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      The Plant Cuticle: An Ancient Guardian Barrier Set Against Long-Standing Rivals

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          Abstract

          The aerial surfaces of plants are covered by a protective barrier formed by the cutin polyester and waxes, collectively referred to as the cuticle. Plant cuticles prevent the loss of water, regulate transpiration, and facilitate the transport of gases and solutes. As the cuticle covers the outermost epidermal cell layer, it also acts as the first line of defense against environmental cues and biotic stresses triggered by a large array of pathogens and pests, such as fungi, bacteria, and insects. Numerous studies highlight the cuticle interface as the site of complex molecular interactions between plants and pathogens. Here, we outline the multidimensional roles of cuticle-derived components, namely, epicuticular waxes and cutin monomers, during plant interactions with pathogenic fungi. We describe how certain wax components affect various pre-penetration and infection processes of fungi with different lifestyles, and then shift our focus to the roles played by the cutin monomers that are released from the cuticle owing to the activity of fungal cutinases during the early stages of infection. We discuss how cutin monomers can activate fungal cutinases and initiate the formation of infection organs, the significant impacts of cuticle defects on the nature of plant–fungal interactions, along with the possible mechanisms raised thus far in the debate on how host plants perceive cutin monomers and/or cuticle defects to elicit defense responses.

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          Most cited references100

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          Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi.

          Approximately a tenth of all described fungal species can cause diseases in plants. A common feature of this process is the necessity to pass through the plant cell wall, an important barrier against pathogen attack. To this end, fungi possess a diverse array of secreted enzymes to depolymerize the main structural polysaccharide components of the plant cell wall, i.e., cellulose, hemicellulose, and pectin. Recent advances in genomic and systems-level studies have begun to unravel this diversity and have pinpointed cell wall-degrading enzyme (CWDE) families that are specifically present or enhanced in plant-pathogenic fungi. In this review, we discuss differences between the CWDE arsenal of plant-pathogenic and non-plant-pathogenic fungi, highlight the importance of individual enzyme families for pathogenesis, illustrate the secretory pathway that transports CWDEs out of the fungal cell, and report the transcriptional regulation of expression of CWDE genes in both saprophytic and phytopathogenic fungi.
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            Sealing plant surfaces: cuticular wax formation by epidermal cells.

            The vital importance of plant surface wax in protecting tissue from environmental stresses is reflected in the huge commitment of epidermal cells to cuticle formation. During cuticle deposition, a massive flux of lipids occurs from the sites of lipid synthesis in the plastid and the endoplasmic reticulum to the plant surface. Recent genetic studies in Arabidopsis have improved our understanding of fatty acid elongation and of the subsequent modification of the elongated products into primary alcohols, wax esters, secondary alcohols, and ketones, shedding light on the enzymes involved in these pathways. In contrast, the biosynthesis of alkanes is still poorly understood, as are the mechanisms of wax transport from the site of biosynthesis to the cuticle. Currently, nothing is known about wax trafficking from the endoplasmic reticulum to the plasma membrane, or about translocation through the cell wall to the cuticle. However, a first breakthrough toward an understanding of wax export recently came with the discovery of ATP binding cassette (ABC) transporters that are involved in releasing wax from the plasma membrane into the apoplast. An overview of our present knowledge of wax biosynthesis and transport and the regulation of these processes during cuticle assembly is presented, including the evidence for coordination of cutin polyester and wax production.
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              The formation and function of plant cuticles.

              The plant cuticle is an extracellular hydrophobic layer that covers the aerial epidermis of all land plants, providing protection against desiccation and external environmental stresses. The past decade has seen considerable progress in assembling models for the biosynthesis of its two major components, the polymer cutin and cuticular waxes. Most recently, two breakthroughs in the long-sought molecular bases of alkane formation and polyester synthesis have allowed construction of nearly complete biosynthetic pathways for both waxes and cutin. Concurrently, a complex regulatory network controlling the synthesis of the cuticle is emerging. It has also become clear that the physiological role of the cuticle extends well beyond its primary function as a transpiration barrier, playing important roles in processes ranging from development to interaction with microbes. Here, we review recent progress in the biochemistry and molecular biology of cuticle synthesis and function and highlight some of the major questions that will drive future research in this field.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                25 June 2021
                2021
                : 12
                : 663165
                Affiliations
                [1] 1Department of Vegetable and Field Crops, Institute of Plant Sciences, Agricultural Research Organization (ARO), Volcani Center , Rishon LeZion, Israel
                [2] 2Plant Pathology and Microbiology Department, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem , Rehovot, Israel
                [3] 3Department of Plant and Environmental Sciences, Weizmann Institute of Science , Rehovot, Israel
                Author notes

                Edited by: Eva Domínguez, Consejo Superior de Investigaciones Científicas, Spanish National Research Council (CSIC), Spain

                Reviewed by: Mario Serrano, National Autonomous University of Mexico, Mexico; Christiane Nawrath, University of Lausanne, Switzerland, in collaboration with reviewer Ulrich Schaffrath

                *Correspondence: Hagai Cohen, hagaic@ 123456volcani.agri.gov.il

                This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2021.663165
                8267416
                34249035
                280000d7-e636-4db8-8726-7dfacca03550
                Copyright © 2021 Arya, Sarkar, Manasherova, Aharoni and Cohen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 02 February 2021
                : 31 May 2021
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 100, Pages: 10, Words: 9495
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                plant cuticle,pathogenic fungi,defense response,epicuticular wax,plant-pathogen interactions

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