Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes

Frontiers in Plant Science

Volumn 6, Issue September, 2015, Pages

  Banhara, Aline ^a   Ding, Yi ^b,c   Kühner, Regina ^a   Zuccaro, Alga ^b,d   Parniske, Martin ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c Boyce Thompson Institute for Plant Research   (United States)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Arabidopsis thaliana; Biotrophy; Common symbiosis genes; Growth promotion; Intracellular colonization; Lotus japonicus; Piriformospora indica

Indexed keywords

EID: 84942896155     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00667     Document Type: Article

References (83)

1. Alber, F., Dokudovskaya, S., Veenhoff, L. M., Zhang, W., Kipper, J., Devos, D., et al. (2007). The molecular architecture of the nuclear pore complex. Nature 450, 695-701. doi: 10.1038/nature06405
2. Ané, J. M., Kiss, G. B., Riely, B. K., Penmetsa, R. V., Oldroyd, G. E., Ayax, C., et al. (2004). Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364-1367. doi: 10.1126/science.1092986
3. Antolín-Llovera, M., Ried, M. K., and Parniske, M. (2014). Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE ectodomain promotes complex formation with Nod factor receptor 5. Curr. Biol. 24, 422-427. doi: 10.1016/j.cub.2013.12.053
4. Basiewicz, M., Weiss, M., Kogel, K. H., Langen, G., Zorn, H., and Zuccaro, A. (2012). Molecular and phenotypic characterization of Sebacina vermifera strains associated with orchids, and the description of Piriformospora williamsii sp. nov. Fungal Biol. 116, 204-213. doi: 10.1016/j.funbio.2011.11.003
5. Binder, A., and Parniske, M. (2013). Analysis of the Lotus japonicus nuclear pore NUP107-160 subcomplex reveals pronounced structural plasticity and functional redundancy. Front. Plant Sci. 4:552. doi: 10.3389/fpls.2013.00552
6. Bonfante, P., and Genre, A. (2010). Mechanisms underlying beneficial plantfungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48. doi: 10.1038/ncomms1046
7. Burow, M., Halkier, B. A., and Kliebenstein, D. J. (2010). Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness. Curr. Opin. Plant Biol. 13, 348-353. doi: 10.1016/j.pbi.2010.02.002
8. Butehorn, B., Rhody, D., and Franken, P. (2000). Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1 alpha of the root endophyte Piriformospora indica. Plant Biol. 2, 687-692. doi: 10.1055/s-2000-16647
9. Camehl, I., Drzewiecki, C., Vadassery, J., Shahollari, B., Sherameti, I., Forzani, C., et al. (2011). The OXI1 kinase pathway mediates Piriformospora indicainduced growth promotion in Arabidopsis. PLoS Pathog. 7:e1002051. doi: 10.1371/journal.ppat.1002051
10. Camehl, I., Sherameti, I., Venus, Y., Bethke, G., Varma, A., Lee, J., et al. (2010). Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol. 185, 1062-1073. doi: 10.1111/j.1469-8137.2009.03149.x
11. Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E., and 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. doi: 10.1105/tpc.108.063255
12. Das, J., Ramesh, K. V., Maithri, U., Mutangana, D., and Suresh, C. K. (2014). Response of aerobic rice to Piriformospora indica. Indian J. Exp. Biol. 52, 237-251.
13. de Castro, E., Sigrist, C. J., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P. S., Gasteiger, E., et al. (2006). ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362-W365. doi: 10.1093/nar/gkl124
14. Delaux, P. M., Séjalon-Delmas, N., Bécard, G., and Ané, J. M. (2013). Evolution of the plant-microbe symbiotic ‘toolkit’. Trends Plant Sci. 18, 298-304. doi: 10.1016/j.tplants.2013.01.008
15. Delaux, P. M., Varala, K., Edger, P. P., Coruzzi, G. M., Pires, J. C., and Ané, J. M. (2014). Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet. 10:e1004487. doi: 10.1371/journal.pgen.1004487
16. De Mendiburu, F. (2010). Agricolae: Statistical Procedures for Agricultural Research. Thesis, National Engineering University (UNI), Lima-Peru.
17. Deshmukh, S., Hückelhoven, R., Schäfer, P., Imani, J., Sharma, M., Weiss, M., et al. (2006). The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Natl. Acad. Sci. U.S.A. 103, 18450-18457. doi: 10.1073/pnas.0605697103
