Discussionmentioning

confidence: 99%

RNA-Seq analysis of compatible and incompatible styles of Pyrus species at the beginning of pollination

Guan

Wang

et al. 2018

Preprint

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In Rosaceae, incompatible pollen can penetrate into the style during the gametophytic self-incompatibility response. It is therefore considered a stylar event rather than a stigmatic event. In this study, we explored the differences in gene expression between compatibility and incompatibility in the early stage of pollination. The self-compatible pear variety “Jinzhuili” is a naturally occurring bud mutant from “Yali”, a leading Chinese native cultivar exhibiting typical gametophytic self-incompatibility. We collected the styles of ‘Yali’ and ‘Jinzhuili’ at 0.5 and 2 h after self-pollination and then performed high-throughput sequencing. According to the pathway enrichment analysis of the differentially expressed genes, “plant-pathogen interaction” was the most represented pathway. Quantitative PCR was used to validate these differential genes. The expression levels of genes related to pollen growth and disease inhibition, such as LRR (LEUCINE-RICH REPEAT EXTENSIN), resistance, and defensin, differed significantly between compatible and incompatible pollination. Interestingly, at 0.5 h, most of these genes were upregulated in the compatible pollination system compared with the incompatible pollination system. Calcium ion transport, which requires ATPase, also demonstrated upregulated expression. In summary, the self-incompatibility reaction was initiated when the pollen came into contact with the stigma.

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“…In the pear system, intake of S-RNase may cause a decrease in intracellular Ca 2+ levels probably by acting on the permeability of the plasma membrane or calcium channels [55]. It is believed that intake of self S-RNase may inhibit the activity of phospholipase C associated with the plasma membrane, which in turn converts phosphatidylinositol 4,5-bisphosphate (PIP 2 ) into inositol 1,4,5-trisphosphate (IP 3 ), an effector capable of opening calcium channels [4]. However, intake of S-RNase may also decrease the apical concentration of ROS [32].…”

Section: The Tgase-cytoskeleton Interplay As a Crucial Player Of Tmentioning

confidence: 99%

“…SI involves a pollen–pistil interaction and a cell–cell recognition system, which regulates the acceptance or rejection of pollen landing on the stigma of the same species, so that SI pollen arrests its tube elongation at a specific stage during pollination, preventing self-fertilization. A single locus controls most of SI systems, the so-called “ S locus” which presents multiple S -alleles, i.e., the pistil- S and pollen- S genes; however, the process of pollen acceptance/rejection involves various other genes, many of which still need to be identified, and many other external factors [4,5]. Up to date two major classes of SI are known at the genetic level: the gametophytic SI (GSI) and the sporophytic SI (SSI).…”

Section: Introduction: the Molecular Basis Of S-rnase-based Gametomentioning

confidence: 99%

Cytoskeleton, Transglutaminase and Gametophytic Self-Incompatibility in the Malinae (Rosaceae)

Duca

Aloisi

Parrotta

et al. 2019

IJMS

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Self-incompatibility (SI) is a complex process, one out of several mechanisms that prevent plants from self-fertilizing to maintain and increase the genetic variability. This process leads to the rejection of the male gametophyte and requires the co-participation of numerous molecules. Plants have evolved two distinct SI systems, the sporophytic (SSI) and the gametophytic (GSI) systems. The two SI systems are markedly characterized by different genes and proteins and each single system can also be divided into distinct subgroups; whatever the mechanism, the purpose is the same, i.e., to prevent self-fertilization. In Malinae, a subtribe in the Rosaceae family, i.e., Pyrus communis and Malus domestica, the GSI requires the production of female determinants, known as S-RNases, which penetrate the pollen tube to interact with the male determinants. Beyond this, the penetration of S-RNase into the pollen tube triggers a series of responses involving membrane proteins, such as phospholipases, intracellular variations of cytoplasmic Ca2+, production of reactive oxygen species (ROS) and altered enzymatic activities, such as that of transglutaminase (TGase). TGases are widespread enzymes that catalyze the post-translational conjugation of polyamines (PAs) to different protein targets and/or the cross-linking of substrate proteins leading to the formation of cross-linked products with high molecular mass. When actin and tubulin are the substrates, this destabilizes the cytoskeleton and inhibits the pollen-tube’s growth process. In this review, we will summarize the current knowledge of the relationship between S-RNase penetration, TGase activity and cytoskeleton function during GSI in the Malinae.

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PLC-Mediated Signaling Pathway in Pollen Tubes Regulates the Gametophytic Self-incompatibility of Pyrus Species

Cited by 26 publications

References 90 publications

Finding a Compatible Partner: Self-Incompatibility in European Pear (Pyrus communis); Molecular Control, Genetic Determination, and Impact on Fertilization and Fruit Set

Finding a Compatible Partner: Self-Incompatibility in European Pear (Pyrus communis); Molecular Control, Genetic Determination, and Impact on Fertilization and Fruit Set

RNA-Seq analysis of compatible and incompatible styles of Pyrus species at the beginning of pollination

Cytoskeleton, Transglutaminase and Gametophytic Self-Incompatibility in the Malinae (Rosaceae)

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