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The Role of Arabinogalactan Proteins (Agps) in Fruit Ripening—Areview Agata Leszczuk 1, Panagiotis Kalaitzis2, Konstantinos N

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The Role of Arabinogalactan Proteins (Agps) in Fruit Ripening—Areview Agata Leszczuk 1, Panagiotis Kalaitzis2, Konstantinos N Leszczuk et al. Horticulture Research (2020) 7:176 Horticulture Research https://doi.org/10.1038/s41438-020-00397-8 www.nature.com/hortres REVIEW ARTICLE Open Access The role of arabinogalactan proteins (AGPs) in fruit ripening—areview Agata Leszczuk 1, Panagiotis Kalaitzis2, Konstantinos N. Blazakis2 and Artur Zdunek1 Abstract Arabinogalactan proteins (AGPs) are proteoglycans challenging researchers for decades. However, despite the extremely interesting polydispersity of their structure and essential application potential, studies of AGPs in fruit are limited, and only a few groups deal with this scientific subject. Here, we summarise the results of pioneering studies on AGPs in fruit tissue with their structure, specific localization pattern, stress factors influencing their presence, and a focus on recent advances. We discuss the properties of AGPs, i.e., binding calcium ions, ability to aggregate, adhesive nature, and crosslinking with other cell wall components that may also be implicated in fruit metabolism. The aim of this review is an attempt to associate well-known features and properties of AGPs with their putative roles in fruit ripening. The putative physiological significance of AGPs might provide additional targets of regulation for fruit developmental programme. A comprehensive understanding of the AGP expression, structure, and untypical features may give new information for agronomic, horticulture, and renewable biomaterial applications. Introduction the molecular level that govern cell-to-cell adhesion and fi 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Fruits are one of the main horticultural products. They remodeling of cell walls is still not suf cient to understand are eaten fresh or processed delivering pro-health and and to control the mechanical properties of the whole nutritional components. Therefore, there is a huge fruit. The current cell wall biomechanical model is com- demand for growers, retailers, food industry, and con- posed of three polysaccharides: cellulose, hemicellulose, sumers for high-quality fruit available throughout the and pectins although the mechanism of how do they – whole year. Although the term “high quality” may mean assembly in the cell wall is still discussed3 6. In general, different properties for each commodity and cultivar, the the cellulose-hemicellulose network performs as a scaf- quality properties of the fruit are formed during its fold7 while pectins perform as matrix plasticizer in cell development and ripening, and depend on resistance to walls8 and as an adhesive component in middle lamella stresses, pathogen infections, and physical disintegration between cells9. This system, especially in the case of of the tissue. Most of the quality parameters of fruit and pectins, is highly dynamic during fruit development and biotechnological usefulness of plants relate to mechanical ripening10. characteristics1. From mechanical point of view, cells The last two decades research on arabinogalactan pro- linked with middle lamella, turgor (water content), teins (AGPs) since its discovery in fruit tissue11 suggests intercellular spaces and cell wall properties play the key that cell wall assembly may be influenced by these pro- role2. Although this macroscopic model of the plant tissue teins and in consequence, may be also very important for biomechanics is accepted, knowledge about processes at fruit properties. AGPs are cell wall proteoglycans impli- cated in numerous, variable functions throughout plant – growth and development12 17. Glycosylation of AGPs Correspondence: Agata Leszczuk ([email protected]) constitutes the basis of their essential function and while 1 ś Institute of Agrophysics, Polish Academy of Sciences, Do wiadczalna 4, 20-290 the molecular mechanisms underlying the function and Lublin, Poland 2Department of Horticultural Genetics and Biotechnology, Mediterranean metabolism of cell wall polysaccharides are well known, Agronomic Institute of Chania, Chania, P.O. Box 85, Chania 73100, Greece © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Leszczuk et al. Horticulture Research (2020) 7:176 Page 2 of 12 the role of AGPs as structural-functional proteoglycans in endoplasmic reticulum