拟南芥RETARDED ROOT GROWTH基因的图位克隆及功能分析
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摘要
植物根中各组织的形成和生长均由根顶端分生组织的细胞增殖、分化而来。正确调控植物根分生组织的细胞分裂对维持根部正常生长是必需的。近些年来,在模式植物拟南芥中已经鉴定了一些重要的细胞分裂调控因子,但目前仍不清楚细胞分裂如何调控植物根的形态和生长。因此,利用相应突变体,研究其在分生组织细胞分裂中的功能有利于在发育水平上揭示细胞分裂调控的分子机制。本研究筛选并鉴定了一个根顶端分生组织有缺陷的突变体retarded root growth-1(rrg-1),克隆了RRG基因,并对其分子调控机制进行了研究,主要结果如下：
1.用EMS诱变拟南芥哥伦比亚野生型(Col-0)种子,构建了含15000个株系的突变体库。从中筛选到一些有明显突变表型且能稳定遗传的突变体。将其中一个根部生长迟缓突变体命名为rrg-1,其表型特征为根短、根毛少而长、地上部分生长慢、种子畸形。
2.遗传分析表明rrg-1突变为单基因隐性突变。用分布于拟南芥五条染色体上的22个SSLP标记对60个极端短根F2植株进行分析,把突变基因初定位在第一染色体nga280和ngal11两标记之间。进一步利用这两个标记之间的8个IND或SNP标记对721个F2短根单株进行分析,将突变基因界定到分子标记CER473407和CER481032之间约25.3kb的区域。通过比较测序,发现rrg-1突变体的Atlg69380有一个G-A的碱基突变,氨基酸则从谷氨酸变成了赖氨酸。
3.构建互补载体并转化rrg-1,转基因植株的表型和野生型无异,证明rrg-1的短根表型是由Atlg69380突变引起的。从拟南芥数据库又鉴定出一个T-DNA插入突变体,表型和rrg-1相似,命名为rrg-2。RT-PCR分析表明,RRG在rrg-1中表达量降低,在rrg-2中不表达。观察发现,两突变体的胚根和野生型的没有明显差异,表明RRG对胚后根发育起调控作用。
4.RRG由7个外显子和6个内含子组成,编码了一个具有373个氨基酸的未知功能蛋白。RRG包含一个N端线粒体信号肽、一个保守的DUF155结构域以及一个C端跨膜结构域。BLAST分析发现在植物、细菌、真菌和其它真核生物中都有RRG的同源基因,所有的同源基因都包含DUF155结构域,但其功能还不清楚。在推测的RRG同源基因中,酵母中的SIF2和RMND1与细胞分裂有关,这暗示RRG可能在拟南芥根分生区的细胞分裂中起作用。
5.构建35S::RRG-GFP载体,转化野生型拟南芥。用共聚焦激光显微境观察拟南芥转化株的根尖,发现RRG-GFP的表达在根细胞中呈点状,表明RRG定位在某细胞器中。再利用线粒体染料MitoTracker Orange对拟南芥转基因植株根尖进行染色,发现MitoTracker Orange和RRG-GFP融合蛋白的荧光重合,证明荧光点就是线粒体。为进一步证明RRG-GFP定位于线粒体,我们用RRG-GFP和线粒体标记载体mt-rk CD3-991共转化烟草叶片表皮细胞,也观察到两载体的荧光在线粒体上共定位,因此确定RRG定位在线粒体。
6.构建pRRG::GUS载体,转化拟南芥植株。GUS组织化学染色发现RRG基因主要在根分生组织的静止中心、皮层/内皮层干细胞及其子细胞、内皮层和中柱细胞表达,表明RRG在这些细胞中起作用。RRG在侧根中的表达模式和主根相同。此外,RRG在叶片和花粉中也有表达。
7.测量WT和rrg突变体根部细胞,发现突变体的根分生组织明显减小,而成熟区皮层细胞长度没有明显变化,表明RRG主要在分生区起作用并正调控分生区大小。同时还发现突变体分生区细胞数目变少、皮层细胞变长。生长动力学研究也表明rrg根分生组织的皮层细胞增加总是比WT慢,rrg突变体的细胞增殖速度降低；在分生区皮层细胞数目变少的同时还发现皮层细胞变长,表明rrg突变体的分生区细胞延长加速。
8.透射电镜观察根分生区细胞中线粒体的数量和结构,发现WT和rrg-2中单位细胞面积中线粒体的数量没有明显差异,但在结构上,与正常的线粒体相比,rrg-2中约82%的线粒体有空泡化现象,表明RRG是维持线粒体正常结构所需的。
9.分析发现,rrg突变体根分生区细胞周期持续时间明显延长。用qRT-PCR分析了一些细胞周期相关基因在rrg-2中的表达量,其中CYCD4;1, E2Fa, DPa, DELI的表达量在rrg-2中没有明显变化,而HISTONE H4, CYCB1;1, CDKB1;1, WEE1在rrg-2中的表达量明显下降。同时,我们还分析了CycB1;1::GFP在根分生区的表达,rrg突变体处于G2-M期的细胞数目明显少于WT。这些实验表明细胞周期过程在突变体中受到影响。另外,细胞倍性分析表明突变体中4C,8C,16C细胞的比例比野生型低,2C细胞比例比WT高,表明突变体核内复制下降,进一步证明细胞分裂受到损害。
10.将SHR::SHR-GFP,SCR::H2B-YFP和WOX5::ERGFP株系和rrg-2杂交,分析这些标记基因在rrg突变体背景下的表达情况。发现这些标记基因在突变体根分生组织中的表达水平和模式都没有改变,表明RRG没有参与调控静止中心(QC)及邻近干细胞的特性,其功能与这些根形态建成基因相独立。
11.观察生长素反应标记载体DR5rev::GFP在rrg-2中的表达,发现RRG的突变并不影响该标记载体的表达；而且施加外源生长素NAA, IAA, IBA,或2,4-D,rrg-2突变体和WT根生长反应是一致的,表明rrg-2突变体对生长素的反应和敏感性没有缺陷。
