Correlative evidence for co-regulation of phosphorus and carbon exchanges with symbiotic fungus in the arbuscular mycorrhizal Medicago truncatula


Autoři: Jan Konečný aff001;  Hana Hršelová aff002;  Petra Bukovská aff002;  Martina Hujslová aff002;  Jan Jansa aff002
Působiště autorů: Department of Experimental Plant Biology, Faculty of Science, Charles University, Viničná, Prague, Czech Republic aff001;  Institute of Microbiology, Czech Academy of Sciences, Vídeňská, Prague, Czech Republic aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224938

Souhrn

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.

Klíčová slova:

Fungal genetics – Fungal physiology – Fungi – Gene expression – Phosphates – Plant physiology – Plants – Symbiosis


Zdroje

1. 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. doi: 10.1111/nph.15775 30843207

2. 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 Medicago truncatula. Plant Cell and Environment. 2019;42(1):270–84.

3. 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. doi: 10.1111/nph.15646 30565261

4. 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.

5. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology. 2008;6(10):763–75. doi: 10.1038/nrmicro1987 18794914

6. 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. doi: 10.5941/MYCO.2017.45.1.20 28435350

7. 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.

8. 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. doi: 10.1073/pnas.1320054111 24639507

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

10. 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. doi: 10.1016/j.plaphy.2019.02.007 30802803

11. 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. doi: 10.1016/j.tplants.2016.07.010 27514454

12. 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.

13. 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.

14. 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.

15. 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. doi: 10.1104/pp.103.024380 12970469

16. Smith SE, Anderson IC, Smith FA. Mycorrhizal associations and phosphorus acquisition: from cells to ecosystems. In: Plaxton WC, Lambers H, editors. Phosphorus Metabolism in Plants2015. p. 409–39.

17. Harrison MJ, Dewbre GR, Liu JY. A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi. Plant Cell. 2002;14(10):2413–29. doi: 10.1105/tpc.004861 12368495

18. 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. doi: 10.1104/pp.111.174581 21467213

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

20. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(5):1720–5. doi: 10.1073/pnas.0608136104 17242358

21. Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, et al. Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant and Cell Physiology. 2006;47(7):807–17. doi: 10.1093/pcp/pcj069 16774930

22. 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. doi: 10.1073/pnas.202474599 12271140

23. 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. doi: 10.1105/tpc.112.104901 23073651

24. Tan ZJ, Hu YL, Lin ZP. PhPT4 is a mycorrhizal-phosphate transporter suppressed by lysophosphatidylcholine in Petunia roots. Plant Molecular Biology Reporter. 2012;30(6):1480–7.

25. Tan ZJ, Hu YL, Lin ZP. Expression of NtPT5 is correlated with the degree of colonization in tobacco roots inoculated with Glomus etunicatum. Plant Molecular Biology Reporter. 2012;30(4):885–93.

26. 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. doi: 10.1038/35106601 11719809

27. Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu GH, et al. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant Journal. 2005;42(2):236–50. doi: 10.1111/j.1365-313X.2005.02364.x 15807785

28. 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. doi: 10.1007/s00425-005-0015-0 16133217

29. Liu JY, Versaw WK, Pumplin N, Gomez SK, Blaylock LA, Harrison MJ. Closely related members of the Medicago truncatula PHT1 phosphate transporter gene family encode phosphate transporters with distinct biochemical activities. Journal of Biological Chemistry. 2008;283(36):24673–81. doi: 10.1074/jbc.M802695200 18596039

30. 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. doi: 10.1111/nph.14967 29292829

31. Salzer P, Hager A. Sucrose utilization of the ectomycorrhizal fungi Amanita muscaria and Hebeloma crustuliniforme depends on the cell wall-bound invertase activity of their host Picea abies. Botanica Acta. 1991;104(6):439–45.

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

33. Harrison MJ. A sugar transporter from Medicago truncatula: Altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant Journal. 1996;9(4):491–503. doi: 10.1046/j.1365-313x.1996.09040491.x 8624512

34. An J, Zeng T, Ji C, de Graaf S, Zheng Z, Xiao TT, et al. A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytologist. 2019;1(224):396–408.

35. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. Plant Cell. 2011;23(10):3812–23. doi: 10.1105/tpc.111.089813 21972259

36. Lahmidi NA, Courty PE, Brule D, Chatagnier O, Arnould C, Doidy J, et al. Sugar exchanges in arbuscular mycorrhiza: RiMST5 and RiMST6, two novel Rhizophagus irregularis monosaccharide transporters, are involved in both sugar uptake from the soil and from the plant partner. Plant Physiology and Biochemistry. 2016;107:354–63. doi: 10.1016/j.plaphy.2016.06.023 27362299

37. Pumplin N, Harrison MJ. Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiology. 2009;151(2):809–19. doi: 10.1104/pp.109.141879 19692536

38. Rich MK, Courty PE, Roux C, Reinhardt D. Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza in Petunia hybrida. Bmc Genomics. 2017;18.

39. 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.

40. 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. doi: 10.1016/j.cub.2012.09.043 23122843

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

42. Bravo A, Brands M, Wewer V, Dormann P, Harrison MJ. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytologist. 2017;214(4):1631–45. doi: 10.1111/nph.14533 28380681

43. 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. doi: 10.1126/science.aam9970 28596307

44. 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. doi: 10.1016/j.tplants.2017.05.008 28622919

45. Brands M, Wewer V, Keymer A, Gutjahr C, Dormann P. The Lotus japonicus acyl-acyl carrier protein thioesterase FatM is required for mycorrhiza formation and lipid accumulation of Rhizophagus irregularis. Plant Journal. 2018;95(2):219–32. doi: 10.1111/tpj.13943 29687516

46. Wewer V, Brands M, Dormann P. Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus. Plant Journal. 2014;79(3):398–412. doi: 10.1111/tpj.12566 24888347

47. 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.

48. Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J. Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Frontiers in plant science. 2017;8.

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

50. 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. doi: 10.1007/s00572-018-0844-x 29931404

51. 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)).

52. 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. doi: 10.1093/nar/30.1.207 11752295

53. 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 Medicago truncatula. Bmc Genomics. 2014;15.

54. Doidy J, van Tuinen D, Lamotte O, Corneillat M, Alcaraz G, Wipf D. The Medicago truncatula sucrose transporter family: Characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. Molecular Plant. 2012;5(6):1346–58. doi: 10.1093/mp/sss079 22930732

55. 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.

56. 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, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta. 2009;229(5):1023–34. doi: 10.1007/s00425-008-0877-z 19169704

57. Baier MC, Keck M, Godde V, Niehaus K, Kuster H, Hohnjec N. Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula. Plant Physiology. 2010;152(2):1000–14. doi: 10.1104/pp.109.149898 20007443

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

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

60. 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.

61. 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. doi: 10.1007/s00572-018-0825-0 29455336

62. Couillerot O, Ramirez-Trujillo A, Walker V, von Felten A, Jansa J, Maurhofer M, et al. Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth. Applied Microbiology and Biotechnology. 2013;97(10):4639–49. doi: 10.1007/s00253-012-4249-z 22805783

63. Slavíková R, Püschel D, Janoušková M, Hujslová M, Konvalinková T, Gryndlerová H, et al. Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi. Mycorrhiza. 2017;27(1):35–51. doi: 10.1007/s00572-016-0731-2 27549438

64. Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J. Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula. Frontiers in plant science. 2015;6:65. doi: 10.3389/fpls.2015.00065 25763002

65. Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, et al. Symbiont identity matters: Carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza. 2011;21(8):689–702. doi: 10.1007/s00572-011-0371-5 21472448

66. 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 Panicum grasses. Plant and Soil. 2018;425(1–2):441–56.

67. 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. doi: 10.1038/nature09606 21107422

68. 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. doi: 10.1126/science.1213351 22157085

69. Lin IW, Sosso D, Chen LQ, Gase K, Kim SG, Kessler D, et al. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature. 2014;508(7497):1–+.

70. Sameeullah M, Demiral T, Aslam N, Baloch FS, Gurel E. In silico functional analyses of SWEETs reveal cues for their role in AMF symbiosis. In: Hakeem K. AM, editor. Plant, Soil and Microbes: Springer, Cham; 2016. p. 45–58.

71. 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.

72. Claeyssen E, Rivoal J. Isozymes of plant hexokinase: Occurrence, properties and functions. Phytochemistry. 2007;68(6):709–31. doi: 10.1016/j.phytochem.2006.12.001 17234224

73. 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. doi: 10.1105/tpc.10.1.105 9477574

74. Lohse S, Schliemann W, Ammer C, Kopka J, Strack D, Fester T. Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiology. 2005;139(1):329–40. doi: 10.1104/pp.105.061457 16126866

75. Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, et al. The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant Journal. 2012;69(5):906–20. doi: 10.1111/j.1365-313X.2011.04842.x 22077667

76. Klepek YS, Volke M, Konrad KR, Wippel K, Hoth S, Hedrich R, et al. Arabidopsis thaliana POLYOL/MONOSACCHARIDE TRANSPORTERS 1 and 2: fructose and xylitol/H+ symporters in pollen and young xylem cells. Journal of experimental botany. 2010;61(2):537–50. doi: 10.1093/jxb/erp322 19969532

77. 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.

78. Liu GW, Sun AL, Li DQ, Athman A, Gilliham M, Liu LH. Molecular identification and functional analysis of a maize (Zea mays) DUR3 homolog that transports urea with high affinity. Planta. 2015;241(4):861–74. doi: 10.1007/s00425-014-2219-7 25522795

79. Bohner A, Kojima S, Hajirezaei M, Melzer M, von Wiren N. Urea retranslocation from senescing Arabidopsis leaves is promoted by DUR3-mediated urea retrieval from leaf apoplast. Plant Journal. 2015;81(3):377–87. doi: 10.1111/tpj.12740 25440717

80. 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. doi: 10.1007/s11427-012-4330-y 22744177

81. Calabrese S, Perez-Tienda J, Ellerbeck M, Arnould C, Chatagnier O, Boller T, et al. GintAMT3—a low-affinity ammonium transporter of the arbuscular mycorrhizal Rhizophagus irregularis. Frontiers in plant science. 2016;7.

82. 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. doi: 10.1016/j.molp.2017.07.012 28782719

83. Luginbuehl LH, Oldroyd GED. Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Current Biology. 2017;27(17):R952–R63. doi: 10.1016/j.cub.2017.06.042 28898668

84. 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. doi: 10.1007/s00122-016-2782-3 27662844

85. 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. doi: 10.1073/pnas.1313452110 24277808

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

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

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

89. Yan N. Structural advances for the major facilitator superfamily (MFS) transporters. Trends in Biochemical Sciences. 2013;38(3):151–9. doi: 10.1016/j.tibs.2013.01.003 23403214

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

91. Bitterlich M, Krügel U, Boldt-Burisch K, Franken P, Kühn C. The sucrose transporter SlSUT2 from tomato interacts with brassinosteroid functioning and affects arbuscular mycorrhiza formation. Plant Journal. 2014;78(5):877–89. doi: 10.1111/tpj.12515 24654931

92. Keymer A, Gutjahr C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Current Opinion in Plant Biology. 2018;44:137–44. doi: 10.1016/j.pbi.2018.04.005 29729528

93. 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.

94. 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.


Článek vyšel v časopise

PLOS One


2019 Číslo 11