Evolution of the symbiosis-specific gras regulatory network in bryophytes

Frontiers in Plant Science

Volumn 871, Issue , 2018, Pages

  Grosche, Christopher ^a   Genau, Anne Christina ^a   Rensing, Stefan A ^a,b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Bryophyte; GRAS; Land plant evolution; Moss; Mycorrhiza; Physcomitrella patens; Symbiotic pathway; Transcription factor

Indexed keywords

EXPANSION; TRANSCRIPTION; TRANSCRIPTION FACTORS;

BRYOPHYTE; GRAS; LAND PLANTS; MOSS; MYCORRHIZA; PHYSCOMITRELLA PATENS; SYMBIOTIC PATHWAY;

PLANTS (BOTANY);

EID: 85058808292     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2018.01621     Document Type: Article

References (120)

1. Achard P., Cheng H., De Grauwe L., Decat J., Schoutteten H., Moritz T., (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science 311 91–94. 10.1126/science.1118642 16400150.
2. Akiyama K., Matsuzaki K., Hayashi H., (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435 824–827. 10.1038/nature03608 15944706.
3. Akiyama K., Ogasawara S., Ito S., Hayashi H., (2010). Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol. 51 1104–1117. 10.1093/pcp/pcq058 20418334.
4. Antolín-Llovera M., Ried M. K., Binder A., Parniske M., (2012). Receptor kinase signaling pathways in plant-microbe interactions. Annu. Rev. Phytopathol. 50 451–473.10.1146/annurev-phyto-081211-173002 22920561.
5. Bago B., Pfeffer P. E., Abubaker J., Jun J., Allen J. W., Brouillette J., (2003). Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol. 131 1496–1507.10.1104/pp.102.007765 12644699.
6. Balzergue C., Puech-Pages V., Bécard G., Rochange S. F., (2011). The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J. Exp. Bot. 62 1049–1060. 10.1093/jxb/erq335 21045005.
7. Besserer A., Puech-Pages V., Kiefer P., Gomez-Roldan V., Jauneau A., Roy S., (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4:e226. 10.1371/journal.pbio.0040226 16787107.
8. Bonfante P., Anca I. A., (2009). Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu. Rev. Microbiol. 63 363–383. 10.1146/annurev.micro.091208.073504.
9. Bonfante P., Genre A., (2010). Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1:48. 10.1038/ncomms1046 20975705.
10. Boullard B., (1988). “Observations on the coevolution of fungi with hepatics,” in Coevolution of Fungi with Plants and Animals, eds Pirozynski K. A., Hawksworth D. L., (Cambridge, MA: Academic Press).
11. Bowman J. L., Kohchi T., Yamato K. T., Jenkins J., Shu S., Ishizaki K., (2017). Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171 287–304.e15. 10.1016/j.cell.2017.09.030 28985561.
12. Bravo A., York T., Pumplin N., Mueller L. A., Harrison M. J., (2016). Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat. Plants 2:15208. 10.1038/nplants.2015.208 27249190.
13. Breuillin F., Schramm J., Hajirezaei M., Ahkami A., Favre P., Druege U., (2010). Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J. 64 1002–1017. 10.1111/j.1365-313X.2010.04385.x 21143680.
14. Carbonnel S., Gutjahr C., (2014). Control of arbuscular mycorrhiza development by nutrient signals. Front. Plant Sci. 5:462. 10.3389/fpls.2014.00462 25309561.
15. Catoira R., Galera C., de Billy F., Penmetsa R. V., Journet E. P., Maillet F., (2000). Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12 1647–1666. 10.1105/tpc.12.9.1647 11006338.
16. Charpentier M., Bredemeier R., Wanner G., Takeda N., Schleiff E., Parniske M., (2008). Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20 3467–3479. 10.1105/tpc.108.063255 19106374.
17. Conn C. E., Nelson D. C., (2015). Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front. Plant Sci. 6:1219. 10.3389/fpls.2015.01219 26779242.
18. Corradi N., Bonfante P., (2012). The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection. PLoS Pathog. 8:e1002600. 10.1371/journal.ppat.1002600 22532798.
19. Croft M. T., Lawrence A. D., Raux-Deery E., Warren M. J., Smith A. G., (2005). Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438 90–93. 10.1038/nature04056 16267554.