综上所述,RRG基因主要在根分生区表达,参与调控拟南芥胚后根的细胞分裂活动,但RRG与生长素信号和根的形态建成无关。RRG基因编码一个线粒体蛋白,rrg突变体中根分生区细胞中线粒体呈现大量的空泡化,表明植物线粒体在细胞分裂调控中起重要作用。我们的研究第一次揭示了拟南芥RRG基因调控根分生区细胞分裂活动,并为植物线粒体参与细胞分裂调控提供了新的证据。
In plants, the formation and growth of all root organizations are derived from cell proliferation and differentiation of root meristem. Accurate regulation of meristem cell division is important for normal root growth. In recent years, a number of important major regulatory factors in cell division have been identified, but how cell division progression regulates the morphology and growth of root meristem is still not clear. Therefore, identification and characterization of mutants that show defects in cell division will be helpful to reveal how cell division regulates the development of root meristem. In our study, we screened an EMS-mutagenized Arabidopsis thaliana mutant library and identified a mutant that displayed retarded root growth-1(rrg-1). We identified the RRG gene using the approach of map-based cloning and characterized its function in regulating root growth. The main results are presented as follows:
1. We eatablished an ethylmethane sulfonate (EMS)-mutagenized Columbia-0(Col-0) pool containing15000lines and identified a number of mutants. One of the mutants displayed retarded root growth and was named as rrg-1. rrg-1has short root, sparse and long root hairs, slowly growth and wrinkle seeds.
2. Genetic analysis indicated that the rrg-1mutation is single recessive. Sixty homozygous mutant plants were selected from the F2population and analyzed with22simple sequence length polymorphism (SSLP) markers evenly distributed on the five Arabidopsis chromosomes. The RRG was firstly located between the markers nga280and ngalll on chromosome1. For fine mapping,721plants conferring the rrg phenotypes were identified from the F2population and genotyped with eight INDEL and SNP markers between nga280and ngalll. The RRG locus was delimited to a25.3-kb region flanked by markers CER473407and CER481032on BAC clones F23O10and F10D13, respectively. Sequencing of the genomic DNA amplified from this region revealed a single G-to-A base change in the rrg-1mutant background, which led to a missense mutation from glutamic (Glu) to lysine (Lys) at the346th amino acid of the encoded protein of the At1g69380gene.
