Abstract
The association of arbuscular mycorrhizal (AM) fungi with plant roots is the oldest and ecologically most important symbiotic relationship between higher plants and microorganisms, yet the mechanism by which these fungi detect the presence of a plant host is poorly understood. Previous studies have shown that roots secrete a branching factor (BF) that strongly stimulates branching of hyphae during germination of the spores of AM fungi. In the BF of Lotus, a strigolactone was found to be the active molecule. Strigolactones are known as germination stimulants of the parasitic plants Striga and Orobanche. In this paper, we show that the BF of a monocotyledonous plant, Sorghum, also contains a strigolactone. Strigolactones strongly and rapidly stimulated cell proliferation of the AM fungus Gigaspora rosea at concentrations as low as 10(-13) M. This effect was not found with other sesquiterperne lactones known as germination stimulants of parasitic weeds. Within 1 h of treatment, the density of mitochondria in the fungal cells increased, and their shape and movement changed dramatically. Strigolactones stimulated spore germination of two other phylogenetically distant AM fungi, Glomus intraradices and Gl. claroideum. This was also associated with a rapid increase of mitochondrial density and respiration as shown with Gl. intraradices. We conclude that strigolactones are important rhizospheric plant signals involved in stimulating both the pre-symbiotic growth of AM fungi and the germination of parasitic plants.
MeSH Terms
Daucus carota/chemistry
Fungi/growth & development
Germination
Hyphae/drug effects,growth & development
Lactones/analysis,pharmacology
Mitochondria/drug effects,metabolism
Mycorrhizae/drug effects,growth & development,metabolism
Orobanchaceae/growth & development
Plant Roots/chemistry
Seeds/growth & development
Sesquiterpenes/analysis,pharmacology
Sorghum/chemistry
Spores, Fungal/physiology
Chemicals
Lactones
Sesquiterpenes
sorgolactone
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Besserer Arnaud
UMR 5546, Pôle de Biotechnologies Végétales, Castanet-Tolosan, France.
Puech-Pagès Virginie
Kiefer Patrick
Gomez-Roldan Victoria
Jauneau Alain
Roy Sébastien
Portais Jean-Charles
Roux Christophe
Bécard Guillaume
Séjalon-Delmas Nathalie
References (22)
22 references, click to expand
-
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
-
Control of mitochondrial shape.
Curr Opin Cell Biol. 2005 Aug;17(4):384-8
PMID: 15975781
-
The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway.
Plant Physiol. 2005 Oct;139(2):920-34
PMID: 16183851
-
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
-
Effects of heat shock on the functional morphology of cell organelles observed by video-enhanced microscopy.
Anat Rec. 1999 Aug 1;255(4):458-64
PMID: 10409818
-
Germination of Witchweed (Striga lutea Lour.): Isolation and Properties of a Potent Stimulant.
Science. 1966 Dec 2;154(3753):1189-90
PMID: 17780042
-
Confirmation and quantification of strigolactones, germination stimulants for root parasitic plants Striga and Orobanche, produced by cotton.
Biosci Biotechnol Biochem. 2005 Jan;69(1):98-102
PMID: 15665473
-
GC-MS analysis of hydrophobic root exudates of sorghum and implications on the parasitic plant Striga asiatica.
J Agric Food Chem. 2001 Nov;49(11):5537-42
PMID: 11714356
-
Root exudation and rhizosphere biology.
Plant Physiol. 2003 May;132(1):44-51
PMID: 12746510
-
Fungal Growth Stimulation by CO(2) and Root Exudates in Vesicular-Arbuscular Mycorrhizal Symbiosis.
Appl Environ Microbiol. 1989 Sep;55(9):2320-5
PMID: 16348012
-
Molecular genetics of the arbuscular mycorrhizal symbiosis.
Curr Opin Plant Biol. 2004 Aug;7(4):414-21
PMID: 15231264
-
Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea.
Plant Physiol. 2003 Mar;131(3):1468-78
PMID: 12644696
-
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
-
Analysis of strigolactones, germination stimulants for striga and orobanche, by high-performance liquid chromatography/tandem mass spectrometry.
J Agric Food Chem. 2003 Feb 26;51(5):1162-8
PMID: 12590450
-
Plant-fungal associations: cue for the branching connection.
Nature. 2005 Jun 9;435(7043):750-1
PMID: 15944687
-
Signalling in arbuscular mycorrhiza: facts and hypotheses.
Adv Exp Med Biol. 2002;505:23-39
PMID: 12083464
-
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
-
Mediation of pathogen resistance by exudation of antimicrobials from roots.
Nature. 2005 Mar 10;434(7030):217-21
PMID: 15759001
-
How plants communicate using the underground information superhighway.
Trends Plant Sci. 2004 Jan;9(1):26-32
PMID: 14729216
-
Merging mitochondria matters: cellular role and molecular machinery of mitochondrial fusion.
EMBO Rep. 2002 Jun;3(6):527-31
PMID: 12052774
-
Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.
Nature. 2005 Jun 9;435(7043):824-7
PMID: 15944706
-
Secondary metabolite signalling in host-parasitic plant interactions.
Curr Opin Plant Biol. 2003 Aug;6(4):358-64
PMID: 12873531