Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria

Science

Volumn 356, Issue 6340, 2017, Pages

  Martin, Francis M ^a   Uroz, Stéphane ^a   Barker, David G ^b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHYTOHORMONE;

ANCESTRY; BACTERIUM; EVOLUTION; FUNGUS; GROWTH; MYCORRHIZA; ROOT COLONIZATION; SOIL MICROORGANISM; TERRESTRIAL ECOSYSTEM;

BACTERIUM; CELL WALL; FUNGUS; HOST RESISTANCE; MICROBIAL COLONIZATION; NITROGEN-FIXING BACTERIUM; NONHUMAN; PLANT; PLANT IMMUNITY; PLANT MICROORGANISM INTERACTION; PRIORITY JOURNAL; REVIEW; ROOT DEVELOPMENT; SYMBIOSIS; EVOLUTION; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHYSIOLOGY; PLANT ROOT;

BACTERIA (MICROORGANISMS); FUNGI;

BACTERIA; BIOLOGICAL EVOLUTION; FUNGI; NITROGEN FIXATION; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANTS; SYMBIOSIS;

EID: 85019699409     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aad4501     Document Type: Review

References (112)

1. L.Margulis, Symbiogenesis and symbionticism.In Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis, L.Margulis, R.Fester, Eds.(MIT Press, 1991), pp.1-14.
2. A.de Bary, Die Erscheinung der Symbiose (Tröbner Verlag, 1879).
3. K.A.Pirozynski, D.W.Malloch, The origin of land plants: A matter of mycotrophism.Biosystems 6, 153-164 (1975).doi: 10.1016/0303-2647(75)90023-4
4. M.A.Selosse, F.Le Tacon, The land flora: A phototrophfungus partnership? Trends Ecol.Evol.13, 15-20 (1998).doi: 10.1016/S0169-5347(97)01230-59
5. J.Lederberg, A.T.McCray, 'Ome Sweet 'Omics-A genealogical treasury of words.Scientist 15, 13313 (2001).
6. A.Sessitsch, B.Mitter, 21st century agriculture: Integration of plant microbiomes for improved crop production and food security.Microb.Biotechnol.8, 32-33 (2015).doi: 10.1111/1751-7915.121800
7. P.E.Busby et al., Research priorities for harnessing plant microbiomes in sustainable agriculture.PLOS Biol.15, e2001793 (2017).doi: 10.1371/journal.pbio.20017938
8. D.B.Möller, C.Vogel, Y.Bai, J.A.Vorholt, The plant microbiota: Systems-level insights and perspectives.Annu.Rev.Genet.50, 211-234 (2016).doi: 10.1146/annurev-genet-120215-0349523
9. S.R.Bordenstein, K.R.Theis, Host biology in light of the microbiome: Ten principles of holobionts and hologenomes.PLOS Biol.13, e1002226 (2015).doi: 10.1371/journal.pbio.10022267
10. N.A.Moran, D.B.Sloan, The hologenome concept: Helpful or hollow? PLOS Biol.13, e1002311 (2015).doi: 10.1371/journal.pbio.10023111
11. G.E.D.Oldroyd, J.D.Murray, P.S.Poole, J.A.Downie, The rules of engagement in the legume-rhizobial symbiosis.Annu.Rev.Genet.45, 119-144 (2011).doi: 10.1146/annurev-genet-110410-1325490
12. M.Parniske, Arbuscular mycorrhiza: The mother of plant root endosymbioses.Nat.Rev.Microbiol.6, 763-775 (2008).doi: 10.1038/nrmicro19874
13. P.Bonfante, A.Genre, Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis.Nat.Commun.1, 48 (2010).pmid: 20975705
14. F.Martin, A.Kohler, C.Murat, C.Veneault-Fourrey, D.S.Hibbett, Unearthing the roots of ectomycorrhizal symbioses.Nat.Rev.Microbiol.14, 760-773 (2016).doi: 10.1038/nrmicro.2016.1497
15. J.Belnap, O.L.Lange, Biological Soil Crusts: Structure, Function, and Management (Springer-Verlag, 2003).
16. D.Edwards, L.Cherns, A.J.Raven, Could land-based early photosynthesizing ecosystems have bioengineered the planet in mid-Palaeozoic times? Palaeontology 58, 803-837 (2015).doi: 10.1111/pala.12187
17. T.M.Lenton et al., Earliest land plants created modern levels of atmospheric oxygen.Proc.Natl.Acad.Sci.U.S.A.113, 9704-9709 (2016).doi: 10.1073/pnas.16047871138
18. W.Remy, T.N.Taylor, H.Hass, H.Kerp, Four hundredmillion-year-old vesicular arbuscular mycorrhizae.Proc.Natl.Acad.Sci.U.S.A.91, 11841-11843 (1994).doi: 10.1073/pnas.91.25.118410
19. M.C.Brundrett, Coevolution of roots and mycorrhizas of land plants.New Phytol.154, 275-304 (2002).doi: 10.1046/j.1469-8137.2002.00397.x
