Advances in molecular genetic mechanism of meiotic recombination and applications in crop breeding
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摘要:
减数分裂是真核生物有性生殖产生染色体数目减半的单倍体配子所必需的生命过程。重组是减数分裂的核心事件之一，既增加了同源染色体间遗传信息的交换，又保证了其在减数分裂后期Ⅰ的正确分离。因此，减数分裂重组不仅增加了后代遗传多样性，还是作物遗传育种的基础。通过提高重组频率或改变其分布可以加速农作物育种进程，而降低或抑制重组可以固定杂种优势。近年来对植物减数分裂重组的分子遗传机制的研究取得了很大进展，包括重组的遗传和表观遗传调控机制，重组的遗传操控技术、固定杂交优势和染色体工程等方面。本文针对以上方面进行了全面的总结，这些内容不仅方便了读者对减数分裂重组的理论认知，还拓展了通过调控减数分裂重组操控生物育种的思路。
Abstract:Meiosis is essential for producing haploid gametes during sexual reproduction in most eukaryotes. Homologous recombination is one of the critical events of meiosis prophase I. It not only leads to the reshuffle of genetic information between homologs, but also ensures their proper segregation at anaphase I. Therefore, meiotic recombination is important to facilitate the genetic diversity and evolution among progeny, and also provides the theoretical basis for crop breeding. As expectedly, increasing the frequency of recombination or changing its distribution can benefit crop breeding, while reducing or inhibiting recombination can sustain heterosis. Over the past decades, numerous achievements have been made in understanding and utilizing meiotic recombination in plants, including mechanisms on genetic and epigenetic regulation of meiotic recombination, manipulation technologies on recombination, fixation of heterosis and chromosome engineering. In this review, we summarize the latest findings and technologies for regulating meiotic recombination, which will enable the readers to have an easy access to understand meiotic recombination, and also expand the idea of manipulating breeding through meiotic recombination.
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图 1 植物减数分裂染色体的牵回环–轴模型
减数分裂同源染色体的配对和联会是重组的重要保证。在减数分裂细线期，联会起始于轴向元件ASY1和ASY3在染色体上的加载，和黏连蛋白REC8一起最终形成一个线性的轴结构，使得姐妹染色单体沿着轴形成一个个DNA环。在细线期和偶线期转换时，DNA环会被牵拉到染色体轴上，由SPO11-MTOPVIB复合体介导双链断裂(DSBs)的产生。随后在偶线期，3′单链DNA会在RAD51-DMC1的介导下入侵到同源染色体间，形成D-loop，从而促进同源染色体配对。在粗线期，中央元件ZYP1加载到一对同源染色体轴中间，最终形成联会复合体的完整结构。在此时，大部分的DSB被修复，少量形成了重组中间体的结构。最后在双线期，联会复合体开始分解，同源染色体分离，只留下重组的区域形成交叉(Crossovers)
Figure 1. The model of tethered loop-axis of meiotic chromosomes in plant
The pairing and synapsis of meiotic homologous chromosomes are important for recombination. At leptotene, the synapsis initiates with the loading of axial elements ASY1 and ASY3 on the chromosome, which eventually forms a linear axis structure together with cohesin REC8. Sister chromosomes form DNA loops to array along the axis. During leptotene-diplotene transition, DNA loops are tethered onto the chromosome axis, and double-strand breaks (DSBs) are induced by SPO11-MTOPVIB complex. Subsequently, 3′ single-strand DNA end searches the homologous chromosome by RAD51-DMC1 to form a D-loop, thus promoting homologous chromosome pairing. At pachytene, the central element ZYP1 is loaded onto the centre of a pair of homologous chromosome axes, and finally forms the complete synaptonemal complex (SC) with axial elements. At this point, most DSBs are repaired, and a small amount forms recombination intermediates. At diplotene , following SC disassembly, homologs are separated except where crossovers have formed
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图 2 植物减数分裂重组修复途径模型
减数分裂的重组起始于双链断裂的形成，由SPO11-MTOPVIB复合体介导。双链断裂末端随后被切割处理形成3′单链尾巴。双链断裂修复可以选择以姐妹染色单体为模板，也可以在RAD51-DMC1的帮助下使3′单链末端入侵同源染色体形成置换环结构进行修复，后者形成减数分裂染色体重组。在以同源染色体为模板的修复中，DNA合成，第2链末端捕获和链接最终形成重组中间体的经典结构——双Holliday交叉，并最终解除形成干涉敏感型交换。同时，还存在着重组蛋白MUS81依赖的干涉不敏感型交换，但是目前植物中的重组中间体以及产物不太清楚。此外，在单链入侵后，当第2末端无法捕获时还存在一条合成依赖的链退火途径，最终也以姐妹染色单体为模板进行修复，并会产生非交换。在重组通路中，还存在着3条不同的重组抑制通路：FIGL1-FLIP、FANCM-MHF1/2和RECQ4A/B-TOP3α-RMI1，都参与抑制MUS81依赖的干涉不敏感型交换途径，并促进合成依赖的链退火
Figure 2. The model for meiotic recombination in plant
