Home LiteratureArticle Details
PMID: 21045005 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events.

Journal of experimental botany ·Vol. 62 ·No. 3 ·2011-01-00 ·Pages 1049-60

Balzergue C, Puech-Pagès V, Bécard G, Rochange SF

Abstract

Most plants form root symbioses with arbuscular mycorrhizal (AM) fungi, which provide them with phosphate and other nutrients. High soil phosphate levels are known to affect AM symbiosis negatively, but the underlying mechanisms are not understood. This report describes experimental conditions which triggered a novel mycorrhizal phenotype under high phosphate supply: the interaction between pea and two different AM fungi was almost completely abolished at a very early stage, prior to the formation of hyphopodia. As demonstrated by split-root experiments, down-regulation of AM symbiosis occurred at least partly in response to plant-derived signals. Early signalling events were examined with a focus on strigolactones, compounds which stimulate pre-symbiotic fungal growth and metabolism. Strigolactones were also recently identified as novel plant hormones contributing to the control of shoot branching. Root exudates of plants grown under high phosphate lost their ability to stimulate AM fungi and lacked strigolactones. In addition, a systemic down-regulation of strigolactone release by high phosphate supply was demonstrated using split-root systems. Nevertheless, supplementation with exogenous strigolactones failed to restore root colonization under high phosphate. This observation does not exclude a contribution of strigolactones to the regulation of AM symbiosis by phosphate, but indicates that they are not the only factor involved. Together, the results suggest the existence of additional early signals that may control the differentiation of hyphopodia.

