@article{hackman_cook_strahm_carter_woodley_garcia_albaugh_rubilar_campoe_2024, title={<i>Pinus</i><i> taeda</i> carryover phosphorus availability on the lower Atlantic Coastal Plain}, volume={555}, ISSN={["1872-7042"]}, DOI={10.1016/j.foreco.2024.121701}, abstractNote={Phosphorus (P) fertilizer that remains in the soil after harvest and into the subsequent rotation is referred to as carryover P. Carryover P is not well understood in loblolly pine (P. taeda) silviculture, especially on highly P responsive sites, where this effect could potentially have the greatest benefit to land managers. Our study aims to determine the duration of the P carryover effect and the magnitude of response to soil P as it relates to previously applied P fertilizer rates from the previous rotation. To address this knowledge gap, we studied two highly weathered sites on the lower Atlantic coastal plain: a somewhat poorly drained Spodosol and a poorly drained Alfisol over three years from pre- to post-harvest. Two years post planting, carryover fertilizer treatments resulted in a 13% increase in height for the 121 kg P ha-1, a 15% for the 81 kg P ha-1, and a 17% increase for the fertilized 40 + 45 kg P ha-1 treatments compared to the control for the Alfisol. Spodosols appeared to respond to any additional fertilization compared to the control group regardless of rate. Importantly, we found that O horizon mass and P content from the first rotation, approximately seven years before harvest, exhibited a positive linear relationship with one-year-old heights in the Spodosol and one- and two-year-old heights in the Alfisol. These findings shed light on the importance of the O horizon characteristics and its potential as an indicator for tree growth in subsequent rotations.}, journal={FOREST ECOLOGY AND MANAGEMENT}, publisher={Elsevier BV}, author={Hackman, Jacob and Cook, Rachel and Strahm, Brian and Carter, David and Woodley, Alex and Garcia, Kevin and Albaugh, Timothy and Rubilar, Rafael and Campoe, Otavio}, year={2024}, month={Mar} }
 @article{rose_dellinger_larmour_polishook_higuita-aguirre_dutta_cook_zimmermann_garcia_2024, title={The ectomycorrhizal fungus <i>Paxillus ammoniavirescens</i> influences the effects of salinity on loblolly pine in response to potassium availability}, volume={26}, ISSN={["1462-2920"]}, url={https://doi.org/10.1111/1462-2920.16597}, DOI={10.1111/1462-2920.16597}, abstractNote={Abstract}, number={3}, journal={ENVIRONMENTAL MICROBIOLOGY}, author={Rose, Benjamin D. and Dellinger, Marissa A. and Larmour, Clancy P. and Polishook, Mira I. and Higuita-Aguirre, Maria I. and Dutta, Summi and Cook, Rachel L. and Zimmermann, Sabine D. and Garcia, Kevin}, year={2024}, month={Mar} }
 @article{hackman_cook_strahm_carter_woodley_garcia_2024, title={Using microdialysis to assess soil diffusive P and translocated sap flow P concentrations in Southern <i>Pinus taeda</i> plantations}, volume={1}, ISSN={["1573-5036"]}, DOI={10.1007/s11104-023-06468-8}, journal={PLANT AND SOIL}, author={Hackman, Jacob and Cook, Rachel and Strahm, Brian and Carter, David and Woodley, Alex and Garcia, Kevin}, year={2024}, month={Jan} }
 @article{dutta_houdinet_nandakafle_kafle_hawkes_garcia_2023, title={Agrobacterium tumefaciens-mediated transformation of Nigrospora sp. isolated from switchgrass leaves and antagonistic toward plant pathogens}, volume={215}, ISSN={["1872-8359"]}, url={http://dx.doi.org/10.1016/j.mimet.2023.106849}, DOI={10.1016/j.mimet.2023.106849}, abstractNote={Nigrospora is a diverse genus of fungi colonizing plants through endophytic, pathogenic, or saprobic interactions. Endophytic isolates can improve growth and development of host plants, as well as their resistance to microbial pathogens, but exactly how they do so remains poorly understood. Developing a reliable transformation method is crucial to investigate these mechanisms, in particular to identify pivotal genes for specific functions that correlate with specific traits. In this study, we identified eight isolates of Nigrospora sp. internally colonizing the leaves of switchgrass plants cultivated in North Carolina. Using an Agrobacterium tumefaciens-mediated transformation approach with control and GFP-expressing vectors, we report the first successful transformation of two Nigrospora isolates. Finally, we demonstrate that wild-type and transgenic isolates both negatively impact the growth of two plant pathogens in co-culture conditions, Bipolaris maydis and Parastagonospora nodorum, responsible for the Southern Leaf Blight and Septoria Nodorum Blotch diseases, respectively. The GFP-transformed strains developed here can therefore serve as accurate reporters of spatial interactions in future studies of Nigrospora and pathogens in the plant. Finally, the transformation method we describe lays the foundation for further genetic research on the Nigrospora genus to expand our mechanistic understanding of plant-endophyte interactions.}, journal={JOURNAL OF MICROBIOLOGICAL METHODS}, author={Dutta, Summi and Houdinet, Gabriella and NandaKafle, Gitanjali and Kafle, Arjun and Hawkes, Christine V. and Garcia, Kevin}, year={2023}, month={Dec} }
 @article{rose_frank_garcia_2023, title={Development of split-root assays for loblolly pine (Pinus taeda L.) seedlings to study ectomycorrhizal symbioses}, volume={10}, ISSN={2215-0161}, url={https://doi.org/10.1016/j.mex.2023.102046}, DOI={10.1016/j.mex.2023.102046}, abstractNote={Split-root techniques are valuable to investigate systemic vs. local plant responses to biotic and abiotic environmental factors, including interactions with soil microbes. Loblolly pine (Pinus taeda L.) is an economically important tree species that associates with many ectomycorrhizal fungi. However, a protocol for the establishment of split-roots experiments with loblolly pine has not been described so far. This method successfully establishes a split-root system in eight weeks following germination of loblolly pine seedlings. Rapid lateral root elongation is promoted by cutting the primary root tip and growing the seedlings in a hydroponic medium. Lateral roots can then be divided into two separated compartments and inoculated with ectomycorrhizal fungi. The method was validated by growth of split roots with or without inoculation. Root dry biomass was not significantly different between separated non-inoculated roots. Ectomycorrhizal colonization was not detected on the non-inoculated side of roots that were inoculated only on one side, demonstrating the success of the technique as a valuable method for split-root experiments in P. taeda. In addition to ectomycorrhizal fungi, researchers can use this method with loblolly pine to study systemic and local responses to a variety of other biotic or abiotic factors in the root environment.•We describe a protocol to produce split-roots in loblolly pine (Pinus taeda L.) in eight weeks.•This protocol uses hydroponics to promote the elongation of loblolly pine roots.•We validated this protocol by determining split-root biomass and inoculating the seedlings with the ectomycorrhizal fungi Paxillus ammoniavirescens or Hebeloma cylindrosporum.}, journal={METHODSX}, author={Rose, Benjamin D. and Frank, Hannah E. R. and Garcia, Kevin}, year={2023} }
 @article{das_kafle_ho-plagaro_zimmermann_bucking_garcia_2023, title={Importance of root symbiomes for plant nutrition: new insights, perspectives and future challenges, volume II}, volume={14}, ISSN={["1664-462X"]}, DOI={10.3389/fpls.2023.1296604}, abstractNote={EDITORIAL article Front. Plant Sci., 04 October 2023Sec. Plant Pathogen Interactions Volume 14 - 2023 | https://doi.org/10.3389/fpls.2023.1296604}, journal={FRONTIERS IN PLANT SCIENCE}, publisher={Frontiers Media SA}, author={Das, Debatosh and Kafle, Arjun and Ho-Plagaro, Tania and Zimmermann, Sabine D. and Bucking, Heike and Garcia, Kevin}, year={2023}, month={Oct} }
 @article{amenc_becquer_trives-segura_zimmermann_garcia_plassard_2023, title={Overexpression of the HcPT1.1 transporter in Hebeloma cylindrosporum alters the phosphorus accumulation of Pinus pinaster and the distribution of HcPT2 in ectomycorrhizae}, volume={14}, ISSN={["1664-462X"]}, url={http://dx.doi.org/10.3389/fpls.2023.1135483}, DOI={10.3389/fpls.2023.1135483}, abstractNote={Ectomycorrhizal (ECM) fungi are associated with the roots of woody plants in temperate and boreal forests and help them to acquire water and nutrients, particularly phosphorus (P). However, the molecular mechanisms responsible for the transfer of P from the fungus to the plant in ectomycorrhizae are still poorly understood. In the model association between the ECM fungus Hebeloma cylindrosporum and its host plant Pinus pinaster, we have shown that the fungus, which possesses three H+:Pi symporters (HcPT1.1, HcPT1.2 and HcPT2), expresses mainly HcPT1.1 and HcPT2 in the extraradical and intraradical hyphae of ectomycorrhizae to transport P from the soil to colonized roots. The present study focuses on the role of the HcPT1.1 protein in plant P nutrition, in function of P availability. We artificially overexpressed this P transporter by fungal Agrotransformation and investigated the effect of the different lines, wild-type and transformed ones, on plant P accumulation, the distribution of HcPT1.1 and HcPT2 proteins in ectomycorrhizae by immunolocalization, and 32P efflux in an experimental system mimicking intraradical hyphae. Surprisingly, we showed that plants interacting with transgenic fungal lines overexpressing HcPT1.1 did not accumulate more P in their shoots than plants colonized with the control ones. Although the overexpression of HcPT1.1 did not affect the expression levels of the other two P transporters in pure cultures, it induced a strong reduction in HcPT2 proteins in ectomycorrhizae, particularly in intraradical hyphae, but still improved the P status of host plant shoots compared with non-mycorrhizal plants. Finally, 32P efflux from hyphae was higher in lines overexpressing HcPT1.1 than in the control ones. These results suggest that a tight regulation and/or a functional redundancy between the H+:Pi symporters of H. cylindrosporum might exist to ensure a sustainable P delivery to P. pinaster roots.}, journal={FRONTIERS IN PLANT SCIENCE}, publisher={Frontiers Media SA}, author={Amenc, Laurie and Becquer, Adeline and Trives-Segura, Carlos and Zimmermann, Sabine D. and Garcia, Kevin and Plassard, Claude}, year={2023}, month={Jun} }
