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      Defense and Offense Strategies: The Role of Aspartic Proteases in Plant–Pathogen Interactions

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          Abstract

          Simple Summary

          Plants are sessile organisms that are continuously exposed to adverse environmental factors, both abiotic and biotic. Plant immunity is an intricate system that involves a remarkable array of structural, chemical, and protein-based layers of defense, aiming to stop pathogens before they cause irreversible damages. Proteases are an integral part of plant defense systems, with several hubs of action, from pathogen recognition and priming to the activation of plant hypersensitive response. Within this wide group of proteolytic enzymes, aspartic proteases have been implicated in several plant development functions and are gaining more prominence due to their involvement in plant–pathogen interactions. In this review, we summarize the current knowledge on plant and pathogenic aspartic proteases and highlight the most recent findings on their participation on plant defense, as well as in pathogen infection strategies.

          Abstract

          Plant aspartic proteases (APs; E.C.3.4.23) are a group of proteolytic enzymes widely distributed among different species characterized by the conserved sequence Asp-Gly-Thr at the active site. With a broad spectrum of biological roles, plant APs are suggested to undergo functional specialization and to be crucial in developmental processes, such as in both biotic and abiotic stress responses. Over the last decade, an increasing number of publications highlighted the APs’ involvement in plant defense responses against a diversity of stresses. In contrast, few studies regarding pathogen-secreted APs and AP inhibitors have been published so far. In this review, we provide a comprehensive picture of aspartic proteases from plant and pathogenic origins, focusing on their relevance and participation in defense and offense strategies in plant–pathogen interactions.

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          Most cited references116

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          Abiotic Stress Signaling and Responses in Plants.

          As sessile organisms, plants must cope with abiotic stress such as soil salinity, drought, and extreme temperatures. Core stress-signaling pathways involve protein kinases related to the yeast SNF1 and mammalian AMPK, suggesting that stress signaling in plants evolved from energy sensing. Stress signaling regulates proteins critical for ion and water transport and for metabolic and gene-expression reprogramming to bring about ionic and water homeostasis and cellular stability under stress conditions. Understanding stress signaling and responses will increase our ability to improve stress resistance in crops to achieve agricultural sustainability and food security for a growing world population.
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            The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database

            Abstract The MEROPS database (http://www.ebi.ac.uk/merops/) is an integrated source of information about peptidases, their substrates and inhibitors. The hierarchical classification is: protein-species, family, clan, with an identifier at each level. The MEROPS website moved to the EMBL-EBI in 2017, requiring refactoring of the code-base and services provided. The interface to sequence searching has changed and the MEROPS protein sequence libraries can be searched at the EMBL-EBI with HMMER, FastA and BLASTP. Cross-references have been established between MEROPS and the PANTHER database at both the family and protein-species level, which will help to improve curation and coverage between the resources. Because of the increasing size of the MEROPS sequence collection, in future only sequences of characterized proteins, and from completely sequenced genomes of organisms of evolutionary, medical or commercial significance will be added. As an example, peptidase homologues in four proteomes from the Asgard superphylum of Archaea have been identified and compared to other archaean, bacterial and eukaryote proteomes. This has given insights into the origins and evolution of peptidase families, including an expansion in the number of proteasome components in Asgard archaeotes and as organisms increase in complexity. Novel structures for proteasome complexes in archaea are postulated.
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              Disease Resistance Mechanisms in Plants

              Plants have developed a complex defense system against diverse pests and pathogens. Once pathogens overcome mechanical barriers to infection, plant receptors initiate signaling pathways driving the expression of defense response genes. Plant immune systems rely on their ability to recognize enemy molecules, carry out signal transduction, and respond defensively through pathways involving many genes and their products. Pathogens actively attempt to evade and interfere with response pathways, selecting for a decentralized, multicomponent immune system. Recent advances in molecular techniques have greatly expanded our understanding of plant immunity, largely driven by potential application to agricultural systems. Here, we review the major plant immune system components, state of the art knowledge, and future direction of research on plant–pathogen interactions. In our review, we will discuss how the decentralization of plant immune systems have provided both increased evolutionary opportunity for pathogen resistance, as well as additional mechanisms for pathogen inhibition of such defense responses. We conclude that the rapid advances in bioinformatics and molecular biology are driving an explosion of information that will advance agricultural production and illustrate how complex molecular interactions evolve.
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                Author and article information

                Contributors
                Role: Academic Editor
                Role: Academic Editor
                Role: Academic Editor
                Journal
                Biology (Basel)
                Biology (Basel)
                biology
                Biology
                MDPI
                2079-7737
                21 January 2021
                February 2021
                : 10
                : 2
                : 75
                Affiliations
                Biosystems & Integrative Sciences Institute, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal; lafigueiredo@ 123456fc.ul.pt (L.F.); aafigueiredo@ 123456fc.ul.pt (A.F.)
                Author notes
                [* ]Correspondence: absantos@ 123456fc.ul.pt ; Tel.: +351-217-522-448
                [†]

                These senior authors contributed to this work equally.

                Author information
                https://orcid.org/0000-0001-9299-840X
                https://orcid.org/0000-0001-7809-6813
                https://orcid.org/0000-0001-8156-7700
                Article
                biology-10-00075
                10.3390/biology10020075
                7909840
                33494266
                d69285e5-b0a8-46c8-a2db-5234818bf6db
                © 2021 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 23 November 2020
                : 19 January 2021
                Categories
                Review

                proteases,development and reproduction,plant immunity,plant–pathogen interaction

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