3. Complementation test was carried out and all transgenic plants obtained were phenotypically indistinguishable from WT plants, confirming that the root growth phenotype observed in rrg-1were caused by the disruption of Atlg69380. In agreement with this result, a T-DNA insertion mutant in which the T-DNA fragment is located in the seventh exon of Atlg69380showed a similar short root phenotype as rrg-1. We thus renamed Atlg69380as RRG and designated the T-DNA mutant rrg-2. Notably, reverse transcription (RT)-PCR analysis of mRNA transcript levels of RRG in rrg-1, rrg-2and WT plants revealed that RRG transcript was absent in rrg-2but still present in rrg-1, although lower than that in WT, suggesting that rrg-1is a knock-down allele whereas rrg-2is null for the RRG gene. No obvious phenotypic abnormality was observed in the embryonic RAM of both mutant alleles when compared with the WT control, indicating that the role of RRG is confined to post-embryonic root development.
4. The RRG gene consists of seven exons and six introns, and encodes a novel protein with373amino acids. More detailed protein sequence analysis revealed a mitochondria signal sequence at the amino terminus of the RRG protein, a conserved DUF155domain and a carboxy terminus transmembrane domain. Sequence search against NCBI protein database with the RRG protein identified putative orthologs of RRG in plant and non-plant organisms such as bacteria, fungi and other eukaryotes. All of these orthologs contain the DUF155domain whose function is not yet known. Two putative yeast orthologs of RRG, Sad1-interacting factor2(SIF2) and Required for Meiotic Nuclear Division1(RMND1), have been associated with cell division. This suggests a role for RRG in meristematic cell division in the Arabidopsis root.
5. To examine the subcellular localization of RRG in living Arabidopsis cells, we generated transgenic Arabidopsis plants with the35S::RRG-GFP construct and analyzed the expression of RRG-GFP in vivo with confocal laser scanning microscope. We found that RRG-GFP expression was confined to small punctuate structures in root cells, indicating that RRG is localized to certain organelles, possibly mitochondria as suggested by protein sequence analysis. Indeed, we confirmed this possibility by showing that the mitochondria-specific dye MitoTracker Orange and the RRG-GFP fusion protein colocalize in the mitochondria. To further reveal the nature of the structures marked by RRG-GFP, we performed in tobacco leaf epidermal cells co-localization experiments of RRG-GFP with mt-rk CD3-991, a well-known mitochondria marker generated with a red fluorescent protein mcherry. We observed that RRG-GFP co-localized with mt-rk CD3-991at mitochondria and thus conclude that RRG is localized to mitochondria.
6. We investigated the expression pattern of RRG gene in the Arabidopsis root and found that the RRG gene is preferentially expressed in quiescent center (QC) cells, cortex/endodermis stem cells and their daughter cells, endodermal and stele cells in the root meristem, suggesting a role for RRG in these cells. Moreover, we found that the expression pattern of pRRG::GUS in lateral roots was identical to that observed in primary roots, and that GUS staining could also be seen in leaves and pollen.
7. The sizes of root meristem of WT and rrg mutants were compared. The average size of the root meristem was significant reduced and the average cortex cell length in the differentiation zone, however, was unchanged between WT and rrg mutants, suggesting that RRG functions specifically in the root meristem and RRG positively regulates the root meristem size. We thus analyzed the average cortex cell number and cell length in the root meristem of WT and rrg mutants. The average cortex cell number in the root meristem of rrg were significantly reduced and the kinematic analysis also showed that the increasing of cortex cells in rrg root meristem was always slower than that in the WT control, suggesting that the rate of cell proliferation was decreased in rrg mutants. In contrast, the cortex cell length in root meristem of rrg mutants was significantly increased compared to the WT control, suggesting that cell elongation in the meristematic cells was accelerated in the rrg mutant background.
8. We examined the number and structure of mitochondria in the root meristem cells of WT and mutant plants by using transmission electron microscope. We analyzed the section plane of mitochondria in multiple sections and found that the number of mitochondria per unit cell area in rrg-2was comparable with that of WT, but a vast majority of mitochondria (82%) in mutant cells displayed internal vacuolization compared to WT controls. The results suggest that RRG is required for the maintenance of mitochondrial structure.