18. Dörmann, P., Kim, H., Ott, T., Schulze-Lefert, P., Trujillo, M., Wewer, V., et al. (2014). Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytol. 204, 815-822. doi: 10.1111/nph.12978
19. Doyle, J. J., and Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 19, 11-15.
20. Esseling, J. J., Lhuissier, F. G., and Emons, A. M. (2004). A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16, 933-944. doi: 10.1105/tpc.019653
21. Evangelisti, E., Rey, T., and Schornack, S. (2014). Cross-interference of plant development and plant-microbe interactions. Curr. Opin. Plant Biol. 20C, 118-126. doi: 10.1016/j.pbi.2014.05.014
22. Fahraeus, G. (1957). The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16, 374-381. doi: 10.1099/00221287-16-2-374
23. Fendrych, M., van Hautegem, T., van Durme, M., Olvera-Carrillo, Y., Huysmans, M., Karimi, M., et al. (2014). Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr. Biol. 24, 931-940. doi: 10.1016/j.cub.2014.03.025
24. Genre, A., Ortu, G., Bertoldo, C., Martino, E., and Bonfante, P. (2009). Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol. 149, 1424-1434. doi: 10.1104/pp.108.132225
25. Gossmann, J. A., Markmann, K., Brachmann, A., Rose, L. E., and Parniske, M. (2012). Polymorphic infection and organogenesis patterns induced by a Rhizobium leguminosarum isolate from Lotus root nodules are determined by the host genotype. New Phytol. 196, 561-573. doi: 10.1111/j.1469-8137.2012.04281.x
26. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., et al. (2010). A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38, W695-W699. doi: 10.1093/nar/gkq313
27. Groth, M., Takeda, N., Perry, J., Uchida, H., Dräxl, S., Brachmann, A., et al. (2010). NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509-2526. doi: 10.1105/tpc.109.069807
28. Gutjahr, C. (2014). Phytohormone signaling in arbuscular mycorhiza development. Curr. Opin. Plant Biol. 20C, 26-34. doi: 10.1016/j.pbi.2014.04.003
29. Gutjahr, C., and Parniske, M. (2013). Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 29, 593-617. doi: 10.1146/annurev-cellbio-101512-122413
30. Hilbert, M., Voll, L. M., Ding, Y., Hofmann, J., Sharma, M., and Zuccaro, A. (2012). Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol. 196, 520-534. doi: 10.1111/j.1469-8137.2012.04275.x
31. Hoagland, D. R., and Arnon, D. I. (1950). The Water-culture Method for Growing Plants without Soil. Berkeley, CA: University of California.
32. Hok, S., Danchin, E. G., Allasia, V., Panabières, F., Attard, A., and Keller, H. (2011). An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease. Plant Cell Environ. 34, 1944-1957. doi: 10.1111/j.1365-3040.2011.02390.x
33. Jacobs, S., Zechmann, B., Molitor, A., Trujillo, M., Petutschnig, E., Lipka, V., et al. (2011). Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol. 156, 726-740. doi: 10.1104/pp.111.176446
34. Jones, P., Binns, D., Chang, H. Y., Fraser, M., Li, W., McAnulla, C., et al. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236-1240. doi: 10.1093/bioinformatics/btu031
35. Kanamori, N., Madsen, L. H., Radutoiu, S., Frantescu, M., Quistgaard, E. M., Miwa, H., et al. (2006). A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 103, 359-364. doi: 10.1073/pnas.0508883103
36. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066. doi: 10.1093/nar/gkf436
37. Kevei, Z., Seres, A., Kereszt, A., Kalò, P., Kiss, P., Tóth, G., et al. (2005). Significant microsynteny with new evolutionary highlights is detected between Arabidopsis and legume model plants despite the lack of macrosynteny. Mol. Genet. Genomics 274, 644-657. doi: 10.1007/s00438-005-0057-9
38. Khatabi, B., Molitor, A., Lindermayr, C., Pfiffi, S., Durner, J., von Wettstein, D., et al. (2012). Ethylene supports colonization of plant roots by the mutualistic fungus Piriformospora indica. PLoS ONE 7:e35502. doi: 10.1371/journal.pone.0035502
39. Kistner, C., Winzer, T., Pitzschke, A., Mulder, L., Sato, S., Kaneko, T., et al. (2005). Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17, 2217-2229. doi: 10.1105/tpc.105.032714