20. Darriba D., Taboada G. L., Doallo R., Posada D., (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27 1164–1165. 10.1093/bioinformatics/btr088 21335321.
21. Decker E. L., Alder A., Hunn S., Ferguson J., Lehtonen M. T., Scheler B., (2017). Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytol. 216 455–468. 10.1111/nph.14506 28262967.
22. Delaux P.-M., Bécard G., Combier J.-P., (2013a). NSP1 is a component of the Myc signaling pathway. New Phytol. 199 59–65. 10.1111/nph.12340 23663036.
23. Delaux P.-M., Séjalon-Delmas N., Bécard G., Ané J.-M., (2013b). Evolution of the plant-microbe symbiotic ‘toolkit’. Trends Plant Sci. 18 298–304. 10.1016/j.tplants.2013.01.008 23462549.
24. Delaux P. M., Radhakrishnan G. V., Jayaraman D., Cheema J., Malbreil M., Volkening J. D., (2015). Algal ancestor of land plants was preadapted for symbiosis. Proc. Natl. Acad. Sci. U.S.A. 112 13390–13395. 10.1073/pnas.1515426112 26438870.
25. Delaux P. M., Varala K., Edger P. P., Coruzzi G. M., Pires J. C., Ane J. M., (2014). Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet. 10:e1004487. 10.1371/journal.pgen.1004487 25032823.
26. ∗-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 156 1990–2010. 10.1104/pp.111.172627 21571671.
27. Favre P., Bapaume L., Bossolini E., Delorenzi M., Falquet L., Reinhardt D., (2014). A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants. BMC Plant Biol. 14:333.10.1186/s12870-014-0333-0 25465219.
28. Feddermann N., Finlay R., Boller T., Elfstrand M., (2010). Functional diversity in arbuscular mycorrhiza – the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecol. 3 1–8. 10.1016/j.funeco.2009.07.003.
29. Field K. J., Pressel S., (2018). Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. New Phytol. 10.1111/nph.15158 [Epub ahead of print]. 29696662.
30. Field K. J., Pressel S., Duckett J. G., Rimington W. R., Bidartondo M. I., (2015). Symbiotic options for the conquest of land. Trends Ecol. Evol. 30 477–486. 10.1016/j.tree.2015.05.007 26111583.
31. Field K. J., Rimington W. R., Bidartondo M. I., Allinson K. E., Beerling D. J., Cameron D. D., (2014). First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO. New Phytol. 205 743–756. 10.1111/nph.13024 25230098.
32. Finn R. D., Clements J., Arndt W., Miller B. L., Wheeler T. J., Schreiber F., (2015). HMMER web server: 2015 update. Nucleic Acids Res. 43 W30–W38. 10.1093/nar/gkv397 25943547.
33. Fitter A. H., (2005). Darkness visible: reflections on underground ecology. J. Ecol. 93 231–243. 10.1111/j.0022-0477.2005.00990.x.
34. Floss D. S., Levy J. G., Levesque-Tremblay V., Pumplin N., Harrison M. J., (2013). DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 110 E5025–E5034. 10.1073/pnas.1308973110 24297892.
35. Gaude N., Schulze W. X., Franken P., Krajinski F., (2012). Cell type-specific protein and transcription profiles implicate periarbuscular membrane synthesis as an important carbon sink in the mycorrhizal symbiosis. Plant Signal. Behav. 7 461–464. 10.4161/psb.19650 22499167.
36. + spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 198 190–202. 10.1111/nph.12146 23384011.
37. Genre A., Russo G., (2016). Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front. Plant Sci. 7:96. 10.3389/fpls.2016.00096 26909085.
38. Gobbato E., Marsh J. F., Vernié T., Wang E., Maillet F., Kim J., (2012). A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr. Biol. 22 2236–2241. 10.1016/j.cub.2012.09.044 23122845.
39. Gobbato E., Wang E., Higgins G., Bano S. A., Henry C., Schultze M., (2013). RAM1 and RAM2 function and expression during arbuscular mycorrhizal symbiosis and Aphanomyces euteiches colonization. Plant Signal. Behav. 8:e26049. 10.4161/psb.26049 24270627.
40. Gutjahr C., (2014). Phytohormone signaling in arbuscular mycorhiza development. Curr. Opin. Plant Biol. 20 26–34. 10.1016/j.pbi.2014.04.003 24853646.