20. T.N.Taylor, W.Remy, H.Hass, H.Kerp, Fossil arbuscular mycorrhizae from the early Devonian.Mycologia 87, 560-573 (1995).doi: 10.2307/3760776
21. P.Kenrick, P.R.Crane, The origin and early evolution of plants on land.Nature 389, 33-39 (1997).doi: 10.1038/37918
22. P.Kenrick, C.H.Wellman, H.Schneider, G.D.Edgecombe, A timeline for terrestrialization: Consequences for the carbon cycle in the Palaeozoic.Philos.Trans.R.Soc.London Ser.B 367, 519-536 (2012).doi: 10.1098/rstb.2011.02714
23. P.Kenrick, C.Strullu-Derrien, The origin and early evolution of roots.Plant Physiol.166, 570-580 (2014).doi: 10.1104/pp.114.2445177
24. C.Strullu-Derrien et al., Fungal associations in Horneophyton ligneri from the Rhynie Chert (c.407 million year old) closely resemble those in extant lower land plants: Novel insights into ancestral plant-fungus symbioses.New Phytol.203, 964-979 (2014).doi: 10.1111/nph.128059
25. J.W.Spatafora et al., A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data.Mycologia 108, 1028-1046 (2016).doi: 10.3852/16-0420
26. K.J.Field et al., First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2.New Phytol.205, 743-756 (2015).doi: 10.1111/nph.130248
27. K.J.Field, S.Pressel, J.G.Duckett, W.R.Rimington, M.I.Bidartondo, Symbiotic options for the conquest of land.Trends Ecol.Evol.30, 477-486 (2015).doi: 10.1016/j.tree.2015.05.0073
28. M.I.Bidartondo et al., The dawn of symbiosis between plants and fungi.Biol.Lett.7, 574-577 (2011).doi: 10.1098/rsbl.2010.12034
29. M.Krings, T.N.Taylor, E.L.Taylor, N.Dotzler, C.Walker, Arbuscular mycorrhizal-like fungi in Carboniferous arborescent lycopsids.New Phytol.191, 311-314 (2011).doi: 10.1111/j.1469-8137.2011.03752.x8
30. J.L.Morris et al., Investigating Devonian trees as geo-engineers of past climates: Linking palaeosols to palaeobotany and experimental geobiology.Palaeontology 58, 787-801 (2015).doi: 10.1111/pala.12185
31. C.Beimforde et al., Ectomycorrhizas from a Lower Eocene angiosperm forest.New Phytol.192, 988-996 (2011).doi: 10.1111/j.1469-8137.2011.03868.x9
32. B.Lepage, R.Currah, R.Stockey, G.Rothwell, Fossil ectomycorrhizae from the middle Eocene.Am.J.Bot.84, 410-412 (1997).doi: 10.2307/24460144
33. A.Kohler et al., Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists.Nat.Genet.47, 410-415 (2015).doi: 10.1038/ng.32235
34. P.B.Matheny et al., Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae.J.Biogeogr.36, 577-592 (2009).doi: 10.1111/j.1365-2699.2008.02055.x
35. O.Schwery et al., As old as the mountains: The radiations of the Ericaceae.New Phytol.207, 355-367 (2015).doi: 10.1111/nph.132343
36. C.Kneip, P.Lockhart, C.Voss, U.-G.Maier, Nitrogen fixation in eukaryotes-New models for symbiosis.BMC Evol.Biol.7, 55-58 (2007).doi: 10.1186/1471-2148-7-555
37. J.Raymond, J.L.Siefert, C.R.Staples, R.E.Blankenship, The natural history of nitrogen fixation.Mol.Biol.Evol.21, 541-554 (2004).doi: 10.1093/molbev/msh0478
38. M.Parniske, Intracellular accommodation of microbes by plants: A common developmental program for symbiosis and disease? Curr.Opin.Plant Biol.3, 320-328 (2000).doi: 10.1016/S1369-5266(00)00088-17
39. D.E.Soltis et al., Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms.Proc.Natl.Acad.Sci.U.S.A.92, 2647-2651 (1995).doi: 10.1073/pnas.92.7.2647
40. G.D.A.Werner, W.K.Cornwell, J.I.Sprent, J.Kattge, E.T.Kiers, A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms.Nat.Commun.5, 4087 (2014).pmid: 24912610
41. S.M.Swensen, The evolution of actinorhizal symbioses: Evidence for multiple origins of the symbiotic association.Am.J.Bot.83, 1503-1512 (1996).doi: 10.2307/2446104
42. S.Svistoonoff, V.Hocher, H.Gherbi, Actinorhizal root nodule symbioses: What is signalling telling on the origins of nodulation? Curr.Opin.Plant Biol.20, 11-18 (2014).doi: 10.1016/j.pbi.2014.03.0017
