Research efforts directed to elucidation of mechanisms behind trading of resources between the partners in the arbuscular mycorrhizal (AM) symbiosis have seen a considerable progress in the recent years. Yet, despite of the recent developments, some key questions still remain unanswered. For example, it is well established that the strictly biotrophic AM fungus releases phosphorus to- and receives carbon molecules from the plant symbiont, but the particular genes, and their products, responsible for facilitating this exchange, are still not fully described, nor are the principles and pathways of their regulation. Here, we made a de novo quest for genes involved in carbon transfer from the plant to the fungus using genome-wide gene expression array targeting whole root and whole shoot gene expression profiles of mycorrhizal and non-mycorrhizal Medicago truncatula plants grown in a glasshouse. Using physiological intervention of heavy shading (90% incoming light removed) and the correlation of expression levels of MtPT4, the mycorrhiza-inducible phosphate transporter operating at the symbiotic interface between the root cortical cells and the AM fungus, and our candidate genes, we demonstrate that several novel genes may be involved in resource tradings in the AM symbiosis established by M. truncatula. These include glucose-6-phosphate/phosphate translocator, polyol/monosaccharide transporter, DUR3-like, nucleotide-diphospho-sugar transferase or a putative membrane transporter. Besides, we also examined the expression of other M. truncatula phosphate transporters (MtPT1-3, MtPT5-6) to gain further insights in the balance between the "direct" and the "mycorrhizal" phosphate uptake pathways upon colonization of roots by the AM fungus, as affected by short-term carbon/energy deprivation. In addition, the role of the novel candidate genes in plant cell metabolism is discussed based on available literature.

Department of Experimental Plant Biology Faculty of Science Charles University Viničná Prague Czech Republic

Institute of Microbiology Czech Academy of Sciences Vídeňská Prague Czech Republic

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Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty PE. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytologist. 2019;223(3):1127–42. 10.1111/nph.15775 PubMed DOI

Kafle A, Garcia K, Wang XR, Pfeffer PE, Strahan GD, Bücking H. Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of PubMed

Dreyer I, Spitz O, Kanonenberg K, Montag K, Handrich MR, Ahmad S, et al. Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view. New Phytologist. 2019;222(2):1043–53. 10.1111/nph.15646 PubMed DOI PMC

di Fossalunga AS, Novero M. To trade in the field: the molecular determinants of arbuscular mycorrhiza nutrient exchange. Chemical and Biological Technologies in Agriculture. 2019;6.

Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology. 2008;6(10):763–75. 10.1038/nrmicro1987 PubMed DOI

Kim SJ, Eo JK, Lee EH, Park H, Eom AH. Effects of arbuscular mycorrhizal fungi and soil conditions on crop plant growth. Mycobiology. 2017;45(1):20–4. 10.5941/MYCO.2017.45.1.20 PubMed DOI PMC

van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature. 1998;396(6706):69–72.

Wagg C, Bender SF, Widmer F, van der Heijden MGA. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(14):5266–70. 10.1073/pnas.1320054111 PubMed DOI PMC

Newsham KK, Fitter AH, Watkinson AR. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends in Ecology & Evolution. 1995;10(10):407–11. PubMed

Bernardo L, Carletti P, Badeck FW, Rizza F, Morcia C, Ghizzoni R, et al. Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiology and Biochemistry. 2019;137:203–12. 10.1016/j.plaphy.2019.02.007 PubMed DOI

Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty PE. Take a trip through the plant and fungal transportome of mycorrhiza. Trends in Plant Science. 2016;21(11):937–50. 10.1016/j.tplants.2016.07.010 PubMed DOI

Řezáčová V, Konvalinková T, Jansa J. Carbon fluxes in mycorrhizal plants. In: Varma A, Prasad R, Tuteja N, editors. Mycorrhiza—Eco-Physiology, Secondary Metabolites, Nanomaterials: Fourth Edition2017. p. 1–21.

Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, et al. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil. 2011;349(1–2):121–56.

Hart MM, Antunes PM, Chaudhary VB, Abbott LK. yy Fungal inoculants in the field: Is the reward greater than the risk? Functional Ecology. 2018;32(1):126–35.

Smith SE, Smith FA, Jakobsen I. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology. 2003;133(1):16–20. 10.1104/pp.103.024380 PubMed DOI PMC

Smith SE, Anderson IC, Smith FA. Mycorrhizal associations and phosphorus acquisition: from cells to ecosystems. In: Plaxton WC, Lambers H, editors. Phosphorus Metabolism in Plants 2015. p. 409–39.

Harrison MJ, Dewbre GR, Liu JY. A phosphate transporter from PubMed DOI PMC

Smith SE, Jakobsen I, Grønlund M, Smith FA. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology. 2011;156(3):1050–7. 10.1104/pp.111.174581 PubMed DOI PMC

Jakobsen I, Rosendahl L. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist. 1990;115(1):77–83.

Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ. A PubMed DOI PMC

Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, et al. Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of PubMed DOI

Paszkowski U, Kroken S, Roux C, Briggs SP. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(20):13324–9. 10.1073/pnas.202474599 PubMed DOI PMC

Yang SY, Gronlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, et al. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell. 2012;24(10):4236–51. 10.1105/tpc.112.104901 PubMed DOI PMC

Tan ZJ, Hu YL, Lin ZP. PhPT4 is a mycorrhizal-phosphate transporter suppressed by lysophosphatidylcholine in

Tan ZJ, Hu YL, Lin ZP. Expression of NtPT5 is correlated with the degree of colonization in tobacco roots inoculated with

Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, et al. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature. 2001;414(6862):462–6. 10.1038/35106601 PubMed DOI

Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu GH, et al. The characterization of novel mycorrhiza-specific phosphate transporters from PubMed DOI

Glassop D, Smith SE, Smith FW. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta. 2005;222(4):688–98. 10.1007/s00425-005-0015-0 PubMed DOI

Liu JY, Versaw WK, Pumplin N, Gomez SK, Blaylock LA, Harrison MJ. Closely related members of the PubMed DOI PMC

Raven JA, Lambers H, Smith SE, Westoby M. Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytologist. 2018;217(4):1420–7. 10.1111/nph.14967 PubMed DOI

Salzer P, Hager A. Sucrose utilization of the ectomycorrhizal fungi

Schaarschmidt S, Hause B. Apoplastic invertases: Multi-faced players in the arbuscular mycorrhization. Plant Signalling Behaviour. 2008;5(1559–2316 (Print)):317–9. PubMed PMC

Harrison MJ. A sugar transporter from PubMed DOI

An J, Zeng T, Ji C, de Graaf S, Zheng Z, Xiao TT, et al. A PubMed

Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus PubMed DOI PMC

Lahmidi NA, Courty PE, Brule D, Chatagnier O, Arnould C, Doidy J, et al. Sugar exchanges in arbuscular mycorrhiza: PubMed DOI

Pumplin N, Harrison MJ. Live-cell imaging reveals periarbuscular membrane domains and organelle location in PubMed DOI PMC

Rich MK, Courty PE, Roux C, Reinhardt D. Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza in PubMed PMC

Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, et al. Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife. 2017;6. PubMed PMC

Wang ET, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, et al. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology. 2012;22(23):2242–6. 10.1016/j.cub.2012.09.043 PubMed DOI

Bravo A, York T, Pumplin N, Mueller LA, Harrison MJ. Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nature Plants. 2016;2(2). PubMed

Bravo A, Brands M, Wewer V, Dormann P, Harrison MJ. Arbuscular mycorrhiza-specific enzymes PubMed DOI

Jiang YN, Wang WX, Xie QJ, Liu N, Liu LX, Wang DP, et al. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science. 2017;356(6343):1172–5. 10.1126/science.aam9970 PubMed DOI