 @misc{houdinet_guerrero-galan_rose_garcia_zimmermann_2023, title={Secrets of the fungus-specific potassium channel TOK family}, volume={31}, ISSN={["1878-4380"]}, DOI={10.1016/j.tim.2022.11.007}, abstractNote={Several families of potassium (K+) channels are found in membranes of all eukaryotes, underlining the importance of K+ uptake and redistribution within and between cells and organs. Among them, TOK (tandem-pore outward-rectifying K+) channels consist of eight transmembrane domains and two pore domains per subunit organized in dimers. These channels were originally studied in yeast, but recent identifications and characterizations in filamentous fungi shed new light on this fungus-specific K+ channel family. Although their actual function in vivo is often puzzling, recent works indicate a role in cellular K+ homeostasis and even suggest a role in plant-fungus symbioses. This review aims at synthesizing the current knowledge on fungal TOK channels and discussing their potential role in yeasts and filamentous fungi.}, number={5}, journal={TRENDS IN MICROBIOLOGY}, publisher={Elsevier BV}, author={Houdinet, Gabriella and Guerrero-Galan, Carmen and Rose, Benjamin D. and Garcia, Kevin and Zimmermann, Sabine D.}, year={2023}, month={May}, pages={511–520} }
 @article{garcia_cloghessy_cooney_shelley_chakraborty_kafle_busidan_sonawala_collier_jayaraman_et al._2023, title={The putative transporter MtUMAMIT14 participates in nodule formation in Medicago truncatula}, volume={13}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-023-28160-8}, abstractNote={Abstract}, number={1}, journal={SCIENTIFIC REPORTS}, publisher={Springer Science and Business Media LLC}, author={Garcia, Kevin and Cloghessy, Kaylee and Cooney, Danielle R. and Shelley, Brett and Chakraborty, Sanhita and Kafle, Arjun and Busidan, Aymeric and Sonawala, Unnati and Collier, Ray and Jayaraman, Dhileepkumar and et al.}, year={2023}, month={Jan} }
 @article{kafle_garcia_2022, title={Cesium could be used as a proxy for potassium in mycorrhizal Medicago truncatula}, volume={17}, ISSN={["1559-2324"]}, url={https://doi.org/10.1080/15592324.2022.2134676}, DOI={10.1080/15592324.2022.2134676}, abstractNote={ABSTRACT Arbuscular mycorrhizal (AM) fungi interact with the roots of most land plants and help them to acquire various mineral resources from the soil, including potassium (K+). However, tracking K+ movement in AM symbiosis remains challenging. Recently, we reported that rubidium can be used as a proxy for K+ in mycorrhizal Medicago truncatula. In the present work, we investigated the possibility of using cesium (Cs+) as another proxy for K+ in AM symbiosis. Plants were placed in growing systems that include a separate compartment only accessible to the AM fungus Rhizophagus irregularis isolate 09 and in which various amounts of cesium chloride (0 mM, 0.5 mM, 1.5 mM, or 3.75 mM) were supplied. Plants were watered with sufficient K+ or K+-free nutrient solutions, and shoot and root biomass, fungal colonization, and K+ and Cs+ concentrations were recorded seven weeks after inoculation. Our results indicate that Cs+ accumulated in plant tissues only when K+ was present in the nutrient solution and when the highest concentration of Cs+ was used in the fungal compartment. Consequently, we conclude that Cs+ could be used as a proxy for K+ in AM symbiosis, but with serious limitations.}, number={1}, journal={PLANT SIGNALING & BEHAVIOR}, author={Kafle, Arjun and Garcia, Kevin}, year={2022}, month={Dec} }
 @article{kafle_cooney_shah_garcia_2022, title={Mycorrhiza-mediated potassium transport in Medicago truncatula can be evaluated by using rubidium as a proxy}, volume={322}, ISSN={["1873-2259"]}, DOI={10.1016/j.plantsci.2022.111364}, abstractNote={Arbuscular mycorrhizal (AM) fungi considerably improve plant nutrient acquisition, particularly phosphorus and nitrogen. Despite the physiological importance of potassium (K+) in plants, there is increasing interest in the mycorrhizal contribution to plant K+ nutrition. Yet, methods to track K+ transport are often costly and limiting evaluation opportunities. Rubidium (Rb+) is known to be transported through same pathways as K+. As such our research efforts attempt to evaluate if Rb+ could serve as a viable proxy for evaluating K+ transport in AM symbiosis. Therefore, we examined the transport of K+ in Medicago truncatula colonized by the AM fungus Rhizophagus irregularis isolate 09 having access to various concentrations of Rb+ in custom-made two-compartment systems. Plant biomass, fungal root colonization, and shoot nutrient concentrations were recorded under sufficient and limited K+ regimes. We report that AM plants displayed higher shoot Rb+ and K+ concentrations and a greater K+:Na+ ratio relative to non-colonized plants in both sufficient and limited K+ conditions. Consequently, our results indicate that Rb+ can be used as a proxy to assess the movement of K+ in AM symbiosis, and suggest the existence of a mycorrhizal uptake pathway for K+ nutrition in M. truncatula.}, journal={PLANT SCIENCE}, author={Kafle, Arjun and Cooney, Danielle R. and Shah, Garud and Garcia, Kevin}, year={2022}, month={Sep} }
 @article{hackman_rose_frank_vilgalys_cook_garcia_2022, title={NPK fertilizer use in loblolly pine plantations: Who are we really feeding?}, volume={520}, ISSN={["1872-7042"]}, url={https://doi.org/10.1016/j.foreco.2022.120393}, DOI={10.1016/j.foreco.2022.120393}, abstractNote={Optimizing loblolly pine (Pinus taeda L.) productivity using fertilizers and various site management practices has been a goal of foresters for decades. Nitrogen (N), phosphorus (P), and potassium (K) are the three most operationally applied fertilizers to loblolly pine silviculture and are of primary importance to their total productivity. Fertilizer recommendations for N, P, and K in loblolly pine are primarily made on abiotic factors such as site and soil characteristics, while the biological factors controlling nutrient uptake are typically overlooked in the production and optimization of these stands. Arguably the most important of these biological factors are the diverse ectomycorrhizal fungal (ECM) communities that colonize the fine roots of almost all loblolly pine trees. The mantle formed by ECM fungi on short-root tips presents a barrier for direct apoplastic uptake of N, P, and K from soil solution by pine roots. In well-colonized roots, the tree is dependent on symplastic fungal transport of N, P, and K foraged from the soil by the extraradical hyphal network. This raises the question: Who are we really feeding if the ECM fungi are the ones assimilating most of the tree's total nutritional requirements? Considering multiple species of ECM fungi can inhabit a single root system, many questions remain regarding the drivers of colonization, why some species are more efficient at taking up and exchanging nutrients with their hosts than others, and why certain fertilizers directly affect the morphology of ECM growth. The purposes of this review are (1) to explore how the most commonly commercially applied macronutrients, N, P, and K, affect the relationship between loblolly pine and ECM communities, and (2) to propose future directions to investigate, preserve, and manipulate these interactions in pine plantations to optimize productivity.}, journal={FOREST ECOLOGY AND MANAGEMENT}, author={Hackman, Jacob J. and Rose, Benjamin D. and Frank, Hannah E. R. and Vilgalys, Rytas and Cook, Rachel L. and Garcia, Kevin}, year={2022}, month={Sep} }