40. Kumar, M., Yadav, V., Kumar, H., Sharma, R., Singh, A., Tuteja, N., et al. (2011). Piriformospora indica enhances plant growth by transferring phosphate. Plant Signal. Behav. 6, 723-725. doi: 10.4161/psb.6.5.15106
41. Lahrmann, U., Ding, Y., Banhara, A., Rath, M., Hajirezaei, M. R., Döhlemann, S., et al. (2013). Host-related metabolic cues affect colonization strategies of a root endophyte. Proc. Natl. Acad. Sci. U.S.A. 110, 13965-13970. doi: 10.1073/pnas.1301653110
42. Lahrmann, U., and Zuccaro, A. (2012). Opprimo ergo sum-evasion and suppression in the root endophytic fungus Piriformospora indica. Mol. Plant Microbe Interact. 25, 727-737. doi: 10.1094/MPMI-11-11-0291
43. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948. doi: 10.1093/bioinformatics/btm404
44. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
45. Maekawa, T., Maekawa-Yoshikawa, M., Takeda, N., Imaizumi-Anraku, H., Murooka, Y., and Hayashi, M. (2009). Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J. 58, 183-194. doi: 10.1111/j.1365-313X.2008.03774.x
46. Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., et al. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-63. doi: 10.1038/nature09622
47. Markmann, K., Giczey, G., and Parniske, M. (2008). Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol. 6:e68. doi: 10.1371/journal.pbio.0060068
48. Mikkelsen, M. D., Fuller, V. L., Hansen, B. G., Nafisi, M., Olsen, C. E., Nielsen, H. B., et al. (2009). Controlled indole-3-acetaldoxime production through ethanol-induced expression of CYP79B2. Planta 229, 1209-1217. doi: 10.1007/s00425-009-0907-5
49. Mukhopadhyay, S., and Jackson, P. K. (2011). The tubby family proteins. Genome Biol. 12:225. doi: 10.1186/gb-2011-12-6-225
50. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497. doi: 10.1111/j.1399-3054.1962.tb08052.x
51. Nongbri, P. L., Johnson, J. M., Sherameti, I., Glawischnig, E., Halkier, B. A., and Oelmüller, R. (2012). Indole-3-acetaldoxime-derived compounds restrict root colonization in the beneficial interaction between Arabidopsis roots and the endophyte Piriformospora indica. Mol. Plant Microbe Interact. 25, 1186-1197. doi: 10.1094/MPMI-03-12-0071-R
52. Oláh, B., Brière, C., Bécard, G., Dénarié, J., and Gough, C. (2005). Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J. 44, 195-207. doi: 10.1111/j.1365-313X.2005.02522.x
53. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775. doi: 10.1038/nrmicro1987
54. Peškan-Berghöfer, T., Shahollari, B., Giong, P. H., Hehl, S., Markert, C., Blanke, V., et al. (2004). Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol. Plant. 122, 465-477. doi: 10.1111/j.1399-3054.2004.00424.x
55. Pham, G., Kumari, R., Singh, A., Malla, R., Prasad, R., Sachdev, M., et al. (2004). "Axenic culture of symbiotic fungus Piriformospora indica," in Plant Surface Microbiology, eds A. Varma, L. Abbott, D. Werner and R. Hampp (Berlin Heidelberg: Springer), 593-613.
56. Qiang, X., Zechmann, B., Reitz, M. U., Kogel, K. H., and Schäfer, P. (2012). The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24, 794-809. doi: 10.1105/tpc.111.093260
57. Radutoiu, S., Madsen, L. H., Madsen, E. B., Felle, H. H., Umehara, Y., Grønlund, M., et al. (2003). Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592. doi: 10.1038/nature 02039
58. R Core Team. (2013). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
59. Reitz, M. U., Bissue, J. K., Zocher, K., Attard, A., Hückelhoven, R., Becker, K., et al. (2012). The subcellular localization of Tubby-like proteins and participation in stress signaling and root colonization by the mutualist Piriformospora indica. Plant Physiol. 160, 349-364. doi: 10.1104/pp.112.201319
60. Reitz, M. U., Pai, S., Imani, J., and Schäfer, P. (2013). New insights into the subcellular localization of Tubby-like proteins and their participation in the Arabidopsis-Piriformospora indica interaction. Plant Signal Behav. 8:e25198. doi: 10.4161/psb.25198
61. Rey, T., Chatterjee, A., Buttay, M., Toulotte, J., and Schornack, S. (2014). Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytol. 206, 497-500. doi: 10.1111/nph.13233
62. Ried, M. K., Antolin-Llovera, M., and Parniske, M. (2014). Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases. Elife 3:e03891. doi: 10.7554/elife.03891
