2024, Vol. 48
文章信息
- 许然, 胡梦阳, 丁淑荃, 李西雷, 张云龙. 2024.
- XU Ran, HU Mengyang, DING Shuquan, LI Xilei, ZHANG Yunlong. 2024.
- 贝类线粒体双单亲遗传研究进展
- Research advances in mitochondrial doubly uniparental inheritance in bivalves
- 海洋科学, 48(5): 107-115
- Marine Sciences, 48(5): 107-115.
- http://dx.doi.org/10.11759/hykx20240126002
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文章历史
- 收稿日期：2024-01-26
- 修回日期：2024-03-11
动物界中, 线粒体基本遵循母系遗传规则(strictly maternal inheritance, SMI), 线粒体由母本传递给子代, 这种遗传模式限制了个体内线粒体的遗传差异。然而, 一些双壳贝类的线粒体还存在另一种遗传模式, 即双单亲遗传(doubly uniparental inheritance, DUI), 该现象自首次发现至今已有30多年[1-6]。在DUI的贝类中, 两种遗传差异极大(核苷酸序列差异可高达50%)的F型和M型线粒体DNA(mtDNA)可同时存在一个个体中, 其中F型随着卵子传递, M型随精子传递[1]。后代中雌性个体一般为F同质型, 即性腺和体细胞组织中主要为F型mtDNA; 雄性个体一般为异质型, 同时含有F型和M型mtDNA, M型mtDNA在雄性性腺中占比高达90%, 在体细胞组织中也有少量分布, 然而其在体细胞组织中分布存在较大个体和物种差异[7-9]。生殖细胞中, 卵细胞线粒体只携带F型mtDNA, 而精子线粒体只携带M型mtDNA(图 1)。然而, 在一些特殊情况下, 雄性生殖细胞中存在F型mtDNA, 其与体细胞中标准的F型mtDNA存在一定差异, 通常其蛋白编码区(或部分)为F型mtDNA, 但是其控制区存在M型mtDNA, 这种母系的F型mtDNA入侵雄性的遗传路线并随精子传递给子代的现象被称为“雄性化”(masculinization)。目前该现象主要在贻贝(Mussels)中发现[1, 10-13], “雄性化”现象在其他种类中是否存在仍需更多研究[14]。
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| 图 1 贝类线粒体双单亲遗传模式简图 Fig. 1 Diagram of doubly uniparental inheritance of mitochondria in bivalves 图中橙红色圆圈表示F型mtDNA, 蓝色圆圈表示M型mtDNA, 圆圈上绿色箭头表示转录, 箭头粗细表示转录水平高低。图示以菲律宾蛤仔为例。 |
类似地, F型mtDNA在雌性性腺和体细胞组织及雄性的体细胞组织中转录水平均较高, 尽管M型mtDNA在体细胞组织中也有分布, 然而其在体细胞组织中转录水平较低, 主要在雄性性腺和精子中大量转录[8, 15]。研究发现, DUI贝类北极蛤(Arctica islandica)体细胞中M型mtDNA的转录导致了电子传递链活动的降低[9]。此外, 研究发现F及M型mtDNA在不同组织中的拷贝数与其转录水平不存在显著关联, 这进一步表明DUI贝类存在复杂的线粒体的转录调控机制[16]。
DUI贝类的F型和M型线粒体基因组还存在一些特殊的结构特征, F和M型mtDNA中还存在一段性别特异的ORF(open reading frame)片段(ORFan), 且编码了对应的蛋白产物, 该片段可能与线粒体向后代传递过程中蛋白间的特异性识别有关[17-20]。有些种类, F型和M型mtDNA分化时间较近, 但出现了大量的基因重排[14]。此外, 不少DUI贝类的COX2基因还呈现出特殊的结构变异, 在菲律宾蛤仔中COX2基因在F型线粒体中出现了重复[21, 22], 而在某些淡水蚌类中COX2出现了M型特异的重复[17], 有些DUI贝类中COX2基因内出现了一段特殊的插入片段, 可能为DUI贝类特殊的内含子结构[23, 24]。DUI贝类呈现的多样化的结构变异特征使其成为研究线粒体结构与功能的宝贵材料。
