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. 2010 Jul;51(7):1118-26.
doi: 10.1093/pcp/pcq084. Epub 2010 Jun 11.

Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice

Mikihisa Umehara  1 , Atsushi Hanada, Hiroshi Magome, Noriko Takeda-Kamiya, Shinjiro Yamaguchi
Affiliations

Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice

Mikihisa Umehara et al. Plant Cell Physiol. 2010 Jul.

Abstract

Strigolactones (SLs) or SL-derived metabolite(s) have recently been shown to act as endogenous inhibitors of axillary bud outgrowth. SLs released from roots induce hyphal branching of arbuscular mycorrhizal (AM) fungi that facilitate the uptake of inorganic nutrients, such as phosphate (Pi) and nitrate, by the host plants. Previous studies have shown that SL levels in root exudates are highly elevated by Pi starvation, which might contribute to successful symbiosis with AM fungi in the rhizosphere. However, how endogenous SL levels elevated by Pi starvation contribute to its hormonal action has been unknown. Here, we show that tiller bud outgrowth in wild-type rice seedlings is inhibited, while root 2'-epi-5-deoxystrigol (epi-5DS) levels are elevated, in response to decreasing Pi concentrations in the media. However, the suppression of tiller bud outgrowth under Pi deficiency does not occur in the SL-deficient and -insensitive mutants. We also show that the responsiveness to exogenous SL is slightly increased by Pi deficiency. When Pi-starved seedlings are transferred to Pi-sufficient media, tiller bud outgrowth is induced following a decrease in root epi-5DS levels. Taken together, these results suggest that elevated SL levels by Pi starvation contribute to the inhibition of tiller bud outgrowth in rice seedlings. We speculate that SL plays a dual role in the adaptation to Pi deficiency; one as a rhizosphere signal to maximize AM fungi symbiosis for improved Pi acquisition and the other as an endogenous hormone or its biosynthetic precursor to optimize shoot branching for efficient Pi utilization.

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Figures

Fig. 1
Fig. 1
The SL-dependent branching inhibition pathway in rice. D17/HTD1, D10 and D27 participate in SL synthesis. The role of CYP711A in rice has not been shown, but Arabidopsis CYP711A1/MAX1 has been shown to act downstream of CCDs. D27 is localized to the plastid, but its relative position in the pathway has not been clear. D3 and D14/D88/HTD2 act in a step downstream of SL synthesis. CCD, carotenoid cleavage dioxygenase.
Fig. 2
Fig. 2
Effect of Pi on tiller bud outgrowth and SL levels. (A) Schematic diagram showing the experimental conditions. Seven-day-old seedlings grown on agar media were transferred to hydroponic culture media containing various concentrations of Pi. (B) Twenty-one-day-old WT and d mutant seedlings grown with or without 600 μM Pi. Red, orange and yellow arrowheads indicate tillers that grew out from the first, second and third leaf, respectively. The scale bar is 5 cm. (C) Number of outgrowing tillers (>2 mm) per plant in six seedlings. (D) SL levels in root exudates and roots. n.d., not detected due to low abundance. Asterisk (*), detected, but could not be quantified reliably due to low abundance. Data are the means ± SD (n = 3) for C and D. (E) Correlation analysis between SL levels and the number of outgrowing tillers in the WT. Solid line with filled circles, SL levels in roots (pg g−1 FW); dashed line with open circles, SL levels in root exudates (pg ml−1).
Fig. 3
Fig. 3
Effect of Pi on SL responsiveness. d10-1 mutant seedlings were grown hydroponically with or without Pi as described in Fig. 2A in the presence of different concentrations of GR24. GR24 was included in the media during the hydroponic culture. Number of outgrowing tillers (>2 mm) per plant in six seedlings is shown. Data are the means ± SD (n = 3). The number of outgrowing tillers was decreased in −Pi relative to +Pi in the following tiller buds: second leaf tiller at 10 μM GR24 (P = 0.057); third leaf tiller at 1 μM GR24 (P = 0.11).
Fig. 4
Fig. 4
Effect of temporal Pi depletion on tiller bud outgrowth and SL levels. (A) Schematic diagram showing the experimental conditions. Brown and orange bars indicate a hydroponic culture with and without Pi, respectively. (B) Number of outgrowing tillers (>2 mm) per plant in six 21-day-old WT seedlings. The tiller bud on the first leaf did not grow out in all samples (not shown). (C) SL levels in root exudates. Data are the means ± SD (n = 3) for B and C.
Fig. 5
Fig. 5
Time course analysis of tiller outgrowth, SL levels and expression of SL biosynthesis genes after Pi supply. (A) Schematic diagram showing the experimental conditions. Brown and orange bars indicate +Pi and −Pi conditions, respectively. Plants were transferred to a larger vial containing fresh medium on the 11th day to minimize the consumption of other nutrients in the −Pi medium. Plants were then transferred to the +Pi or −Pi media on the 14th day. (B) Tiller length of WT seedlings under +Pi and −Pi conditions. The tiller bud on the first leaf was <1 mm in size in all samples (not shown). Data are the means ± SD (n = 18). (C) epi-5DS levels in roots. Data are the means ± SD (n = 3). (D) Transcript levels of SL-related genes in roots and in the basal part (1.5 cm) of shoots (‘shoot’) of WT seedlings. RAP IDs (http://rapdb.dna.affrc.go.jp/) are given for MAX1 homologs. Data are the means ± SD (n = 3). n.d., not detected due to low abundance.
Fig. 6
Fig. 6
A model for the role of SL in the adaptation to Pi deficiency. Left: when Pi (and other nutrients) are sufficient, SL levels are low in roots and tiller outgrowth is not inhibited. Right: under low Pi conditions, SL levels in roots are highly elevated and they contribute to the inhibition of tiller bud outgrowth in shoots. Arrowheads highlight outgrowing tillers. Thick arrows depict an increase or a decrease in SL levels. Black arrows indicate the exudation of SL to the rhizosphere and the possible upward movement of SL or SL-derived signal to shoots. The T-bar denotes the inhibitory effect on tiller bud outgrowth. Although only root-derived SL is highlighted here, a contribution of SL synthesis in the shoot to this response cannot be ruled out.
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