 @article{cope_kafle_yakha_pfeffer_strahan_garcia_subramanian_bucking_2022, title={Physiological and transcriptomic response of Medicago truncatula to colonization by high- or low-benefit arbuscular mycorrhizal fungi}, volume={32}, ISSN={["1432-1890"]}, url={https://doi.org/10.1007/s00572-022-01077-2}, DOI={10.1007/s00572-022-01077-2}, abstractNote={Arbuscular mycorrhizal (AM) fungi form a root endosymbiosis with many agronomically important crop species. They enhance the ability of their host to obtain nutrients from the soil and increase the tolerance to biotic and abiotic stressors. However, AM fungal species can differ in the benefits they provide to their host plants. Here, we examined the putative molecular mechanisms involved in the regulation of the physiological response of Medicago truncatula to colonization by Rhizophagus irregularis or Glomus aggregatum, which have previously been characterized as high- and low-benefit AM fungal species, respectively. Colonization with R. irregularis led to greater growth and nutrient uptake than colonization with G. aggregatum. These benefits were linked to an elevated expression in the roots of strigolactone biosynthesis genes (NSP1, NSP2, CCD7, and MAX1a), mycorrhiza-induced phosphate (PT8), ammonium (AMT2;3), and nitrate (NPF4.12) transporters and the putative ammonium transporter NIP1;5. R. irregularis also stimulated the expression of photosynthesis-related genes in the shoot and the upregulation of the sugar transporters SWEET1.2, SWEET3.3, and SWEET 12 and the lipid biosynthesis gene RAM2 in the roots. In contrast, G. aggregatum induced the expression of biotic stress defense response genes in the shoots, and several genes associated with abiotic stress in the roots. This suggests that either the host perceives colonization by G. aggregatum as pathogen attack or that G. aggregatum can prime host defense responses. Our findings highlight molecular mechanisms that host plants may use to regulate their association with high- and low-benefit arbuscular mycorrhizal symbionts.}, number={3-4}, journal={MYCORRHIZA}, publisher={Springer Science and Business Media LLC}, author={Cope, Kevin R. and Kafle, Arjun and Yakha, Jaya K. and Pfeffer, Philip E. and Strahan, Gary D. and Garcia, Kevin and Subramanian, Senthil and Bucking, Heike}, year={2022}, month={May} }
 @article{shively_cook_maier_garcia_albaugh_campoe_leggett_2022, title={Readily available resources across sites and genotypes result in greater aboveground growth and reduced fine root production in Pinus taeda}, volume={521}, ISSN={["1872-7042"]}, url={http://europepmc.org/abstract/AGR/IND607837981}, DOI={10.1016/j.foreco.2022.120431}, abstractNote={Fine roots serve as the primary interface between trees and the soil, and they are dynamic in their response to environmental conditions.Among many functions, they are principle in gathering nutrients and water, and they constitute a major component of the tree.Their overall contribution to soil carbon flux is not well understood, nor is the effect of site and genotype on their dynamics, and these factors are crucial to understanding nutrient cycles and tree growth under variable conditions.This study evaluated how the fine root dynamics of loblolly pine (Pinus taeda L.) might be different between genotypes and on different sites.Three loblolly pine plantations were established, two in 2009 in North Carolina (NC) and Virginia (VA), and one in 2011 in Brazil (BR).Root biomass was estimated with soil cores across the three sites and between two genotypes in 2020.Seasonal and annual fine root production was measured at the NC and VA sites over the 12th growing season using ingrowth cores.The trees in BR that were two years younger were much larger than those in NC and VA and had more fine root biomass at initial sampling than those in NC, despite similar levels of fertility.Meanwhile, fine root production rates decreased with higher rates of aboveground productivity across all measured plots in NC and VA.These results indicate that (1) standing fine root biomass may be related to environmental conditions that are not easily manipulated, which could inform modeling of carbon cycles, and (2) in these intensively managed plots, sufficient resources were available to allow for increased aboveground growth despite lower rates of fine root production, which supports the employment of these intensive silvicultural practices.}, journal={FOREST ECOLOGY AND MANAGEMENT}, author={Shively, Timothy J. and Cook, Rachel and Maier, Chris A. and Garcia, Kevin and Albaugh, Timothy J. and Campoe, Otavio and Leggett, Zakiya}, year={2022}, month={Oct} }
 @misc{kafle_frank_rose_garcia_2022, title={Split down the middle: studying arbuscular mycorrhizal and ectomycorrhizal symbioses using split-root assays}, volume={73}, ISSN={["1460-2431"]}, url={https://doi.org/10.1093/jxb/erab489}, DOI={10.1093/jxb/erab489}, abstractNote={Abstract}, number={5}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, publisher={Oxford University Press (OUP)}, author={Kafle, Arjun and Frank, Hannah E. R. and Rose, Benjamin D. and Garcia, Kevin}, editor={Gifford, MiriamEditor}, year={2022}, month={Mar}, pages={1288–1300} }
 @article{frank_garcia_2021, title={Benefits provided by four ectomycorrhizal fungi to Pinus taeda under different external potassium availabilities}, volume={8}, ISSN={["1432-1890"]}, url={https://doi.org/10.1007/s00572-021-01048-z}, DOI={10.1007/s00572-021-01048-z}, abstractNote={Ectomycorrhizal fungi contribute to the nutrition of many woody plants, including those in the Pinaceae family. Loblolly pine (Pinus taeda L.), a native species of the Southeastern USA, can be colonized by multiple species of ectomycorrhizal fungi. The role of these symbionts in P. taeda potassium (K + ) nutrition has not been previously investigated. Here, we assessed the contribution of four ectomycorrhizal fungi, Hebeloma cylindrosporum, Paxillus ammoniavirescens, Laccaria bicolor, and Suillus cothurnatus, in P. taeda K +  acquisition under different external K +  availabilities. Using a custom-made two-compartment system, P. taeda seedlings were inoculated with one of the four fungi, or kept non-colonized, and grown under K + -limited or -sufficient conditions for 8 weeks. Only the fungi had access to separate compartments in which rubidium, an analog tracer for K + , was supplied before harvest. Resulting effects of the fungi were recorded, including root colonization, biomass, and nutrient concentrations. We also analyzed the fungal performance in axenic conditions under varying supply of K +  and sodium. Our study revealed that these four ectomycorrhizal fungi are differentially affected by external K +  and sodium variations, that they are not able to provide similar benefits to the host P. taeda in our growing conditions, and that rubidium may be used with some limitations to estimate K +  transport from ectomycorrhizal fungi to colonized plants.}, journal={MYCORRHIZA}, publisher={Springer Science and Business Media LLC}, author={Frank, Hannah E. R. and Garcia, Kevin}, year={2021}, month={Aug} }
 @misc{usman_ho-plagaro_frank_calvo-polanco_gaillard_garcia_zimmermann_2021, title={Mycorrhizal Symbiosis for Better Adaptation of Trees to Abiotic Stress Caused by Climate Change in Temperate and Boreal Forests}, volume={4}, ISSN={["2624-893X"]}, DOI={10.3389/ffgc.2021.742392}, abstractNote={Global climate changes have serious consequences on natural ecosystems and cause diverse environmental abiotic stressors that negatively affect plant growth and development. Trees are dependent on their symbiosis with mycorrhizal fungi, as the hyphal network significantly improves the uptake of water and essential mineral nutrients by colonized roots. A number of recent studies has enhanced our knowledge on the functions of mycorrhizal associations between fungi and plant roots. Moreover, a series of timely studies have investigated the impact and benefit of root symbioses on the adaptation of plants to climate change-associated stressors. Trees in temperate and boreal forests are increasingly exposed to adverse environmental conditions, thus affecting their durable growth. In this mini-review, we focus our attention on the role mycorrhizal symbioses play in attenuating abiotic stressors imposed on trees facing climatic changes, such as high temperatures, drought, salinity, and flooding.}, journal={FRONTIERS IN FORESTS AND GLOBAL CHANGE}, publisher={Frontiers Media SA}, author={Usman, Muhammad and Ho-Plagaro, Tania and Frank, Hannah E. R. and Calvo-Polanco, Monica and Gaillard, Isabelle and Garcia, Kevin and Zimmermann, Sabine D. D.}, year={2021}, month={Sep} }
 @article{garcia_bücking_zimmermann_2020, title={Editorial: Importance of Root Symbiomes for Plant Nutrition: New Insights, Perspectives and Future Challenges}, volume={11}, DOI={10.3389/fpls.2020.00594}, abstractNote={HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés. Editorial: Importance of Root Symbiomes for Plant Nutrition: New Insights, Perspectives and Future Challenges Kévin Garcia, Heike Bücking, Sabine Zimmermann}, journal={Frontiers in Plant Science}, publisher={Frontiers Media SA}, author={Garcia, Kevin and Bücking, Heike and Zimmermann, Sabine D.}, year={2020}, month={May} }