2 分类概述与DUI起源假说贝类线粒体双单亲遗传最早发现于紫贻贝(Mytilus edulis), 目前已在超过100种双壳贝类中发现了该现象[25]。近年来, 又有一些新的DUI贝类被发现, 如雌雄同体的贻贝(Semimytilus algosus)[26]及浅蛤属的3个种类等[14], DUI的数量随着研究的深入仍将会进一步增加。在已知的DUI种类中, 淡水蚌目(Unionida)占比较多, 主要分布在海丽贝科(Hyriidae)、珍珠蚌科(Margaritiferidae)、蚌科(Unionidae)。贻贝目(Mytiloida)、帘蛤目(Venerida)等也有较多分布(图 2)。这种分布差异与DUI的鉴定方式有关, 早期DUI的鉴定主要依靠M型线粒体特异的引物扩增, 而M型线粒体进化速率较快, 很难获得通用引物对其进行扩增。因此在不少种类中利用引物扩增进行DUI的发掘仍有一定困难。
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| 图 2 线粒体双单亲遗传贝类的种类和分布 Fig. 2 Taxonomy and distribution of bivalves with a doubly uniparental inheritance system |
作为动物界中线粒体SMI遗传的唯一例外, DUI的起源一直是线粒体生物学中一个主要的谜。关于DUI是单起源还是多起源目前学术界有两种声音, 单起源派根据DUI在双壳贝类中的分布情况基于最大简约法的原则认为DUI可能起源于双壳贝类的祖先(瓣鳃类), 后来在某些双壳贝类(海扇蛤目(Pectinoida)、牡蛎目(Ostreoida))中丢失[27, 28]; 多起源派则基于F型及M型线粒体基因的系统发生关系认为DUI贝类中F型及M型线粒体基因组为多次、独立的多起源[25, 29, 30]。MAEDA等[30]利用现有的38种DUI物种的线粒体COX1基因建立的系统发生树显示双壳贝类中至少有15次独立起源的F和M型线粒体基因组。
关于DUI系统是如何起源的尚无定论, DUI系统与SMI最显著的不同是DUI贝类中选择压力还可以作用于M型mtDNA, 并且该基因组还可以随精子传递给雄性子代。目前关于DUI起源的主流猜想主要有互不相斥的两种。一种认为DUI特有的雄性传递的线粒体可以允许选择压力作用于M型线粒体基因组从而增加雄性的适应性, 增强精子活性或者受精成功率[3, 31]。然而, 在贻贝中带有“雄性化”F型基因组的精子比原本带有M型线粒体基因组的精子有更好的活力[32-34]。BETTINAZZI等[27]比较SMI和DUI的精子的运动能力和活力时发现, SMI的精子活力比DUI的精子活力更好, 但是DUI贝类精子的运动速度慢且有突出的曲线运动的能力。另一种猜想认为DUI起源于一种自私的遗传元件(selfish genetic element), 该元件入侵了精子的线粒体基因组成功定植并传递给后代的精子[28, 35]。通过对DUI贝类中的ORFan片段进行分子特征分析, 有学者推测该片段可能为DUI贝类独有的自私遗传元件[17-19]。无论是哪一种情况, DUI贝类都展现出了独特的遗传方式和演化历程, 是研究线粒体遗传的极佳材料。
3 双单亲遗传的线粒体与核共调控策略线粒体母系遗传在进化过程中有着诸多优势, 可以将线粒体的有害突变固定在一个谱系内防止有害突变造成的谱系灭绝, 还可以避免因细胞质融合造成的胞质基因冲突[2]。然而, 在DUI贝类中母系遗传和父系遗传的线粒体基因组同时存在于同一生物体中, 这种双重遗传系统可能导致核基因和不同线粒体基因组之间的相互作用或冲突, 即核质冲突。核质冲突可能涉及资源竞争、基因差异表达或与能量生产和细胞功能相关的其他过程, 进而引起物种分化[36]。DUI贝类如何协调核质冲突目前仍不清楚, 解析DUI贝类调控核质冲突的机制对扩充核质冲突理论有重要意义。