41. Gutjahr C., Gobbato E., Choi J., Riemann M., Johnston M. G., Summers W., (2015). Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350 1521–1524. 10.1126/science.aac9715 26680197.
42. Gutjahr C., Parniske M., (2013). Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 29 593–617. 10.1146/annurev-cellbio-101512-122413 24099088.
43. Hanke S. T., Rensing S. A., (2010). In vitro association of non-seed plant gametophytes with arbuscular mycorrhiza fungi. Endocyt. Cell. Res. 20 95–101.
44. Harrison M. J., Dewbre G. R., Liu J., (2002). A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14 2413–2429. 10.1105/tpc.004861 12368495.
45. Heck C., Kuhn H., Heidt S., Walter S., Rieger N., Requena N., (2016). Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1. Curr. Biol. 26 2770–2778. 10.1016/j.cub.2016.07.059 27641773.
46. Hempel M., Blume M., Blindow I., Gross E. M., (2008). Epiphytic bacterial community composition on two common submerged macrophytes in brackish water and freshwater. BMC Microbiol. 8:58. 10.1186/1471-2180-8-58 18402668.
47. Hirano Y., Nakagawa M., Suyama T., Murase K., Shirakawa M., Takayama S., (2017). Structure of the SHR-SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD. Nat. Plants 3:17010. 10.1038/nplants.2017.10 28211915.
48. Hirsch S., Kim J., Munoz A., Heckmann A. B., Downie J. A., Oldroyd G. E., (2009). GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21 545–557. 10.1105/tpc.108.064501 19252081.
49. Hirsch S., Oldroyd G. E., (2009). GRAS-domain transcription factors that regulate plant development. Plant Signal. Behav. 4 698–700. 10.4161/psb.4.8.9176.
50. Hofferek V., Mendrinna A., Gaude N., Krajinski F., Devers E. A., (2014). MiR171h restricts root symbioses and shows like its target NSP2 a complex transcriptional regulation in Medicago truncatula. BMC Plant Biol. 14:199. 10.1186/s12870-014-0199-1 25928247.
51. Hohnjec N., Czaja-Hasse L. F., Hogekamp C., Kuster H., (2015). Pre-announcement of symbiotic guests: transcriptional reprogramming by mycorrhizal lipochitooligosaccharides shows a strict co-dependency on the GRAS transcription factors NSP1 and RAM1. BMC Genomics 16:994. 10.1186/s12864-015-2224-7 26597293.
52. Hom E. F., Murray A. W., (2014). Plant-fungal ecology. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345 94–98. 10.1126/science.1253320 24994654.
53. Humphreys C. P., Franks P. J., Rees M., Bidartondo M. I., Leake J. R., Beerling D. J., (2010). Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat. Commun. 1:103. 10.1038/ncomms1105 21045821.
54. Kataržytė M., Vaičiūtė D., Bučas M., Gyraitė G., Petkuvienė J., (2017). Microorganisms associated with charophytes under different salinity conditions. Oceanologia 59 177–186. 10.1016/j.oceano.2016.10.002.
55. Katoh K., Standley D. M., (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 772–780. 10.1093/molbev/mst010 23329690.
56. Kistner C., Parniske M., (2002). Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7 511–518. 10.1016/S1360-1385(02)02356-7.
57. Koide R. T., Schreiner R. P., (1992). Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 557–581. 10.1146/annurev.pp.43.060192.003013.
58. Kowal J., Pressel S., Duckett J. G., Bidartondo M. I., Field K. J., (2018). From rhizoids to roots? Experimental evidence of mutualism between liverworts and ascomycete fungi. Ann. Bot. 121 221–227. 10.1093/aob/mcx126 29300826.
59. Lang D., Ullrich K. K., Murat F., Fuchs J., Jenkins J., Haas F. B., (2018). The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J. 93 515–533. 10.1111/tpj.13801 29237241.
60. Lang D., Weiche B., Timmerhaus G., Richardt S., Riano-Pachon D. M., Correa L. G., (2010). Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biol. Evol. 2 488–503. 10.1093/gbe/evq032 20644220.
61. Lauressergues D., Delaux P. M., Formey D., Lelandais-Briere C., Fort S., Cottaz S., (2012). The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J. 72 512–522. 10.1111/j.1365-313X.2012.05099.x 22775306.
