摘要
甘蓝型油菜细胞核雄性不育系7365A由于能够产生全不育群体,恢复源广,易获得强优势组合,在油菜杂种优势育种中被广泛利用。7365A的育性受两对基因(Bnms3和BnRF)互作控制。为揭示7365A的雄性不育机理,本研究通过图位克隆的方法分离了7365A的育性恢复基因BnaC9.Tic40(BnMS3),并对Tic40在芸薹科中进化模式进行详细分析。同时,利用细胞学和分子生物学方法,阐述了7365A的雄性不育机理及BnaC9.Tic40在油菜花药发育中的功能。主要研究结果如下：
1.甘蓝型油菜7365A败育的细胞学观察
透射电镜结果表明,7365A花药的绒毡层细胞在减数分裂时期异常膨大。在四分体阶段,7365A绒毡层细胞液泡化且细胞壁完整,质体、内质网、分泌小泡稀少。随着花药发育,7365A的绒毡层质体中没有脂质积累,且四分体周围的胼胝质壁也无法降解。最终,小孢子以四分体的形式被瓦解。脂染色和TUNEL实验表明,在整个花药发育期间7365A绒毡层质体中始终无法合成和积累脂质；绒毡层细胞PCD被延迟。以上研究表明,7365A花药的败育发生在减数分裂时期,由于绒毡层细胞无法向分泌型转移,导致其分泌功能缺失,从而导致不育。具体表现为绒毡层质体中脂类合成异常、胼胝质酶分泌缺失、PCD延迟等。
2.恢复基因BnaC9.Tic40的克隆
本研究结合芸薹科基因组信息,通过IP标记的开发以及两个BnMs3/Bnms3的近等基因系群体的筛选,将BnMs3定位在分子标记IP20和IP17之间。随后,利用甘蓝和甘蓝型油菜Tapidor的BAC文库构建了BnMs3定位区间的BAC重叠群,完成BnMs3物理图谱的构建。最近两个标记间的物理距离为49.279Kb。对这49.279Kb序列进行ORF分析,获得4个候选基因。这4个候选基因的遗传转化实验最终确定,与拟南芥Tic40(at5g16620)同源的基因BnaC9,Tic40即是7365A的恢复基因BnMs3。
3.恢复基因BnaC9.Tic40的表达和功能研究
RT-PCR结果表明BnaC9.Tic40在油菜幼苗、花药和授粉20天后的种子中表达较强。利用启动子分析和RNA原位杂交实验对BnaC9.Tic40在花药中的表达进行详细分析,结果表明：BnaC9.Tic40在花药发育第5期开始在绒毡层和花粉母细胞中表达；在四分体时期达到最强；随着小孢子发育和绒毡层降解,表达逐渐降低；直至花粉成熟,表达消失。亚细胞定位实验表明,BnaC9.Tic40定位在原生质体的叶绿体上。而其同源基因,AtTic40是叶绿体内膜上通道蛋白复合体的成员,参与叶绿体内膜上蛋白的转运。据此推测,BnaC9.Tic40主要参与绒毡层质体上蛋白的转运。
4.芸薹属基本种中Tic40的复制和丢失
由于芸薹族祖先种基因组的三倍化,Tic40基因组区域发生了3次重复。随后,在芸薹族祖先种染色体二倍化过程中,这3次重复的Tic40基因组区域中出现了频繁的基因片段化现象,导致甘蓝C3和白菜A3中对应的Tic40位点被丢失。最终,在芸薹属三个基本种中进化出两个Tic40位点。
5.部分同源染色体(A10和C9)的重组导致BnaC9.Tic40(BnMs3)起源于BolC9.Tic40,而bnac9.tic40(Bnms3)起源于BraA10.Tic40
Tic40的进化树和序列一致性分析表明恢复基因BnaC9.Tic40在进化上起源于BolC9.Tic40,而其等位基因bnac9.tic40则起源于BraA10.Tic40。23个BnaC9.Tic40和bnac9. tic40侧翼基因序列与甘蓝C9和白菜A10基因组中同源序列的核苷酸多态性分析则证明,在甘蓝型油菜7365B中N19上Tic40周围区域发生了部分同源染色体(A10和C9)的重组,导致7365A中N19连锁群上Tic40位点周围约2Mb的序列来源于白菜A10基因组,从而使bnac9.tic40起源于BraA10.Tic40。
6.正向选择使芸薹属基本种中Tic40发生功能分歧,导致BolC9.Tic40发生功能获得型变异
芸薹属三个基本种及拟南芥中Tic40拷贝的功能分析表明,相对于芸薹科祖先Tic40而言,甘蓝BolC9. Tic40发生了功能获得型变异。6个可能造成功能变异的氨基酸位点存在其功能结构域TPR和Hop上,导致BolC9.Tic40及BnaC9.Tic40可以恢复由于显性基因BnRf的效应引起的7365A的不育性,且Tic40的这一功能获得型变异仅存在于甘蓝及甘蓝的衍生种中。而对芸薹科中Tic40的选择压力分析表明,在芸薹属三个基本种分化前,芸薹科中Tic40的分子进化表现为较强的纯化选择。在三个基本种分化后,在甘蓝BolC9.Tic40这一进化分枝中表现出明显的正向选择。且6个可能造成功能分歧的氨基酸位点受到正向选择的概率均超过90%,其中3个位点正向选择概率大于99%。
The Brassica napus recessive genetic male sterility7365A was considered to be an efficient way in the heterosis utilization of rapeseed, because it can be generated a100%male sterile population by crossing with temporary maintain line and it has wide restores. The male sterility of7365A was controlled by two interacting genes (Bnms3and BnRf). In order to understand the sterile molecular mechanism of7365A, the restoring gene BnaC9. Tic40(BnMs3) was isolated by a map-based cloning approach. Then the evolution dynamics of Tic40in the Brassicaceae genomes was analyzed. Furthermore, the sterile molecular mechanism of7365A and the function of the restoring gene BnaC9.Tic40in anther development were studied by cytological and molecular biological methods. The results were described as follows:
1. The phenotypic characterization of7365A by cytological analyses
Results of transmission electron microscopy (TEM) suggested, at the meiosis stage, in the7365A mutant, the tapetal cells became abnormally enlarged. At the tetrad stage, the mutant tapetal cell walls were still intact and the tapetal cell seemed to be vacuolated. The organelles in the tapetum such as plastids, endoplasmic reticulum and vesicles were seldom. Subsequently, the tapetal cells in the7365A mutant did not synthesize and accumulate lipid compounds. The callose wall surrounding the tetrads was not dissolved. Finally, the microspores were degraded as tetrads. Lipid staining and TUNEL assay showed the tapetal cells in the7365A mutant could not synthesize and accumulate lipid compounds throughout anther development, and the retardation of tapetal PCD resulted in the failure of timely tapetal degradation in the7365A mutant. These results suggested the defects of the7365A mutant anther development were initiated at the meiosis stage. The transition of the tapetal cells to the secretory cells in7365A was defective, resulting in a loss of the secretory function of the tapetum, as suggested by abortive lipid accumulation, absent callose dissolution and retarded tapetal degradation.