43. G.E.D.Oldroyd, Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants.Nat.Rev.Microbiol.11, 252-263 (2013).doi: 10.1038/nrmicro29905
44. M.Venkateshwaran, J.D.Volkening, M.R.Sussman, J.-M.Ané, Symbiosis and the social network of higher plants.Curr.Opin.Plant Biol.16, 118-127 (2013).doi: 10.1016/j.pbi.2012.11.0078
45. P.-M.Delaux et al., Algal ancestor of land plants was preadapted for symbiosis.Proc.Natl.Acad.Sci.U.S.A.112, 13390-13395 (2015).doi: 10.1073/pnas.15154261120
46. K.Garcia, P.M.Delaux, K.R.Cope, J.-M.Ané, Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses.New Phytol.208, 79-87 (2015).doi: 10.1111/nph.134239
47. G.E.D.Oldroyd, J.A.Downie, Nuclear calcium changes at the core of symbiosis signalling.Curr.Opin.Plant Biol.9, 351-357 (2006).doi: 10.1016/j.pbi.2006.05.0039
48. F.Maillet et al., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.Nature 469, 58-63 (2011).doi: 10.1038/nature096229
49. A.Genre et al., Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone.New Phytol.198, 190-202 (2013).doi: 10.1111/nph.121461
50. C.Gutjahr, M.Parniske, Cell and developmental biology of arbuscular mycorrhiza symbiosis.Annu.Rev.Cell Dev.Biol.29, 593-617 (2013).doi: 10.1146/annurev-cellbio-101512-1224138
51. K.Miyata et al., The bifunctional plant receptor, OsCERK1, regulates both chitin-Triggered immunity and arbuscular mycorrhizal symbiosis in rice.Plant Cell Physiol.55, 1864-1872 (2014).doi: 10.1093/pcp/pcu1290
52. X.Zhang et al., The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling.Plant J.81, 258-267 (2015).doi: 10.1111/tpj.127231
53. L.Buendia, T.Wang, A.Girardin, B.Lefebvre, The LysM receptor-like kinase SlLYK10 regulates the arbuscular mycorrhizal symbiosis in tomato.New Phytol.210, 184-195 (2016).doi: 10.1111/nph.137535
54. G.Carotenuto et al., The rice LysM receptor-like kinase OsCERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling.New Phytol.214, 1440-1446 (2017).doi: 10.1111/nph.145394
55. M.Chabaud et al., Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca.New Phytol.209, 86-93 (2016).doi: 10.1111/nph.137320
56. E.Granqvist et al., Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and nonlegumes.New Phytol.207, 551-558 (2015).doi: 10.1111/nph.134647
57. A.Genre, M.Chabaud, T.Timmers, P.Bonfante, D.G.Barker, Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection.Plant Cell 17, 3489-3499 (2005).doi: 10.1105/tpc.105.0354104
58. J.Fournier et al., Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization.Plant Physiol.148, 1985-1995 (2008).doi: 10.1104/pp.108.1256745
59. B.J.Sieberer, M.Chabaud, J.Fournier, A.C.J.Timmers, D.G.Barker, A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula.Plant J.69, 822-830 (2012).doi: 10.1111/j.1365-313X.2011.04834.x1
60. M.Held et al., Common and not so common symbiotic entry.Trends Plant Sci.15, 540-545 (2010).doi: 10.1016/j.tplants.2010.08.0014
61. J.D.Murray, Invasion by invitation: Rhizobial infection in legumes.Mol.Plant Microbe Interact.24, 631-639 (2011).doi: 10.1094/MPMI-08-10-01816
62. M.R.Cerri et al., The symbiosis-related ERN transcription factors act in concert to coordinate rhizobial host root infection.Plant Physiol.171, 1037-1054 (2016).pmid: 27208242
63. T.Laloum et al., Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legumerhizobia endosymbiosis.Plant J.79, 757-768 (2014).doi: 10.1111/tpj.125873
64. N.D.Young et al., The Medicago genome provides insight into the evolution of rhizobial symbioses.Nature 480, 520-524 (2011).pmid: 22089132
65. N.Pumplin et al., Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis.Plant J.61, 482-494 (2010).doi: 10.1111/j.1365-313X.2009.04072.x7
66. J.D.Murray et al., Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula.Plant J.65, 244-252 (2011).doi: 10.1111/j.1365-313X.2010.04415.x9