62. Li S., Zhao Y., Zhao Z., Wu X., Sun L., Liu Q., (2016). Crystal structure of the GRAS domain of SCARECROW-LIKE7 in Oryza sativa. Plant Cell 28 1025–1034. 10.1105/tpc.16.00018 27081181.
63. Ligrone R., Carafa A., Lumini E., Bianciotto V., Bonfante P., Duckett J. G., (2007). Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am. J. Bot. 94 1756–1777. 10.3732/ajb.94.11.1756 21636371.
64. Ligrone R., Duckett J. G., Renzaglia K. S., (2012). Major transitions in the evolution of early land plants: a bryological perspective. Ann. Bot. 109 851–871. 10.1093/aob/mcs017 22356739.
65. Liu J., Maldonado-Mendoza I., Lopez-Meyer M., Cheung F., Town C. D., Harrison M. J., (2007). Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 50 529–544. 10.1111/j.1365-313X.2007.03069.x 17419842.
66. Liu W., Kohlen W., Lillo A., Op den Camp R., Ivanov S., (2011). Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell Online 23 3853–3865. 10.1105/tpc.111.089771 22039214.
67. Luginbuehl L. H., Oldroyd G. E. D., (2017). Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Curr. Biol. 27 R952–R963. 10.1016/j.cub.2017.06.042 28898668.
68. MacLean A. M., Bravo A., Harrison M. J., (2017). Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. Plant Cell 29 2319–2335. 10.1105/tpc.17.00555 28855333.
69. Maillet F., Poinsot V., André O., Puech-Pages V., Haouy A., Gueunier M., (2012). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469 58–63. 10.1038/nature09622 21209659.
70. Martin F. M., Uroz S., Barker D. G., (2017). Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356:eaad4501. 28546156.
71. Martin-Rodriguez J. A., Huertas R., Ho-Plagaro T., Ocampo J. A., Tureckova V., Tarkowska D., (2016). Gibberellin-abscisic acid balances during arbuscular mycorrhiza formation in tomato. Front. Plant Sci. 7:1273. 10.3389/fpls.2016.01273 27602046.
72. Matasci N., Hung L. H., Yan Z., Carpenter E. J., Wickett N. J., Mirarab S., (2014). Data access for the 1,000 Plants (1KP) project. Gigascience 3:17. 10.1186/2047-217X-3-17 25625010.
73. Morris J. L., Puttick M. N., Clark J. W., Edwards D., Kenrick P., Pressel S., (2018). The timescale of early land plant evolution. Proc. Natl. Acad. Sci. U.S.A. 115 E2274–E2283. 10.1073/pnas.1719588115 29463716.
74. Oldroyd G. E., (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11 252–263. 10.1038/nrmicro2990 23493145.
75. Park H.-J., Floss D. S., Levesque-Tremblay V., Bravo A., Harrison M. J., (2015). Hyphal branching during arbuscule development requires reduced arbuscular mycorrhiza1. Plant Physiol. 169 2774–2788. 26511916.
76. Parke J. L., Linderman R. G., (1980). Association of vesicular-arbuscular mycorrhizal fungi with the moss Funaria hygrometrica. Can. J. Bot. 58 1898–1904. 10.1139/b80-218.
77. Peng J., Richards D. E., Hartley N. M., Murphy G. P., Devos K. M., Flintham J. E., (1999). ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400 256–261. 10.1038/22307 10421366.
78. Perroud P. F., Haas F. B., Hiss M., Ullrich K. K., Alboresi A., Amirebrahimi M., (2018). The Physcomitrella patens gene atlas project: large scale RNA-seq based expression data. Plant J. 95 168–182. 10.1111/tpj.13940 29681058.
79. Pimprikar P., Carbonnel S., Paries M., Katzer K., Klingl V., Bohmer M. J., (2016). A CCaMK-CYCLOPS-DELLA complex activates transcription of Ram1 to regulate arbuscule branching. Curr. Biol. 26 987–998. 10.1016/j.cub.2016.01.069 27020747.
80. Pimprikar P., Gutjahr C., (2018). Transcriptional regulation of arbuscular mycorrhiza development. Plant Cell Physiol. 59 673–690. 10.1093/pcp/pcy024 29425360.
81. Pirozynski K. A., Malloch D. W., (1975). The origin of land plants: a matter of mycotrophism. Biosystems 6 153–164. 10.1016/0303-2647(75)90023-4 1120179.
