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      Interspecific Potato Breeding Lines Display Differential Colonization Patterns and Induced Defense Responses after Ralstonia solanacearum Infection

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          Abstract

          Potato ( Solanum tuberosum L.) is one of the main hosts of Ralstonia solanacearum, the causative agent of bacterial wilt. This plant pathogen bacteria produce asymptomatic latent infections that promote its global spread, hindering disease control. A potato breeding program is conducted in Uruguay based on the introgression of resistance from the wild native species S. commersonii Dun. Currently, several backcrosses were generated exploiting the high genetic variability of this wild species resulting in advanced interspecific breeding lines with different levels of bacterial wilt resistance. The overall aim of this work was to characterize the interaction of the improved potato germplasm with R. solanacearum. Potato clones with different responses to R. solanacearum were selected, and colonization, dissemination and multiplication patterns after infection were evaluated. A R. solanacearum strain belonging to the phylotype IIB-sequevar 1, with high aggressiveness on potato was genetically modified to constitutively generate fluorescence and luminescence from either the green fluorescence protein gene or lux operon. These reporter strains were used to allow a direct and precise visualization of fluorescent and luminescent cells in plant tissues by confocal microscopy and luminometry. Based on wilting scoring and detection of latent infections, the selected clones were classified as susceptible or tolerant, while no immune-like resistance response was identified. Typical wilting symptoms in susceptible plants were correlated with high concentrations of bacteria in roots and along the stems. Tolerant clones showed a colonization pattern restricted to roots and a limited number of xylem vessels only in the stem base. Results indicate that resistance in potato is achieved through restriction of bacterial invasion and multiplication inside plant tissues, particularly in stems. Tolerant plants were also characterized by induction of anatomical and biochemical changes after R. solanacearum infection, including hyperplasic activity of conductor tissue, tylose production, callose and lignin deposition, and accumulation of reactive oxygen species. This study highlights the potential of the identified tolerant interspecific potato clones as valuable genetic resources for potato-breeding programs and leads to a better understanding of resistance against R. solanacearum in potato.

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          Most cited references48

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          THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.

          Rapid generation of superoxide and accumulation of H2O2 is a characteristic early feature of the hypersensitive response following perception of pathogen avirulence signals. Emerging data indicate that the oxidative burst reflects activation of a membrane-bound NADPH oxidase closely resembling that operating in activated neutrophils. The oxidants are not only direct protective agents, but H2O2 also functions as a substrate for oxidative cross-linking in the cell wall, as a threshold trigger for hypersensitive cell death, and as a diffusible signal for induction of cellular protectant genes in surrounding cells. Activation of the oxidative burst is a central component of a highly amplified and integrated signal system, also involving salicylic acid and perturbations of cytosolic Ca2+, which underlies the expression of disease-resistance mechanisms.
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            Pathogenomics of the Ralstonia solanacearum species complex.

            Ralstonia solanacearum is a major phytopathogen that attacks many crops and other plants over a broad geographical range. The extensive genetic diversity of strains responsible for the various bacterial wilt diseases has in recent years led to the concept of an R. solanacearum species complex. Genome sequencing of more than 10 strains representative of the main phylogenetic groups has broadened our knowledge of the evolution and speciation of this pathogen and led to the identification of novel virulence-associated functions. Comparative genomic analyses are now opening the way for refined functional studies. The many molecular determinants involved in pathogenicity and host-range specificity are described, and we also summarize current understanding of their roles in pathogenesis and how their expression is tightly controlled by an intricate virulence regulatory network.
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              The role of the secondary cell wall in plant resistance to pathogens

              Plant resistance to pathogens relies on a complex network of constitutive and inducible defensive barriers. The plant cell wall is one of the barriers that pathogens need to overcome to successfully colonize plant tissues. The traditional view of the plant cell wall as a passive barrier has evolved to a concept that considers the wall as a dynamic structure that regulates both constitutive and inducible defense mechanisms, and as a source of signaling molecules that trigger immune responses. The secondary cell walls of plants also represent a carbon-neutral feedstock (lignocellulosic biomass) for the production of biofuels and biomaterials. Therefore, engineering plants with improved secondary cell wall characteristics is an interesting strategy to ease the processing of lignocellulosic biomass in the biorefinery. However, modification of the integrity of the cell wall by impairment of proteins required for its biosynthesis or remodeling may impact the plants resistance to pathogens. This review summarizes our understanding of the role of the plant cell wall in pathogen resistance with a focus on the contribution of lignin to this biological process.
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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
                28 August 2017
                2017
                : 8
                : 1424
                Affiliations
                [1] 1Departamento de Biociencias, Facultad de Química, Universidad de la República Montevideo, Uruguay
                [2] 2Unidad de Horticultura, INIA Las Brujas Canelones, Uruguay
                [3] 3Departamento de Producción Vegetal, Centro Regional Sur, Facultad de Agronomía, Universidad de la República Canelones, Uruguay
                [4] 4Instituto de Biología Molecular y Celular de Rosario (CONICET-UNR) Rosario, Argentina
                [5] 5Área Biología Molecular, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario Rosario, Argentina
                [6] 6Área Biología Vegetal (CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario Rosario, Argentina
                [7] 7Center for Research in Agricultural Genomics, CSIC, IRTA, UAB, UB Barcelona, Spain
                [8] 8Department of Genetics, Universitat de Barcelona Barcelona, Spain
                Author notes

                Edited by: Philippe Prior, INRA, France

                Reviewed by: Jose Ignacio Ruiz De Galarreta, NEIKER, Spain; Carlos Alberto Lopes, Brazilian Agricultural Research Corporation, Brazil

                *Correspondence: María I. Siri, msiri@ 123456fq.edu.uy

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

                Article
                10.3389/fpls.2017.01424
                5581342
                28894453
                cef84ed9-98c4-46ec-8165-462e2209a111
                Copyright © 2017 Ferreira, Pianzzola, Vilaró, Galván, Tondo, Rodriguez, Orellano, Valls and Siri.

                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) or licensor 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
                : 30 June 2017
                : 02 August 2017
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 55, Pages: 14, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                bacterial wilt,ralstonia solanacearum,potato,solanum commersonii,plant breeding,disease resistance,latent infections

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