67. A.Genre et al., Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas.Plant Cell Physiol.53, 244-255 (2012).doi: 10.1093/pcp/pcr1709
68. J.Fournier et al., Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair.Plant Physiol.167, 1233-1242 (2015).doi: 10.1104/pp.114.2533022
69. A.Breakspear et al., The root hair "infectome" of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for Auxin signaling in rhizobial infection.Plant Cell 26, 4680-4701 (2014).doi: 10.1105/tpc.114.1334967
70. M.Miri, P.Janakirama, M.Held, L.Ross, K.Szczyglowski, Into the root: How cytokinin controls rhizobial infection.Trends Plant Sci.21, 178-186 (2016).doi: 10.1016/j.Tplants.2015.09.0035
71. B.Péret et al., Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca.Plant Physiol.144, 1852-1862 (2007).doi: 10.1104/pp.107.1013377
72. D.S.Floss, J.G.Levy, V.Lévesque-Tremblay, N.Pumplin, M.J.Harrison, DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis.Proc.Natl.Acad.Sci.U.S.A.110, E5025-E5034 (2013).doi: 10.1073/pnas.13089731102
73. N.Yu et al., A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants.Cell Res.24, 130-133 (2014).doi: 10.1038/cr.2013.1676
74. H.J.Park, D.S.Floss, V.Levesque-Tremblay, A.Bravo, M.J.Harrison, Hyphal branching during arbuscule development requires Reduced Arbuscular Mycorrhiza1.Plant Physiol.169, 2774-2788 (2015).pmid: 26511916
75. L.Xue et al., Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus.Plant Physiol.167, 854-871 (2015).doi: 10.1104/pp.114.2554307
76. P.Pimprikar et al., A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching.Curr.Biol.26, 987-998 (2016).doi: 10.1016/j.cub.2016.01.0697
77. C.Heck et al., Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1.Curr.Biol.26, 2770-2778 (2016).doi: 10.1016/j.cub.2016.07.0593
78. C.Gutjahr, Phytohormone signaling in arbuscular mycorhiza development.Curr.Opin.Plant Biol.20, 26-34 (2014).doi: 10.1016/j.pbi.2014.04.0036
79. M.J.Pozo, J.A.López-Ráez, C.Azcón-Aguilar, J.M.García-Garrido, Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses.New Phytol.205, 1431-1436 (2015).doi: 10.1111/nph.132521
80. K.Garcia, J.Doidy, S.D.Zimmermann, D.Wipf, P.E.Courty, Take a trip through the plant and fungal transportome of mycorrhiza.Trends Plant Sci.21, 937-950 (2016).doi: 10.1016/j.tplants.2016.07.0104
81. P.-M.Delaux et al., Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution.PLOS Genet.10, e1004487 (2014).doi: 10.1371/journal.pgen.10044873
82. P.Favre et al., A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants.BMC Plant Biol.14, 333 (2014).doi: 10.1186/s12870-014-0333-09
83. A.Bravo, T.York, N.Pumplin, L.A.Mueller, M.J.Harrison, Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics.Nat.Plants 2, 15208 (2016).doi: 10.1038/nplants.2015.2080
84. X.Zhang, N.Pumplin, S.Ivanov, M.J.Harrison, EXO70I is required for development of a sub-domain of the periarbuscular membrane during arbuscular mycorrhizal symbiosis.Curr.Biol.25, 2189-2195 (2015).doi: 10.1016/j.cub.2015.06.0753
85. R.Huisman et al., A symbiosis-dedicated SYNTAXIN OF PLANTS 13II isoform controls the formation of a stable host-microbe interface in symbiosis.New Phytol.211, 1338-1351 (2016).doi: 10.1111/nph.139732
86. T.Suzaki, M.Kawaguchi, Root nodulation: A developmental program involving cell fate conversion triggered by symbiotic bacterial infection.Curr.Opin.Plant Biol.21, 16-22 (2014).doi: 10.1016/j.pbi.2014.06.002
87. S.Bensmihen, Hormonal control of lateral root and nodule development in legumes.Plants 4, 523-547 (2015).doi: 10.3390/plants40305230
88. L.Tirichine et al., A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis.Science 315, 104-107 (2007).doi: 10.1126/science.11323977
89. J.Plet et al., MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula.Plant J.65, 622-633 (2011).doi: 10.1111/j.1365-313X.2010.04447.x5
