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      Changes in benzoxazinoid contents and the expression of the associated genes in rye ( Secale cereale L.) due to brown rust and the inoculation procedure

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          Abstract

          Benzoxazinoids (BXs) are secondary metabolites with diverse functions, but are primarily involved in protecting plants, mainly from the family Poaceae, against insects and fungal pathogens. Rye is a cereal crop that is highly resistant to biotic stresses. However, its susceptibility to brown rust caused by Puccinia recondita f. sp. secalis ( Prs) is still a major problem affecting its commercial production. Additionally, the genetic and metabolic factors related to this disease remain poorly characterized. In this study, we investigated whether and to what extent the brown rust infection and the inoculation procedure affect the contents of specific BXs (HBOA, GDIBOA, DIBOA, GDIMBOA, DIMBOA, and MBOA) and the expression of genes related to BX ( ScBx1–5, ScIgl, and Scglu). We revealed that treatments with water and a urediniospore suspension usually downregulate gene expression levels. Moreover, HBOA and DIBOA contents decreased, whereas the contents of the remaining metabolites increased. Specifically, the MBOA content increased more after the mock treatment than after the Prs treatment, whereas the increase in GDIBOA and GDIMBOA levels was usually due to the Prs infection, especially at two of the most critical time-points, 17 and 24 h post-treatment. Therefore, GDIBOA and GDIMBOA are glucosides that are important components of rye defence responses to brown rust. Furthermore, along with MBOA, they protect rye against the stress associated with the inoculation procedure used in this study.

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          Most cited references43

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          Wheat leaf rust caused by Puccinia triticina.

          Leaf rust, caused by Puccinia triticina, is the most common rust disease of wheat. The fungus is an obligate parasite capable of producing infectious urediniospores as long as infected leaf tissue remains alive. Urediniospores can be wind-disseminated and infect host plants hundreds of kilometres from their source plant, which can result in wheat leaf rust epidemics on a continental scale. This review summarizes current knowledge of the P. triticina/wheat interaction with emphasis on the infection process, molecular aspects of pathogenicity, rust resistance genes in wheat, genetics of the host parasite interaction, and the population biology of P. triticina. Puccinia triticina Eriks.: kingdom Fungi, phylum Basidiomycota, class Urediniomycetes, order Uredinales, family Pucciniaceae, genus Puccinia. Telial/uredinial (primary) hosts: common wheat (Triticum aestivum L.), durum wheat (T. turgidum L. var. durum), cultivated emmer wheat (T. dicoccon) and wild emmer wheat (T. dicoccoides), Aegilops speltoides, goatgrass (Ae. cylindrica), and triticale (X Triticosecale). Pycnial/aecial (alternative) hosts: Thalictrum speciosissimum (= T. flavum glaucum) and Isopyrum fumaroides. Leaf rust is characterized by the uredinial stage. Uredinia are up to 1.5 mm in diameter, erumpent, round to ovoid, with orange to brown uredinia that are scattered on both the upper and the lower leaf surfaces of the primary host. Uredinia produce urediniospores that are sub-globoid, average 20 microm in diameter and are orange-brown, with up to eight germ pores scattered in thick, echinulate walls. Wheat varieties that are fully susceptible have large uredinia without causing chlorosis or necrosis in the host tissues. Resistant wheat varieties are characterized by various responses from small hypersensitive flecks to small to moderate size uredinia that may be surrounded by chlorotic and/or necrotic zones. USDA Cereal Disease Laboratory: http://www.ars.usda.gov/mwa/cdl.
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            Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals.

