Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 44, 2017, Pages E9403-E9412

  Almario, Juliana ^a,b   Jeena, Ganga ^a   Wunder, Jörg ^b   Langen, Gregor ^a   Zuccaro, Alga ^a   Coupland, George ^a,b   Bucher, Marcel ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Brassicaceae; Fungal endophyte; Helotiales; Microbiome; Nutrient transfer

Indexed keywords

INTERNAL TRANSCRIBED SPACER 2; PHOSPHORUS;

AMPLICON; ARABIS; ARABIS ALPINA; ARTICLE; ENDOPHYTE; FUNGAL COMMUNITY; FUNGUS GROWTH; GENETIC VARIATION; GENOME ANALYSIS; HELOTIALES; MICROBIAL COLONIZATION; MYCOBIOME; NONHUMAN; PLANT FUNGUS INTERACTION; PLANT GROWTH; PLANT NUTRITION; PLANT ROOT; PRIORITY JOURNAL; RHIZOSPHERE FUNGUS; SHOOT; SYMBIOSIS; METABOLISM; MICROBIOLOGY; MICROFLORA; MYCORRHIZA; PHYSIOLOGY; RHIZOSPHERE; SOIL;

ARABIS; MICROBIOTA; MYCORRHIZAE; PHOSPHORUS; PLANT ROOTS; RHIZOSPHERE; SOIL; SYMBIOSIS;

EID: 85032621160     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1710455114     Document Type: Article

References (53)

1. Bulgarelli D, et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95.
2. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486.
3. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: Endophytes and microbiomes. Annu Rev Phytopathol 49:291–315.
4. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206.
5. Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI (2015) Symbiotic options for the conquest of land. Trends Ecol Evol 30:477–486.
6. Smith SE, Read DJ (2010) Mycorrhizal Symbiosis (Academic, London).
7. Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26.
8. Delaux P-M, et al. (2014) Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 10:e1004487.
9. Lambers H, et al. (2015) Phosphorus nutrition in Proteaceae and beyond. Nat Plants 1: 15109.
10. van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytol 205:1406–1423.
11. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996.
12. Hiruma K, et al. (2016) Root endophyte colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–474.
13. Bakshi M, et al. (2015) WRKY6 restricts Piriformospora indica-stimulated and phosphate-induced root development in Arabidopsis. BMC Plant Biol 15:305.
14. Yadav V, et al. (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544.
15. Lundberg DS, et al. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90.
16. Dombrowski N, et al. (2017) Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME J 11: 43–55.
17. Wagner MR, et al. (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151.
18. Shakya M, et al. (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8: e76382.
19. de Souza RSC, et al. (2016) Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci Rep 6:28774.
20. Coleman-Derr D, et al. (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811.
21. Kohler A, et al.; Mycorrhizal Genomics Initiative Consortium (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415.
22. Peter M, et al. (2016) Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nat Commun 7:12662.
23. Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/ mutualism continuum in Arabidopsis. Curr Opin Microbiol 32:103–112.
24. Toräng P, et al. (2015) Large-scale adaptive differentiation in the alpine perennial herb Arabis alpina. New Phytol 206:459–470.
25. Willing E-M, et al. (2015) Genome expansion of Arabis alpina linked with retro-transposition and reduced symmetric DNA methylation. Nat Plants 1:14023.
26. Edwards J, et al. (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920.
27. Peiffer JA, et al. (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553.
28. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797.
29. Guindon S, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.
30. Glynou K, et al. (2016) The local environment determines the assembly of root endophytic fungi at a continental scale. Environ Microbiol 18:2418–2434.
31. Larsen J, Thingstrup I, Jakobsen I, Rosendahl S (1996) Benomyl inhibits phosphorus transport but not fungal alkaline phosphatase activity in a Glomus–cucumber symbiosis. New Phytol 132:127–133.
32. Persson BL, et al. (1998) Phosphate permeases of Saccharomyces cerevisiae. Biochim Biophys Acta 1365:23–30.
33. Tedersoo L, et al. (2014) Fungal biogeography. Global diversity and geography of soil fungi. Science 346:1256688.
34. Talbot JM, et al. (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci USA 111:6341–6346.
35. Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14:434–447.
36. Peay KG, Bidartondo MI, Arnold AE (2010) Not every fungus is everywhere: Scaling to the biogeography of fungal-plant interactions across roots, shoots and ecosystems. New Phytol 185:878–882.
37. Willmann M, et al. (2013) Mycorrhizal phosphate uptake pathway in maize: Vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Front Plant Sci 4:533.
38. Alcázar R, Parker JE (2011) The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 16:666–675.
39. Toju H, Tanabe AS, Ishii HS (2016) Ericaceous plant-fungus network in a harsh alpine-subalpine environment. Mol Ecol 25:3242–3257.
40. Tedersoo L, et al. (2009) Ascomycetes associated with ectomycorrhizas: Molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 11:3166–3178.
41. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20.
42. Bougoure J, et al. (2014) High-resolution secondary ion mass spectrometry analysis of carbon dynamics in mycorrhizas formed by an obligately myco-heterotrophic orchid: Rhizanthella nanoSIMS analysis. Plant Cell Environ 37:1223–1230.
43. Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184.
44. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577.
45. Lahrmann U, et al. (2015) Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity. New Phytol 207:841–857.
46. Kubicek CP, Starr TL, Glass NL (2014) Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annu Rev Phytopathol 52:427–451.
47. Hacquard S, et al. (2016) Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat Commun 7:13072.
48. Schloss PD, et al. (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.
49. Oksanen J, Blanchet G, Kindt R (2016) Vegan: Community Ecology Package. Available at cran.r-project.org/package=vegan.
50. Dray S, Dufour A-B (2007) The ade4 package: Implementing the duality diagram for ecologists. J Stat Softw 22:1–20.
51. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 362:319–334.
52. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552.
53. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224.