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. 2011 Feb;155(2):974-87.
doi: 10.1104/pp.110.164640. Epub 2010 Nov 30.

Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis

Wouter Kohlen  1 , Tatsiana Charnikhova, Qing Liu, Ralph Bours, Malgorzata A Domagalska, Sebastien Beguerie, Francel Verstappen, Ottoline Leyser, Harro Bouwmeester, Carolien Ruyter-Spira
Affiliations

Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis

Wouter Kohlen et al. Plant Physiol. 2011 Feb.

Abstract

The biosynthesis of the recently identified novel class of plant hormones, strigolactones, is up-regulated upon phosphate deficiency in many plant species. It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates hyphal branching of arbuscular mycorrhizal fungi. In this work, we demonstrate that this induction is conserved in Arabidopsis (Arabidopsis thaliana), although Arabidopsis is not a host for arbuscular mycorrhizal fungi. We demonstrate that the increase in strigolactone production contributes to the changes in shoot architecture observed in response to phosphate deficiency. Using high-performance liquid chromatography, column chromatography, and multiple reaction monitoring-liquid chromatography-tandem mass spectrometry analysis, we identified two strigolactones (orobanchol and orobanchyl acetate) in Arabidopsis and have evidence of the presence of a third (5-deoxystrigol). We show that at least one of them (orobanchol) is strongly reduced in the putative strigolactone biosynthetic mutants more axillary growth1 (max1) and max4 but not in the signal transduction mutant max2. Orobanchol was also detected in xylem sap and up-regulated under phosphate deficiency, which is consistent with the idea that root-derived strigolactones are transported to the shoot, where they regulate branching. Moreover, two additional putative strigolactone-like compounds were detected in xylem sap, one of which was not detected in root exudates. Together, these results show that xylem-transported strigolactones contribute to the regulation of shoot architectural response to phosphate-limiting conditions.

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Figures

Figure 1.
Figure 1.
Germination of P. ramosa seeds induced by root exudates of Arabidopsis (Col-0). A, Effect of phosphate starvation on the germination stimulatory capacity of 20-fold-concentrated Arabidopsis root exudates. Bars represent the average of three independent biological replicates ± se. * Significant difference between limiting phosphate (–Pi) and sufficient phosphate (+Pi) treatment (P < 0.05). B, Effect of treatments, sufficient phosphate (+Pi), limiting phosphate (–Pi), and limiting phosphate plus fluridone (–Pi + fluridone), on the germination stimulatory capacity of HPLC fractions of Arabidopsis root exudates. Bars represent the average of five independent biological replicates ± se. * Significant difference between –Pi and +Pi treatment; • significant difference between –Pi + fluridone treatment and –Pi treatment (P < 0.05). The dashed line indicates the HPLC gradient of acetonitrile concentration, and arrowheads point to fractions in which strigolactone standards elute: 1, solanacol and 7-hydroxyorobanchyl acetate; 2, 2′-epiorobanchol, orobanchol, strigol, and sorgomol; 3, GR24; 4, orobanchyl acetate; 5, sorgolactone; 6, 5-deoxystrigol.
Figure 2.
Figure 2.
Germination of P. ramosa seeds induced by HPLC fractions 17 and 20 of Arabidopsis (Col-0, max1-1, max2-1, and max4-1) root exudates. Bars represent the average of three independent biological replicates ± se. * Significant difference from Col-0 (P < 0.05).
Figure 3.
Figure 3.
MRM-LC-MS/MS analysis of Arabidopsis root exudates of plants grown under phosphate starvation. A, Transitions 347 > 233, 347 > 205, and 347 > 96.8 for orobanchol. B, Transitions 389.2 > 233 and 389.2 > 347 for orobanchyl acetate. C, Full daughter ion scan MS/MS spectrum of orobanchol in Arabidopsis exudate and orobanchol standard. D, Full daughter ion scan MS/MS spectrum of orobanchyl acetate in Arabidopsis exudate and orobanchyl acetate standard.
Figure 4.
Figure 4.
Analysis of orobanchol content in Arabidopsis Col-0, max1-1, max2-1, and max4-1. A, Effect of treatments with sufficient phosphate (+Pi) and limiting phosphate (–Pi) on root extracts (mean value for orobanchol level in Col-0 +Pi root extract was set to 100%). Bars represent the average of three independent biological replicates. • Significant –Pi up-regulation within genotypes (P < 0.05); * significant difference compared with Col-0 +Pi (P < 0.05). B, Root exudate analysis of –Pi (mean value for orobanchol level in Col-0 –Pi [P < 0.05] root exudate was set to 100%). Bars represent the average of three independent biological replicates each consisting of about 800 plants ± se. * Significant difference compared with Col-0 (P < 0.05).
Figure 5.
Figure 5.
The effect of phosphate levels on Arabidopsis axillary shoot branching. Measurements were done 2 weeks after initiation of the treatments in 7-week-old plants grown under long-day conditions. Bars indicate average of 10 independent replicates ± se. A, Effect of phosphate starvation on the number of secondary rosette branches. * Significant difference of low-phosphate (10% Pi) from high-phosphate (100% Pi) treatment (P < 0.05). B, Col-0 grown under phosphate-sufficient conditions (left) and under low phosphate (right). C, max4-1 grown under phosphate-sufficient conditions (left) and under low phosphate (right). Arrowheads point to secondary rosette branches. [See online article for color version of this figure.]
Figure 6.
Figure 6.
Germination of P. ramosa seeds induced by xylem sap collected from Arabidopsis. A, Effect of several concentrations of xylem sap of Col-0, grown under sufficient phosphate (+Pi) and limiting phosphate (–Pi) levels, on germination of P. ramosa. Bars represent the average of three independent biological replicates ± se. * Significant difference of low-phosphate from high-phosphate treatment (P < 0.05). B, Effect of treatments with sufficient phosphate and limiting phosphate on germination stimulatory capacity of HPLC-fractioned xylem sap. Bars represent the average of three independent biological replicates ± se. * Significant difference of low-phosphate from high-phosphate treatment (P < 0.05). C, Germination induced by HPLC fractions 17 and 20 of Arabidopsis (Col-0 and max4-1) xylem sap. Bars represent the average of three independent biological replicates ± se. * Significant difference compared with Col-0 (P < 0.05). D, Germination induced by HPLC fraction 11 of Arabidopsis (Col-0, max1-1, max2-1, and max4-1) xylem sap. Bars represent the average of three independent biological replicates ± se. * Significant difference compared with Col-0 (P < 0.05).
Figure 7.
Figure 7.
A, MRM-LC-MS/MS analysis of Arabidopsis xylem sap (Col-0) showing transitions 347 > 233, 347 > 205, and 347 > 96.8 for orobanchol. B, MRM-LC-MS/MS analysis of tomato xylem sap (cv Craigella) showing transitions 347 > 233, 347 > 205, and 347 > 96.8 for orobanchol. C, Full daughter ion scan MS/MS spectrum of orobanchol in tomato xylem sap and orobanchyl acetate standard.
Figure 8.
Figure 8.
Analysis of orobanchol content of Arabidopsis Col-0 xylem sap. * Significant difference compared with sufficient phosphate conditions (+Pi; P < 0.05).
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