氧化磷酸化(oxidative phosphorylation, OXPHOS)过程是大多数动物细胞中受线粒体和核基因共同调控的关键产能过程, 该过程产能占机体总量的90%以上。线粒体与核基因之间的协作调控是维持线粒体稳态的重要基础, 线粒体与核编码的OXPHOS亚基需要处于动态平衡状态从而确保OXPHOS复合物准确装配并行使相应功能, 该过程涉及复杂的信号传导和调控网络[37]。在模式生物中, 一些核编码基因如转录因子TFAM, NRF-1, PGC-1等可以同时参与调控线粒体与核氧化磷酸化过程, 实现线粒体和核基因之间的双向调控[38]。此外, 一些调控方式如转录翻译调控、蛋白降解等也参与共同调控过程[39]。在小鼠和人类一些组织中, VAN等[40]发现核基因编码的OXPHOS基因在转录水平上出现了较强的共表达信号, 且同一个OXPHOS复合物中这种共表达信号更强。BARSHAD等[41]在人类不同组织中检测到线粒体与核编码的OXPHOS基因在转录水平上存在较强的共调控信号。COUVILLION等[42]发现在酵母线粒体的生物发生过程中, 线粒体与核编码的OXPHOS基因在转录水平上并不同步, 但在翻译水平上快速同步调控。然而, 在人类多个细胞系中, 线粒体与核编码的OXPHOS基因在转录水平上呈现了共调控信号, 这种共调控信号在翻译水平上进一步加强, 其中LRPPRC蛋白在翻译水平的共调控中起重要作用[43]。
在贝类中线粒体与核共调控策略的研究则更为滞后, 目前尚未有发现参与线粒体与核共调控的转录因子。然而, 在DUI贝类菲律宾蛤仔中发现其F和M型mtDNA中存在一些高表达的非编码RNA(small mitochondrial highly-transcribed RNAs, smithRNAs), 表现出miRNA类似的功能, 这些smithRNAs可通过RNA干扰的方式影响核基因表达并参与性腺的形成[44-46]。此外, 基因共表达调控显示在双单亲遗传系统的菲律宾蛤仔中, F型与M型mtDNA编码的OXPHOS基因与核编码的OXPHOS基因在转录水平上缺乏共调控信号, 但线粒体基因与核基因编码的OXPHOS基因经历了不同程度的翻译选择(translational selection), 可能在翻译水平存在共调控[15]。DUI贝类独特的线粒体遗传方式是研究线粒体与核基因共调控与核质冲突的理想材料。
4 双单亲性别遗传与性别决定贝类有着复杂的有性生殖方式, 包括功能性的同时雌雄同体(simultaneous hermaphroditism)、顺序性雌雄同体(sequential hermaphroditism)、雌雄异体(gonochorism)等。贝类的性别决定机制目前尚不清楚, 尚未发现雌雄异形的性染色体, 现有研究显示, 贝类的性别决定可能是有多基因控制的, 同时环境变化也可能引起性别转变。有些贝类如菲律宾蛤仔(Ruditapes philippinarum)、牡蛎(Crassostrea gigas)等在养殖环境下其性别在生命周期中可能随着外界条件变化出现转换[47]。对于性别较为稳定的种类(虾夷扇贝(Patinopecten yessoensis)等), 其性别决定类型主要为遗传型性别决定, 对于性别不稳定的种类(牡蛎等), 其性别决定为遗传和环境共同决定[48, 49]。
基于DUI贝类性别特异的线粒体遗传系统, 有学者提出该系统的出现可能有利于雄性/精子的功能, 并与DUI贝类的性别决定有关。目前, 该猜想还存在较大争议, 尚无直接证据显示DUI贝类中线粒体与性别遗传的关联。现有研究显示, 在最早发现DUI现象的贻贝属中, 使用不同母本可以出现性别比例差异极高的后代家系, 包括全雌、雌雄比例1∶1和极端的雄性比例后代, 而使用相同母本不同父本的后代雌雄比例近乎1∶1[50-52]。类似地, GHISELLI等[53]在利用菲律宾蛤仔野生父母本随机交配建立的家系中也发现了极端雌雄比例的家系, 不同家系中雄性比例在8%到83%不等。此外, 研究显示贻贝中精子线粒体在受精卵分裂中的模式在雄性后代和雌性后代中有明显差异, 雄性偏向的家系中精子传递的线粒体在早期细胞分裂中呈现出聚集模式, 而雌性偏向的家系中精子传递的线粒体在早期细胞分裂中呈现分散模式[54]。类似的模式在菲律宾蛤仔(Ruditapes philippinarum)中也被观测到, 然而线粒体在菲律宾蛤仔受精卵中的聚集和分散程度弱于贻贝[55]。