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1. Split-root assays for studying legume–rhizobia symbioses, rhizodeposition, and belowground nitrogen transfer in legumes

Author

Malinda S. Thilakarathna and Kevin R. Cope

Subjects
0106 biological sciences, 0301 basic medicine, Nitrogen, Physiology, chemistry.chemical_element, Plant Science, Root system, Biology, Plant Root Nodulation, Plant Roots, 01 natural sciences, Rhizobia, 03 medical and health sciences, Symbiosis, Nitrogen Fixation, Botany, Legume, Abiotic component, fungi, food and beverages, Fabaceae, biology.organism_classification, 030104 developmental biology, chemistry, Shoot, Nitrogen fixation, Root Nodules, Plant, Rhizobium, 010606 plant biology & botany
Abstract

Split-root assays have been used widely in studies focused on understanding the complex regulatory mechanisms in legume–rhizobia symbioses, root nitrogen rhizodeposition, and belowground nitrogen transfer, and the effects of different biotic/abiotic factors on this symbiotic interaction. This assay allows a plant to have a root system that is physically divided into two distinct sections that are both still attached to a common shoot. Thus, each root section can be treated separately to monitor local and systemic plant responses. Different techniques are used to establish split-root assemblies, including double-pot systems, divided growth pouches, elbow root assembly, twin-tube systems, a single pot or chamber with a partition in the center, and divided agar plates. This review is focused on discussing the various types of split-root assays currently used in legume-based studies, and their associated advantages and limitations. Furthermore, this review also focuses on how split-root assays have been used for studies on nitrogen rhizodeposition, belowground nitrogen transfer, systemic regulation of nodulation, and biotic and abiotic factors affecting legume–rhizobia symbioses.

Published
2021
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2. Perception of lipo-chitooligosaccharides by the bioenergy cropPopulus

Author

Thomas B. Irving, Sanhita Chakraborty, Kevin R. Cope, and Jean-Michel Ané

Subjects
Crops, Agricultural, Lipopolysaccharides, 0106 biological sciences, 0301 basic medicine, Organogenesis, Review, Plant Science, 01 natural sciences, Rhizobia, Crop, 03 medical and health sciences, Symbiosis, Bioenergy, Mycorrhizae, Mycorrhizal fungi, Botany, Gene, biology, fungi, food and beverages, biology.organism_classification, Populus, 030104 developmental biology, Biofuels, Nuclear calcium, Root Nodules, Plant, Rhizobium, 010606 plant biology & botany
Abstract

Populus sp. is a developing feedstock for second-generation biofuel production. To ensure its success as a sustainable biofuel source, it is essential to capitalize on the ability of Populus sp. to associate with beneficial plant-associated microbes (e.g., mycorrhizal fungi) and engineer Populus sp. to associate with non-native symbionts (e.g., rhizobia). Here, we review recent research into the molecular mechanisms that control ectomycorrhizal associations in Populus sp. with particular emphasis on the discovery that ectomycorrhizal fungi produce lipochitooligosaccharides capable of activating the common symbiosis pathway. We also present new evidence that lipo-chitooligosaccharides produced by both ectomycorrhizal fungi and various species of rhizobia that do not associate with Populus sp. can induce nuclear calcium spiking in the roots of Populus sp. Thus, we argue Populus sp. already possesses the molecular machinery necessary for perceiving rhizobia, and the next step in engineering symbiosis with rhizobia should be focused on inducing bacterial accommodation and nodule organogenesis. The gene Nodule INception is central to these processes, and several putative orthologs are present in Populus sp. Manipulating the promoters of these genes to match that of plants in the nitrogen-fixing clade may be sufficient to introduce nodulation in Populus sp.

Published
2021
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3. The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots

Author

Nathaniel Schleif, Steven H. Strauss, Emmeline Fung, Sara S. Jawdy, Heike Bücking, Jessy Labbé, Edward Steigerwald, Fabienne Maillet, Tomás Allen Rush, Virginie Puech-Pagès, Kimberly G. Schnell, Kevin R. Cope, Muthusubramanian Venkateshwaran, Junko Maeda, Jean-Michel Ané, Cathleen Ma, Kevin Garcia, Guillaume Bécard, Jonathan Setzke, Patricia Jargeat, Yunqian Wang, Adeline Bascaules, Thomas B. Irving, University of Wisconsin-Madison, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Oregon State University (OSU), Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC, South Dakota State University (SDSTATE), Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Evolution et Diversité Biologique (EDB), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Interactions Microbiennes dans la Rhizosphère et les Racines, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Evolution des Interactions Plantes-Microorganismes, Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), United States Department of Agriculture (USDA) : 2017-67014-26530 WIS01695, National Science Foundation (NSF) : DGE-1256259, United States Department of Energy (DOE) : DE-SC0018247, National Science Foundation (NSF) : 1546742, 1331098, Tree Genomics and Biosafety Cooperative at Oregon State University, NSF Center for Advanced Forestry Systems : 1238305, Plant-Microbe Interfaces Scientific Focus Area in the Genomic Science Program, Office of Biological and Environmental Research in the DOE, Office of Science, United States Department of Energy (DOE) : DE-AC05-00OR22725, ANR-14-CE18-0008,NICE CROPS,Bio-stimulateurs chitiniques naturels pour une agriculture durable(2014), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010), ANR-11-INBS-0010,METABOHUB,Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation(2011), Erist, Montpellier, Appel à projets générique - Bio-stimulateurs chitiniques naturels pour une agriculture durable - - NICE CROPS2014 - ANR-14-CE18-0008 - Appel à projets générique - VALID, Towards a Unified theory of biotic Interactions: the roLe of environmental - - TULIP2010 - ANR-10-LABX-0041 - LABX - VALID, Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation - - METABOHUB2011 - ANR-11-INBS-0010 - INBS - VALID, Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), MetaToul Agromix, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), and Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
0106 biological sciences, 0301 basic medicine, Lipopolysaccharides, MESH: Signal Transduction, [SDV]Life Sciences [q-bio], Plant Science, Fungus, Biology, Root hair, Photosynthesis, MESH: Plant Roots / microbiology, 01 natural sciences, MESH: Lipopolysaccharides / chemistry, [SDV.BV.BOT] Life Sciences [q-bio]/Vegetal Biology/Botanics, Laccaria, 03 medical and health sciences, Symbiosis, Laccaria bicolor, MESH: Calcium / metabolism, Mycorrhizae, Botany, MESH: Populus / metabolism, Colonization, MESH: Gene Expression Regulation, Plant, MESH: Mycorrhizae / physiology, Research Articles, [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Lateral root, fungi, Cell Biology, [SDV.EE.IEO] Life Sciences [q-bio]/Ecology, environment/Symbiosis, 15. Life on land, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, biology.organism_classification, [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, MESH: Laccaria / metabolism, 030104 developmental biology, Populus, MESH: Symbiosis / physiology, Actinorhizal plant, 010606 plant biology & botany, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor. Compared with the wildtype Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.

Published
2019
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4. Harnessing Soil Microbes to Improve Plant Phosphate Efficiency in Cropping Systems

Author

Jaya Krishna Yakha, Heike Bücking, Rachel Raths, Kevin R. Cope, Senthil Subramanian, Arjun Kafle, and Kevin Garcia

Subjects
0106 biological sciences, Agroecosystem, arbuscular mycorrhizal symbiosis, chemistry.chemical_element, 01 natural sciences, lcsh:Agriculture, Crop, phosphate efficiency, 03 medical and health sciences, chemistry.chemical_compound, Ecosystem, 030304 developmental biology, 0303 health sciences, business.industry, Phosphorus, fungi, lcsh:S, food and beverages, ectomycorrhizal symbiosis, Phosphate, Phosphate solubilizing bacteria, phosphate solubilizing bacteria, chemistry, Agronomy, Agriculture, Environmental science, business, Agronomy and Crop Science, Cropping, 010606 plant biology & botany
Abstract

Phosphorus is an essential macronutrient required for plant growth and development. It is central to many biological processes, including nucleic acid synthesis, respiration, and enzymatic activity. However, the strong adsorption of phosphorus by minerals in the soil decreases its availability to plants, thus reducing the productivity of agricultural and forestry ecosystems. This has resulted in a complete dependence on non-renewable chemical fertilizers that are environmentally damaging. Alternative strategies must be identified and implemented to help crops acquire phosphorus more sustainably. In this review, we highlight recent advances in our understanding and utilization of soil microbes to both solubilize inorganic phosphate from insoluble forms and allocate it directly to crop plants. Specifically, we focus on arbuscular mycorrhizal fungi, ectomycorrhizal fungi, and phosphate-solubilizing bacteria. Each of these play a major role in natural and agroecosystems, and their use as bioinoculants is an increasing trend in agricultural practices.

Published
2019
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5. Mediation of plant-mycorrhizal interaction by a lectin receptor-like kinase

Author

Kaijie Zheng, Joel Martin, Jeremy Schmutz, Lee E. Gunter, Zhihao Zhang, Anthony C. Bryan, Juan Wang, Daniel Jacobson, Lucas Gontijo Silva Maia, Meng Xie, Xiaoping Wang, Ritesh Mewalal, Jessy Labbé, Xiaohan Yang, Olaf Czarnecki, Wendy Schackwitz, Priya Ranjan, Kerrie Barry, Gerald A. Tuskan, Peter Meidl, Sara S. Jawdy, Erika Lindquist, Jin Zhang, Ting Li, Kevin R. Cope, Jin-Gui Chen, Timothy J. Tschaplinski, Hemeng Wang, Wellington Muchero, Jennifer L. Morrell-Falvey, Yongil Yang, Jean-Michel Ané, Dongfang Wang, François Le Tacon, Oak Ridge National Laboratory, University of Wisconsin-Madison, DOE Joint Genome Inst, Interactions Arbres-Microorganismes (IAM), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL), LabEx ARBRE : Advanced Research on the Biology of Tree and Forest Ecosystems ([LabEx ARBRE]), and Office National des Forêts (ONF)-AgroParisTech-Institut National de la Recherche Agronomique (INRA)-Centre National de la Propriété Forestière-CRITT Bois-European Forest Institute = Institut Européen de la Forêt = Euroopan metsäinstituutti (EFI)-Université de Lorraine (UL)