90. T.Suzaki et al., Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response.Development 139, 3997-4006 (2012).doi: 10.1242/dev.0840794
91. J.L.P.Ng et al., Flavonoids and auxin transport inhibitors rescue symbiotic nodulation in the Medicago truncatula cytokinin perception mutant cre1.Plant Cell 27, 2210-2226 (2015).doi: 10.1105/tpc.15.002315
92. S.Svistoonoff et al., The independent acquisition of plant root nitrogen-fixing symbiosis in fabids recruited the same genetic pathway for nodule organogenesis.PLOS ONE 8, e64515 (2013).doi: 10.1371/journal.pone.00645156
93. J.Felten et al., The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling.Plant Physiol.151, 1991-2005 (2009).doi: 10.1104/pp.109.1472319
94. A.Vayssières et al., Development of the poplar-Laccaria bicolor ectomycorrhiza modifies root auxin metabolism, signaling, and response.Plant Physiol.169, 890-902 (2015).doi: 10.1104/pp.114.2556201
95. F.A.Ditengou et al., Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture.Nat.Commun.6, 6279 (2015).doi: 10.1038/ncomms72794
96. J.M.Plett et al., Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots.New Phytol.202, 270-286 (2014).doi: 10.1111/nph.12655
97. S.Fabre et al., Nod factor-independent nodulation in Aeschynomene evenia required the common plant-microbe symbiotic toolkit.Plant Physiol.169, 2654-2664 (2015).pmid: 26446590
98. J.E.Behm, R.Geurts, E.T.Kiers, Parasponia: A novel system for studying mutualism stability.Trends Plant Sci.19, 757-763 (2014).doi: 10.1016/j.tplants.2014.08.007
99. R.L.Peterson, H.B.Massicotte, Exploring structural definitions of mycorrhizas, with emphasis on nutrientexchange interfaces.Can.J.Bot.82, 1074-1088 (2004).doi: 10.1139/b04-071
100. E.Tisserant et al., Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.Proc.Natl.Acad.Sci.U.S.A.110, 20117-20122 (2013).doi: 10.1073/pnas.13134521108
101. K.Lin et al., Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus.PLOS Genet.10, e1004078 (2014).doi: 10.1371/journal.pgen.10040785
102. S.Kloppholz, H.Kuhn, N.Requena, A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy.Curr.Biol.21, 1204-1209 (2011).doi: 10.1016/j.cub.2011.06.0444
103. J.M.Plett et al., A secreted effector protein of Laccaria bicolor is required for symbiosis development.Curr.Biol.21, 1197-1203 (2011).doi: 10.1016/j.cub.2011.05.0332
104. J.M.Plett et al., Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes.Proc.Natl.Acad.Sci.U.S.A.111, 8299-8304 (2014).doi: 10.1073/pnas.13226711118
105. C.Zipfel, G.E.D.Oldroyd, Plant signalling in symbiosis and immunity.Nature 543, 328-336 (2017).doi: 10.1038/nature220090
106. D.Bulgarelli, K.Schlaeppi, S.Spaepen, E.Ver Loren van Themaat, P.Schulze-Lefert, Structure and functions of the bacterial microbiota of plants.Annu.Rev.Plant Biol.64, 807-838 (2013).doi: 10.1146/annurev-Arplant-050312-1201068
107. S.Uroz, M.Buée, A.Deveau, S.Mieszkin, F.Martin, Ecology of the forest microbiome: Highlights of temperate and boreal ecosystems.Soil Biol.Biochem.103, 471-488 (2016).doi: 10.1016/j.soilbio.2016.09.006
108. R.Zgadzaj et al., Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities.Proc.Natl.Acad.Sci.U.S.A.113, E7996-E8005 (2016).doi: 10.1073/pnas.16165641131
109. N.Bodenhausen, M.Bortfeld-Miller, M.Ackermann, J.A.Vorholt, A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota.PLOS Genet.10, e1004283 (2014).doi: 10.1371/journal.pgen.10042839
110. K.G.Peay, P.G.Kennedy, J.M.Talbot, Dimensions of biodiversity in the Earth mycobiome.Nat.Rev.Microbiol.14, 434-447 (2016).doi: 10.1038/nrmicro.2016.592
111. S.L.Lebeis et al., Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa.Science 349, 860-864 (2015).doi: 10.1126/science.aaa87645
112. B.Beckers et al., Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome.Proc.Natl.Acad.Sci.U.S.A.113, 2312-2317 (2016).doi: 10.1073/pnas.15232641134