9. To further dissect the role of RRG on cell proliferation, we estimated the average cell cycle duration in the root meristem of rrg mutants and WT and found that the rrg mutations led to increased cell cycle duration in the root mersitem. We then examined the expression level of some cell cycle progression related genes in WT and rrg-2by qRT-PCR, the results showed that the expression of CYCD4;1and E2Fa, DPa and DELI did not change significantly, but HISTONE H4, CYCB1;1, CDKB1;1and WEE1were significantly down-regulated in rrg-2mutant compared to the WT controls. In agreement with this indication, we found that the number of root meristem cells at the G2-M phase, revealed by the CycB1;1::GFP marker, was strongly reduced in rrg mutants than in WT. The experiments indicated that cell cycle progression was impaired in rrg-2mutant. Because mutants affecting cell division always display altered endoreduplication levels, we compared the ploidy levels of WT and rrg mutant roots. We found that, at9days after germination, the proportions of root cells with nuclear contents of4C,8C and16C were lower in rrg mutants than in WT, indicating that endoreduplication was seriously compromised in rrg mutants. By contrast, the proportion of2C cells was increased in rrg-2null mutants, further confirming that cell division was impaired.
10. We analyzed the expression levels and patterns of pSHR::SHR-GFP, pSCR::H2B-YFP and pWOX5::ERGFP in the rrg mutant background and found that the expression levels and patterns of these markers in the root meristem were not obviously affected by the rrg mutations, suggesting that RRG is not involved in the regulation of QC and proximal root stem cell identity and functions independently of the key patterning genes.
11. To learn whether the phenotypes observed in rrg mutants were caused by changes in auxin level and response, we examined the expression of the auxin-responsive marker DR5rev::GFP in rrg mutants. No obvious differences between rrg mutants and WT seedlings were detected with regard to the expression level and pattern of DR5rev::GFP in the root tip, suggesting that the RRG mutations did not cause changes in auxin level and response. Consistently, we found that rrg-2mutants exhibited a WT-like root growth response to NAA, IAA, IBA, or2,4-D at all concentration examined, indicating that rrg-2mutants are not defective in auxin response or sensitivity.
Taken together, RRG is preferentially expressed in the root meristem and required for the cell division activity of postembryonic root meristem in Arabidopsis. The function of RRG is independent of auxin signalling and root patterning. RRG encodes a mitochondrial protein, and the mitochondria in root meristem cells of rrg mutants display extensive vocalization, implicating plant mitochondria has an important role in the regulation of cell division. Our data reveal for the first time the role of the Arabidopsis RRG gene in regulating cell division in the root meristem, and provide a new evidence for the involvement of plant mitochondria in cell division.
1.用EMS诱变拟南芥哥伦比亚野生型(Col-0)种子,构建了含15000个株系的突变体库。从中筛选到一些有明显突变表型且能稳定遗传的突变体。将其中一个根部生长迟缓突变体命名为rrg-1,其表型特征为根短、根毛少而长、地上部分生长慢、种子畸形。