Subjects
0106 biological sciences, 0301 basic medicine, [SDV]Life Sciences [q-bio], Plant Science, Fungus, Biology, 01 natural sciences, Plant Roots, Laccaria, 03 medical and health sciences, Symbiosis, Gene mapping, Laccaria bicolor, Mycorrhizae, Receptor like kinase, Plant Proteins, Genetics, Kinase, fungi, Lectin, biology.organism_classification, 030104 developmental biology, Populus, biology.protein, Molecular targets, Protein Kinases, 010606 plant biology & botany
Abstract

International audience; The molecular mechanisms underlying mycorrhizal symbioses, the most ubiquitous and impactful mutualistic plant-microbial interaction in nature, are largely unknown. Through genetic mapping, resequencing and molecular validation, we demonstrate that a G-type lectin receptor-like kinase (lecRLK) mediates the symbiotic interaction between Populus and the ectomycorrhizal fungus Laccaria bicolor. This finding uncovers an important molecular step in the establishment of symbiotic plant-fungal associations and provides a molecular target for engineering beneficial mycorrhizal relationships.

Published
2016
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6. Sensitivity of Seven Diverse Species to Blue and Green Light: Interactions With Photon Flux

Author

Chase Snowden, Kevin R. Cope, Bruce Bugbee, and PLOS

Subjects
0106 biological sciences, 0301 basic medicine, Chlorophyll, Pigments, Leaves, Chloroplasts, Light, Daily light integral, lcsh:Medicine, Plant Science, Photosynthetic efficiency, 01 natural sciences, Biochemistry, chemistry.chemical_compound, Solanum lycopersicum, Vegetables, Photosynthesis, lcsh:Science, Flowering Plants, green light, Multidisciplinary, Ecology, Plant Stems, Plant Biochemistry, Plant Anatomy, Physics, Electromagnetic Radiation, food and beverages, Agriculture, Plants, Lettuce, Horticulture, Physical Sciences, Wheat, Other Plant Sciences, Cellular Structures and Organelles, Cellular Types, Capsicum, Research Article, Ecological Metrics, Plant Cell Biology, Materials Science, Soil Science, Crops, Brassica, Biology, 03 medical and health sciences, Shade avoidance, Dry weight, Plant Cells, Pepper, Botany, Grasses, Materials by Attribute, Sunlight, Photons, Organic Pigments, lcsh:R, Ecology and Environmental Sciences, Plant Sciences, Organisms, Biology and Life Sciences, Cell Biology, sensitivity, blue light, photon flux, Photosynthetic Efficiency, Plant Leaves, 030104 developmental biology, chemistry, Radish, lcsh:Q, Cucumis sativus, 010606 plant biology & botany, Crop Science, Cereal Crops
Abstract

Despite decades of research, the effects of spectral quality on plant growth, and development are not well understood. Much of our current understanding comes from studies with daily integrated light levels that are less than 10% of summer sunlight thus making it difficult to characterize interactions between light quality and quantity. Several studies have reported that growth is increased under fluorescent lamps compared to mixtures of wavelengths from LEDs. Conclusions regarding the effect of green light fraction range from detrimental to beneficial. Here we report the effects of eight blue and green light fractions at two photosynthetic photon fluxes (PPF; 200 and 500 μmol m-2 s-1; with a daily light integral of 11.5 and 29 mol m-2 d-1) on growth (dry mass), leaf expansion, stem and petiole elongation, and whole-plant net assimilation of seven diverse plant species. The treatments included cool, neutral, and warm white LEDs, and combinations of blue, green and/or red LEDs. At the higher PPF (500), increasing blue light in increments from 11 to 28% reduced growth in tomato, cucumber, and pepper by 22, 26, and 14% respectively, but there was no statistically significant effect on radish, soybean, lettuce or wheat. At the lower PPF (200), increasing blue light reduced growth only in tomato (41%). The effects of blue light on growth were mediated by changes in leaf area and radiation capture, with minimal effects on whole-plant net-assimilation. In contrast to the significant effects of blue light, increasing green light in increments from 0 to 30% had a relatively small effect on growth, leaf area and net assimilation at either low or high PPF. Surprisingly, growth of three of the seven species was not reduced by a treatment with 93% green light compared to the broad spectrum treatments. Collectively, these results are consistent with a shade avoidance response associated with either low blue or high green light fractions.

Published
2016

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