MeSH Terms
Fungi/physiology Mycorrhizae/physiology Peas/microbiology,physiology Phosphates/metabolism Plant Roots/microbiology,physiology Signal Transduction Symbiosis
Chemicals
Phosphates
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Balzergue Coline
Université de Toulouse, UPS, UMR 5546, Surfaces Cellulaires et Signalisation chez les Végétaux, BP 42617, F-31326 Castanet-Tolosan, France.
Puech-Pagès Virginie
Bécard Guillaume
Rochange Soizic F
References (52)
52 references, click to expand
  1. Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae.
    Plant J. 2001 Sep;27(6):561-9 PMID: 11576439
  2. Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis.
    Plant J. 2010 Feb 1;61(3):482-94 PMID: 19912567
  3. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.
    Nature. 2005 Jun 9;435(7043):824-7 PMID: 15944706
  4. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi
    Appl Environ Microbiol. 1998 Dec;64(12):5004-7 PMID: 9835596
  5. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation.
    New Phytol. 2008;178(4):863-874 PMID: 18346111
  6. Separated components of root exudate and cytosol stimulate different morphologically identifiable types of branching responses by arbuscular mycorrhizal fungi.
    Mycol Res. 2007 Apr;111(Pt 4):487-92 PMID: 17544057
  7. Rhizosphere communication of plants, parasitic plants and AM fungi.
    Trends Plant Sci. 2007 May;12(5):224-30 PMID: 17416544
  8. Flavonoids released naturally from alfalfa promote development of symbiotic glomus spores in vitro.
    Appl Environ Microbiol. 1991 May;57(5):1485-8 PMID: 16348488
  9. Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots.
    Mol Plant Microbe Interact. 2002 Apr;15(4):334-40 PMID: 12026171
  10. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells.
    Mol Plant Microbe Interact. 2000 Oct;13(10):1109-20 PMID: 11043472
  11. Strigolactone inhibition of shoot branching.
    Nature. 2008 Sep 11;455(7210):189-94 PMID: 18690209
  12. A phosphate transporter expressed in arbuscule-containing cells in potato.
    Nature. 2001 Nov 22;414(6862):462-70 PMID: 11719809
  13. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria.
    PLoS Biol. 2006 Jul;4(7):e226 PMID: 16787107
  14. Fabacyl acetate, a germination stimulant for root parasitic plants from Pisum sativum.
    Phytochemistry. 2009 Jan;70(2):211-5 PMID: 19155028
  15. Can Fertilization of Soil Select Less Mutualistic Mycorrhizae?
    Ecol Appl. 1993 Nov;3(4):749-757 PMID: 27759303
  16. Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization.
    Mol Plant Microbe Interact. 2003 May;16(5):382-8 PMID: 12744508
  17. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula.
    Plant Physiol. 2003 Mar;131(3):952-62 PMID: 12644648
  18. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces.
    New Phytol. 2007;173(1):11-26 PMID: 17176390
  19. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells.
    Plant Physiol. 2007 Jun;144(2):673-81 PMID: 17142489
  20. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.
    Plant Physiol. 2003 Sep;133(1):16-20 PMID: 12970469
  21. Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots.
    New Phytol. 2009;183(1):53-61 PMID: 19555369
  22. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles.
    Plant Cell Environ. 2007 Mar;30(3):310-322 PMID: 17263776
  23. Inhibition of shoot branching by new terpenoid plant hormones.
    Nature. 2008 Sep 11;455(7210):195-200 PMID: 18690207
  24. Isolation and Identification of Vesicular-Arbuscular Mycorrhiza-Stimulatory Compounds from Clover (Trifolium repens) Roots.
    Appl Environ Microbiol. 1991 Feb;57(2):434-9 PMID: 16348409
  25. The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates.
    Mol Plant Microbe Interact. 2000 Jun;13(6):693-8 PMID: 10830269
  26. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites.
    Planta. 2007 Mar;225(4):1031-8 PMID: 17260144
  27. Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H+-ATPase genes from the mycorrhizal fungus Glomus mosseae.
    Plant Physiol. 2003 Jul;132(3):1540-9 PMID: 12857834
  28. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis.
    Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):13324-9 PMID: 12271140
  29. Hyphal Elongation of Glomus fasciculatus in Response to Root Exudates.
    Appl Environ Microbiol. 1987 Aug;53(8):1928-33 PMID: 16347418
  30. Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants.
    New Phytol. 2008 Jul;179(2):484-494 PMID: 19086293
  31. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites.
    Planta. 2007 Dec;227(1):125-32 PMID: 17684758
  32. Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis.
    Plant J. 2006 Jul;47(2):165-73 PMID: 16762030
  33. The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus.
    Can J Microbiol. 2007 Jun;53(6):702-9 PMID: 17668030
  34. Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots.
    Plant Cell Environ. 2008 Dec;31(12):1834-43 PMID: 18771575
  35. Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum.
    Physiol Plant. 2010 Feb;138(2):226-37 PMID: 20015123
  36. Regulatory network of microRNA399 and PHO2 by systemic signaling.
    Plant Physiol. 2008 Jun;147(2):732-46 PMID: 18390805
  37. 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. 2005 Oct;44(2):195-207 PMID: 16212600
  38. Arbuscular mycorrhiza: the mother of plant root endosymbioses.
    Nat Rev Microbiol. 2008 Oct;6(10):763-75 PMID: 18794914
  39. Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated.
    New Phytol. 2009 Mar;181(4):950-959 PMID: 19140941
  40. Membrane-mediated decrease in root exudation responsible for phorphorus inhibition of vesicular-arbuscular mycorrhiza formation.
    Plant Physiol. 1981 Sep;68(3):548-52 PMID: 16661955
  41. Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris.
    New Phytol. 1996 Feb;132(2):281-8 PMID: 11541132
  42. Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis.
    Mol Plant Microbe Interact. 2010 Jul;23(7):915-26 PMID: 20521954
  43. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi.
    Plant Cell. 2002 Oct;14(10):2413-29 PMID: 12368495
  44. Phosphate availability regulates root system architecture in Arabidopsis.
    Plant Physiol. 2001 Jun;126(2):875-82 PMID: 11402214
  45. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes.
    Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9823-8 PMID: 18606999
  46. GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism.
    Plant Physiol. 2008 Sep;148(1):402-13 PMID: 18614712
  47. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis.
    Plant J. 2008 Mar;53(5):731-8 PMID: 17988220
  48. Low phosphorus tolerance mechanisms: phosphorus recycling and photosynthate partitioning in the tropical forage grass, Brachiaria hybrid cultivar Mulato compared with rice.
    Plant Cell Physiol. 2004 Apr;45(4):460-9 PMID: 15111721
  49. Community-level consequences of mycorrhizae depend on phosphorus availability.
    Ecology. 2009 Sep;90(9):2567-76 PMID: 19769134
  50. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis.
    Plant Cell. 2010 May;22(5):1483-97 PMID: 20453115
  51. Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula.
    Mol Plant Microbe Interact. 2004 Dec;17(12):1385-93 PMID: 15597744
  52. Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice.
    Plant Cell Physiol. 2010 Jul;51(7):1118-26 PMID: 20542891
Article Info
Journal
Journal of experimental botany
Abbr.
J Exp Bot
ISSN
1460-2431
Published
2011-01-00
Epub
2010-00-02
Pages
1049-60
Language
English
Region
England
NLM ID
9882906
PMCID
PMC3022399
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com