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Euphorbia Latex Biochemistry: Complex Interactions in a Complex Environment

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Euphorbia Latex Biochemistry: Complex Interactions in a Complex Environment Plant Biosystems ISSN: 1126-3504 (Print) 1724-5575 (Online) Journal homepage: http://www.tandfonline.com/loi/tplb20 Euphorbia latex biochemistry: Complex interactions in a complex environment F. Pintus , R. Medda , A. C. Rinaldi , D. Spanò & G. Floris To cite this article: F. Pintus , R. Medda , A. C. Rinaldi , D. Spanò & G. Floris (2010) Euphorbia latex biochemistry: Complex interactions in a complex environment, Plant Biosystems, 144:2, 381-391, DOI: 10.1080/11263500903396016 To link to this article: https://doi.org/10.1080/11263500903396016 Published online: 04 Aug 2010. Submit your article to this journal Article views: 134 View related articles Citing articles: 9 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tplb20 Plant Biosystems, Vol. 144, No. 2, June 2010, pp. 381–391 Euphorbia latex biochemistry: Complex interactions in a complex environment F. PINTUS1, R. MEDDA1, A. C. RINALDI2, D. SPANÒ1, & G. FLORIS1 1Dipartimento di Scienze Applicate ai Biosistemi, Università di Cagliari, Italy and 2Dipartimento di Scienze e Tecnologie Biomediche, Università di Cagliari, Italy (TaylorReceived and Francis 25 November 2008; Accepted 7 May 2009) 10.1080/11263500903396016 Abstract Plant latex is a complex environment. Occurring in hundreds of plant species and contained in a tube system called laticifers, latex is a milky sap with a diverse composition that includes alkaloids, terpenoid compounds, other secondary metabolites and a number of enzymes. These substances are collectively believed to provide an important contribution to plant defence mechanisms by repelling and killing phytopathogens, and sealing wounded areas. This review provides insights of what is currently known about the biochemistry and molecular biology of plant latex, as studied in various model systems, above all the economically important rubber tree, Hevea brasiliensis. Selecting the Mediterranean shrub Euphorbia characias as a complementary experimental model, we have recently begun to disclose the properties of several components of the enzymatic machinery present in its latex. Although the scheme of multi-enzymatic interactions taking place in the E. characias latex depicted to date is certainly incomplete, the emerging scenario suggests that the role played by latex in plants might be significantly less passive than previously believed. Keywords: Amine oxidase, antiquitin, calmodulin, catalase, Euphorbia, peroxidase A large number of plant species may exudate an Plantae has not been explained to date (Pickard often milky, variously coloured sap known as latex. 2008). According to Kekwick (2001), latex occurs in some Latex is an emulsion with a diversified composition 12,500 species, belonging to 900 genera from that includes alkaloids, terpenoid compounds, poly- about 20 families – most of which are dicotyledons – meric substances, such as resins and gums, starch, oils, growing in different ecological settings. Indeed, latex and a large number of proteins and enzymatic activ- constitutes the cytoplasmic content of laticifers ities (Han et al. 2000; Kekwick 2001; Ko et al. 2003). (Hagel et al. 2008), specialised elongated cells or Currently, no universally shared view exists about the vessel-like series of cells that permeate various aerial biological role(s) of latex. A function as nutrition or tissues of the plant, including sometimes the fruits water reserve, or as an excretory product where waste and also the root system. Laticifers lack chloroplasts, plant metabolites are confined, has been repeatedly and are generally classified as articulated, that is, proposed. Most authors, however, consider it more composed of a longitudinal series of cells joined or likely that latex provides an important contribution to fused together, and as non-articulated, that is, plant defence mechanisms by repelling browsing descended from a single cell present in the embryo animals and insects, killing or controlling the growth that has grown in a branched or unbranched of microbial phytopathogens and sealing wounded manner. These structures and their features are areas (Kekwick 2001; Giordani et al. 2002). often used as elements to infer taxonomic and phylo- Most of our knowledge on the biochemistry of genetic relationships between specific plant groups latex and laticifers stems from studies on Hevea (Rudall 1994; Webster 1994; Vega et al. 2002), brasiliensis, a member of the Euphorbiaceae and an although the phyletic distribution of laticifers in the economically valuable tree as the main source of Correspondence: G. Floris, Dipartimento di Scienze Applicate ai Biosistemi, Università di Cagliari, Cittadella