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      Manipulation of Bryophyte Hosts by Pathogenic and Symbiotic Microbes

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          Abstract

          The colonization of plant tissues by pathogenic and symbiotic microbes is associated with a strong and directed effort to reprogram host cells in order to permit, promote and sustain microbial growth. In response to colonization, hosts accommodate or sequester invading microbes by activating a set of complex regulatory programs that initiate symbioses or bolster defenses. Extensive research has elucidated a suite of molecular and physiological responses occurring in plant hosts and their microbial partners; however, this information is mostly limited to model systems representing evolutionarily young plant lineages such as angiosperms. The extent to which these processes are conserved across land plants is therefore poorly understood. In this review, we outline key aspects of host reprogramming that occur during plant–microbe interactions in early diverging land plants belonging to the bryophytes (liverworts, hornworts and mosses). We discuss how further knowledge of bryophyte–microbe interactions will advance our understanding of how plants and microbes co-operated and clashed during the conquest of land.

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          Most cited references95

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          The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants.

          We report the draft genome sequence of the model moss Physcomitrella patens and compare its features with those of flowering plants, from which it is separated by more than 400 million years, and unicellular aquatic algae. This comparison reveals genomic changes concomitant with the evolutionary movement to land, including a general increase in gene family complexity; loss of genes associated with aquatic environments (e.g., flagellar arms); acquisition of genes for tolerating terrestrial stresses (e.g., variation in temperature and water availability); and the development of the auxin and abscisic acid signaling pathways for coordinating multicellular growth and dehydration response. The Physcomitrella genome provides a resource for phylogenetic inferences about gene function and for experimental analysis of plant processes through this plant's unique facility for reverse genetics.
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            Systemic acquired resistance: turning local infection into global defense.

            Systemic acquired resistance (SAR) is an induced immune mechanism in plants. Unlike vertebrate adaptive immunity, SAR is broad spectrum, with no specificity to the initial infection. An avirulent pathogen causing local programmed cell death can induce SAR through generation of mobile signals, accumulation of the defense hormone salicylic acid, and secretion of the antimicrobial PR (pathogenesis-related) proteins. Consequently, the rest of the plant is protected from secondary infection for a period of weeks to months. SAR can even be passed on to progeny through epigenetic regulation. The Arabidopsis NPR1 (nonexpresser of PR genes 1) protein is a master regulator of SAR. Recent study has shown that salicylic acid directly binds to the NPR1 adaptor proteins NPR3 and NPR4, regulates their interactions with NPR1, and controls NPR1 protein stability. However, how NPR1 interacts with TGA transcription factors to activate defense gene expression is still not well understood. In addition, redox regulators, the mediator complex, WRKY transcription factors, endoplasmic reticulum-resident proteins, and DNA repair proteins play critical roles in SAR.
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              A translocation signal for delivery of oomycete effector proteins into host plant cells.

              Bacterial, oomycete and fungal plant pathogens establish disease by translocation of effector proteins into host cells, where they may directly manipulate host innate immunity. In bacteria, translocation is through the type III secretion system, but analogous processes for effector delivery are uncharacterized in fungi and oomycetes. Here we report functional analyses of two motifs, RXLR and EER, present in translocated oomycete effectors. We use the Phytophthora infestans RXLR-EER-containing protein Avr3a as a reporter for translocation because it triggers RXLR-EER-independent hypersensitive cell death following recognition within plant cells that contain the R3a resistance protein. We show that Avr3a, with or without RXLR-EER motifs, is secreted from P. infestans biotrophic structures called haustoria, demonstrating that these motifs are not required for targeting to haustoria or for secretion. However, following replacement of Avr3a RXLR-EER motifs with alanine residues, singly or in combination, or with residues KMIK-DDK--representing a change that conserves physicochemical properties of the protein--P. infestans fails to deliver Avr3a or an Avr3a-GUS fusion protein into plant cells, demonstrating that these motifs are required for translocation. We show that RXLR-EER-encoding genes are transcriptionally upregulated during infection. Bioinformatic analysis identifies 425 potential genes encoding secreted RXLR-EER class proteins in the P. infestans genome. Identification of this class of proteins provides unparalleled opportunities to determine how oomycetes manipulate hosts to establish infection.
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                Author and article information

                Journal
                Plant Cell Physiol
                Plant Cell Physiol
                pcp
                Plant and Cell Physiology
                Oxford University Press
                0032-0781
                1471-9053
                April 2018
                21 November 2017
                21 November 2017
                : 59
                : 4 , Special Focus Issue: Cellular Reprogramming in Plants
                : 656-665
                Affiliations
                Sainsbury Laboratory, University of Cambridge, 47 Bateman Street, Cambridge, UK
                Author notes
                Corresponding author: E-mail: sebastian.schornack@ 123456slcu.cam.ac.uk
                Author information
                http://orcid.org/0000-0002-5467-7290
                Article
                pcx182
                10.1093/pcp/pcx182
                6018959
                29177478
                610533f4-85e5-43bb-89d5-017bdd090e6b
                © The Author 2017. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 September 2017
                : 7 November 2017
                Page count
                Pages: 10
                Funding
                Funded by: Gatsby Charitable Foundation 10.13039/501100000324
                Award ID: RG62472
                Funded by: Royal Society 10.13039/501100000288
                Award ID: RG69135
                Funded by: Natural Environment Research Council 10.13039/501100000270
                Award ID: NERC; NE/N00941X/1
                Categories
                Special Issue – Reviews

                Plant science & Botany
                bryophytes,fungi,hornworts,liverworts,plant–pathogen interactions,symbiosis
                Plant science & Botany
                bryophytes, fungi, hornworts, liverworts, plant–pathogen interactions, symbiosis

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