82. Proust H., Hoffmann B., Xie X., Yoneyama K., Schaefer D. G., Yoneyama K., (2011). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138 1531–1539. 10.1242/dev.058495 21367820.
83. Pysh L. D., Wysocka-Diller J. W., Camilleri C., Bouchez D., Benfey P. N., (1999). The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18 111–119. 10.1046/j.1365-313X.1999.00431.x 10341448.
84. Read D. J. D., Ducket J. G. J., Francis R. R., Ligron R. R., Russell A. A., (2000). Symbiotic fungal associations in ‘lower’ land plants. Philos. Trans. R. Soc. B Biol. Sci. 355 815–811. 10.1098/rstb.2000.0617 10905611.
85. Rensing S. A., (2014). Gene duplication as a driver of plant morphogenetic evolution. Curr. Opin. Plant Biol. 17 43–48. 10.1016/j.pbi.2013.11.002 24507493.
86. Rensing S. A., (2017). Why we need more non-seed plant models. New Phytol. 216 355–360. 10.1111/nph.14464 28191633.
87. Rey T., Bonhomme M., Chatterjee A., Gavrin A., Toulotte J., Yang W., (2017). The Medicago truncatula GRAS protein RAD1 supports arbuscular mycorrhiza symbiosis and Phytophthora palmivora susceptibility. J. Exp. Bot. 68 5871–5881. 10.1093/jxb/erx398 29186498.
88. Rey T., Chatterjee A., Buttay M., Toulotte J., Schornack S., (2015). Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytol. 206 497–500. 10.1111/nph.13233 25495186.
89. Rich M. K., Courty P. E., Roux C., Reinhardt D., (2017). Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza in Petunia hybrida. BMC Genomics 18:589. 10.1186/s12864-017-3988-8 28789611.
90. Rich M. K., Schorderet M., Bapaume L., Falquet L., Morel P., Vandenbussche M., (2015). The petunia GRAS transcription factor ATA/RAM1 regulates symbiotic gene expression and fungal morphogenesis in arbuscular mycorrhiza. Plant Physiol. 168 788–797. 10.1104/pp.15.00310 25971550.
91. Rodriguez R. J., White J. F., Jr. Arnold A. E., Redman R. S., (2009). Fungal endophytes: diversity and functional roles. New Phytol. 182 314–330. 10.1111/j.1469-8137.2009.02773.x 19236579.
92. Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Hohna S., (2012). MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61 539–542. 10.1093/sysbio/sys029 22357727.
93. Santi C., Bogusz D., Franche C., (2013). Biological nitrogen fixation in non-legume plants. Ann. Bot. 111 743–767.10.1093/aob/mct048 23478942.
94. Simao F. A., Waterhouse R. M., Ioannidis P., Kriventseva E. V., Zdobnov E. M., (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31 3210–3212. 10.1093/bioinformatics/btv351 26059717.
95. Singh S., Katzer K., Lambert J., Cerri M., Parniske M., (2014). CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15 139–152. 10.1016/j.chom.2014.01.011 24528861.
96. Smit P., Raedts J., Portyanko V., Debellé F., Gough C., Bisseling T., (2005). NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308 1789–1791. 10.1126/science.1111025 15961669.
97. Sun J., Miller J. B., Granqvist E., Wiley-Kalil A., Gobbato E., Maillet F., (2015). Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27 823–838. 10.1105/tpc.114.131326 25724637.
98. Sun T. P., (2011). The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21 R338–R345. 10.1016/j.cub.2011.02.036 21549956.
99. Sun X., Xue B., Jones W. T., Rikkerink E., Dunker A. K., Uversky V. N., (2011). A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol. Biol. 77 205–223. 10.1007/s11103-011-9803-z 21732203.
100. Szovenyi P., Perroud P. F., Symeonidi A., Stevenson S., Quatrano R. S., Rensing S. A., (2014). De novo assembly and comparative analysis of the Ceratodon purpureus transcriptome. Mol. Ecol. Resour. 15 203–215. 10.1111/1755-0998.12284 24862584.
101. Szovenyi P., Rensing S. A., Lang D., Wray G. A., Shaw A. J., (2010). Generation-biased gene expression in a bryophyte model system. Mol. Biol. Evol. 28 803–812. 10.1093/molbev/msq254 20855429.