2.遗传分析表明rrg-1突变为单基因隐性突变。用分布于拟南芥五条染色体上的22个SSLP标记对60个极端短根F2植株进行分析,把突变基因初定位在第一染色体nga280和ngal11两标记之间。进一步利用这两个标记之间的8个IND或SNP标记对721个F2短根单株进行分析,将突变基因界定到分子标记CER473407和CER481032之间约25.3kb的区域。通过比较测序,发现rrg-1突变体的Atlg69380有一个G-A的碱基突变,氨基酸则从谷氨酸变成了赖氨酸。
3.构建互补载体并转化rrg-1,转基因植株的表型和野生型无异,证明rrg-1的短根表型是由Atlg69380突变引起的。从拟南芥数据库又鉴定出一个T-DNA插入突变体,表型和rrg-1相似,命名为rrg-2。RT-PCR分析表明,RRG在rrg-1中表达量降低,在rrg-2中不表达。观察发现,两突变体的胚根和野生型的没有明显差异,表明RRG对胚后根发育起调控作用。
4.RRG由7个外显子和6个内含子组成,编码了一个具有373个氨基酸的未知功能蛋白。RRG包含一个N端线粒体信号肽、一个保守的DUF155结构域以及一个C端跨膜结构域。BLAST分析发现在植物、细菌、真菌和其它真核生物中都有RRG的同源基因,所有的同源基因都包含DUF155结构域,但其功能还不清楚。在推测的RRG同源基因中,酵母中的SIF2和RMND1与细胞分裂有关,这暗示RRG可能在拟南芥根分生区的细胞分裂中起作用。
5.构建35S::RRG-GFP载体,转化野生型拟南芥。用共聚焦激光显微境观察拟南芥转化株的根尖,发现RRG-GFP的表达在根细胞中呈点状,表明RRG定位在某细胞器中。再利用线粒体染料MitoTracker Orange对拟南芥转基因植株根尖进行染色,发现MitoTracker Orange和RRG-GFP融合蛋白的荧光重合,证明荧光点就是线粒体。为进一步证明RRG-GFP定位于线粒体,我们用RRG-GFP和线粒体标记载体mt-rk CD3-991共转化烟草叶片表皮细胞,也观察到两载体的荧光在线粒体上共定位,因此确定RRG定位在线粒体。
6.构建pRRG::GUS载体,转化拟南芥植株。GUS组织化学染色发现RRG基因主要在根分生组织的静止中心、皮层/内皮层干细胞及其子细胞、内皮层和中柱细胞表达,表明RRG在这些细胞中起作用。RRG在侧根中的表达模式和主根相同。此外,RRG在叶片和花粉中也有表达。
7.测量WT和rrg突变体根部细胞,发现突变体的根分生组织明显减小,而成熟区皮层细胞长度没有明显变化,表明RRG主要在分生区起作用并正调控分生区大小。同时还发现突变体分生区细胞数目变少、皮层细胞变长。生长动力学研究也表明rrg根分生组织的皮层细胞增加总是比WT慢,rrg突变体的细胞增殖速度降低；在分生区皮层细胞数目变少的同时还发现皮层细胞变长,表明rrg突变体的分生区细胞延长加速。
8.透射电镜观察根分生区细胞中线粒体的数量和结构,发现WT和rrg-2中单位细胞面积中线粒体的数量没有明显差异,但在结构上,与正常的线粒体相比,rrg-2中约82%的线粒体有空泡化现象,表明RRG是维持线粒体正常结构所需的。
9.分析发现,rrg突变体根分生区细胞周期持续时间明显延长。用qRT-PCR分析了一些细胞周期相关基因在rrg-2中的表达量,其中CYCD4;1, E2Fa, DPa, DELI的表达量在rrg-2中没有明显变化,而HISTONE H4, CYCB1;1, CDKB1;1, WEE1在rrg-2中的表达量明显下降。同时,我们还分析了CycB1;1::GFP在根分生区的表达,rrg突变体处于G2-M期的细胞数目明显少于WT。这些实验表明细胞周期过程在突变体中受到影响。另外,细胞倍性分析表明突变体中4C,8C,16C细胞的比例比野生型低,2C细胞比例比WT高,表明突变体核内复制下降,进一步证明细胞分裂受到损害。
10.将SHR::SHR-GFP,SCR::H2B-YFP和WOX5::ERGFP株系和rrg-2杂交,分析这些标记基因在rrg突变体背景下的表达情况。发现这些标记基因在突变体根分生组织中的表达水平和模式都没有改变,表明RRG没有参与调控静止中心(QC)及邻近干细胞的特性,其功能与这些根形态建成基因相独立。
11.观察生长素反应标记载体DR5rev::GFP在rrg-2中的表达,发现RRG的突变并不影响该标记载体的表达；而且施加外源生长素NAA, IAA, IBA,或2,4-D,rrg-2突变体和WT根生长反应是一致的,表明rrg-2突变体对生长素的反应和敏感性没有缺陷。
综上所述,RRG基因主要在根分生区表达,参与调控拟南芥胚后根的细胞分裂活动,但RRG与生长素信号和根的形态建成无关。RRG基因编码一个线粒体蛋白,rrg突变体中根分生区细胞中线粒体呈现大量的空泡化,表明植物线粒体在细胞分裂调控中起重要作用。我们的研究第一次揭示了拟南芥RRG基因调控根分生区细胞分裂活动,并为植物线粒体参与细胞分裂调控提供了新的证据。
In plants, the formation and growth of all root organizations are derived from cell proliferation and differentiation of root meristem. Accurate regulation of meristem cell division is important for normal root growth. In recent years, a number of important major regulatory factors in cell division have been identified, but how cell division progression regulates the morphology and growth of root meristem is still not clear. Therefore, identification and characterization of mutants that show defects in cell division will be helpful to reveal how cell division regulates the development of root meristem. In our study, we screened an EMS-mutagenized Arabidopsis thaliana mutant library and identified a mutant that displayed retarded root growth-1(rrg-1). We identified the RRG gene using the approach of map-based cloning and characterized its function in regulating root growth. The main results are presented as follows:
1. We eatablished an ethylmethane sulfonate (EMS)-mutagenized Columbia-0(Col-0) pool containing15000lines and identified a number of mutants. One of the mutants displayed retarded root growth and was named as rrg-1. rrg-1has short root, sparse and long root hairs, slowly growth and wrinkle seeds.
