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Compatible and Incompatible Pollen-Styles Interaction in Pyrus Communis L

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Compatible and Incompatible Pollen-Styles Interaction in Pyrus Communis L fpls-10-00741 June 12, 2019 Time: 19:21 # 1 ORIGINAL RESEARCH published: 07 June 2019 doi: 10.3389/fpls.2019.00741 Compatible and Incompatible Pollen-Styles Interaction in Pyrus communis L. Show Different Transglutaminase Features, Polyamine Pattern and Metabolomics Profiles Manuela Mandrone1, Fabiana Antognoni2, Iris Aloisi3, Giulia Potente2, Ferruccio Poli1, Giampiero Cai4, Claudia Faleri4, Luigi Parrotta3 and Stefano Del Duca3* 1 Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy, 2 Department for Life Quality Studies, Edited by: University of Bologna, Rimini, Italy, 3 Department of Biological, Geological and Environmental Sciences, University Antonio F. Tiburcio, of Bologna, Bologna, Italy, 4 Department of Life Sciences, University of Siena, Siena, Italy University of Barcelona, Spain Reviewed by: Pollen-stigma interaction is a highly selective process, which leads to compatible Penglin Sun, University of California, Riverside, or incompatible pollination, in the latter case, affecting quantitative and qualitative United States aspects of productivity in species of agronomic interest. While the genes and the Milagros Bueno, Universidad de Jaén, Spain corresponding protein partners involved in this highly specific pollen-stigma recognition *Correspondence: have been studied, providing important insights into pollen-stigma recognition in self- Stefano Del Duca incompatible (SI), many other factors involved in the SI response are not understood [email protected] yet. This work concerns the study of transglutaminase (TGase), polyamines (PAs) Specialty section: pattern and metabolomic profiles following the pollination of Pyrus communis L. This article was submitted to pistils with compatible and SI pollen in order to deepen their possible involvement in Plant Metabolism the reproduction of plants. Immunolocalization, abundance and activity of TGase as and Chemodiversity, a section of the journal well as the content of free, soluble-conjugated and insoluble-bound PAs have been Frontiers in Plant Science investigated. 1H NMR-profiling coupled with multivariate data treatment (PCA and Received: 15 March 2019 PLS-DA) allowed to compare, for the first time, the metabolic patterns of not-pollinated Accepted: 17 May 2019 Published: 07 June 2019 and pollinated styles. Results clearly indicate that during the SI response TGase activity Citation: increases, resulting in the accumulation of PAs conjugated to hydroxycinnamic acids Mandrone M, Antognoni F, Aloisi I, and other small molecules. Metabolomic analysis showed a remarkable differences Potente G, Poli F, Cai G, Faleri C, between pollinated and not-pollinated styles, where, except for glucose, all the other Parrotta L and Del Duca S (2019) Compatible and Incompatible metabolites where less concentrated. Moreover, styles pollinated with compatible pollen Pollen-Styles Interaction in Pyrus showed the highest amount of sucrose than SI pollinated ones, which, in turn, contained communis L. Show Different Transglutaminase Features, highest amount of all the other metabolites, including aromatic compounds, such as Polyamine Pattern and Metabolomics flavonoids and a cynnamoil derivative. Profiles. Front. Plant Sci. 10:741. doi: 10.3389/fpls.2019.00741 Keywords: self-incompatibility, Pyrus communis, transglutaminase, 1H NMR-metabolomics, polyamines Frontiers in Plant Science| www.frontiersin.org 1 June 2019| Volume 10| Article 741 fpls-10-00741 June 12, 2019 Time: 19:21 # 2 Mandrone et al. Transglutaminase and Metabolites in Style-Pollination INTRODUCTION from bacteria to plants (Antognoni et al., 1999; Fujita and Shinozaki, 2014). Despite the wide array of investigations on In order to prevent self-fertilization, plants have evolved different PA roles in plant cells, little information is available on their strategies, from the temporally asynchronous development of role during the apical growth of pollen within the styles. male and female reproductive organs, to their specific localization PAs biosynthesis increased during pollen tube emergence and within the flower, up to genetic-based strategies called “self- elongation and they are released in the external space (Bagni incompatibility” (SI) (Barrett, 2003; Ashman et al., 2004). The et al., 1981) where they affected RNAse activity (Speranza et al., latter process prevents self-fertilization by the rejection of pollen 1984). Together with the decrease in free PAs, changes in the of the same species. Based on whether the gametophytic or levels of PAs bound to low- and high-mass molecules take the sporophytic genome will determine pollen rejection, SI is place inside the pollen tube (Antognoni and Bagni, 2008). classified into