 @article{garcia_guerrero-galán_frank_haider_delteil_conéjéro_lambilliotte_fizames_sentenac_zimmermann_2020, title={Fungal Shaker-like channels beyond cellular K+ homeostasis: A role in ectomycorrhizal symbiosis between Hebeloma cylindrosporum and Pinus pinaster}, url={https://doi.org/10.1371/journal.pone.0242739}, DOI={10.1371/journal.pone.0242739}, abstractNote={Potassium (K+) acquisition, translocation and cellular homeostasis are mediated by various membrane transport systems in all organisms. We identified and described an ion channel in the ectomycorrhizal fungusHebeloma cylindrosporum(HcSKC) that harbors features of animal voltage-dependentShaker-like K+channels, and investigated its role in both free-living hyphae and symbiotic conditions. RNAi lines affected in the expression ofHcSKCwere produced and used forin vitromycorrhizal assays with the maritime pine as host plant, under standard or low K+conditions. The adaptation ofH.cylindrosporumto the downregulation ofHcSKCwas analyzed by qRT-PCR analyses for other K+-related transport proteins: the transportersHcTrk1,HcTrk2, andHcHAK, and the ion channelsHcTOK1,HcTOK2.1, andHcTOK2.2. DownregulatedHcSKCtransformants displayed greater K+contents at standard K+only. In such conditions, plants inoculated with these transgenic lines were impaired in K+nutrition. Taken together, these results support the hypothesis that the reduced expression ofHcSKCmodifies the pool of fungal K+available for the plant and/or affects its symbiotic transfer to the roots. Our study reveals that the maintenance of K+transport inH.cylindrosporum, through the regulation ofHcSKCexpression, is required for the K+nutrition of the host plant.}, journal={PLOS ONE}, author={Garcia, Kevin and Guerrero-Galán, Carmen and Frank, Hannah E. R. and Haider, Muhammad Zulqurnain and Delteil, Amandine and Conéjéro, Geneviève and Lambilliotte, Raphaël and Fizames, Cécile and Sentenac, Hervé and Zimmermann, Sabine D.}, editor={Kothe, ErikaEditor}, year={2020}, month={Nov} }
 @article{rush_puech-pages_bascaules_jargeat_maillet_haouy_maes_carriel_khokhani_keller-pearson_et al._2020, title={Lipo-chitooligosaccharides as regulatory signals of fungal growth and development}, volume={11}, ISSN={["2041-1723"]}, DOI={10.1038/s41467-020-17615-5}, abstractNote={Abstract}, number={1}, journal={NATURE COMMUNICATIONS}, publisher={Springer Science and Business Media LLC}, author={Rush, Tomas Allen and Puech-Pages, Virginie and Bascaules, Adeline and Jargeat, Patricia and Maillet, Fabienne and Haouy, Alexandra and Maes, Arthur QuyManh and Carriel, Cristobal Carrera and Khokhani, Devanshi and Keller-Pearson, Michelle and et al.}, year={2020}, month={Aug} }
 @article{ruytinx_kafle_usman_coninx_zimmermann_garcia_2020, title={Micronutrient transport in mycorrhizal symbiosis; zinc steals the show}, url={https://doi.org/10.1016/j.fbr.2019.09.001}, DOI={10.1016/j.fbr.2019.09.001}, abstractNote={Mycorrhizas are mutually beneficial associations between soil-borne fungi and plant roots. Mycorrhizal fungi provide their host plant with essential nutrients in exchange for sugars and/or lipids. Traditionally, transport and translocation of macronutrients, including nitrogen and phosphorus, throughout the fungal mycelium and towards the host plant are well studied. However, the regulation of nutrient exchange and their contribution in the morphogenesis and development of mycorrhizas remains unclear. In this Opinion, we argue that adding micronutrients in the current models of symbiotic transport is essential to fully understand the establishment, maintenance, and functioning of mycorrhizal associations. Homeostatic mechanisms at the cellular level and the first transport proteins involved have been recently documented for zinc (Zn) in arbuscular mycorrhizal, ectomycorrhizal, and ericoid mycorrhizal fungi. Mycorrhizal plants benefit from an improved Zn status in control conditions and are better protected when environmental Zn availability fluctuates. These recent progresses are paving the way for a better understanding of micronutrient allocation in mycorrhizas. Revising our vision on the role of micronutrients, particularly of Zn, in these interactions will allow a better use of mycorrhizal fungi in sustainable agriculture and forestry, and will increase management practices in waste land, as well as in agricultural and natural ecosystems.}, journal={Fungal Biology Reviews}, author={Ruytinx, Joske and Kafle, Arjun and Usman, Muhammad and Coninx, Laura and Zimmermann, Sabine D. and Garcia, Kevin}, year={2020}, month={Mar} }
 @article{cope_kafle_yakha_pfeffer_strahan_garcia_subramanian_bücking_2020, title={Physiological and transcriptomic response of Medicago truncatula to colonization with high and low benefit arbuscular mycorrhizal fungi}, volume={12}, url={https://doi.org/10.1101/2020.12.11.421693}, DOI={10.1101/2020.12.11.421693}, abstractNote={ABSTRACT}, publisher={Cold Spring Harbor Laboratory}, author={Cope, Kevin R. and Kafle, Arjun and Yakha, Jaya K. and Pfeffer, Philip E. and Strahan, Gary D. and Garcia, Kevin and Subramanian, Senthil and Bücking, Heike}, year={2020}, month={Dec} }
 @article{schenck_westphal_jayaraman_garcia_wen_mysore_ané_sumner_maeda_2020, title={Role of cytosolic, tyrosine‐insensitive prephenate dehydrogenase in            Medicago truncatula}, volume={4}, DOI={10.1002/pld3.218}, abstractNote={Abstract}, number={5}, journal={Plant Direct}, publisher={Wiley}, author={Schenck, Craig A. and Westphal, Josh and Jayaraman, Dhileepkumar and Garcia, Kevin and Wen, Jiangqi and Mysore, Kirankumar S. and Ané, Jean‐Michel and Sumner, Lloyd W. and Maeda, Hiroshi A.}, year={2020}, month={May} }
 @article{kafle_garcia_peta_yakha_soupir_bücking_2019, title={Beneficial Plant Microbe Interactions and Their Effect on Nutrient Uptake, Yield, and Stress Resistance of Soybeans}, DOI={10.5772/intechopen.81396}, abstractNote={Plants are meta-organisms that are associated with complex microbiomes. Many of the microorganisms that reside on plant surfaces (epiphytes) or within plant tissues (endophytes) do not cause any plant diseases but often contribute significantly to the nutrient supply of their host plant and can help the plant to overcome a variety of biotic or abiotic stresses. The yield potential of any plant depends not only on successful plant traits that improve, for example, the adaptation to low input conditions or other stressful environments but also on the plant microbiome and its potential to promote plant growth under these conditions. There is a growing interest to unravel the mechanisms underlying these beneficial plant microbe interactions because the activities of these microbial communities are of critical importance for plant growth under abiotic and biotic stresses and could lead to the development of novel strategies to improve yields and stress resistances of agronomically important crops. In this chapter, we summarize our current understanding of the beneficial interactions of soybean plants with arbuscular mycorrhizal fungi, nitrogen-fixing rhizobia, and fungal and bacterial endophytes and identify major knowledge gaps that need to be filled to use beneficial microbes to their full potential.}, journal={Soybean - Biomass, Yield and Productivity}, publisher={IntechOpen}, author={Kafle, Arjun and Garcia, Kevin and Peta, Vincent and Yakha, Jaya and Soupir, Alex and Bücking, Heike}, year={2019}, month={Feb} }
 @article{kafle_cope_raths_yakha_subramanian_bücking_garcia_2019, title={Harnessing Soil Microbes to Improve Plant Phosphate Efficiency in Cropping Systems}, volume={9}, url={https://doi.org/10.3390/agronomy9030127}, DOI={10.3390/agronomy9030127}, abstractNote={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.}, number={3}, journal={Agronomy}, publisher={MDPI AG}, author={Kafle, Arjun and Cope, Kevin and Raths, Rachel and Yakha, Jaya Krishna and Subramanian, Senthil and Bücking, Heike and Garcia, Kevin}, year={2019}, month={Mar}, pages={127} }
 @article{kafle_garcia_wang_pfeffer_strahan_bücking_2019, title={Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula}, volume={6}, url={https://doi.org/10.1111/pce.13359}, DOI={10.1111/pce.13359}, abstractNote={Abstract}, journal={Plant, Cell & Environment}, publisher={Wiley}, author={Kafle, Arjun and Garcia, Kevin and Wang, Xiurong and Pfeffer, Philip E. and Strahan, Gary D. and Bücking, Heike}, year={2019}, month={Jan} }
 @article{plassard_becquer_garcia_2019, title={Phosphorus Transport in Mycorrhiza: How Far Are We?}, volume={24}, url={https://doi.org/10.1016/j.tplants.2019.06.004}, DOI={10.1016/j.tplants.2019.06.004}, abstractNote={Mycorrhizal fungi considerably improve plant nutrition and help them to cope with changing environments. Particularly, these fungi express proteins to transfer inorganic phosphate (Pi) from the soil to colonized roots through symbiotic interfaces. The mechanisms involved in Pi transfer from fungal to plant cells are still largely unknown. Here, we discuss the recent progress made on the description of these mechanisms and we propose the most promising hypotheses and alternative mechanisms for this process. Specifically, we present a phylogenetic survey of candidate Pi transporters of mycorrhizal fungi that might ensure Pi unload into the symbiotic interfaces. Gathering additional knowledge on mycorrhizal Pi transport will improve the Pi-useefficiency in agroecological systems and will guide towards addressing future research challenges.}, number={9}, journal={Trends in Plant Science}, publisher={Elsevier BV}, author={Plassard, Claude and Becquer, Adeline and Garcia, Kevin}, year={2019}, month={Sep}, pages={794–801} }
 @article{cope_bascaules_irving_venkateshwaran_maeda_garcia_rush_ma_labbé_jawdy_et al._2019, title={The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots}, volume={31}, url={https://doi.org/10.1105/tpc.18.00676}, DOI={10.1105/tpc.18.00676}, abstractNote={The ectomycorrhizal fungus Laccaria bicolor produces lipochitooligosaccharides that activate nuclear calcium spiking in its Populus host and then uses the common symbiosis pathway to colonize Populus. 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 wild-type 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.}, number={10}, journal={The Plant Cell}, publisher={American Society of Plant Biologists (ASPB)}, author={Cope, Kevin R. and Bascaules, Adeline and Irving, Thomas B. and Venkateshwaran, Muthusubramanian and Maeda, Junko and Garcia, Kevin and Rush, Tomás A. and Ma, Cathleen and Labbé, Jessy and Jawdy, Sara and et al.}, year={2019}, month={Oct}, pages={2386–2410} }