63. Saito, K., Yoshikawa, M., Yano, K., Miwa, H., Uchida, H., Asamizu, E., et al. (2007). NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19, 610-624. doi: 10.1105/tpc.106.046938
64. Schäfer, P., Pfiffi, S., Voll, L. M., Zajic, D., Chandler, P. M., Waller, F., et al. (2009). Phytohormones in plant root-Piriformospora indica mutualism. Plant Signal. Behav. 4, 669-671. doi: 10.4161/psb.4.7.9038
65. Scholl, R. L., May, S. T., and Ware, D. H. (2000). Seed and molecular resources for Arabidopsis. Plant Physiol. 124, 1477-1480. doi: 10.1104/pp.124.4.1477
66. Schüßler, A., and Walker, C. (2011). "Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota," in Evolution of fungi and fungal-like organisms, eds. S. Pöggeler and J. Wöstemeyer (Berlin Heidelberg: Springer), 163-185.
67. Selosse, M. A., Dubois, M. P., and Alvarez, N. (2009). Do Sebacinales commonly associate with plant roots as endophytes? Mycol. Res. 113, 1062-1069. doi: 10.1016/j.mycres.2009.07.004
68. Shahollari, B., Vadassery, J., Varma, A., and Oelmüller, R. (2007). A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J. 50, 1-13. doi: 10.1111/j.1365-313X.2007.03028.x
69. Sherameti, I., Tripathi, S., Varma, A., and Oelmüller, R. (2008). The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol. Plant Microbe Interact. 21, 799-807. doi: 10.1094/MPMI-21-6-0799
70. Singh, S., Katzer, K., Lambert, J., Cerri, M., and Parniske, M. (2014). CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15, 139-152. doi: 10.1016/j.chom.2014.01.011
71. Singh, S., and Parniske, M. (2012). Activation of calcium-and calmodulindependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr. Opin. Plant Biol. 15, 444-453. doi: 10.1016/j.pbi.2012.04.002
72. Smith, S. E., and Read, D. J. (2008). Mycorrhizal Symbiosis. Amsterdam: Academic.
73. Svistoonoff, S., Hocher, V., and Gherbi, H. (2014). Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation? Curr. Opin. Plant Biol. 20, 11-18. doi: 10.1016/j.pbi.2014.03.001
74. Takeda, N., Maekawa, T., and Hayashi, M. (2012). Nuclear-localized and deregulated calcium-and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24, 810-822. doi: 10.1105/tpc.111.091827
75. Takeda, N., Sato, S., Asamizu, E., Tabata, S., and Parniske, M. (2009). Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus. Plant J. 58, 766-777. doi: 10.1111/j.1365-313X.2009.03824.x
76. Vadassery, J., Ritter, C., Venus, Y., Camehl, I., Varma, A., Shahollari, B., et al. (2008). The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol. Plant Microbe Interact. 21, 1371-1383. doi: 10.1094/MPMI-21-10-1371
77. Venkateshwaran, M., Cosme, A., Han, L., Banba, M., Satyshur, K. A., Schleiff, E., et al. (2012). The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24, 2528-2545. doi: 10.1105/tpc.112.098475
78. Venus, Y., and Oelmüller, R. (2013). Arabidopsis ROP1 and ROP6 influence germination time, root morphology, the formation of F-actin bundles, and symbiotic fungal interactions. Mol. Plant 6, 872-886. doi: 10.1093/mp/sss101
79. Verma, S., Varma, A., Rexer, K.-H., Hassel, A., Kost, G., Sarbhoy, A., et al. (1998). Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90, 896-903. doi: 10.2307/3761331
80. Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., et al. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. U.S.A. 102, 13386-13391. doi: 10.1073/pnas.0504423102
81. Webb, K. J., Skøt, L., Nicholson, M. N., Jørgensen, B., and Mizen, S. (2000). Mesorhizobium loti increases root-specific expression of a calcium-binding protein homologue identified by promoter tagging in Lotus japonicus. Mol. Plant Microbe Interact. 13, 606-616. doi: 10.1094/MPMI.2000.13.6.606
82. Wiermer, M., Cheng, Y. T., Imkampe, J., Li, M., Wang, D., Lipka, V., et al. (2012). Putative members of the Arabidopsis Nup107-160 nuclear pore sub-complex contribute to pathogen defense. Plant J. 70, 796-808. doi: 10.1111/j.1365-313X.2012.04928.x
83. Zuccaro, A., Lahrmann, U., Güldener, U., Langen, G., Pfiffi, S., Biedenkopf, D., et al. (2011). Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 7:e1002290. doi: 10.1371/journal.ppat.1002290