Meiotic recombination initiates with the formation of DSBs, which are mediated by the SPO11-MTOPVIB complex. DSB ends are cleaved to form 3′ single-strand tails. Subsequently, DSB can be repaired by selecting the sister chromatids as the template. Alternatively, 3′ single-strand ends invade the homolog to form a D-loop for repair, which is known as recombination. Following the repair progress, DNA synthesis, second strand end capture and ligation lead to the formation of double Holliday junctions (dHJs), which are the classical structure of the recombination intermediates and finally resolved as ZMM-dependent interference-sensitive crossovers (Type I COs). Meanwhile, MUS81-dependent pathway results in interference-insensitive crossovers (Type II CO) , but the recombination intermediates and their products in plants are not well understood. In addition, single-strand invasion can be processed by synthesis-dependent strand annealing pathway (SDSA), and chooses the sister chromatids as the template for repair to produce NCO. During meiotic recombination, there are also three different recombination inhibitory pathways, including FIGL1-FLIP, FANCM-MHF1/2 and RECQ4A/ B-Top3α-RMI1, which are involved in the inhibition of MUS81-dependent Type II CO and promote SDSA
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图 3 拟南芥减数分裂重组(CO)热点的基因组/染色质特征和调控模型
减数分裂重组在染色体上不是均匀分布的。通常倾向于发生在常染色质区，并且DSB通常发生于基因的转录起始位点或转录终止位点。重组热区伴随着低核小体密度、H2A.Z和H3K4me3的富集，并且含有AT-rich 和CTT 基序。而在异染色质区通常结构致密，TE和重复序列富集，伴随高非CG甲基化和H3K9me2，这些都是重组的抑制因素。在常染色质区提高减数分裂重组的方法有：突变重组抑制子、过表达重组酶HEI10和突变MET1和DDM1；而在异染色质区提高重组通常通过降低非CG甲基化或H3K9me2，另外还可以通过定向重组的方法提高目标区域重组
Figure 3. The model for regulation of Arabidopsis meiotic crossover hotspots by genomic and chromatin features
The distribution of meiotic recombination events is not uniformly along chromosomes. The crossovers (COs) generally tends to occur in euchromatin regions, and DSBs usually occur in transcription start sites (TSS) or transcription stop sites (TTS). Meiotic recombination hotspots display low nucleosome density, occupancy of H2A.Z and H3K4me3 enrichment with AT-rich and CTT motifs. Heterochromatin is highly compacted with lots of TE and repeat sequences accompanied by high non-CG methylation and H3K9me2, which are the inhibitors of recombination. The approaches for improving meiotic recombination frequency on euchromatin are as follows: Mutating anti-CO genes, overexpressing the recombinase HEI10 or mutating DNA methyltransferases MET1 and remodeler DDM1. Increasing COs on heterochromatin can be achieved by reducing non-CG methylation or H3K9me2, and targeted recombination
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图 4 操纵减数分裂创新作物种质
植物杂交后代具有较亲本优越的表型或适应性称为杂种优势。在有性生殖过程中，F1代杂交植物经历减数分裂染色体重组和分离，导致配子间的等位基因再分配。而后植物双受精使雄配子与雌配子融合，由于减数分裂重组，在F1代中观察到的理想杂种优势性状通常在其后代中丢失。与此相反，无融合生殖依赖于未减数孢子分裂、孤雌生殖和不依赖受精的功能性胚乳的形成。在改良的植物无融合生殖中，通过对有丝分裂代替减数分裂(Mitosis instead of Meiosis, MiMe)和BBM1/MTL基因的遗传操作，分别诱导有丝分裂代替细胞分裂，产生二倍体配子，而后通过孤雌生殖实现种子克隆。克隆种子与F1杂交植株基因一致，可以在后代中保持杂种优势。此外，还可以通过MiMe实现后代多倍化，从而提高后代植物重组频率，整合并增强优良性状
Figure 4. Manipulating meiosis for crop improvement
Heterosis is a phenomenon among progenies of plants, which is known as that hybrid plants can have superior traits compared to their parents. In the process of sexual reproduction, F1 hybrid plants undergo meiotic recombination and chromosome segregation, leading to redistribution of alleles among gametes. Then plant double fertilization is the fusion of male gametes and female gametes. Due to meiotic recombination, the desirable traits observed in F1 hybrid plants are usually lost in their progenies. In contrast, apomixis relies on the apomeiosis, parthenogenesis and autonomous endosperm. In the improved apomixis of plant, MiMe induced by genetic manipulation produces diploid gametes and misexpression of BBM1/MTL in egg cell triggers parthenogenesis, thereby producing the clonal reproduction through seeds. The genome of cloned seeds is consistent with F1 hybrid plants, which can maintain heterosis in the progeny. In addition, diploid gametes can be achieved through MiMe to produce polyploid offspring, which may improve the frequency of recombination and enhance superior traits
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