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      Genetic resistance in barley against Japanese soil-borne wheat mosaic virus functions in the roots

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          Abstract

          Infection by the Japanese soil-borne wheat mosaic virus (JSBWMV) can lead to substantial losses in the grain yield of barley and wheat crops. While genetically based resistance to this virus has been documented, its mechanistic basis remains obscure. In this study, the deployment of a quantitative PCR assay showed that the resistance acts directly against the virus rather than by inhibiting the colonization of the roots by the virus’ fungal vector Polymyxa graminis. In the susceptible barley cultivar (cv.) Tochinoibuki, the JSBWMV titre was maintained at a high level in the roots during the period December–April, and the virus was translocated from the root to the leaf from January onwards. In contrast, in the roots of both cv. Sukai Golden and cv. Haruna Nijo, the titre was retained at a low level, and translocation of the virus to the shoot was strongly suppressed throughout the host’s entire life cycle. The roots of wild barley ( Hordeum vulgare ssp. spontaneum) accession H602 responded in the early stages of infection similarly to those of the resistant cultivated forms, but the host was unable to suppress the translocation of the virus to the shoot from March onwards. The virus titre in the root was presumed to have been restricted by the action of the gene product of Jmv1 (on chromosome 2H), while the stochastic nature of the infection was suppressed by the action of that of Jmv2 (on chromosome 3H), a gene harbored by cv. Sukai Golden but not by either cv. Haruna Nijo or accession H602.

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          Most cited references39

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          Mechanisms of plant resistance to viruses.

          Plants have evolved in an environment rich with microorganisms that are eager to capitalize on the plants' biosynthetic and energy-producing capabilities. There are approximately 450 species of plant-pathogenic viruses, which cause a range of diseases. However, plants have not been passive in the face of these assaults, but have developed elaborate and effective defence mechanisms to prevent, or limit, damage owing to viral infection. Plant resistance genes confer resistance to various pathogens, including viruses. The defence response that is initiated after detection of a specific virus is stereotypical, and the cellular and physiological features associated with it have been well characterized. Recently, RNA silencing has gained prominence as an important cellular pathway for defence against foreign nucleic acids, including viruses. These pathways function in concert to result in effective protection against virus infection in plants.
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            Secondary plant metabolites in phytoremediation and biotransformation.

            For millennia, secondary plant metabolites have antagonized microorganisms, insects and humans alike, ultimately generating a complex and dynamic mixture of facultative and obligate interactions from symbioses to pathogenicity. Secondary plant metabolites have an important role in developing the myriad of organic pollutant-degrading enzymes found in nature. The link between secondary plant metabolites and enzymatic diversity has yet to be exploited, with potential applications in fields as varied as pest management, bioremediation and fine chemical production.
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              The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.).

              Virus diseases are widespread threats for crop production, which can, in many cases, be controlled efficiently by exploiting naturally occurring resistance. Barley, an important cereal species of the Triticeae, carries two genes, rym4 and rym5, which are located in the telomeric region of chromosome 3HL and confer recessive resistance to various strains of the Barley yellow mosaic virus complex. The barley 'eukaryotic translation initiation factor 4E' (Hv-eIF4E) was identified as a candidate for resistance gene function by physical mapping on a 650 kb contig. It is located in a chromosomal region characterized by suppressed recombination, in a position collinear to its homologue on rice chromosome 1L. Sequence diversity in the coding region of Hv-eIF4E, as calculated from a collection of unrelated barley accessions, revealed non-silent single nucleotide polymorphisms (SNPs) in four of its five exons. Stable transformation of a resistant barley genotype with a genomic fragment or a full-length cDNA of Hv-eIF4E derived from susceptible cultivars induced susceptibility to Barley mild mosaic virus. Moreover, the identification of SNPs diagnostic for rym4 and rym5 provides evidence that these are two alleles, which confer different resistance specificities. These findings demonstrate that variants of Hv-eIF4E confer multiallelic recessive virus resistance in a monocot species. The identification of eIF4E as the causal host factor for bymovirus resistance illustrates that mutations in this basic component of the eukaryotic translation complex form a seminal mechanism for recessive virus resistance in both dicot and monocot plants.
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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
                10 March 2023
                2023
                : 14
                : 1149752
                Affiliations
                [1] 1 Tochigi Prefectural Agricultural Experiment Station , Utsunomiya, Tochigi, Japan
                [2] 2 Crop Research Institute, Shandong Academy of Agricultural Sciences (SAAS) , Ji’nan, Shandong, China
                [3] 3 Institute of Crop Science, National Agriculture and Food Research Organization (NARO) , Kan-non-dai, Ibaraki, Japan
                [4] 4 Graduate School of Horticulture, Chiba University , Matsudo, Chiba, Japan
                Author notes

                Edited by: Ryo Fujimoto, Kobe University, Japan

                Reviewed by: Viktor Korzun, KWS SAAT SE & Co. KGaA, Germany; Yang Jian, Ningbo University, China; Ping Yang, Institute of Crop Sciences (CAAS), China

                *Correspondence: Takao Komatsuda, takao_komatsuda@ 123456kzc.biglobe.ne.jp ; Wenjing Xu, 992456577@ 123456qq.com

                †These authors have contributed equally to this work

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

                Article
                10.3389/fpls.2023.1149752
                10036763
                3ac72d6c-08a4-4065-93bc-a1d5ea66096f
                Copyright © 2023 Okada, Xu, Mishina, Oono, Kato, Namai and Komatsuda

                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
                : 23 January 2023
                : 17 February 2023
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 39, Pages: 8, Words: 3974
                Funding
                This research was supported by the Director’s Discretionary Research Funds 20902 (2017, 2018, and 2020) of NARO (to TK), the Innovation Program 2019 of NARO (to TK and YO), the Shandong Province Double-Hundred Talent Program (WST2020012 to TK), and the Shandong Academy of Agricultural Sciences Leading Talent Research Startup Fee (CXGC2021B01 to TK).
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                barley,soil-borne disease,polymyxa graminis,viral pathogenetic,genetic resistance,root

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