Discovery, utilization and molecular mechanisms of CMS-WA in rice
Discovery, utilization and molecular mechanisms of CMS-WA in rice
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DOI：
10.1360/n972016-01044
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发表时间：
2016-10
影响因子：
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通讯作者：
Letian Chen;Yaoguang Liu
中科院分区：
文献类型：
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作者：
Letian Chen;Yaoguang Liu
野生败育型细胞质雄性不育系（CMS-WA）的发现和利用是杂交水稻杂种优势利用育种的关键问题，也是农业利用野生植物资源最成功的案例。本文回顾了CMS-WA的发现和研究历史，介绍了CMS-WA的分子基础及其修复和相关基因进化的最新研究进展。自1964年以来，中国科学家袁隆平率先研究了水稻雄性不育。20世纪70年代，袁的研究小组发现了一种雄性不育野生稻（Oryza rufipogon Griff）。中国海南岛的野生败育（Wild Abortive（WA））。遗传学研究表明，这种雄性不育是由细胞质赋予的，因此被称为CMS-WA。我国育种工作者通过回交将CMS-WA细胞质导入到许多水稻品种中，培育了大量的不育系。在此基础上，选育出相应的保持系和恢复系，成功地建立了杂交水稻“三系”体系。我国杂交水稻自1976年推广以来，从80年代后期开始，杂交水稻种植面积已占全国水稻种植面积的50%左右，使粮食产量提高了20%-30%。近年来，科学家们在CMS-WA及其恢复的分子研究以及该系统基因的进化方面取得了很大进展。作为该领域的代表，刘耀光等从线粒体基因组中分离到CMS-WA基因WA 352，这是一个由多个功能未知的线粒体基因组片段组成的新基因。WA 352组成型表达为三种转录物，但WA 352蛋白在小孢子母细胞阶段特异性地积累在花药绒毡层细胞中，并直接与细胞色素c氧化酶的组装因子核编码蛋白COX 11相互作用，COX 11也具有抑制活性氧（ROS）和抑制程序性细胞死亡（PCD）的作用。当WA 352通过相互作用阻止COX 11时，ROS的代谢受到影响，导致ROS爆发和细胞色素c释放到细胞质中，并触发绒毡层中的过早PCD。这种绒毡层的异常退化最终导致花粉败育。两个位点，Rf 3和Rf 4，分别定位在第1和第10染色体上，CMS-WA的恢复基因。Rf 4是最近由Liu等人首次克隆的。Rf 4编码一个五肽重复序列（PPR）蛋白（PPR 9 -782-M），具有线粒体转运信号和18个PPR基序，与CMS-BT系统Rf 1a编码的PPR 3 -791-M高度相似。Rf 4蛋白降低WA 352的mRNA水平，从而恢复WA 352介导的雄性不育可能在转录后机制。然而，Rf 3不影响WA 352转录物丰度，但损害WA 352蛋白的产生。因此，研究表明植物CMS/恢复系统在分子水平上包括多层次的细胞质-核基因相互作用。最近，LIU的团队通过鉴定和表征野生稻中与WA 352相关的一些线粒体基因组重组结构，进一步研究了WA 352的进化轨迹。这些结构起源于O.普通猪毛菜该研究揭示了功能性CMS基因通过基于序列变异的功能化以及亚化学计量转换（即，拷贝数变异）。最后，对杂交水稻育种的关键问题和未来发展方向进行了讨论。
The discovery and exploitation of the Wild Abortive type cytoplasmic male sterility (CMS-WA) is a key issue in hybrid rice breeding for utilization of heterosis, which is the best successful case for exploitation of wild plant resources in agriculture. In this review, we traced the history of discovery and research of CMS-WA, and introduced the latest progresses on study of the molecular basis of CMS-WA and its restoration as well as the evolution of the related genes. The Chinese scientist Yuan LongPing pioneered the study of male sterility in rice since 1964. In 1970s, Yuan’s group discovered a male sterile wild rice ( Oryza rufipogon Griff.) plant in Hainan Island of China, and designated this material as “Wild Abortive (WA)”. Genetic study showed that this male sterility is conferred by the cytoplasm, thus is called CMS-WA. Chinese breeders made great efforts to breed CMS lines by introgression of the CMS-WA cytoplasm into a number of rice cultivars via backcrossing. Accordingly, related maintainer lines and restorer lines were bred to successfully develop the “three-line” system for hybrid rice production. The commercial hybrid rice was released in 1976 in China, and has occupied about 50% of the total rice planting area since the late 1980s, which increased grain yield by 20%–30%. In recent years, scientists have made great progress on the molecular studies of CMS-WA and its restoration, and the evolution of the genes for this system. As representative in this field, LIU YaoGuang’s group isolated the CMS-WA gene WA352 from the mitochondrial genome, which is a new gene consisting of multiple mitochondrial genomic segments of unknown function. WA352 is expressed constitutively into three transcripts, but the WA352 protein accumulates specifically in the anther tapetal cells at the microspore mother cell stage, and interacts directly with a nucleus-encoded protein COX11, which is the assembly factor for cytochrome c oxidase and also has a role in scavenge of reactive oxygen species (ROS) and inhibition of programmed cell death (PCD). When WA352 arrests COX11 by the interaction, the metabolism of ROS is affected, leading to ROS burst and cytochrome c release to the cytosol and triggering premature PCD in the tapetum. This abnormal tapetal degeneration eventually causes pollen abortion. Two loci, Rf3 and Rf4 , were mapped on chromosome 1 and 10, respectively, as the restorer genes for CMS-WA. Rf4 was firstly cloned recently by Liu’s group. Rf4 encodes a pentatricopeptide repeat (PPR) protein (PPR9-782-M) possessing a mitochondrial transit signal and 18 PPR motifs, with high similarity to PPR3-791-M encoded by Rf1a of the CMS-BT system. The Rf4 protein decreases the mRNA level of WA352 , thereby restoring WA352 -mediated male sterility probably in a post-transcriptional mechanism. However, Rf3 does not affect the WA352 transcript abundance but impairs the production of WA352 protein. Thus, the studies indicate that plant CMS/restoration systems comprises multiple layers of cytoplasmic-nuclear gene interactions in the molecular level. Recently, LIU’s group further studied the evolutionary trajectory of WA352 by identification and characterization of a number of mitochondrial genomic recombinant structures related to WA352 in the wild rice. These structures originated and evolved through complex evolutionary routes by multiple rearrangements in the mitochondrial genome of O. rufipogon. The study revealed that functional CMS genes originated from non-CMS protogenes by sequence variation-based functionalization as well as substoichiometric shifting (i.e., copy number variation). Finally, this review discussed the key issues and future directions of the hybrid rice breeding programs.