102. Takeda N., Haage K., Sato S., Tabata S., Parniske M., (2011). Activation of a Lotus japonicus subtilase gene during arbuscular mycorrhiza is dependent on the common symbiosis genes and two cis-active promoter regions. Mol. Plant Microbe Interact. 24 662–670. 10.1094/MPMI-09-10-0220 21261463.
103. Takeda N., Handa Y., Tsuzuki S., Kojima M., Sakakibara H., Kawaguchi M., (2015). Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol. 167 545–557. 10.1104/pp.114.247700 25527715.
104. Takeda N., Tsuzuki S., Suzaki T., Parniske M., Kawaguchi M., (2013). CERBERUS and NSP1 of Lotus japonicus are common symbiosis genes that modulate arbuscular mycorrhiza development. Plant Cell Physiol. 54 1711–1723. 10.1093/pcp/pct114 23926062.
105. Thieulin-Pardo G., Avilan L., Kojadinovic M., Gontero B., (2015). Fairy “tails”: flexibility and function of intrinsically disordered extensions in the photosynthetic world. Front. Mol. Biosci. 2:23. 10.3389/fmolb.2015.00023.
106. Venkateshwaran M., Jayaraman D., Chabaud M., Genre A., Balloon A. J., Maeda J., (2015). A role for the mevalonate pathway in early plant symbiotic signaling. Proc. Natl. Acad. Sci. U.S.A. 112 9781–9786. 10.1073/pnas.1413762112 26199419.
107. Veresoglou S. D., Chen B., Rillig M. C., (2012). Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol. Biochem. 46 53–62. 10.1016/j.soilbio.2011.11.018.
108. Volkmar U., Knoop V., (2010). Introducing intron locus cox1i624 for phylogenetic analyses in Bryophytes: on the issue of Takakia as sister genus to all other extant mosses. J. Mol. Evol. 70 506–518. 10.1007/s00239-010-9348-9 20473660.
109. Wang B., Qiu Y. L., (2006). Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16 299–363. 10.1007/s00572-005-0033-6 16845554.
110. Wang B., Yeun L. H., Xue J.-Y., Liu Y., Ané J.-M., Qiu Y.-L., (2010). Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol. 186 514–525. 10.1111/j.1469-8137.2009.03137.x 20059702.
111. Wang E., Schornack S., Marsh J. F., Gobbato E., Schwessinger B., Eastmond P., (2012). A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22 2242–2246. 10.1016/j.cub.2012.09.043 23122843.
112. Waterhouse A. M., Procter J. B., Martin D. M. A., Clamp M., Barton G. J., (2009). Jalview version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 1189–1191. 10.1093/bioinformatics/btp033 19151095.
113. Wickett N. J., Mirarab S., Nguyen N., Warnow T., Carpenter E., Matasci N., (2014). Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl. Acad. Sci. U.S.A. 111 E4859–E4868. 10.1073/pnas.1323926111 25355905.
114. Wilhelmsson P. K. I., Muhlich C., Ullrich K. K., Rensing S. A., (2017). Comprehensive genome-wide classification reveals that many plant-specific transcription factors evolved in streptophyte algae. Genome Biol. Evol. 9 3384–3397. 10.1093/gbe/evx258 29216360.
115. Wurzbacher C. M., Bärlocher F., Grossart H. P., (2010). Fungi in lake ecosystems. Aquat. Microb. Ecol. 59 125–149. 10.3354/ame01385.
116. Xue L., Cui H., Buer B., Vijayakumar V., Delaux P. M., Junkermann S., (2015). Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiol. 167 854–871. 10.1104/pp.114.255430 25560877.
117. Yu N., Luo D., Zhang X., Liu J., Wang W., Jin Y., (2014). A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res. 24 130–133. 10.1038/cr.2013.167 24343576.
118. Zhang D., Iyer L. M., Aravind L., (2012). Bacterial GRAS domain proteins throw new light on gibberellic acid response mechanisms. Bioinformatics 28 2407–2411. 10.1093/bioinformatics/bts464 22829623.
119. Zhang Q., Blaylock L. A., Harrison M. J., (2010). Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22 1483–1497. 10.1105/tpc.110.074955 20453115.
120. Zhang X., Dong W., Sun J., Feng F., Deng Y., He Z., (2015). The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J. 81 258–267. 10.1111/tpj.12723 25399831.