2. The cloning of the restoring gene BnaC9.Tic40
The BnMs3gene was located between the molecar markers IP20and IP17by exploiting IP markers and scanning of two BnMs3/Bnms3near-isogenic line populations. Subsequently, the BAC overlapping clusters about the target region was constructed using the BAC libraries of B. oleracea and the B. napus cultivar Tapidor. Then the BnMs3gene was narrowed into a49.279kb region between T1and T4. By ORF finding, four candidate genes were identified in this region. Four resulting complementation constructs were introduced into the7365A line by Agrobacterium tumefaciens-mediated transformation. The genetic complementation suggested BnaC9.Tic40, the ortholog of atTic40, corresponds to the restoring gene BnMs3.
3. The expression patterns and function study of BnaC9.Tic40
RT-PCR analysis suggested that BnaC.Tic40was highly expressed in seedlings, anthers and20-dayold seeds. The expression of the fusion construct, Pro BnaC9.Tic40-GUS and RNA in situ hybridization of BnaC9. Tic40in Arabidopsis wild-type anthers, were used to determine precisely the spatial and temporal patterns of BnaC9. Tic40expression during anther development. At stage5, the BnaC.Tic40gene was first expressed in the tapetum and microspore mother cells. The expression level became higher at the tetrad stage, and was reduced in the tapetum and microspores along with microspore development and tapetal degradation. The expression was disappeared when pollen became mature. The subcelluar localization assay showed the BnaC.Tic40protein was localized in the chloroplast of the protoplast, which is consistent with its ortholog atTic40. Tic40is an inner membrane-anchored translocon in the chloroplast and functions during protein translocation across the inner membrane. It is proposed that BnaC.Tic40participates in protein translocation in the tapetal plastid.
4. Duplication and deletion of Tic40in the diploid Brassica species
The genomic regions around Tic40in the Brassicaceae species were conserved and displayed high microsynteny. The Tic40genomic regions were triplicate duo to the whole-genome triplication of the tribe Brassiceae ancestry. Subsequently, in the diploidization process of the tribe Brassiceae ancestry, frequent gene loss was present in the triplicate Tic40genomic regions, resulting in the deletion of Tic40locus in the B. oleracea C3and B. rapa A3syntenic regions. Currently, the diploid Brassica species B. oleracea, B. rapa and B. nigra have two Tic40loci, located on B. oleracea C2and C9, B. rapa A2and A10, respectively.
5. Homeologous chromosomal rearrangement between A10and C9caused different origins of BnaC9.Tic40(BnMs3) and bnac9.tic40(Bnms3), originating from BolC9.Tic40and BraA10.Tic40, respectively
Phylogenetic tree constructed and sequence identity analysis revealed that BnaC9.Tic40originated from BolC9.Tic40. However, its allele bnac9.tic40was derived from BraA10.Tic40. Partial sequences of twenty-three flanking genes ofBnaC9.Tic40and bnac9.tic40were used to compare with their homologs from B. oleracea C9, and B. rapa A10. Nucleotide diversity demonstrated that chromosomal rearrangement around the Tic40in B. napus N19linkage was caused by homeologous recombination between A10and C9. Finally, about2Mb fragments around Tic40in the N19linkage of7365A was derived from B. rapa A10homologs, resulting in the evolutionarily close between bnac9.tic40and BraA10. Tic40.
6. Function divergence of Tic40in the diploid Brassica species resulted by positive selection, caused a gain-of-function variation of BolC9.Tic40
Genetic complementation assay of Tic40genes from three diploid Brassica species and A. thaliana indicated that in comparison with the Brassicaceae ancestral Tic40, BolC9.Tic40had a gain-of-function variation. The six possible variation sites related to function differences exits in the TPR and Hop domains, resulting in BolC9. Tic40and its derivative BnaC9.Tic40gain a new function which can restore the fertility of7365A duo to present of the dominant gene BnRf. And only B. oleracea and its derivatives displayed the possible gain-of-function variation sites. Subsequently, selective pressure analysis explored strong purifying selection of Tic40in the Brassicaceae before the Brassica genus divergence from other genus of the tribe Brassiceae. After divergence of the Brassica genus, the evolutionary clade of BolC9.Tic40displayed distinct positive selection. Furthermore, the six possible variation sites related to function differences had a Bayesian posterior probability greater than90%, and3of6with a probability more than
引文
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