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(Musa Spp.) to the Burrowing Nematode Radopholus Similis

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(Musa Spp.) to the Burrowing Nematode Radopholus Similis Phenalenone-type phytoalexins mediate resistance of banana plants (Musa spp.) to the burrowing nematode Radopholus similis Dirk Hölschera,b,1,2, Suganthagunthalam Dhakshinamoorthyc,1, Theodore Alexandrovd,e,f,g, Michael Beckerh, Tom Bretschneideri, Andreas Buerkertb, Anna C. Creceliusj, Dirk De Waelec,k, Annemie Elsenl, David G. Heckelm, Heike Heklaun, Christian Hertwecki, Marco Kaio, Katrin Knopj, Christoph Krafftp, Ravi K. Maddulao, Christian Matthäusp, Jürgen Poppp,q, Bernd Schneidera, Ulrich S. Schubertj,r, Richard A. Sikoras, Aleš Svatošo, and Rony L. Swennenc,t,u aNuclear Magnetic Resonance Research Group, oMass Spectrometry Research Group, mDepartment of Entomology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; bDepartment of Organic Plant Production and Agroecosystems Research in the Tropics and Subtropics, University of Kassel, 37213 Witzenhausen, Germany; cLaboratory of Tropical Crop Improvement, Division of Crop Biotechnics, Faculty of Bioscience Engineering, Department of Biosystems, University of Leuven, 3001 Leuven, Belgium; dCenter for Industrial Mathematics, Department of Mathematics, University of Bremen, 28359 Bremen, Germany; eSteinbeis Innovation Center for Scientific Computing in Life Sciences, 28359 Bremen, Germany; fScientific Computing in Life Sciences (SCiLS) GmbH, 28359 Bremen, Germany; gSkaggs School of Pharmacy and Pharmaceutical Science, University of California, San Diego, La Jolla, CA 92093; hDepartment of Applications Matrix-Assisted Laser Desorption/Ionization - Time of Flight (MALDI-TOF), Bruker Daltonik GmbH, 28359 Bremen, Germany; iDepartment of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, 07745 Jena, Germany; jLaboratory of Organic and Macromolecular Chemistry, Jena Center for Soft Matter, qInstitute for Physical Chemistry and Abbe Center of Photonics, Department of Chemistry and Earth Sciences, Friedrich Schiller University of Jena, 07743 Jena, Germany; kUnit of Environmental Sciences and Management, Department of Nematology, North-West University, Potchefstroom 2520, South Africa; lDepartment of Research and Development, Soil Service of Belgium, 3001 Leuven Heverlee, Belgium; nDepartment of Geobotany, Martin Luther University of Halle-Wittenberg, 06108 Halle, Germany; pWorkgroup Spectroscopy/Imaging, Institute of Photonic Technology, 07745 Jena, Germany; rDutch Polymer Institute, 5612 AB, Eindhoven, The Netherlands; sInstitute of Crop Science and Resource Conservation-Phytomedicine, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany; tBioversity International, 3001 Leuven, Belgium; and uInternational Institute of Tropical Agriculture, Croydon CR9 3EE, United Kingdom Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved November 14, 2013 (received for review August 8, 2013) The global yield of bananas—one of the most important food accumulate through nontarget organisms in the food chain (7). crops—is severely hampered by parasites, such as nematodes, After the withdrawal of many effective nematicides, such as methyl which cause yield losses up to 75%. Plant–nematode interactions bromide, from the market (8), organophosphate and carbamate of two banana cultivars differing in susceptibility to Radopholus nematicides are still intensively applied to banana and therefore similis were investigated by combining the conventional and spa- continue to threaten the health of agricultural workers and the tially resolved analytical techniques 1H NMR spectroscopy, matrix- environment (9). Although several biological control approaches, free UV-laser desorption/ionization mass spectrometric imaging, and including the application of both single and multiple control Raman microspectroscopy. This innovative combination of analytical organisms—such as Fusarium oxysporum, Paecilomyces lilacinus, SCIENCES techniques was applied to isolate, identify, and locate the banana- Trichoderma atroviride isolates, and Bacillus firmus—have proved AGRICULTURAL specific type of phytoalexins, phenylphenalenones, in the R. similis- promising under greenhouse conditions, the control they confer caused lesions of the plants. The striking antinematode activity of to banana plants most probably does not protect plants for more the phenylphenalenone anigorufone, its ingestion by the nema- than one cycle in the field, and most of these organisms have yet tode, and its subsequent localization in lipid droplets within the to be tested under field conditions (10). nematode is reported. The importance of varying local concentra- tions of these specialized metabolites in infected plant tissues, their Significance involvement in the plant’s defense system, and derived