gametophytic SI (GSI) or sporophytic SI (SSI) (Fujii Moreover, PAs are directly involved in ROS regulation, whose et al., 2016). Most of SI systems are controlled by a single gene concentration is essential for pollen tube growth (Wu et al., 2010; locus, the so-called “S locus” which presents multiple S-alleles, Aloisi et al., 2015). i.e., the pistil-S and pollen-S genes; however, several other genes, Metabolomics is a novel inductive approach, relying on proteins and external factors are involved in the process of pollen untargeted analysis protocols, whose results are handled by acceptance/rejection (Serrano et al., 2015; Qu et al., 2017). multivariate data treatment. This workflow proved to be In the last decades, both genetic and molecular factors successful in several research fields, from human diagnostics involved in SI have been studied in Malinae, as GSI affects both and epidemiology to plant science (Wolfender et al., 2015; quantitative and qualitative aspects of productivity in agricultural An¡elkovic´ et al., 2017), where it resulted particularly helpful to species of great economic interest (Del Duca et al., 2019). In the face the challenges posed by the complexity of natural product GSI of Malinae, the stylar S locus plays an important role, since it chemistry (Pauli et al., 2012). For instance, metabolomics has encodes for glycoproteins with ribonuclease (S-RNase) activities been employed to facilitate the identification of medicinal plants that enter inside the pollen tube. Once inside, they are degraded active principles (Go¡evac et al., 2018; Mandrone et al., 2018). in case of compatible pollen, allowing pollen tubes to grow, In this work, styles of Pyrus communis L. cv Abbé Fétel while in SI pollen the S-RNases are kept active, causing the were pollinated with compatible Williams pollen (AxW) and degradation of pollen RNA and the cell death of pollen tube, with incompatible Abbé Fétel pollen (AxA) in order to which generally reaches only the upper third part of the style induce SI response. (De Franceschi et al., 2012). As many changes occur (i.e., in the cell wall) during the Several evidences highlight the involvement of transglu- growth of pollen tube inside the style, it is interesting to check if taminase (TGase) in the process of pollen rejection, not only in this is complemented by variation in metabolomics profile that Malinae (Gentile et al., 2012; Aloisi et al., 2016a; Del Duca et al., has been analyzed in not-pollinated (NP) styles and in styles 2019). TGases are ubiquitous enzymes that catalyze the post- pollinated with compatible and SI pollen, at 48 h after pollination. translational modification of proteins, through the incorporation Besides, the metabolomic analyses, performed for the first time of primary amines or by protein cross-linking, resulting often on SI systems, will add knowledge enlarging the picture of factors in high molecular mass products (Griffin et al., 2002). In plants, involved in the SI process and will help to clarify what are the TGases are distributed in different cell compartments where they main actors playing into the SI response in the complex molecular exert a structural or conformational role (Del Duca and Serafini- networks of pear SI system. For example, it is reasonable to Fracassini, 2005; Serafini-Fracassini and Del Duca, 2008; Serafini- hypothesize changes in cell wall as well as in phenolic compounds Fracassini et al., 2009). The post-translational modification of or hydroxycinnamoyl-derivatives that could take place because of proteins by polyamines (PAs) and the catalysis of isopeptide the pollen-style interaction. bonds are the main TGase reaction studied in plant (Del Duca As the cytoskeleton is a target of SI response (Thomas et al., et al., 2000; Aloisi et al., 2016b). Although TGase could also 2006), and TGase affects the organization of microfilaments catalyze the deamidation of endoglutamine residues of protein and microtubules (Del Duca et al., 1997, 2009), TGase amount, substrates, up to now this reaction has been scarcely considered activity, and localization have been checked. In particular, in plants. TGase is a crucial factor for the growth of pollen analysis were carried out at different time intervals, from the first tubes as is involved in the cross-link of several substrates (mainly hours until 48 h after pollination. Moreover, given the role of cytoskeleton proteins) and in the post-translational modification PAs in fertilization process (Aloisi et al., 2016a), and the role of of proteins (Di Sandro et al., 2010; Aloisi et al., 2016a). TGase TGase as a mediator of PAs action (Del Duca et al., 2014a), their activity increases during the SI response (Del Duca et al., profiles and their changes in styles pollinated with compatible 2010; Gentile et al., 2012) and programmed cell death (PCD)- and SI pollen have been investigated.
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