 @article{becquer_garcia_plassard_2018, title={HcPT1.2 participates in Pi acquisition in Hebeloma cylindrosporum external hyphae of ectornycorrhizas under high and low phosphate conditions}, volume={13}, ISSN={["1559-2324"]}, url={https://doi.org/10.1080/15592324.2018.1525997}, DOI={10.1080/15592324.2018.1525997}, abstractNote={ABSTRACT Ectomycorrhizal fungi improve tree phosphorus nutrition through transporters specifically localized at soil-hyphae and symbiotic interfaces. In the model symbiosis between the fungus Hebeloma cylindrosporum and the maritime pine (Pinus pinaster), several transporters possibly involved in phosphate fluxes were identified, including three H+:Pi transporters. Among these three, we recently unraveled the function of one of them, named HcPT2, in both pure culture and symbiotic interaction with P. pinaster. Here we investigated the transporter named HcPT1.2, by analyzing inorganic phosphate transport ability in a yeast complementation assay, assessing its expression in the fungus associated or not with the plant, and immunolocalizing the proteins in ectomycorrhizas. We also evaluated the effect of external Pi concentration on expression and localization of HcPT1.2. Our results revealed that HcPT1.2 is involved in Pi acquisition by H. cylindrosporum mycelium, irrespective of the external Pi concentrations.}, number={10}, journal={PLANT SIGNALING & BEHAVIOR}, publisher={Informa UK Limited}, author={Becquer, Adeline and Garcia, Kevin and Plassard, Claude}, year={2018} }
 @article{guerrero-galán_garcia_houdinet_zimmermann_2018, title={HcTOK1 participates in the maintenance of K+ homeostasis in the ectomycorrhizal fungus Hebeloma cylindrosporum, which is essential for the symbiotic K+ nutrition of Pinus pinaster}, volume={13}, url={https://doi.org/10.1080/15592324.2018.1480845}, DOI={10.1080/15592324.2018.1480845}, abstractNote={ABSTRACT Most land plants rely on root symbioses to complement or improve their mineral nutrition. Recent researches have put forward that mycorrhizal fungi efficiently absorb and transfer potassium (K+) from the soil to host plant roots, but the molecular mechanisms involved are not completely elucidated yet. We have recently revealed that K+ is likely released from the fungal Hartig net to the plant by TOK channels in the ectomycorrhizal model Hebeloma cylindrosporum – Pinus pinaster. H. cylindrosporum harbours three TOK members. Herein, we report that one of them, HcTOK1, has similar features than the yeast ScTOK1. Moreover, we propose a role for this channel in the transport of K+ from the medium to ectomycorrhizal roots under K+ starvation.}, number={6}, journal={Plant Signaling & Behavior}, publisher={Informa UK Limited}, author={Guerrero-Galán, C. and Garcia, K. and Houdinet, G. and Zimmermann, S. D.}, year={2018}, month={Jun}, pages={e1480845} }
 @article{guerrero-galán_delteil_garcia_houdinet_conéjéro_gaillard_sentenac_zimmermann_2018, title={Plant potassium nutrition in ectomycorrhizal symbiosis: properties and roles of the three fungal TOK potassium channels in Hebeloma cylindrosporum.}, volume={4}, url={http://europepmc.org/abstract/med/29614209}, DOI={10.1111/1462-2920.14122}, abstractNote={Summary}, journal={Environmental microbiology}, author={Guerrero-Galán, C and Delteil, A and Garcia, K and Houdinet, G and Conéjéro, G and Gaillard, I and Sentenac, H and Zimmermann, SD}, year={2018}, month={Apr} }
 @article{becquer_garcia_amenc_rivard_doré_trives-segura_szponarski_russet_baeza_lassalle-kaiser_et al._2018, title={The Hebeloma cylindrosporum HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis}, volume={6}, DOI={10.1111/nph.15281}, abstractNote={Summary}, journal={New Phytologist}, publisher={Wiley}, author={Becquer, Adeline and Garcia, Kevin and Amenc, Laurie and Rivard, Camille and Doré, Jeanne and Trives-Segura, Carlos and Szponarski, Wojciech and Russet, Sylvie and Baeza, Yoan and Lassalle-Kaiser, Benedikt and et al.}, year={2018}, month={Jun} }
 @article{guerrero-galan_houdinet_calvo-polanco_bonaldi_garcia_zimmermann_2018, title={The Role of Plant Transporters in Mycorrhizal Symbioses}, volume={87}, ISSN={["2162-5948"]}, DOI={10.1016/bs.abr.2018.09.012}, abstractNote={Membrane transport systems are crucial elements for plant nutrition and development as they play a key role in the absorption of mineral nutrients and water at the root level but also in the translocation within the plant. Moreover, membrane transport is involved in signalling and communication e.g. to adapt and interact with the environment. Most plants live in tight contact with beneficial soil microbes, such as bacteria and mycorrhizal fungi, which contribute to plant nutrition in part through modulation of the expression and functioning of plant transporter systems, as ion channels and transporters. In addition, mycorrhizal fungi largely increase the absorption surface of roots thereby promoting plant's access to soil resources as minerals and water. In turn, plants “reward” mycorrhizal fungi with sugars and/or lipids. This “fair trade” requires specific communication and a series of exchanges between the two symbiotic partners enabled by the adaptability and plasticity of their transporters. Here, we summarize recent advances allowing molecular insight in the impact of mycorrhizal symbiosis on the plant “transportome”. We highlight results obtained in ecto- and endomycorrhizal associations for plant transporters involved in the absorption of mineral nutrients and water released by the fungus at the symbiotic interface, and molecular players responsible for carbon and lipid nutrition of the fungal partner. We focus also on plant membrane transport systems implicated in early communication between plant and fungal partners.}, journal={MEMBRANE TRANSPORT IN PLANTS}, publisher={Elsevier}, author={Guerrero-Galan, Carmen and Houdinet, Gabriella and Calvo-Polanco, Monica and Bonaldi, Katia E. and Garcia, Kevin and Zimmermann, Sabine Dagmar}, year={2018}, pages={303–342} }
 @article{becquer_guerrero-galán_eibensteiner_houdinet_bücking_zimmermann_garcia_2018, title={The ectomycorrhizal contribution to tree nutrition}, DOI={10.1016/bs.abr.2018.11.003}, abstractNote={Trees can be associated with dozens of fungi helping them to acquire resources from forest soils. The most widespread mutualistic association in boreal and temperate forests is the ectomycorrhizal symbiosis. This symbiosis involves mushroom-forming fungi of basidiomycota, ascomycota, and some zygomycota clades and the roots of woody plant species, including oaks, poplars or pines. Although the impact of this association on ecosystem production and tree nutrition is investigated for about a century, our understanding on the molecular mechanisms that control water and nutrient fluxes between plant and fungal partners is still limited. Here, we review the recent knowledge on the ectomycorrhizal contribution to tree nutrition. We specifically highlight the molecular mechanisms driving the acquisition, translocation and release of water and nutrients in ectomycorrhizal systems. We particularly focus on the transport of macronutrients, including nitrogen, phosphorus, potassium, sulphur and calcium, micronutrients, and water by the symbiotic partner. We also provide background on the evolution, diversity, and importance of this symbiosis, identify knowledge gaps, and propose future research directions.}, journal={Advances in Botanical Research}, publisher={Elsevier}, author={Becquer, Adeline and Guerrero-Galán, Carmen and Eibensteiner, Janice L. and Houdinet, Gabriella and Bücking, Heike and Zimmermann, Sabine D. and Garcia, Kevin}, year={2018} }
 @article{garcia_chasman_roy_ane_2017, title={Physiological responses and gene co-expression network of mycorrhizal roots under K+ deprivation}, volume={2}, url={https://doi.org/10.1104/pp.16.01959}, DOI={10.1104/pp.16.01959}, abstractNote={Arbuscular mycorrhizal symbiosis compensates the transcriptional response of M. truncatula roots at low potassium level and activates specific mechanisms to tolerate long-term potassium deprivation. Arbuscular mycorrhizal (AM) associations enhance the phosphorous and nitrogen nutrition of host plants, but little is known about their role in potassium (K+) nutrition. Medicago truncatula plants were cocultured with the AM fungus Rhizophagus irregularis under high and low K+ regimes for 6 weeks. We determined how K+ deprivation affects plant development and mineral acquisition and how these negative effects are tempered by the AM colonization. The transcriptional response of AM roots under K+ deficiency was analyzed by whole-genome RNA sequencing. K+ deprivation decreased root biomass and external K+ uptake and modulated oxidative stress gene expression in M. truncatula roots. AM colonization induced specific transcriptional responses to K+ deprivation that seem to temper these negative effects. A gene network analysis revealed putative key regulators of these responses. This study confirmed that AM associations provide some tolerance to K+ deprivation to host plants, revealed that AM symbiosis modulates the expression of specific root genes to cope with this nutrient stress, and identified putative regulators participating in these tolerance mechanisms.}, number={3}, journal={Plant Physiology}, publisher={American Society of Plant Biologists (ASPB)}, author={Garcia, Kevin and Chasman, Deborah and Roy, Sushmita and Ane, Jean-Michel}, year={2017}, month={Feb}, pages={pp.01959.2016} }
