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Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1.

Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang JL, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J - Nat Commun (2012)

Bottom Line: We demonstrate that TE encodes a rice homologue of Cdh1, and that TE acts as an activator of the anaphase promoting complex/cyclosome (APC/C) complex.We show that TE coexpresses with MOC1 in the axil of leaves, where the APC/C(TE) complex mediates the degradation of MOC1 by the ubiquitin-26S proteasome pathway, and consequently downregulates the expression of the meristem identity gene Oryza sativa homeobox 1, thus repressing axillary meristem initiation and formation.We conclude that besides having a conserved role in regulating cell cycle, APC/C(TE) has a unique function in regulating the plant-specific postembryonic shoot branching and tillering, which are major determinants of plant architecture and grain yield.

View Article: PubMed Central - PubMed

Affiliation: National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China.

ABSTRACT
Rice MONOCULM 1 (MOC1) and its orthologues LS/LAS (lateral suppressor in tomato and Arabidopsis) are key promoting factors of shoot branching and tillering in higher plants. However, the molecular mechanisms regulating MOC1/LS/LAS have remained elusive. Here we show that the rice tiller enhancer (te) mutant displays a drastically increased tiller number. We demonstrate that TE encodes a rice homologue of Cdh1, and that TE acts as an activator of the anaphase promoting complex/cyclosome (APC/C) complex. We show that TE coexpresses with MOC1 in the axil of leaves, where the APC/C(TE) complex mediates the degradation of MOC1 by the ubiquitin-26S proteasome pathway, and consequently downregulates the expression of the meristem identity gene Oryza sativa homeobox 1, thus repressing axillary meristem initiation and formation. We conclude that besides having a conserved role in regulating cell cycle, APC/C(TE) has a unique function in regulating the plant-specific postembryonic shoot branching and tillering, which are major determinants of plant architecture and grain yield.

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Conserved role of TE in cell-cycle regulation.(a) Growth of S. pombe transformed with the empty vector pREP1 and pREP1-TE in the presence (+thiamine, the expression of TE is repressed in the presence of thiamine) or absence of thiamine (−thiamine, the expression of TE is induced in the absence of thiamine). (b) The observation of S. pombe cells under light microscopy and 4′,6-diamidino-2-phenylindole (DAPI)-stained cells under UV light showing the S. pombe cells transformed with pREP1-TE in the absence of thiamine became much larger and longer concomitant with bigger nuclei compared with pREP1. LM, light microscopy; UV, observation of DAPI-stained cells under UV light. (c,d) Flow cytometry analysis showing that some (about 25%) flag leaf cells of te mutant (d) have 4C DNA content compared with WT (c). (e,f) Microscopy images of transverse sections (stained with DAPI) showing that the flag leaves of te (f) have more cells with two nuclei (indicated by arrowheads) compared with WT flag leaves (e). The inset magnified parts in f showing two nuclei in one cell. (b) Scale bar, 10 μm and (e,f) 50 μm.
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f3: Conserved role of TE in cell-cycle regulation.(a) Growth of S. pombe transformed with the empty vector pREP1 and pREP1-TE in the presence (+thiamine, the expression of TE is repressed in the presence of thiamine) or absence of thiamine (−thiamine, the expression of TE is induced in the absence of thiamine). (b) The observation of S. pombe cells under light microscopy and 4′,6-diamidino-2-phenylindole (DAPI)-stained cells under UV light showing the S. pombe cells transformed with pREP1-TE in the absence of thiamine became much larger and longer concomitant with bigger nuclei compared with pREP1. LM, light microscopy; UV, observation of DAPI-stained cells under UV light. (c,d) Flow cytometry analysis showing that some (about 25%) flag leaf cells of te mutant (d) have 4C DNA content compared with WT (c). (e,f) Microscopy images of transverse sections (stained with DAPI) showing that the flag leaves of te (f) have more cells with two nuclei (indicated by arrowheads) compared with WT flag leaves (e). The inset magnified parts in f showing two nuclei in one cell. (b) Scale bar, 10 μm and (e,f) 50 μm.

Mentions: As reported for other Cdh1 homologues such as AtCCS52A1 and AtCCS52A28, transient expression analysis in Arabidopsis protoplasts revealed that the TE–GFP fusion protein is predominantly targeted to the nucleus (Fig. 2f). Overexpression of TE in Schizosaccharomyces pombe inhibited cell division and caused cell enlargement (Fig. 3a,b). Consistent with this observation, flow cytometry and 4′,6-diamidino-2-phenylindole staining analyses showed that some cells in the te flag leaves had 4C DNA content and were binucleated compared with WT, suggesting a delay in mitotic exit in some te leaf cells (Fig. 3c–f). Notably, more binucleated cells have been observed in mice Fzr1−/− mouse embryonic fibroblasts (Cdh1-deficient cells) because of delayed mitotic exit27. Taken together, these results support the notion that TE has an evolutionarily conserved role in cell-cycle regulation22728.


Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1.

Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang JL, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J - Nat Commun (2012)

Conserved role of TE in cell-cycle regulation.(a) Growth of S. pombe transformed with the empty vector pREP1 and pREP1-TE in the presence (+thiamine, the expression of TE is repressed in the presence of thiamine) or absence of thiamine (−thiamine, the expression of TE is induced in the absence of thiamine). (b) The observation of S. pombe cells under light microscopy and 4′,6-diamidino-2-phenylindole (DAPI)-stained cells under UV light showing the S. pombe cells transformed with pREP1-TE in the absence of thiamine became much larger and longer concomitant with bigger nuclei compared with pREP1. LM, light microscopy; UV, observation of DAPI-stained cells under UV light. (c,d) Flow cytometry analysis showing that some (about 25%) flag leaf cells of te mutant (d) have 4C DNA content compared with WT (c). (e,f) Microscopy images of transverse sections (stained with DAPI) showing that the flag leaves of te (f) have more cells with two nuclei (indicated by arrowheads) compared with WT flag leaves (e). The inset magnified parts in f showing two nuclei in one cell. (b) Scale bar, 10 μm and (e,f) 50 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3316886&req=5

f3: Conserved role of TE in cell-cycle regulation.(a) Growth of S. pombe transformed with the empty vector pREP1 and pREP1-TE in the presence (+thiamine, the expression of TE is repressed in the presence of thiamine) or absence of thiamine (−thiamine, the expression of TE is induced in the absence of thiamine). (b) The observation of S. pombe cells under light microscopy and 4′,6-diamidino-2-phenylindole (DAPI)-stained cells under UV light showing the S. pombe cells transformed with pREP1-TE in the absence of thiamine became much larger and longer concomitant with bigger nuclei compared with pREP1. LM, light microscopy; UV, observation of DAPI-stained cells under UV light. (c,d) Flow cytometry analysis showing that some (about 25%) flag leaf cells of te mutant (d) have 4C DNA content compared with WT (c). (e,f) Microscopy images of transverse sections (stained with DAPI) showing that the flag leaves of te (f) have more cells with two nuclei (indicated by arrowheads) compared with WT flag leaves (e). The inset magnified parts in f showing two nuclei in one cell. (b) Scale bar, 10 μm and (e,f) 50 μm.
Mentions: As reported for other Cdh1 homologues such as AtCCS52A1 and AtCCS52A28, transient expression analysis in Arabidopsis protoplasts revealed that the TE–GFP fusion protein is predominantly targeted to the nucleus (Fig. 2f). Overexpression of TE in Schizosaccharomyces pombe inhibited cell division and caused cell enlargement (Fig. 3a,b). Consistent with this observation, flow cytometry and 4′,6-diamidino-2-phenylindole staining analyses showed that some cells in the te flag leaves had 4C DNA content and were binucleated compared with WT, suggesting a delay in mitotic exit in some te leaf cells (Fig. 3c–f). Notably, more binucleated cells have been observed in mice Fzr1−/− mouse embryonic fibroblasts (Cdh1-deficient cells) because of delayed mitotic exit27. Taken together, these results support the notion that TE has an evolutionarily conserved role in cell-cycle regulation22728.

Bottom Line: We demonstrate that TE encodes a rice homologue of Cdh1, and that TE acts as an activator of the anaphase promoting complex/cyclosome (APC/C) complex.We show that TE coexpresses with MOC1 in the axil of leaves, where the APC/C(TE) complex mediates the degradation of MOC1 by the ubiquitin-26S proteasome pathway, and consequently downregulates the expression of the meristem identity gene Oryza sativa homeobox 1, thus repressing axillary meristem initiation and formation.We conclude that besides having a conserved role in regulating cell cycle, APC/C(TE) has a unique function in regulating the plant-specific postembryonic shoot branching and tillering, which are major determinants of plant architecture and grain yield.

View Article: PubMed Central - PubMed

Affiliation: National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China.

ABSTRACT
Rice MONOCULM 1 (MOC1) and its orthologues LS/LAS (lateral suppressor in tomato and Arabidopsis) are key promoting factors of shoot branching and tillering in higher plants. However, the molecular mechanisms regulating MOC1/LS/LAS have remained elusive. Here we show that the rice tiller enhancer (te) mutant displays a drastically increased tiller number. We demonstrate that TE encodes a rice homologue of Cdh1, and that TE acts as an activator of the anaphase promoting complex/cyclosome (APC/C) complex. We show that TE coexpresses with MOC1 in the axil of leaves, where the APC/C(TE) complex mediates the degradation of MOC1 by the ubiquitin-26S proteasome pathway, and consequently downregulates the expression of the meristem identity gene Oryza sativa homeobox 1, thus repressing axillary meristem initiation and formation. We conclude that besides having a conserved role in regulating cell cycle, APC/C(TE) has a unique function in regulating the plant-specific postembryonic shoot branching and tillering, which are major determinants of plant architecture and grain yield.

Show MeSH
Related in: MedlinePlus