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      Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture

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          Abstract

          The mutualistic association of roots with ectomycorrhizal fungi promotes plant health and is a hallmark of boreal and temperate forests worldwide. In the pre-colonization phase, before direct contact, lateral root (LR) production is massively stimulated, yet little is known about the signals exchanged during this step. Here, we identify sesquiterpenes (SQTs) as biologically active agents emitted by Laccaria bicolor while interacting with Populus or Arabidopsis. We show that inhibition of fungal SQT production by lovastatin strongly reduces LR proliferation and that (–)-thujopsene, a low-abundance SQT, is sufficient to stimulate LR formation in the absence of the fungus. Further, we show that the ectomycorrhizal ascomycote, Cenococcum geophilum, which cannot synthesize SQTs, does not promote LRs. We propose that the LR-promoting SQT signal creates a win-win situation by enhancing the root surface area for plant nutrient uptake and by improving fungal access to plant-derived carbon via root exudates.

          Abstract

          Soil-dwelling ectomycorrhizal fungi trigger remodelling of root architecture as part of a mutualistic symbiotic relationship with host plants. Here, Ditengou et al. identify fungal-derived sesquiterpenes as volatile signals capable of stimulating lateral root production in Arabidopsis and Populus.

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          Most cited references49

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          Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.

          Cell expansion is a central process in plant morphogenesis, and the elongation of roots and root hairs is essential for uptake of minerals and water from the soil. Ca2+ influx from the extracellular store is required for (and sets the rates of) cell elongation in roots. Arabidopsis thaliana rhd2 mutants are defective in Ca2+ uptake and consequently cell expansion is compromised--rhd2 mutants have short root hairs and stunted roots. To determine the regulation of Ca2+ acquisition in growing root cells we show here that RHD2 is an NADPH oxidase, a protein that transfers electrons from NADPH to an electron acceptor leading to the formation of reactive oxygen species (ROS). We show that ROS accumulate in growing wild-type (WT) root hairs but their levels are markedly decreased in rhd2 mutants. Blocking the activity of the NADPH oxidase with diphenylene iodonium (DPI) inhibits ROS formation and phenocopies Rhd2-. Treatment of rhd2 roots with ROS partly suppresses the mutant phenotype and stimulates the activity of plasma membrane hyperpolarization-activated Ca2+ channels, the predominant root Ca2+ acquisition system. This indicates that NADPH oxidases control development by making ROS that regulate plant cell expansion through the activation of Ca2+ channels.
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            Recruitment of entomopathogenic nematodes by insect-damaged maize roots.

            Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E)-beta-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E)-beta-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-beta-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.
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              Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root.

              The balance between cellular proliferation and differentiation is a key aspect of development in multicellular organisms. Using high-resolution expression data from the Arabidopsis root, we identified a transcription factor, UPBEAT1 (UPB1), that regulates this balance. Genomewide expression profiling coupled with ChIP-chip analysis revealed that UPB1 directly regulates the expression of a set of peroxidases that modulate the balance of reactive oxygen species (ROS) between the zones of cell proliferation and the zone of cell elongation where differentiation begins. Disruption of UPB1 activity alters this ROS balance, leading to a delay in the onset of differentiation. Modulation of either ROS balance or peroxidase activity through chemical reagents affects the onset of differentiation in a manner consistent with the postulated UPB1 function. This pathway functions independently of auxin and cytokinin plant hormonal signaling. Comparison to ROS-regulated growth control in animals suggests that a similar mechanism is used in plants and animals. Copyright © 2010 Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                23 February 2015
                : 6
                : 6279
                Affiliations
                [1 ]Institute of Biology II, Faculty of Biology, Albert-Ludwigs-University of Freiburg , Schänzlestrasse 1, D-79104 Freiburg, Germany
                [2 ]Forest Botany and Tree Physiology, Georg-August Universität Göttingen , Büsgenweg 2, D-37077 Göttingen, Germany
                [3 ]Research Unit Environmental Simulation, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München—German Research Center for Environmental Health (GmbH) , Ingolstädter Landstrasse 1, D-85764 Neuherberg, Germany
                [4 ]Umeå Plant Science Center, Department for Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences , SE-901 83 Umeå, Sweden
                [5 ]INRA and Lorraine University, UMR 1136, Interactions Arbres/Micro-organismes, Centre INRA de Nancy , 54280 Champenoux, France
                [6 ]BIOSS Centre of Biological Systems Analysis, Albert-Ludwigs-University of Freiburg , Habsburgerstrasse 49, D-79104 Freiburg, Germany
                [7 ]Freiburg Institute of Advanced Sciences (FRIAS), Albert-Ludwigs-University of Freiburg , Albertstrasse 19, D-79104 Freiburg, Germany
                [8 ]Centre for Biological Signalling Studies (BIOSS), Albert-Ludwigs-University of Freiburg , Schänzlestrasse 18, D-79104 Freiburg, Germany
                Author notes
                [*]

                These authors contributed equally to this work

                [†]

                Present address: University Blaise Pascal and INRA, UMR 547 PIAF, 24 avenue des Landais, BP 80026 63171 Aubière Cedex, France

                Author information
                http://orcid.org/0000-0002-0444-822X
                Article
                ncomms7279
                10.1038/ncomms7279
                4346619
                25703994
                4c81a84d-5242-4816-a0e3-706a295c76cb
                Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 27 June 2014
                : 13 January 2015
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