 @article{garcia_ané_2017, title={Polymorphic responses of Medicago truncatula accessions to potassium deprivation.}, volume={12}, url={http://europepmc.org/abstract/med/28340327}, DOI={10.1080/15592324.2017.1307494}, abstractNote={ABSTRACT Potassium (K+) is an essential macronutrient for plants and the most abundant cation in cells. Due to variable K+ availability in the environment, plants must be able to adjust their developmental, physiological and transcriptional responses. The plant development to K+ deprivation was not well studied in legumes thus far. We recently described the first adaptation mechanisms of the model legume Medicago truncatula Jemalong A17 to long-term K+ deprivation and analyzed these responses in the context of arbuscular mycorrhizal symbiosis. Here we report polymorphic growth variations of two genetically very different accessions of M. truncatula to K+-limiting conditions, Jemalong A17, and the Tunisian accession Tn11.1. The faster adaptation of Tn11.1 than A17 to K+ shortage might be due to its greater adaptation to saline soils. Examining in a more systematic way the developmental adaptation of various M. truncatula accessions to K+ deprivation will provide a better understanding of how legume evolved to cope with this stressful condition.}, number={4}, journal={Plant Signaling & Behavior}, publisher={Informa UK Limited}, author={Garcia, K and Ané, JM}, year={2017}, month={Mar}, pages={e1307494} }
 @article{marx_minogue_jayaraman_richards_kwiecien_siahpirani_rajasekar_maeda_garcia_valle-echevarria_et al._2016, title={A proteomic atlas of the legume Medicago truncatula and its nitrogen-fixing endosymbiont Sinorhizobium meliloti}, volume={34}, DOI={10.1038/nbt.3681}, abstractNote={Legumes are essential components of agricultural systems because they enrich the soil in nitrogen and require little environmentally deleterious fertilizers. A complex symbiotic association between legumes and nitrogen-fixing soil bacteria called rhizobia culminates in the development of root nodules, where rhizobia fix atmospheric nitrogen and transfer it to their plant host. Here we describe a quantitative proteomic atlas of the model legume Medicago truncatula and its rhizobial symbiont Sinorhizobium meliloti, which includes more than 23,000 proteins, 20,000 phosphorylation sites, and 700 lysine acetylation sites. Our analysis provides insight into mechanisms regulating symbiosis. We identify a calmodulin-binding protein as a key regulator in the host and assign putative roles and targets to host factors (bioactive peptides) that control gene expression in the symbiont. Further mining of this proteomic resource may enable engineering of crops and their microbial partners to increase agricultural productivity and sustainability.}, number={11}, journal={Nature Biotechnology}, publisher={Springer Nature}, author={Marx, Harald and Minogue, Catherine E and Jayaraman, Dhileepkumar and Richards, Alicia L and Kwiecien, Nicholas W and Siahpirani, Alireza F and Rajasekar, Shanmugam and Maeda, Junko and Garcia, Kevin and Valle-Echevarria, Angel R Del and et al.}, year={2016}, month={Oct}, pages={1198–1205} }
 @article{garcia_ané_2016, title={Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins}, volume={7}, DOI={10.3389/fmicb.2016.01734}, abstractNote={Ectomycorrhizal (ECM) symbioses are major components of boreal and temperate forest ecosystems (Smith and Read, 2008; Clemmensen et al., 2013). Although well studied for several decades, very little is known about the molecular players involved in the establishment and maintenance of ECM symbioses (Garcia et al., 2015). Identifying the symbiont secretome is a promising way to dissect the fungal contribution to the mutualistic molecular dialog. Pellegrin et al. (2015) compared for the first time the predicted secretome of 49 soil-borne ECM, saprotrophic and pathogenic fungi, revealing shared and specific features between species, and providing a better understanding of the ECM lifestyle evolution.}, journal={Frontiers in Microbiology}, publisher={Frontiers Media SA}, author={Garcia, Kevin and Ané, Jean-Michel}, year={2016}, month={Nov} }
 @article{mus_crook_garcia_costas_geddes_kouri_paramasivan_ryu_oldroyd_poole_et al._2016, title={Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes}, volume={82}, DOI={10.1128/aem.01055-16}, abstractNote={ABSTRACT}, number={13}, journal={Applied and Environmental Microbiology}, publisher={American Society for Microbiology}, author={Mus, Florence and Crook, Matthew B. and Garcia, Kevin and Costas, Amaya Garcia and Geddes, Barney A. and Kouri, Evangelia D. and Paramasivan, Ponraj and Ryu, Min-Hyung and Oldroyd, Giles E. D. and Poole, Philip S. and et al.}, editor={Kelly, R. M.Editor}, year={2016}, month={Apr}, pages={3698–3710} }
 @article{garcia_doidy_zimmermann_wipf_courty_2016, title={Take a Trip Through the Plant and Fungal Transportome of Mycorrhiza}, volume={21}, DOI={10.1016/j.tplants.2016.07.010}, abstractNote={Soil nutrient acquisition and exchanges through symbiotic plant-fungus interactions in the rhizosphere are key features for the current agricultural and environmental challenges. Improved crop yield and plant mineral nutrition through a fungal symbiont has been widely described. In return, the host plant supplies carbon substrates to its fungal partner. We review here recent progress on molecular players of membrane transport involved in nutritional exchanges between mycorrhizal plants and fungi. We cover the transportome, from the transport proteins involved in sugar fluxes from plants towards fungi, to the uptake from the soil and exchange of nitrogen, phosphate, potassium, sulfate, and water. Together, these advances in the comprehension of the mycorrhizal transportome will help in developing the future engineering of new agro-ecological systems.}, number={11}, journal={Trends in Plant Science}, publisher={Elsevier BV}, author={Garcia, Kevin and Doidy, Joan and Zimmermann, Sabine D. and Wipf, Daniel and Courty, Pierre-Emmanuel}, year={2016}, month={Nov}, pages={937–950} }
 @article{courty_doidy_garcia_wipf_zimmermann_2016, title={The transportome of mycorrhizal systems}, DOI={10.1002/9781118951446.ch14}, abstractNote={Nutrient uptake from soil and exchanges between fungal and plant partners forming mycorrhizal symbioses present a mean feature among the beneficial effects of these mutualistic relationships. Improved plant mineral nutrition through the fungal partner was first described a long time ago; in return, the plant delivers carbon substrates to the fungal partner. The first transport systems involved in plant-microorganism interactions in plants and fungi were also identified years ago. Within this chapter, recent knowledge concerning mycorrhizal nutrient exchanges and the involved molecular players in membrane transport of the ecto- and endomycorrhizal partners will be presented. First, transport of sugars from plants towards mycorrhizal fungi is summarized. Then, uptake and exchange of main nutrients such as nitrogen, phosphate, sulfate, potassium, and water by the symbiotic partners will be reviewed.}, journal={Molecular Mycorrhizal Symbiosis}, publisher={Wiley-Blackwell}, author={Courty, Pierre-Emmanuel and Doidy, Joan and Garcia, Kevin and Wipf, Daniel and Zimmermann, Sabine Dagmar}, year={2016}, month={Oct}, pages={239–256} }
 @article{garcia_delaux_cope_ané_2015, title={Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses}, volume={208}, DOI={10.1111/nph.13423}, abstractNote={Summary}, number={1}, journal={New Phytologist}, publisher={Wiley-Blackwell}, author={Garcia, Kevin and Delaux, Pierre-Marc and Cope, Kevin R. and Ané, Jean-Michel}, year={2015}, month={Apr}, pages={79–87} }
 @article{garcia_delteil_conéjéro_becquer_plassard_sentenac_zimmermann_2014, title={Potassium nutrition of ectomycorrhizal Pinus pinaster : overexpression of the Hebeloma cylindrosporum Hc Trk1 transporter affects the translocation of both K + and phosphorus in the host plant}, volume={201}, DOI={10.1111/nph.12603}, abstractNote={Summary}, number={3}, journal={New Phytologist}, publisher={Wiley-Blackwell}, author={Garcia, Kevin and Delteil, Amandine and Conéjéro, Geneviève and Becquer, Adeline and Plassard, Claude and Sentenac, Hervé and Zimmermann, Sabine}, year={2014}, pages={951–960} }
 @article{garcia_zimmermann_2014, title={The role of mycorrhizal associations in plant potassium nutrition}, volume={5}, DOI={10.3389/fpls.2014.00337}, abstractNote={Potassium (K+) is one of the most abundant elements of soil composition but it's very low availability limits plant growth and productivity of ecosystems. Because this cation participates in many biological processes, its constitutive uptake from soil solution is crucial for the plant cell machinery. Thus, the understanding of strategies responsible of K+ nutrition is a major issue in plant science. Mycorrhizal associations occurring between roots and hyphae of underground fungi improve hydro-mineral nutrition of the majority of terrestrial plants. The contribution of this mutualistic symbiosis to the enhancement of plant K+ nutrition is not well understood and poorly studied so far. This mini-review examines the current knowledge about the impact of both arbuscular mycorrhizal and ectomycorrhizal symbioses on the transfer of K+ from the soil to the plants. A model summarizing plant and fungal transport systems identified and hypothetically involved in K+ transport is proposed. In addition, some data related to benefits for plants provided by the improvement of K+ nutrition thanks to mycorrhizal symbioses are presented.}, journal={Frontiers in Plant Science}, publisher={Frontiers Media SA}, author={Garcia, Kevin and Zimmermann, Sabine D.}, year={2014}, month={Jul} }