2. Genetic analysis indicated that the rrg-1mutation is single recessive. Sixty homozygous mutant plants were selected from the F2population and analyzed with22simple sequence length polymorphism (SSLP) markers evenly distributed on the five Arabidopsis chromosomes. The RRG was firstly located between the markers nga280and ngalll on chromosome1. For fine mapping,721plants conferring the rrg phenotypes were identified from the F2population and genotyped with eight INDEL and SNP markers between nga280and ngalll. The RRG locus was delimited to a25.3-kb region flanked by markers CER473407and CER481032on BAC clones F23O10and F10D13, respectively. Sequencing of the genomic DNA amplified from this region revealed a single G-to-A base change in the rrg-1mutant background, which led to a missense mutation from glutamic (Glu) to lysine (Lys) at the346th amino acid of the encoded protein of the At1g69380gene.
3. Complementation test was carried out and all transgenic plants obtained were phenotypically indistinguishable from WT plants, confirming that the root growth phenotype observed in rrg-1were caused by the disruption of Atlg69380. In agreement with this result, a T-DNA insertion mutant in which the T-DNA fragment is located in the seventh exon of Atlg69380showed a similar short root phenotype as rrg-1. We thus renamed Atlg69380as RRG and designated the T-DNA mutant rrg-2. Notably, reverse transcription (RT)-PCR analysis of mRNA transcript levels of RRG in rrg-1, rrg-2and WT plants revealed that RRG transcript was absent in rrg-2but still present in rrg-1, although lower than that in WT, suggesting that rrg-1is a knock-down allele whereas rrg-2is null for the RRG gene. No obvious phenotypic abnormality was observed in the embryonic RAM of both mutant alleles when compared with the WT control, indicating that the role of RRG is confined to post-embryonic root development.
4. The RRG gene consists of seven exons and six introns, and encodes a novel protein with373amino acids. More detailed protein sequence analysis revealed a mitochondria signal sequence at the amino terminus of the RRG protein, a conserved DUF155domain and a carboxy terminus transmembrane domain. Sequence search against NCBI protein database with the RRG protein identified putative orthologs of RRG in plant and non-plant organisms such as bacteria, fungi and other eukaryotes. All of these orthologs contain the DUF155domain whose function is not yet known. Two putative yeast orthologs of RRG, Sad1-interacting factor2(SIF2) and Required for Meiotic Nuclear Division1(RMND1), have been associated with cell division. This suggests a role for RRG in meristematic cell division in the Arabidopsis root.
5. To examine the subcellular localization of RRG in living Arabidopsis cells, we generated transgenic Arabidopsis plants with the35S::RRG-GFP construct and analyzed the expression of RRG-GFP in vivo with confocal laser scanning microscope. We found that RRG-GFP expression was confined to small punctuate structures in root cells, indicating that RRG is localized to certain organelles, possibly mitochondria as suggested by protein sequence analysis. Indeed, we confirmed this possibility by showing that the mitochondria-specific dye MitoTracker Orange and the RRG-GFP fusion protein colocalize in the mitochondria. To further reveal the nature of the structures marked by RRG-GFP, we performed in tobacco leaf epidermal cells co-localization experiments of RRG-GFP with mt-rk CD3-991, a well-known mitochondria marker generated with a red fluorescent protein mcherry. We observed that RRG-GFP co-localized with mt-rk CD3-991at mitochondria and thus conclude that RRG is localized to mitochondria.
