Abstract
Brachypodium distachyon is a grass species that serves as a useful model for wheat and also for many of the grass species proposed as feedstocks for bioenergy production. Here, we monitored B. distachyon symbioses with five different arbuscular mycorrhizal (AM) fungi and identified symbioses that vary functionally with respect to plant performance. Three symbioses promoted significant increases in shoot phosphorus (P) content and shoot growth of Brachypodium, while two associations were neutral. The Brachypodium/Glomus candidum symbiosis showed a classic ‘Paris-type’ morphology. In the other four AM symbioses, hyphal growth was exclusively intracellular and linear; hyphal coils were not observed and arbuscules were abundant. Expression of the Brachypodium ortholog of the symbiosis-specific phosphate (Pi) transporter MtPT4 did not differ significantly in these five interactions indicating that the lack of apparent functionality did not result from a failure to express this gene or several other AM symbiosis-associated genes. Analysis of the expression patterns of the complete PHT1 Pi transporter gene family and AMT2 gene family in B. distachyon/G. intraradices mycorrhizal roots identified additional family members induced during symbiosis and again, transcript levels were similar in the different Brachypodium AM symbioses. This initial morphological, molecular and functional characterization provides a framework for future studies of functional diversity in AM symbiosis in B. distachyon.
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References
Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931
Alves SC, Worland B, Thole V, Snape JW, Bevan MW, Vain P (2009) A protocol for Agrobacterium-mediated transformation of Brachypodium distachyon community standard line Bd21. Nat Protoc 4:638–649
Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Meth Enzymol 8:115–118
Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from 2N-15-labeled sources by Glomus mosseae, a vesicular arbuscular mycorrhizal fungus. New Phytol 95:381–396
Antonsen H, Olsson PA (2005) Relative importance of burning, mowing and species translocation in the restoration of a former boreal hayfield: responses of plant diversity and the microbial community. J Appl Ecol 42:337–347
Berbee ML, Taylor JW (2000) In: Mclaughlin JW, Mclaughlin EG, Lemke PA (eds) The mycota, fungal molecular evolution: gene trees and geologic time. Springer-Verlag, NY, pp 229–246
Bevan MW, Garvin DF, Vogel JP (2010) Brachypodium distachyon genomics for sustainable food and fuel production. Curr Opin Biotechnol 21:211–217
Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84:71–82
Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21
Blancaflor EB, Zhao LM, Harrison MJ (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217:154–165
Bookout A, Mangelsdorf D (2003) Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl Recept Signal 1:e012
Bouton JH (2007) Molecular breeding of switchgrass for use as a biofuel crop. Curr Opin Genet Dev 17:553–558
Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2011) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017
Brkljacic J, Grotewold E, Scholl R, Mockler T, Garvin DF, Vain P, Brutnell T, Sibout R, Bevan M, Budak H, Caicedo AL, Gao C, Gu Y, Hazen SP, Holt BF III, Hong S-Y, Jordan M, Manzaneda AJ, Mitchell-Olds T, Mochida K, Mur LAJ, Park C-M, Sedbrook J, Watt M, Zheng SJ, Vogel JP (2011) Brachypodium as a model for the grasses: today and the future. Plant Physiol 157:3–13
Brundrett M, Kendrick B (1990) The roots and mycorrhizas of herbaceous woodland plants. 1. Structural aspects of morphology. New Phytol 114:469–479
Burleigh SH, Cavagnaro T, Jakobsen I (2002) Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53:1593–1601
Chen C, Gao M, Liu J, Zhu H (2007) Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/Calmodulin-dependent protein kinase. Plant Physiol 145:1619–1628
Chen CY, Ane JM, Zhu HY (2008) OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol 180:311–315
Christiansen P, Andersen CH, Didion T, Folling M, Nielsen KK (2005) A rapid and efficient transformation protocol for the grass Brachypodium distachyon. Plant Cell Rep 23:751–758
Clark RB, Zobel RW, Zeto SK (1999) Effects of mycorrhizal fungus isolates on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176
Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loucao MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792
Dickson S (2004) The Arum–Paris continuum of mycorrhizal symbioses. New Phytol 163:187–200
Dickson S, Smith FA, Smith SE (2007) Structural differences in arbuscular mycorrhizal symbioses: more than 100 years after Gallaud, where next? Mycorrhiza 17:375–393
Draper J, Mur LAJ, Jenkins G, Ghosh-Biswas GC, Bablak P, Hasterok R, Routledge APM (2001) Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol 127:1539–1555
Furrazola E, Herrera-Peraza R, Kaonongbua W, Bever JD (2010) Glomus candidum, a new species of arbuscular mycorrhizal fungi from North American grassland. Mycotaxon 113:101–109
Gallaud I (1905) Etudes sur les mycorrhizes endotrophes. Révue Generale de Botanique 17:5–48
Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2011) Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69:510–528
Gehrig A, Schüßler A, Kluge M (1996) Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (Cyanobacteria) is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43:71–81
Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698
Glassop D, Godwin RM, Smith SE, Smith FW (2007) Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Canadian Journal of Botany-Revue Canadienne De Botanique 85:644–651
Gomez SK, Javot H, Deewatthanawong P, Torrez-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9:1–19
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194
Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823
Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83
Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102:8066–8070
Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005
Gutjahr C, Casieri L, Paszkowski U (2009) Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytol 182:829–837
Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, Casieri L, An K, An G, Guiderdoni E, Kumar CS, Sundaresan V, Harrison MJ, Paszkowski U (2011) The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J 69:906–920
Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant-Microbe Interact 6:643–654
Harrison MJ, Dewbre GR, 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
Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci USA 103:11206–11210
Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Kuster H (2011) Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 157:2023–2043
Jakobsen I, Smith SE, Smith FA (2002) Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. In: Sanders IR, Van der Heijden MGA (eds) Mycorrhizal ecology. Springer-Verlag, Berlin, pp 75–92
Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725
Javot H, Penmetsa RV, Breuillin FJ, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965
Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29
Kling M, Jakobsen I (1998) Arbuscular mycorrhiza in soil quality assessment. Ambio 27:29–34
Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415
Liu J, Blaylock L, Harrison MJ (2004) cDNA arrays as tools to identify mycorrhiza-regulated genes: identification of mycorrhiza-induced genes that encode or generate signaling molecules implicated in the control of root growth. Can J Bot 82:1177–1185
Liu J, Maldonado-Mendoza IE, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) The 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
Magdoff F (2001) Concept, components, and strategies of soil health in agroecosystems. J Nematol 33:169–172
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method that gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501
Mur LAJ, Allainguillaume J, Catalan P, Hasterok R, Jenkins G, Lesniewska K, Thomas I, Vogel J (2011) Exploiting the Brachypodium Tool Box in cereal and grass research. New Phytol 191:334–347
Murakoshi T, Motoaki T, Walker C, Saito M (1998) Arbuscular mycorrhizal fungi on adjacent semi-natural grasslands with different vegetation in Japan. Myoscience 39:455–462
Nagy R, Vasconcelos MJV, Zhao S, McElver J, Bruce W, Amrhein N, Raghothama KG, Bucher M (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol 8:186–197
Newsham KK, Fitter AH, Watterson AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000
Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329
Paszkowski U, Jakovleva L, Boller T (2006) Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant J 47:165–173
Rae AL, Cybinski DH, Jarmey JM, Smith FW (2003) Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Mol Biol 53:27–36
Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA (2006) Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia 147:348–358
Rillig MC, Wright SF, Eviner VT (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Saito M, Oba H, Kojima T (2011) Effect of nitrogen on the sporulation of arbuscular mycorrhizal fungi colonizing several gramineous plant species. Soil Sci Plant Nutr 57:29–34
Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97
Schroeder P, Herzig R, Bojinov B, Ruttens A, Nehnevajova E, Stamatiadis S, Memon A, Vassilev A, Caviezel M, Vangronsveld J (2008) Bioenergy to save the world: producing novel energy plants for growth on abandoned land. Environ Sci Pollut Res 15:196–204
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1414–1421
Smith FA, Smith SE (1997) Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137:373–388
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20
Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524
St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332
Stewart JR, Toma Y, Fernandez FG, Nishiwaki A, Yamada T, Bollero G (2009) The ecology and agronomy of Miscanthus sinensis, a species important to bioenergy crop development, in its native range in Japan: a review. Glob Change Biol Bioenerg 1:126–153
Thole V, Peraldi A, Worland B, Nicholson P, Doonan JH, Vain P (2011) T-DNA mutagenesis in Brachypodium distachyon. J Exp Bot 63:567–576
Tilman D, Hill J, Lehman C (2006) Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314:1598–1600
Vain P (2011) Brachypodium as a model system for grass research. J Cereal Sci 54:1–7
van der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett 7:293–303
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occuring plant. New Phytol 157:569–578
van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752
Vogel J, Hill T (2008) High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep 27:471–478
Vogel JP, Garvin DF, Mockler TC, Schmutz J, Rokhsar D, Bevan MW, Barry K, Lucas S, Harmon-Smith M, Lail K, Tice H, Grimwood J, McKenzie N, Huo NX, Gu YQ, Lazo GR, Anderson OD, You FM, Luo MC, Dvorak J, Wright J, Febrer M, Idziak D, Hasterok R, Lindquist E, Wang M, Fox SE, Priest HD, Filichkin SA, Givan SA, Bryant DW, Chang JH, Wu HY, Wu W, Hsia AP, Schnable PS, Kalyanaraman A, Barbazuk B, Michael TP, Hazen SP, Bragg JN, Laudencia-Chingcuanco D, Weng YQ, Haberer G, Spannagl M, Mayer K, Rattei T, Mitros T, Lee SJ, Rose JKC, Mueller LA, York TL, Wicker T, Buchmann JP, Tanskanen J, Schulman AH, Gundlach H, de Oliveira AC, Maia LD, Belknap W, Jiang N, Lai JS, Zhu LC, Ma JX, Sun C, Pritham E, Salse J, Murat F, Abrouk M, Bruggmann R, Messing J, Fahlgren N, Sullivan CM, Carrington JC, Chapman EJ, May GD, Zhai JX, Ganssmann M, Gurazada SGR, German M, Meyers BC, Green PJ, Tyler L, Wu JJ, Thomson J, Chen S, Scheller HV, Harholt J, Ulvskov P, Kimbrel JA, Bartley LE, Cao PJ, Jung KH, Sharma MK, Vega-Sanchez M, Ronald P, Dardick CD, De Bodt S, Verelst W, Inze D, Heese M, Schnittger A, Yang XH, Kalluri UC, Tuskan GA, Hua ZH, Vierstra RD, Cui Y, Ouyang SH, Sun QX, Liu ZY, Yilmaz A, Grotewold E, Sibout R, Hematy K, Mouille G, Hofte H, Pelloux J, O’Connor D, Schnable J, Rowe S, Harmon F, Cass CL, Sedbrook JC, Byrne ME, Walsh S, Higgins J, Li PH, Brutnell T, Unver T, Budak H, Belcram H, Charles M, Chalhoub B, Baxter I, Int Brachypodium I (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768
Wilson GWT, Hartnett DC (1997) Effects of mycorrhizae on plant growth and dynamics in experimental tallgrass prairie microcosms. Am J Bot 84:478–482
Wilson GWT, Hartnett DC, Smith MD, Kobbeman K (2001) Effects of mycorrhizae on growth and demography of tallgrass prairie forbs. Am J Bot 88:1452–1457
Zhang Q, Blaylock LA, Harrison MJ (2010) Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22:1483–1497
Acknowledgments
Financial support was provided by the Office of Science (BER), U.S Dept. of Energy, Grant No. DE FG02-08ER64628. The authors thank Dr. J. Bever for the generous gift of G. candidum and Gi. decipiens inocula and North Carolina field soil.
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Hong, J.J., Park, YS., Bravo, A. et al. Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon . Planta 236, 851–865 (2012). https://doi.org/10.1007/s00425-012-1677-z
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DOI: https://doi.org/10.1007/s00425-012-1677-z