 @article{casieri_lahmidi_doidy_veneault-fourrey_migeon_bonneau_courty_garcia_charbonnier_delteil_et al._2013, title={Biotrophic transportome in mutualistic plant–fungal interactions}, volume={23}, DOI={10.1007/s00572-013-0496-9}, abstractNote={Understanding the mechanisms that underlie nutrient use efficiency and carbon allocation along with mycorrhizal interactions is critical for managing croplands and forests soundly. Indeed, nutrient availability, uptake and exchange in biotrophic interactions drive plant growth and modulate biomass allocation. These parameters are crucial for plant yield, a major issue in the context of high biomass production. Transport processes across the polarized membrane interfaces are of major importance in the functioning of the established mycorrhizal association as the symbiotic relationship is based on a 'fair trade' between the fungus and the host plant. Nutrient and/or metabolite uptake and exchanges, at biotrophic interfaces, are controlled by membrane transporters whose regulation patterns are essential for determining the outcome of plant-fungus interactions and adapting to changes in soil nutrient quantity and/or quality. In the present review, we summarize the current state of the art regarding transport systems in the two major forms of mycorrhiza, namely ecto- and arbuscular mycorrhiza.}, number={8}, journal={Mycorrhiza}, publisher={Springer Nature}, author={Casieri, Leonardo and Lahmidi, Nassima Ait and Doidy, Joan and Veneault-Fourrey, Claire and Migeon, Aude and Bonneau, Laurent and Courty, Pierre-Emmanuel and Garcia, Kevin and Charbonnier, Maryse and Delteil, Amandine and et al.}, year={2013}, month={Apr}, pages={597–625} }
 @article{martinez-garcia_garcia_hammer_vayssières_2013, title={Mycorrhiza for all: an under-earth revolution}, volume={198}, DOI={10.1111/nph.12239}, abstractNote={In recent years, mycorrhizal research has undergone rapid expansion. Breakthroughs in genomics and other modern techniques have allowed us to break new ground in multiple domains, such as evolution, physiology, function, community patterns and biogeography of mycorrhizal fungi. The International Conference on Mycorrhiza (ICOM) is the most important platform for mycorrhizal scientists to present and discuss their work in both theoretical and applied areas of mycorrhizal symbiosis. ICOM 7 was held in New Delhi (India), January 6–11, 2013, and attracted over 400 participants from 48 countries. The theme of the conference was ‘Mycorrhiza for All: An Under-Earth Revolution’, stressing the importance of addressing scientific findings within an applied context to strengthen field implementations and improve sustainable agriculture (Fig. 1). It addressed the urgent need to apply mycorrhizal research to the environmental crises that threatens our planet. ‘Reciprocal rewards stabilize the cooperation between plants and mycorrhizal fungi in order to avoid cheaters and less cooperative partners.’ These genomic data together with the recent transcriptomic analysis of Glomus intraradices (Tisserant et al., 2012), provide fundamental resources for physiological and functional research on symbiotic developmental and metabolic pathways. Natalia Requena (KIT, Germany) presented recent research on the mechanisms influencing plant–fungus recognition. She showed how G. intraradices secretes a protein, SP7, which counteracts plant immune program, consequently benefiting arbuscular mycorrhizal (AM) fungi colonization (Kloppholz et al., 2011). She also highlighted the role of the sugar transporter MST2 of G. intraradices in arbuscule formation (Helber et al., 2011). Similarly, Luisa Lanfranco (University of Turin, Italy) explored the molecular signals controlling the fungal morphogenesis via the analysis of G. intraradices NOX NADPH oxidase genes. Regarding the ECM symbiosis, Anders Tunlid (Lund University, Sweden) used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ECM fungus Paxillus involutus degrades organic matter when acquiring nitrogen (N) from plant litter. He observed that this fungus secretes similar enzymes to those involved in brown-rot fungi Fenton oxidative degradation (Rineau et al., 2012). Additionally, François Buscot (UFZ, Germany) investigated gene expression patterns linked to resources allocation processes in a multitrophic system form by oak roots, the ECM fungus Piloderma croceum and the root pathogen Phytophthora quercina. This emerging knowledge emphasizes the power of genomic data for understanding the establishment, durability and functionality of mycorrhizal symbioses. A central and re-occurring topic at ICOM 7 was the balance of reciprocal rewards (‘tit for tat’ principle) in mycorrhizal symbioses and the role of each partner in the establishment and transfer of nutrients across the soil–fungus–plant continuum. Recent research findings show that both-sided control of nutrient transfer exists between plant carbon (C) and fungal phosphorus (P; Lekberg et al., 2010; Hammer et al., 2011; Kiers et al., 2011) or N (Fellbaum et al., 2012), regulating the choice of partner and maintenance of evolutionary stability in AM symbiosis. In accordance with these results, Toby Kiers (Institute of Ecological Science, the Netherlands) presented this ‘fair trade’ system as a key evolutionary element. Reciprocal rewards stabilize the cooperation between plants and mycorrhizal fungi in order to avoid cheaters and less cooperative partners. Opposing this general theory, Pierre-Emmanuel Courty (University of Basel, Switzerland) indicated that there might be situations where investment and rewards are not directly correlated (Walder et al., 2012). Several presenters emphasized the additional complexity of reciprocal rewards in nutrient exchanges in natural communities connected by a common mycorrhizal network (CMN). Heike Bücking (South Dakota State University, Brookings, SD, USA) used shaded plants to manipulate the C strength, that is amount of C that is available to the plant for investments, while Edith Hammer (FU Berlin, Germany) used plants of different ages to measure nutrient allocation to CMN members investing different amounts of C into the mycelium network. Both conclude that C strength determines the plant's access to nutrients in the CMN. However, Hammer and Marcel van der Heijden (Agroscope, Switzerland) pointed out that health status of the older plant, different species identity and adult-seedling species combinations can lead to outcomes differing from growth enhancement to strong repression of young plants. A situation where the ‘tit for tat’ principle is clearly undermined is in mycoheterotrophy. Duncan Cameron (University of Sheffield, UK) and Lee Taylor (University of Alaska, Fairbanks, AL, USA) both presented evidence that the parasitic C transfer to heterotrophic orchids occurs via N-compounds, most likely glutamine. Regarding nutrient exchange in the mycorrhizal symbiosis, it has been assumed that sucrose is released into the mycorrhizal apoplasm and converted into glucose and fructose that are in turn assimilated by the fungus via transporters. However most of the molecular mechanisms involved in nutrient exchange are yet to be elucidated. Philipp Franken (IGZ, Germany) presented P- and C-transporter mutants that can help to clarify these gaps. Examining ectomycorrhizas, Uwe Nehls (University of Bremen, Germany) showed that a family of plant glucose facilitator genes (coding for SWEET proteins: Chen et al., 2010) is expressed during ECM formation. Consequently, it appears that this hexose could be the most important direct C source for the fungal partner in ECM. These findings support the concept that nutrients are main regulators of the mycorrhizal symbiosis in general, driving partner selection and the stability of the mutualism. Identifying the drivers that structure mycorrhizal communities and populations was one of the hot topics during the conference. Many speakers highlighted the importance of biotic (host species) and abiotic (soil chemistry, rainfall, temperature) factors structuring mycorrhizal fungal communities. Nancy Johnson (North Arizona University, Flagstaff, AZ, USA) remarked that multiple-metrics experiments are necessary to characterize fungal communities. Further, Thorunn Helgason (University of York, UK) emphasized the need to consider temporal and environmental variation in designing sampling strategies for biogeography studies. While several studies on fungal communities have rejected the Baas Becking hypothesis: ‘Everything is everywhere, but the environment selects’ (Taylor et al., 2006; Peay et al., 2007), Christina Hazard (University of Aberdeen, UK) presented results in an Ireland-based study suggesting that the Baas Becking hypothesis may be supported for AM fungi at a regional