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, 51 (7), 1127-35

FINE CULM1 (FC1) Works Downstream of Strigolactones to Inhibit the Outgrowth of Axillary Buds in Rice

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FINE CULM1 (FC1) Works Downstream of Strigolactones to Inhibit the Outgrowth of Axillary Buds in Rice

Kosuke Minakuchi et al. Plant Cell Physiol.

Abstract

Recent studies of highly branched mutants of pea, Arabidopsis and rice have demonstrated that strigolactones (SLs) act as hormones that inhibit shoot branching. The identification of genes that work downstream of SLs is required for a better understanding of how SLs control the growth of axillary buds. We found that the increased tillering phenotype of fine culm1 (fc1) mutants of rice is not rescued by the application of 1 microM GR24, a synthetic SL analog. Treatment with a high concentration of GR24 (10 microM) causes suppression of tiller growth in wild-type plants, but is not effective on fc1 mutants, implying that proper FC1 functioning is required for SLs to inhibit bud growth. Overexpression of FC1 partially rescued d3-2 defects in the tiller growth and plant height. An in situ hybridization analysis showed that FC1 mRNA accumulates in axillary buds, the shoot apical meristem, young leaves, vascular tissues and the tips of crown roots. FC1 mRNA expression was not significantly affected by GR24, suggesting that transcriptional induction may not be the mechanism by which SLs affect FC1 functioning. On the other hand, the expression level of FC1 is negatively regulated by cytokinin treatment. We propose that FC1 acts as an integrator of multiple signaling pathways and is essential to the fine-tuning of shoot branching in rice.

Figures

Fig. 1
Fig. 1
Loss-of-function mutants of FC1, which encodes a TCP family transcription factor. (A) Phenotypes of 3-month-old wild-type (WT), fc1-2, d10-2 and d3-2 rice plants. The fc1-2 plant is shorter than the wild type and has an increased number of tillers. This phenotype is milder than that of d3-2, an SL-insensitive mutant. (B) Diagram of the FC1 protein showing the TCP domain and the locations of the fc1-1 and fc1-2 mutations. The fc1-1 allele was described previously (Takeda et al. 2003). The amino acids in the TCP domain are shown below the diagram. Red letters indicate amino acids that are altered in the mutant proteins. The red bar indicates a deletion and the red star represents a translation termination codon. The TCP and R domains are indicated as a blue and a pink box, respectively. The R domain is an 18–20 residue arginine-rich motif with unknown function. (C) Phylogenetic tree of TB1 from maize and the TCP proteins of rice, sorghum and Arabidopsis that are in the CYC/TB1 subclade. Amino acid sequences of the TCP domain were used for the analysis. (D) Feedback regulation of D10 expression. To evaluate precisely the degree of feedback regulation, D10 expression was examined by real-time PCR in d3-1, d10-1, d14-1, d17-1, T65 and fc1-1 plants. Expression levels are shown as relative values to that of wild-type Shiokari. S and T65 indicate Shiokari cultivar and Taichung 65 cultivar background, respectively.
Fig. 2
Fig. 2
fc1 mutants are insensitive to GR24. (A) Responses of d10-2 and fc1-2 plants to GR24 application. Two-week-old wild-type (WT) and mutant plants were treated with 1 μM GR24. In the absence of GR24 treatment, the tillers in the axils of the first (blue arrowhead) and second (red arrowhead) leaves did not grow in the wild-type plants but did grow in the mutants. The outgrowth of tillers in d10-2, but not in fc1-2, was suppressed by the application of GR24. Scale bars = 1 cm. (B) Tiller numbers of d10-2 and fc1-2 plants with and without GR24 treatment. The numbers of tillers showing outgrowth (>2 mm) in six seedlings are shown for wild-type Nipponbare [WT (N)] and mutant plants. The blue and red bars indicate the first and second leaf buds, respectively. Error bars represent the SD (n = 6). (C) LC-MS/MS analysis of endogenous levels of epi-5DS in WT (N) and fc1-2 mutants. Error bars represent the SD (n = 3). (D) LC-MS/MS analysis of epi-5DS levels in root exudates of WT (N) and fc1-2 mutants. Error bars represent the SD (n = 3).
Fig. 3
Fig. 3
Interaction of FC1 function and the SL pathway. (A) Responses of fc1 mutant growth in a high concentration of GR24. Plants were grown in hydroponic culture with or without 10 μM GR24. The tiller lengths of the first to sixth leaves were measured 6 weeks after the initiation of the hydroponic culture. The sums of the average of tiller lengths of three plants are shown. The mutant fc1-1 was derived from wild-type (WT) Taichung (T), and fc1-2 and d3-2 were derived from Nipponbare (N). (B) Partial rescue of the d3-2 mutant phenotype by overexpression of FC1. Left, wild-type plant; centre, 35S-FC1/d3-2 plant; right, d3-2 plant. (C) Double mutant of fc1-2 d17-2.
Fig. 4
Fig. 4
Spatial distribution of FC1 mRNA. (A) A longitudinal section of a young rice plant. Axillary buds are shown inside red circles. Arrowhead: shoot apical meristem (SAM). (B) A close-up of the SAM in A. (C) An axillary meristem in the axil of the P5 leaf. (D) An axillary bud in the axil of the P7 leaf. FC1 expression is observed in the axillary bud and the leaf epidermis (arrow). (E) An axillary bud in the axil of the P6 leaf. (F) A horizontal section of a seedling at the level of the top of the SAM. FC1 signal is observed in young leaves of the axillary bud and the main shoot (arrowhead), and in the SAM (arrow). (G) A horizontal section of a seedling at the level of the node. FC1 signal is observed in the tips of the crown roots and the vascular bundles. (H) A close-up of an initiating crown root. Bars: 200 μm in A; 100 μm in B, H; 50 μm in C–E.
Fig. 5
Fig. 5
Hormonal control of FC1 expression. (A) Response of FC1 mRNA expression to treatment with 2 μM GR24. (B) Response of FC1promoter::GUS expression to treatment with 2 μM GR24. (C and D) Responses of OsIAA20 (C) and FC1 (D) mRNA expression to treatment with various concentrations of IAA. (E) Response of FC1 mRNA expression to treatment with various concentrations of benzyl aminopurine (BAP). (F and G) Responses of OsIPT2 (F) and OsIPT4 (G) mRNA expression to treatment with various concentrations of IAA. Expression levels are shown as values relative to that of mock treatment.
Fig. 6
Fig. 6
A model of the hormonal control of tiller bud outgrowth in rice. In this model, apically derived auxin negatively and positively regulates cytokinin (CK) and strigolactone (SL) biosynthesis, respectively. Subsequently, cytokinins negatively regulate expression of the TCP genes. The function of the TCP genes is positively controlled by SL at the level of mRNA accumulation in Arabidopsis, while the relationship between FC1 and SL remains unclear in rice. SL biosynthesis is under the control of feedback regulation. Solid lines show relationships that are confirmed in rice, while the dotted line represents a relationship that remains to be confirmed in rice.

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