and the Golgi apparatus. To fruit ripening is described only in several experimental date, 17 different genes implicated in sugar domain data. The involvement of AGPs in abscission zone dif- synthesis from the gene family GT31, GT14, GT37, GT29, ferentiation and organ detachment progression is cur- and GT37 are known. All these genes encode 7 rently under investigation indicating that AGPs might distinct glycosyltransferases corresponding to particular play a regulatory role18. Considering that cell wall dis- sugar residues of AGPs, e.g., hydroxyproline O- solution is necessary for both fruit softening and abscis- β-galactosylotransferase initiating the synthesis process by sion zone cell separation to occur it is possible that AGPs the addition of the galactose residue onto the hydro- might also play a regulatory role in fruit ripening pro- xyproline residue core, β-glucuronosyltransferase by the gression. Although the supposed importance of AGP for addition of glucuronic acid to galactose chains, and α- fruit development and ripening was surely the reason for fucosyltransferase by the addition of α-fucose residue to – the rapid increase of published research devoted for fruit AGPs19 22. in recent years. Since research on AGPs in fruit is still scarce, possible The aim of this review is an attempt to associate well- role for fruit quality might be elucidated to some extent known features and properties of AGPs with their puta- from results obtained for other plant organs. The function tive roles in fruit ripening. The putative physiological of AGPs depends on their precise distribution in cell and significance of AGPs might provide additional targets of their unique chemistry, i.e., a strict structured glycomotif + regulation for this developmental programme. with coupled glucuronic acid residues which bind Ca2 ,23. Generally, AGPs are heavily glycosylated Genetic manipulation of the protein backbone and hydroxyproline-rich glycoproteins (HRGPs), which con- changes in glycan moieties by construct transgenic lines sist of up to 95% of carbohydrates. The protein backbone shade light on AGP functions. Suppression of prolyl 4 has covalently attached type II arabinogalactan (AG) to hydroxylases (P4Hs) activity due to silencing of P4H genes polysaccharides made of β-(1,3)-galactan backbones with results in either lower content or complete absence of α-arabinose, β-(1,6)-galactose, β-glucuronic acid, α- AGPs. Lack of proline hydroxylation results in lack of rhamnose, and α-fucose. The carbohydrate moiety is glycosylation of AGPs, leading to alterations in their characterized by polydispersity due to the different synthesis and, consequently, their degradation or a shift to numbers of repetitive AG subunits (1-15)19,20. The pro- lower molecular weight polypeptides24. In turn, normal tein moiety is characterised by the presence of Ala-Pro, glycosylation has an impact on the proper action of AGPs Pro-Ala, Thr-Pro, Ser-Pro, Val-Pro, and Gly-Pro peptide and thus exerts an effect on cells in many important repeats. Due to the existence of a glycosylpho- aspects: ion binding (1), the establishment of cell wall- sphatidylinositol (GPI) anchor on their C-terminus, AGPs plasma membrane integrity (2), and cross-linking with are described as GPI-anchored proteins, which are cou- other cell wall constituents (3). It is well known that these pled to the outer leaflet of the plasma membrane21. The phenomens occur in plants but are particularly important presence of specific phospholipases allows their release for fruit quality (Fig. 1). into the cell wall and their role as extracellular biosensors. AGPs are proposed as essential extracellular matrix + The AGP glycosylation takes place in both the components that chelate Ca2 by glucuronic carboxyl Fig. 1 AGPs properties and functions. Mutual correlations between selected AGPs properties, their possible impact on cell metabolism, and involvement in fruit process (fruit metabolism) Leszczuk et al. Horticulture Research (2020) 7:176 Page 3 of 12 + groups as putative intramolecular Ca2 -binding sites. between AGPs. It is well known that calcium ion-driven + Thus, AGPs are implicated in the Ca2 signaling path- interactions between AGPs and acidic pectic poly- way25. There are three presumptions to accept this saccharides are the force supporting their cross-linking hypothesis. Firstly, simulations of the molecular dynamics between the carboxyl groups of uronic acid residues in + showed that Hyp-AG subunits (repetitive β-(1-3)-linked
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