Rich MK, Nouri E, Courty PE, Reinhardt D. Diet of arbuscular mycorrhizal fungi: Bread and butter? Trends in Plant Science. 2017;22(8):652–60. 10.1016/j.tplants.2017.05.008 PubMed DOI

Brands M, Wewer V, Keymer A, Gutjahr C, Dormann P. The PubMed DOI

Wewer V, Brands M, Dormann P. Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus PubMed DOI

Řezáčová V, Gryndler M, Bukovská P, Šmilauer P, Jansa J. Molecular community analysis of arbuscular mycorrhizal fungi—contributions of PCR primer and host plant selectivity to the detected community profiles. Pedobiologia. 2016;59(4):179–87.

Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J. Arbuscular mycorrhiza stimulates biological nitrogen fixation in two PubMed PMC

Hewitt EJ. Sand and water culture methods used in the study of plant nutrition: Commonwealth Agricultural Bureaux; 1966.

Gryndler M, Šmilauer P, Püschel D, Bukovská P, Hršelová H, Hujslová M, et al. Appropriate nonmycorrhizal controls in arbuscular mycorrhiza research: a microbiome perspective. Mycorrhiza. 2018;28(5–6):435–50. 10.1007/s00572-018-0844-x PubMed DOI

Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, et al. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Advanced Bioinformatics. 2008;420747(1687–8035 (Electronic)). PubMed PMC

Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research. 2002;30(1):207–10. 10.1093/nar/30.1.207 PubMed DOI PMC

Tang HB, Krishnakumar V, Bidwell S, Rosen B, Chan AN, Zhou SG, et al. An improved genome release (version Mt4.0) for the model legume PubMed PMC

Doidy J, van Tuinen D, Lamotte O, Corneillat M, Alcaraz G, Wipf D. The PubMed DOI

Hruz T, Wyss M, Docquier M, Pfaffl MW, Masanetz S, Borghi L, et al. RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization. Bmc Genomics. 2011;12. PubMed PMC

Grunwald U, Guo WB, Fischer K, Isayenkov S, Ludwig-Muller J, Hause B, et al. Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, P PubMed DOI PMC

Baier MC, Keck M, Godde V, Niehaus K, Kuster H, Hohnjec N. Knockdown of the symbiotic sucrose synthase PubMed DOI PMC

Team RStudio. RStudio: Integrated Development for R. 0.99.902 ed: RStudio, Inc, Boston, MA: 2015.

R Development Core Team. R: A language and environment for statistical computing 3.0.0 ed: R Foundation for Statistical Computing; 2008.

Ohno T, Zibilske LM. Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Science Society of America Journal. 1991;55(3):892–5.

Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Hujslová M, Püschel D, et al. Utilization of organic nitrogen by arbuscular mycorrhizal fungi—Is there a specific role for protists and ammonia oxidizers? Mycorrhiza. 2018;28(3):269–83. 10.1007/s00572-018-0825-0 PubMed DOI

Couillerot O, Ramirez-Trujillo A, Walker V, von Felten A, Jansa J, Maurhofer M, et al. Comparison of prominent PubMed DOI

Slavíková R, Püschel D, Janoušková M, Hujslová M, Konvalinková T, Gryndlerová H, et al. Monitoring CO PubMed DOI

Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J. Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of PubMed DOI PMC

Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, et al. Symbiont identity matters: Carbon and phosphorus fluxes between PubMed DOI

Řezáčová V, Slavíková R, Zemková L, Konvalinková T, Procházková V, Št'ovíček V, et al. Mycorrhizal symbiosis induces plant carbon reallocation differently in C-3 and C-4

Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010;468(7323):527–U199. 10.1038/nature09606 PubMed DOI PMC

Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2012;335(6065):207–11. 10.1126/science.1213351 PubMed DOI

Lin IW, Sosso D, Chen LQ, Gase K, Kim SG, Kessler D, et al. Nectar secretion requires sucrose phosphate synthases and the sugar transporter PubMed

Sameeullah M, Demiral T, Aslam N, Baloch FS, Gurel E.