strategies for improving banana resistance are highlighted. The ongoing decline of banana yields caused by pathogens and the use of toxic chemicals to manage them has attracted con- plant protection | induced plant defense | matrix-free LDI-MSI siderable attention because of the importance of bananas as a major staple food for more than 400 million people. We dem- ananas and plantains (Musa spp.) are among the world’s onstrate that secondary metabolites (phenylphenalenones) of Bmost important food and cash crops, with a global pro- Musa are the reason for differences in cultivar resistance, and duction of about 138 million tons in 2010. These crops are part of detected the phenylphenalenone anigorufone in greater con- a well-balanced human diet and are a major food staple for more centrations in lesions in roots of a nematode-resistant cultivar than 400 million people in the tropics (1, 2). About 82% of the than in those of a susceptible one. An in vitro bioassay identified world’s banana production is consumed locally, particularly in anigorufone as the most active nematostatic and nematocidal India, China, and many African countries (Table S1) (1, 2). Export compound. We discovered that large lipid–anigorufone complex of bananas to the northern hemisphere represents an important droplets are formed in the bodies of Radopholus similis exposed source of employment in countries such as Costa Rica, Ecuador, to anigorufone, resulting in the nematode being killed. Colombia, and the Philippines (Table S2) (1, 2). Banana yields are severely hampered by fungi, insects, and plant-parasitic nematodes. Author contributions: D.H., S.D., A.B., D.G.H., B.S., R.A.S., and R.L.S. designed research; D.H., S.D., M.B., T.B., A.C.C., H.H., M.K., K.K., R.K.M., and C.M. performed research; D.H., S.D., T.A., The burrowing nematode, Radopholus similis (Cobb, 1893) Thorne, T.B., A.C.C., D.D.W., A.E., M.K., K.K., C.K., C.M., J.P., U.S.S., and A.S. analyzed data; and D.H., 1949, is the key nematode pathogen, causing yield losses up to S.D., T.A., T.B., A.C.C., D.D.W., A.E., C.H., M.K., K.K., C.K., C.M., J.P., B.S., U.S.S., R.A.S., A.S., 75% (3). R. similis is found in all major banana-producing and R.L.S. wrote the paper. regions of the world; its best-known hosts are bananas, black The authors declare no conflict of interest. pepper, Citrus spp. (4), and coffee (5). R. similis causes extensive This article is a PNAS Direct Submission. root lesions that can lead to toppling of banana plants (6). 1D.H. and S.D. contributed equally to this work. Plant-parasitic nematodes have been effectively managed 2To whom correspondence should be addressed. E-mail: [email protected]. through the use of nematicides. However, their high toxicity has This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. adverse effects on humans and their toxic residues are known to 1073/pnas.1314168110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1314168110 PNAS | January 7, 2014 | vol. 111 | no. 1 | 105–110 Downloaded by guest on September 26, 2021 The in-depth investigation of the plant–nematode interactions at the cellular and molecular level could lead to the development of more rational and efficient control strategies (11). The pro- duction of toxic, herbivore-deterrent or -repellent secondary meta- bolites, which is typical for many plant defense systems, is particu- larly interesting in this context. Musa cultivars resistant to R. similis have been identified, especially the cultivar Yangambi km5 (Ykm5) (12). Histochemical and ultrastructural investigations of lesions caused by R. similis in Ykm5 revealed the accumulation of phenolic compounds in response to infection (13). Unfortunately, many of these studies were based solely on histochemical staining methods and did not identify the chemical structures of nematicidal sec- ondary metabolites (7, 14, 15). Initial phytochemical analyses of R. similis-infected roots of the Musa cultivar Pisang sipulu identified the phenylphenalenone anigorufone (1) as a phytoalexin produced in response to nematode damage and confirmed earlier suggestions of the significant role of phytoalexins in the plant defense system (16). Phenylphenalenones are a group of special phenylpropanoid- derived natural products (17), which are known as Musaceae phy- toalexins (18). The activity of phenylalanine ammonia lyase (EC 4.3.15), the entry-point enzyme of the phenylpropanoid pathway, is correlated to the biosynthesis of specific phenylpropanoids involved in defense and was substantially induced in nematode infected roots of Ykm5 (19). Phenylphenalenone-related compounds show bi- Fig. 1. Photographs of the root system of Musa spp. cv. GN and cv.Ykm5 ological activity against bacteria, fungi, algae, and diatoms (18, 20– infected with R. similis.(A) Young, developing,
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