Universitaria, I–09042 Monserrato (CA), Italy. Tel: +39 070 6754519. Fax: +39 070 6754523. Email: [email protected] ISSN 1126-3504 print/ISSN 1724-5575 online © 2010 Società Botanica Italiana DOI: 10.1080/11263500903396016 Published online 04 Aug 2010 382 F. Pintus et al. natural rubber. The proteome of H. brasiliensis latex has been investigated in some detail also because it contains a range of proteins that can cause allergenic reactions in sensitised persons upon regular use of products made from natural rubber, such as health- care workers wearing examination and surgical gloves (Arif et al. 2004; Wagner et al. 2007). Our knowledge of the protein functions within Hevea latex, including lectin-binding proteins, and enzymes involved in the isoprenoid pathway, continues to progress, leading to the recent sketching of a new proposed model for rubber latex coagulation (see Wititsuwannakul et al. 2008). Conversely, relatively little is known on the biochemical features of the latex of plants belonging to the large genus Euphor- bia, although several authors are working to fill this gap (e.g., Yadav et al. 2006; Mazoir et al. 2008). We have selected the Mediterranean spurge, Euphorbia characias – a shrubby, non-succulent euphorb commonly occurring in various habitats (rocky hillsides, along road verges, in open woods and in olive groves) in vast areas of the Mediterranean basin – as an alternative and complementary experi- mental model to study the complexity of plant latex biochemistry (Figure 1). Figure 1. EuphorbiaThe characias, the Mediterraneanplant’s spurge: (a) Plant habit; (b)latex a detail of the leaves; and has(c) latex exudate frombeen a broken branch. extensively studied with characterisation of a large number of diterpene compounds, responsible for the plant’s irritant effect (Seip & Hecker 1983; Appendino et al. 2000; Corea et al. 2004). Screening of the latex of E. characias has also revealed the presence of numerous enzymes, some of which might well be directly or indirectly involved in plant defence mechanisms. The present review reports on the isolation and characterisation of several of these molecules (and/or of their genes), namely a peroxidase regulated by the Ca2+/calmodu- lin system, copper amine oxidase, catalase and antiq- uitin (Atq), and describes how these could interact between themselves and with other latex substances to assure some form of plant protection against invading pathogens and/or environmental stresses. It is our belief that what is learned on the biochemistry of E. characias latex will ultimately contribute to a broader understanding of the metabolism and func- tion of this plant product. Peroxidase and calmodulin The superfamily of haem-containing peroxidases (EC 1.11.1.7, donor: hydrogen peroxide oxidoreductase) is a widely distributed group of enzymes found in bacteria, fungi, plants and animals that utilise hydro- gen peroxide or other peroxides to catalyse a number of oxidative reactions (Welinder 1992). Non-animal Figure 1. Euphorbia characias, the Mediterranean spurge: (a) peroxidases can be divided into three classes on the Plant habit; (b) a detail of the leaves; and (c) latex exudate from a broken branch. basis of their amino acid sequence: Class I contains Euphorbia latex biochemistry 383 bacterial, fungal and plant intracellular enzymes from mitochondria and chloroplasts, such as ascorbate peroxidase and cytochrome c peroxidase; Class II consists of secreted fungal peroxidases, good exam- ples of these being manganese peroxidase and lignin- degrading peroxidase; Class III is made up of secreted plant peroxidases, with horseradish peroxidase (HRP) as its best-known member. Plant peroxidases – for which crystal structures and a number of site-directed mutants have become available in several cases along the years – are found in the cytosol, vacuole, apoplast or cell wall, and participate in crucial physiological events, such as development and growth induction, polymerisation of cell wall lignin and suberin precursors, auxin catabolism, wound healing and defence against pathogen infection (Passardi et al. 2005). Typically, Class III peroxidases may exist under an extremely high number of isoforms within the same species, potentially implicated in different functions (Veitch 2004). The HRP isozyme C, for example, one of the more than 30 isoforms of HRP, classified as acidic, neutral and basic forms, has been the archetypal example of Class III higher plant peroxidases. HRP- C is a single glycosylated polypeptide chain containing high-spin Fe3+ in a protoporphyrin IX pentacoordinated to a “proximal” histidine ligand that functions to stabilise the higher oxidation states of the iron atom (Poulos et al. 1993). Another histi- dine, known as the “distal”, functions as an acid– base catalyst to accept one proton from
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