Manck-Götzenberger J, Requena N. Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Frontiers in plant science. 2016;7. PubMed PMC

Claeyssen E, Rivoal J. Isozymes of plant hexokinase: Occurrence, properties and functions. Phytochemistry. 2007;68(6):709–31. 10.1016/j.phytochem.2006.12.001 PubMed DOI

Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, et al. Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: The glucose 6-phosphate phosphate antiporter. Plant Cell. 1998;10(1):105–17. 10.1105/tpc.10.1.105 PubMed DOI PMC

Lohse S, Schliemann W, Ammer C, Kopka J, Strack D, Fester T. Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of PubMed DOI PMC

Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, et al. The half-size ABC transporters PubMed DOI

Klepek YS, Volke M, Konrad KR, Wippel K, Hoth S, Hedrich R, et al. PubMed DOI PMC

Schott S, Valdebenito B, Bustos D, Gomez-Porras JL, Sharma T, Dreyer I. Cooperation through competition—Dynamics and microeconomics of a minimal nutrient trade system in arbuscular mycorrhizal symbiosis. Frontiers in plant science. 2016;7. PubMed PMC

Liu GW, Sun AL, Li DQ, Athman A, Gilliham M, Liu LH. Molecular identification and functional analysis of a maize ( PubMed DOI

Bohner A, Kojima S, Hajirezaei M, Melzer M, von Wiren N. Urea retranslocation from senescing PubMed DOI PMC

Jin HR, Liu J, Huang XW. Forms of nitrogen uptake, translocation, and transfer via arbuscular mycorrhizal fungi: A review. Science China-Life Sciences. 2012;55(6):474–82. 10.1007/s11427-012-4330-y PubMed DOI

Calabrese S, Perez-Tienda J, Ellerbeck M, Arnould C, Chatagnier O, Boller T, et al. PubMed PMC

Wang WX, Shi JC, Xie QJ, Jiang YN, Yu N, Wang ET. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Molecular Plant. 2017;10(9):1147–58. 10.1016/j.molp.2017.07.012 PubMed DOI

Luginbuehl LH, Oldroyd GED. Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Current Biology. 2017;27(17):R952–R63. 10.1016/j.cub.2017.06.042 PubMed DOI

Sakiroglu M, Brummer EC. Identification of loci controlling forage yield and nutritive value in diploid alfalfa using GBS-GWAS. Theoretical and Applied Genetics. 2017;130(2):261–8. 10.1007/s00122-016-2782-3 PubMed DOI

Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, et al. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(50):20117–22. 10.1073/pnas.1313452110 PubMed DOI PMC

Balestrini R, Bonfante P. Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Frontiers in plant science. 2014;5. PubMed PMC

Underwood W. The plant cell wall: a dynamic barrier against pathogen invasion. Frontiers in plant science. 2012;3. PubMed PMC

Bellincampi D, Cervone F, Lionetti V. Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Frontiers in plant science. 2014;5 10.3389/fpls.2014.00005 PubMed DOI PMC

Yan N. Structural advances for the major facilitator superfamily (MFS) transporters. Trends in Biochemical Sciences. 2013;38(3):151–9. 10.1016/j.tibs.2013.01.003 PubMed DOI

Harley JL, Harley EL. A check-list of mycorrhiza in the brittish flora*. New Phytologist. 1987;105:1–102.

Bitterlich M, Krügel U, Boldt-Burisch K, Franken P, Kühn C. The sucrose transporter PubMed DOI

Keymer A, Gutjahr C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Current Opinion in Plant Biology. 2018;44:137–44. 10.1016/j.pbi.2018.04.005 PubMed DOI

Bender SF, van der Heijden MGA. Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. Journal of Applied Ecology. 2015;52(1):228–39.

van de Wiel CCM, van der Linden CG, Scholten OE. Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica. 2016;207(1):1–22.