拟南芥生长素响应因子ARF17调控花粉壁模式形成
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摘要
雄配子发育是生物生命周期的最关键步骤，外界环境对其影响重大。生长素对植物高温雄性不育的恢复有重要作用。但生长素在雄配子发生过程中的作用机理尚不清楚。
在这项研究中，我们发现拟南芥生长素响应因子ARF17对初生外壁形成和花粉壁模式形成具有关键作用。ARF17的敲除突变体呈现完全雄性不育表型，但其营养生长没有可见异常。半薄切片显示，arf17小孢子从四分体释放以后开始发生降解。进一步透射电镜发现arf17初生外壁存在缺失，从而导致花粉壁模式的缺陷和花粉降解。此外，ARF17突变还引起雄配子的传递率降低。花粉管体外和体内萌发表明，arf17花粉管较野生型生长慢。通过原位杂交和融合蛋白观察发现，ARF17在小孢子母细胞和四分体时期高度表达。胼胝质染色显示四分体时期arf17突变体胼胝质积累减少，与此相一致的是胼胝质合酶基因CALLOSESYNTHASE5(CalS5)的表达也显著降低，大约为野生型的10%。ARF家族蛋白能特异地结合到基因启动子区域的生长素响应元件(AuxREs)TGTCTC/GAGATA上调控其表达。CALS5上游-863to-858包含一个生长素响应元件GAGATA。染色质免疫共沉淀和凝胶阻滞实验表明ARF17能直接结合到CALS5启动子上。表达抑制型化学短肽融合ARF17蛋白的植株初生外壁缺失，胼胝质沉积和CALS5表达降低，这与arf17突变体表型非常类似，表明ARF17是一个转录激活因子。通过检测生长素响应基因DR5::GFP表达，我们发现花药生长素信号特异地受到影响。
我们的研究表明，ARF17至少通过直接结合CALS5启动子，调控胼胝质合成和初生外壁形成，这些工作揭示了一种生长素信号途径参与的花粉壁调控模式，为研究花粉壁模式形成的分子机制提供了新的线索。
In angiosperms, pollen wall pattern formation is determined by primexinedeposition on the microspores. In this study, we show that an auxin response factor,ARF17plays an essential role for primexine formation and pollen wall developmentin Arabidopsis thaliana. The knock out mutant of arf17exhibited a male sterilephenotype with normal vegetative growth. ARF17was expressed in microsporocytesand microgametophytes from meiosis to the bicellular microspore stage. Semi-thincross sections and transmission electron microscopy (TEM) observation showed thatprimexine was absent in the arf17mutant, which leads to pollen wall patterningdefects and pollen degradation. In addition, ARF17mutation caused reduced malegametophyte transmission efficiency. In vitro and in vivo pollen geimination analysisshowed that pollen tube growth waa slower that that in wild type. Callose deposition,as well as he expression of CALLOSE SYNTHASE5(CalS5) was significantly reduced inthe arf17mutan. ARF proteins can regulate the expression of genes with an AuxRE(TGTCTC/GAGACA) in their promoter. The CalS5promoter contains one AuxRE (-863to-858). Both Chromatin immunoprecipitation (ChIP) and Electrophoretic MobilityShift Assay (EMSA) showed that ARF17can directly bind to the CalS5promoter.Plants expressing the chimeric ARF17repressor under ARF17native promoter(ARF17-SRDX) mimics phenotype of arf17at both cytological and molecular level,suggesting ARF17functions as a transcriptional activator. As indicated by expressionof the DR5::GFP auxin reporter, auxin signaling appeared to be specifically impairedin arf17anthers. Taken together, our results suggest that ARF17is essential for pollenwall patterning in Arabidopsis by modulating primexine formation at least partiallythrough direct regulation of CalS5gene expression. Our study provides importantevidence that auxin signaling pathway plays an important role in pollen walldevelopment and new insight for pollen wall pattern formation through ARF17mediated signaling pathway.
在这项研究中，我们发现拟南芥生长素响应因子ARF17对初生外壁形成和花粉壁模式形成具有关键作用。ARF17的敲除突变体呈现完全雄性不育表型，但其营养生长没有可见异常。半薄切片显示，arf17小孢子从四分体释放以后开始发生降解。进一步透射电镜发现arf17初生外壁存在缺失，从而导致花粉壁模式的缺陷和花粉降解。此外，ARF17突变还引起雄配子的传递率降低。花粉管体外和体内萌发表明，arf17花粉管较野生型生长慢。通过原位杂交和融合蛋白观察发现，ARF17在小孢子母细胞和四分体时期高度表达。胼胝质染色显示四分体时期arf17突变体胼胝质积累减少，与此相一致的是胼胝质合酶基因CALLOSESYNTHASE5(CalS5)的表达也显著降低，大约为野生型的10%。ARF家族蛋白能特异地结合到基因启动子区域的生长素响应元件(AuxREs)TGTCTC/GAGATA上调控其表达。CALS5上游-863to-858包含一个生长素响应元件GAGATA。染色质免疫共沉淀和凝胶阻滞实验表明ARF17能直接结合到CALS5启动子上。表达抑制型化学短肽融合ARF17蛋白的植株初生外壁缺失，胼胝质沉积和CALS5表达降低，这与arf17突变体表型非常类似，表明ARF17是一个转录激活因子。通过检测生长素响应基因DR5::GFP表达，我们发现花药生长素信号特异地受到影响。
我们的研究表明，ARF17至少通过直接结合CALS5启动子，调控胼胝质合成和初生外壁形成，这些工作揭示了一种生长素信号途径参与的花粉壁调控模式，为研究花粉壁模式形成的分子机制提供了新的线索。
In angiosperms, pollen wall pattern formation is determined by primexinedeposition on the microspores. In this study, we show that an auxin response factor,ARF17plays an essential role for primexine formation and pollen wall developmentin Arabidopsis thaliana. The knock out mutant of arf17exhibited a male sterilephenotype with normal vegetative growth. ARF17was expressed in microsporocytesand microgametophytes from meiosis to the bicellular microspore stage. Semi-thincross sections and transmission electron microscopy (TEM) observation showed thatprimexine was absent in the arf17mutant, which leads to pollen wall patterningdefects and pollen degradation. In addition, ARF17mutation caused reduced malegametophyte transmission efficiency. In vitro and in vivo pollen geimination analysisshowed that pollen tube growth waa slower that that in wild type. Callose deposition,as well as he expression of CALLOSE SYNTHASE5(CalS5) was significantly reduced inthe arf17mutan. ARF proteins can regulate the expression of genes with an AuxRE(TGTCTC/GAGACA) in their promoter. The CalS5promoter contains one AuxRE (-863to-858). Both Chromatin immunoprecipitation (ChIP) and Electrophoretic MobilityShift Assay (EMSA) showed that ARF17can directly bind to the CalS5promoter.Plants expressing the chimeric ARF17repressor under ARF17native promoter(ARF17-SRDX) mimics phenotype of arf17at both cytological and molecular level,suggesting ARF17functions as a transcriptional activator. As indicated by expressionof the DR5::GFP auxin reporter, auxin signaling appeared to be specifically impairedin arf17anthers. Taken together, our results suggest that ARF17is essential for pollenwall patterning in Arabidopsis by modulating primexine formation at least partiallythrough direct regulation of CalS5gene expression. Our study provides importantevidence that auxin signaling pathway plays an important role in pollen walldevelopment and new insight for pollen wall pattern formation through ARF17mediated signaling pathway.
引文
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