scale. From a broader scale, Leho Tedersoo (University of Tartu, Estonia) and Nadia Soudzilovaskaia (VU-University of Amsterdam, the Netherlands) contributed to the mycorrhizal global distribution map (Read, 1991) forming novel hypotheses to explain mycorrhizal biogeography. From a community composition perspective, Tedersoo showed that host family strongly determines the phylogenetic structure of ECM fungi communities (Tedersoo et al., 2012). Taking a morphological approach, Soudzilovaskaia showed that soil fertility and pH determined mycorrhizal infection. She observed that harsh environment relates with major mycorrhizal infection. Most of the studies focused on either AM or ECM fungi, however, the mycorrhizal dominant type in an ecosystem is not a static feature but one that changes with time. To understand mycorrhizal type transitions it is necessary to understand their ecosystem functions. Ian Dickie (Landcare Research, Lincoln, New Zealand) tested several accepted opinions on functional differences between ECM and AM fungi and he concluded that some major concepts need to be re-examined, such as differences in mineral weathering, belowground feedback and foliar traits (Koele et al., 2012). Over a geological timescale, Jonathan Leake (University of Sheffield, UK) showed that from an evolutionary point of view the weathering function of mycorrhizas increases from AM to ECM and from gymnosperms to angiosperms, accelerating global biogeochemical cycles (Quirk et al., 2012). Both speakers highlighted the important role of mycorrhiza on geochemical cycles as ecosystems drivers (Orwin et al., 2011). The use of high-throughput sequencing techniques was a common methodology in many community studies. Novel techniques such as restriction-site DNA (RDA) and molecule real-time (SMRT) sequencing will contribute to more detailed information on AM fungal assemblages. The use of such techniques in AM studies continues adding information to the knowledge of AM fungal genetic diversity and therefore the Glomeromycota taxonomy is in a continuous state of change. One example was the suggestion of a major revision of Oehl et al. (2011) taxonomy proposed by Arthur Schüβler (University Munich, Germany). At the same time, the increased use of the MaarjAM database for AM fungi environmental studies brings an alternative to the traditional nomenclature using the virtual taxa (VT) nomenclature (Opik et al., 2010), that could help to solve the controversy in the Glomeromycota taxonomy. Over-exploitation of natural resources and misuse of technological development have caused an environmental crisis with serious consequences for agronomic services (Tilman et al., 2002). ICOM 7 accentuated the applied aspects of mycorrhizal research. André Fortin (University of Laval, Quebec, Canada), Joyce M. Jefwa (CIAT, Nairobi, Kenya), and Alok Adholeya (TERI, New Delhi, India) presented progress in inoculum production and application that promote sustainable agriculture and rebuild soil biota. They highlighted the importance of isolating mycorrhizal strains with selected traits and functions, as well as the importance of producing inoculum compatible with conventional agricultural practices. Martina Janouskova (IEB, Prague, Czech Republic) emphasized the necessity to investigate the competitive performance and persistence of the inoculum, when applied to natural soils, with the existing AMF community. Presenters described current research programs that apply different types of mycorrhizal fungi; such as ECM fungi for forests conservation, AM fungi to tropical reforestation and Sebacinales fungi, which also form orchid mycorrhiza, to increase switchgrass production. Another potential application presented by Mohamed Hijri (University of Montreal, Canada) was the use of AM inoculum as biological control organisms for pathogens. Speakers also highlighted the importance of considering the impact of agricultural practices on the native mycorrhizal community to achieve successful land management practices. In this context, Luise Olbrecht (Agroscope, Switzerland) showed that soil tillage drastically changes AM fungal communities with direct consequences on plant communities and nutrient leaching losses. Many speakers addressed environmental applications, looking at the effects of mycorrhizal fungi on plant growth under harsh conditions, and their utility in phytoremediation of polluted soils. Contributing to this research field, John Klironomos (University of Guelph, Canada) stressed that one of the major benefits of mycorrhizal symbiosis to plants is the increase of host niche size and therefore mycorrhizal fungi might favor plants growing under stressful conditions and in variable environments. Applied knowledge of mycorrhizas is of worldwide interest because it addresses the current urgency to develop methods that guarantee world food supply and ecosystems conservation. Mycorrhizal science is progressing quickly. When we look back at previous ICOMs, we observed that ICOM 5 (2006, Granada) represented a turning point, as Selosse & Duplessis (2006) highlighted in ICOM 5 report section titled ‘The dawn of genomics in the mycorrhizal world’. It is encouraging to see how genomics has helped to clarify previous gaps, such as molecular mechanisms on the plant–fungal interface, evolution or biogeography. Two of the emerging research areas from ICOM 7 were the functioning of mycorrhizas in biogeochemical cycles (cf. Näsholm et al., 2013) and the complexity of multitrophic interactions in the rhizosphere. Addressing these questions requires an integration of disciplines such as chemistry, geology and pedobiology with more traditional mycorrhizal disciplines such as ecology, physiology and mycology. We believe that the theme of the next ICOM (ICOM 8) ‘Mycorrhizal Integration across Continents and Scales’, to be held in Flagstaff (Arizona, USA), August 26–31, 2015, will provide a perfect framework for discussions towards this end. The authors acknowledge the Energy and Resources Institute (TERI) and the International Mycorrhiza Society for organizing the conference. They also thank all the attendees who contributed with talks and posters and provided a stimulating forum including, and especially those whose names are not mentioned here due to space constrains. The authors thank F. Martin, I. Dickie and S. Hortal for helpful comments on the report. L.B.M-G. acknowledges core funding for Crown Research Institutes from the New Zealand Ministry of Business, Innovation and Employment's Science and Innovation Group through the Landcare Research Hayward Postdoctoral Fellowship. E.C.H. acknowledges the Marie Curie postdoctoral fellowship NANOSOIL, and K.G., the French Minister of Research and Technology. A.V.'s laboratory is supported by the Laboratory of Excellence ARBRE (ANR-12-LABXARBRE-01).}, number={3}, journal={New Phytologist}, publisher={Wiley-Blackwell}, author={Martinez-Garcia, Laura B. and Garcia, Kevin and Hammer, Edith C. and Vayssières, Alice}, year={2013}, month={Apr}, pages={652–655} }
 @article{garcia_haider_delteil_corratgé-faillie_conéjero_tatry_becquer_amenc_sentenac_plassard_et al._2013, title={Promoter-dependent expression of the fungal transporter HcPT1.1 under Pi shortage and its spatial localization in ectomycorrhiza}, volume={58-59}, DOI={10.1016/j.fgb.2013.06.007}, abstractNote={Mycorrhizal exchange of nutrients between fungi and host plants involves a specialization and polarization of the fungal plasma membrane adapted for the uptake from the soil and for secretion of nutrient ions towards root cells. In addition to the current progress in identification of membrane transport systems of both symbiotic partners, data concerning the transcriptional and translational regulation of these proteins are needed to elucidate their role for symbiotic functions. To answer whether the formerly described Pi-dependent expression of the phosphate transporter HcPT1.1 from Hebeloma cylindrosporum is the result of its promoter activity, we introduced promoter-EGFP fusion constructs in the fungus by Agrotransformation. Indeed, HcPT1.1 expression in pure fungal cultures quantified and visualized by EGFP under control of the HcPT1.1 promoter was dependent on external Pi concentrations, low Pi stimulating the expression. Furthermore, to study expression and localization of the phosphate transporter HcPT1.1 in symbiotic conditions, presence of transcripts and proteins was analyzed by the in situ hybridization technique as well as by immunostaining of proteins. In ectomycorrhiza, expression of the phosphate transporter was clearly enhanced by Pi-shortage indicating its role in Pi nutrition in the symbiotic association. Transcripts were detected in external hyphae and in the hyphal mantle, proteins in addition also within the Hartig net. Exploiting the transformable fungus H. cylindrosporum, Pi-dependent expression of the fungal transporter HcPT1.1 as result from its promoter activity as well as transcript and protein localization in ectomycorrhizal symbiosis are shown.}, journal={Fungal Genetics and Biology}, publisher={Elsevier BV}, author={Garcia, Kevin and Haider, Muhammad Zulqurnain and Delteil, Amandine and Corratgé-Faillie, Claire and Conéjero, Geneviève and Tatry, Marie-Violaine and Becquer, Adeline and Amenc, Laurie and Sentenac, Hervé and Plassard, Claude and et al.}, year={2013}, month={Sep}, pages={53–61} }