            H Niemeyer (2009)
            Many cereals accumulate hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one. These benzoxazinoid hydroxamic acids are involved in defense of maize against various lepidopteran pests, most notably the European corn borer, in defense of cereals against various aphid species, and in allelopathy affecting the growth of weeds associated with rye and wheat crops. The role of benzoxazinoid hydroxamic acids in defense against fungal infection is less clear and seems to depend on the nature of the interactions at the plant-fungus interface. Efficient use of benzoxazinoid hydroxamic acids as resistance factors has been limited by the inability to selectively increase their levels at the plant growth stage and the plant tissues where they are mostly needed for a given pest. Although the biosynthesis of benzoxazinoid hydroxamic acids has been elucidated, the genes and mechanisms controlling their differential expression in different plant tissues and along plant ontogeny remain to be unraveled.
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              Metabolic Regulation of the Maize Rhizobiome by Benzoxazinoids

              The rhizobiome is an important regulator of plant growth and health. Plants shape their rhizobiome communities through production and release of primary and secondary root metabolites. Benzoxazinoids (BXs) are common tryptophan-derived secondary metabolites in grasses that regulate below- and aboveground biotic interactions. In addition to their biocidal activity, BXs can regulate plant-biotic interactions as semiochemicals or within-plant defence signals. However, the full extent and mechanisms by which BXs shape the root-associated microbiome has remained largely unexplored. Here, we have taken a global approach to examine the regulatory activity of BXs on the maize root metabolome and associated bacterial and fungal communities. Using untargeted mass spectrometry in combination with prokaryotic and fungal amplicon sequencing, we compared the impacts of three genetic mutations in different steps in the BX pathway. We show that BXs regulate global root metabolism and concurrently influence the rhizobiome in a root type-dependent manner. Correlation analysis between BX-controlled root metabolites and bacterial taxa suggests a dominant role for BX-dependent controlled metabolites, particularly flavonoids, in constraining a range of soil microbial taxa, while specifically stimulating methylophilic bacteria. Our study supports a multilateral model by which BXs control root-microbe interactions via a global regulatory function in root secondary metabolism.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: VisualizationRole: Writing – original draft
                Role: MethodologyRole: Visualization
                Role: MethodologyRole: Validation
                Role: Methodology
                Role: Formal analysis
                Role: Methodology
                Role: Software
                Role: ConceptualizationRole: SupervisionRole: ValidationRole: Writing – original draft
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 May 2020
                2020
                : 15
                : 5
                : e0233807
                Affiliations
                [1 ] Department of Plant Genetics, Breeding and Biotechnology, Institute of Biology, Warsaw University of Life Sciences (SGGW), Warsaw, Poland
                [2 ] Department of Genetic Engineering, Plant Breeding and Acclimatization Institute–National Research Institute, Radzików, Błonie, Poland
                [3 ] Department of Horticultural Plant Genetics and Breeding, Institute of Plant Genetics, Breeding and Biotechnology, University of Life Sciences in Lublin, Lublin, Poland
                [4 ] Department of Biochemistry and Crop Quality, Institute of Soil Science and Plant Cultivation—State Research Institute, Puławy, Poland
                [5 ] Department of Forest Silviculture, Institute of Forest Sciences, Warsaw University of Life Sciences (SGGW), Warsaw, Poland
                National Institute of Technology Rourkela, INDIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-4526-0418
                http://orcid.org/0000-0003-3595-5651
                http://orcid.org/0000-0001-6891-0471
                Article
                PONE-D-20-03469
                10.1371/journal.pone.0233807
                7259783
                32470009
                509c0628-446c-42d5-b61d-b3acd13905cb
                © 2020 Święcicka et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 February 2020
                : 12 May 2020
                Page count
                Figures: 7, Tables: 0, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: No. 015/19/B/NZ9/00921 and No. 2018/31/B/NZ9/00439
                Award Recipient :
                This study was financially supported by National Science Centre, grants: No. 2015/19/B/NZ9/00921 and No. 2018/31/B/NZ9/00439.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Rye
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Seedlings
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Maize
                Research and Analysis Methods
                Model Organisms
                Maize
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Maize
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Plant and Algal Models
                Maize
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Mycology
                Fungal Structure
                Appressoria
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Inbred Strains
                Biology and Life Sciences
                Biochemistry
                Biosynthesis
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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