6. We investigated the expression pattern of RRG gene in the Arabidopsis root and found that the RRG gene is preferentially expressed in quiescent center (QC) cells, cortex/endodermis stem cells and their daughter cells, endodermal and stele cells in the root meristem, suggesting a role for RRG in these cells. Moreover, we found that the expression pattern of pRRG::GUS in lateral roots was identical to that observed in primary roots, and that GUS staining could also be seen in leaves and pollen.
7. The sizes of root meristem of WT and rrg mutants were compared. The average size of the root meristem was significant reduced and the average cortex cell length in the differentiation zone, however, was unchanged between WT and rrg mutants, suggesting that RRG functions specifically in the root meristem and RRG positively regulates the root meristem size. We thus analyzed the average cortex cell number and cell length in the root meristem of WT and rrg mutants. The average cortex cell number in the root meristem of rrg were significantly reduced and the kinematic analysis also showed that the increasing of cortex cells in rrg root meristem was always slower than that in the WT control, suggesting that the rate of cell proliferation was decreased in rrg mutants. In contrast, the cortex cell length in root meristem of rrg mutants was significantly increased compared to the WT control, suggesting that cell elongation in the meristematic cells was accelerated in the rrg mutant background.
8. We examined the number and structure of mitochondria in the root meristem cells of WT and mutant plants by using transmission electron microscope. We analyzed the section plane of mitochondria in multiple sections and found that the number of mitochondria per unit cell area in rrg-2was comparable with that of WT, but a vast majority of mitochondria (82%) in mutant cells displayed internal vacuolization compared to WT controls. The results suggest that RRG is required for the maintenance of mitochondrial structure.
9. To further dissect the role of RRG on cell proliferation, we estimated the average cell cycle duration in the root meristem of rrg mutants and WT and found that the rrg mutations led to increased cell cycle duration in the root mersitem. We then examined the expression level of some cell cycle progression related genes in WT and rrg-2by qRT-PCR, the results showed that the expression of CYCD4;1and E2Fa, DPa and DELI did not change significantly, but HISTONE H4, CYCB1;1, CDKB1;1and WEE1were significantly down-regulated in rrg-2mutant compared to the WT controls. In agreement with this indication, we found that the number of root meristem cells at the G2-M phase, revealed by the CycB1;1::GFP marker, was strongly reduced in rrg mutants than in WT. The experiments indicated that cell cycle progression was impaired in rrg-2mutant. Because mutants affecting cell division always display altered endoreduplication levels, we compared the ploidy levels of WT and rrg mutant roots. We found that, at9days after germination, the proportions of root cells with nuclear contents of4C,8C and16C were lower in rrg mutants than in WT, indicating that endoreduplication was seriously compromised in rrg mutants. By contrast, the proportion of2C cells was increased in rrg-2null mutants, further confirming that cell division was impaired.
10. We analyzed the expression levels and patterns of pSHR::SHR-GFP, pSCR::H2B-YFP and pWOX5::ERGFP in the rrg mutant background and found that the expression levels and patterns of these markers in the root meristem were not obviously affected by the rrg mutations, suggesting that RRG is not involved in the regulation of QC and proximal root stem cell identity and functions independently of the key patterning genes.
11. To learn whether the phenotypes observed in rrg mutants were caused by changes in auxin level and response, we examined the expression of the auxin-responsive marker DR5rev::GFP in rrg mutants. No obvious differences between rrg mutants and WT seedlings were detected with regard to the expression level and pattern of DR5rev::GFP in the root tip, suggesting that the RRG mutations did not cause changes in auxin level and response. Consistently, we found that rrg-2mutants exhibited a WT-like root growth response to NAA, IAA, IBA, or2,4-D at all concentration examined, indicating that rrg-2mutants are not defective in auxin response or sensitivity.
Taken together, RRG is preferentially expressed in the root meristem and required for the cell division activity of postembryonic root meristem in Arabidopsis. The function of RRG is independent of auxin signalling and root patterning. RRG encodes a mitochondrial protein, and the mitochondria in root meristem cells of rrg mutants display extensive vocalization, implicating plant mitochondria has an important role in the regulation of cell division. Our data reveal for the first time the role of the Arabidopsis RRG gene in regulating cell division in the root meristem, and provide a new evidence for the involvement of plant mitochondria in cell division.
引文
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