在大多数动物中, 精子携带的父系线粒体会被一系列的途径消除, 最近研究发现人类精子无完整的线粒体且缺乏线粒体转录因子TFAM, 此外线粒体在受精前或者受精后通过一系列的途径如自噬、泛素化途径等被降解[56-58]。目前尚不清楚DUI贝类中精子携带的线粒体如何从这条严格的父系线粒体消除路径中实现逃逸。有学者推测DUI贝类M型mtDNA的控制区的短保守序列——精子传递元件(sperm transmission element, STE)可能参与保护DUI贝类父系传递的线粒体从而实现逃逸[59, 60]。此外, XU等[61]通过比较基因组和转录组研究发现, 菲律宾蛤仔雌雄差异的单核苷酸多态性标记(single-nucleotide polymorphism, SNP)所在的基因富集到大量与线粒体功能相关的通路。基于DUI贝类中呈现的线粒体与性别之间的遗传关系, 很多学者分析DUI贝类中性别差异表达基因与性别特异的线粒体传递相关的基因, 并提供了一系列候选基因和通路, 如泛素化基因、DNA甲基转移酶基因等[53, 62, 63]。
胞质基因与核基因互作从而决定物种性别的现象在植物中较为普遍, 最常见的类型是胞质雄性不育(cytoplasmic male sterility, CMS)。在CMS植物中, 有一些线粒体基因可以阻止花粉发育, 而特定的核基因可以与这些线粒体基因互作, 从而使育性恢复[64]。据目前的研究显示, CMS相关的基因主要有2类, 一类是包含部分线粒体基因的嵌合基因, 还有一类是无其他物种中同源基因的新基因[65]。植物线粒体常出现重组、结构变化和水平基因转移等, 因此CMS现象在植物中存在多种不同的机制。DUI贝类与植物的CMS有一些共同点, 主要包括新型的F型和M型的ORFans及ORFan区域附近的线粒体控制区的重组事件, 因此有学者推测DUI贝类的性别决定可能与CMS植物的类似, 由胞质基因和核基因互作决定[66]。然而这一推测还需要更多的实验数据支撑。
5 低氧环境耐受双壳纲(Bivalvia)是一类古老且成功的分类单元, 在漫长的演化历程中适应了多变的栖息和摄食环境, 成功占据海水、淡水和陆地等多种生态环境。双壳贝类的成功很大程度上与其强大的环境耐受能力有关, 如低氧耐受, 研究显示贝类的低氧耐受能力高于鱼类和甲壳类[67]。低氧环境对有氧呼吸的种类来说是一种重要的线粒体应激源, 可导致线粒体损伤、能量代谢异常甚至细胞死亡[68, 69]。很多贝类尤其是潮间带的海水贝类会经历周期性的缺氧-复氧(hypoxia- reoxygenation)的变化过程, 因此这些种类演化出一系列响应措施来应对低氧环境, 包括抑制ATP需求高的生物学功能、上调电子传递链的能力、反向抑制OXPHOS过程、上调线粒体质量控制通路等[68-70]。细胞胞内低氧信号主要通过低氧诱导因子-脯氨酸羟化酶(hypoxia inducible factor-prolyl hydroxylase, HIF-PHD)途径控制, 该途径可以促进细胞对氧气的运输和对低氧的适应[71]。然而, 与哺乳动物在低氧条件下可以通过HIF-α进行糖酵解产能不同, 贝类在持续低氧情况下还可通过调控磷酸烯醇丙酮酸羧激酶(phosphoenolpyruvate carboxykinase, PEPCK)来产能[70, 72]。此外, 研究发现贝类线粒体内膜上有替代氧化酶(alternative oxidase, AOX)蛋白, 可以直接从泛醌接收电子并将氧气还原成水而不涉及细胞色素连接的电子传递链, 这使其在环境波动时限制活性氧(reactive oxygen species, ROS)的释放, 减轻细胞伤害[73, 74]。贝类对低氧的多样化应对策略使其成为研究低氧适应性的理想材料。
低氧会使得OXPHOS速率降低, 导致ATP的产生量减少, 及ROS的大量积累, 而ROS的积累会引发级联反应损伤电子传递链, 加剧ATP的缺失, 最终可能引发线粒体自噬。因此, 如何通过调整OXPHOS和电子传递链过程规避缺氧引发的代谢异常和氧化还原问题是缺氧适应的关键机制之一。TIAN等[75, 76]对低氧耐受能力不同物种的遗传分析发现耐受种类在ETS、OXPHOS和TCA循环过程中的关键基因经历了强烈的正向选择和趋同进化。在SMI贝类中, 精子主要通过OXPHOS来获得后期更持久的活力[77], 而DUI贝类雌雄生殖细胞中拥有两套不同的氧化磷酸化系统, 相比于卵细胞中F型线粒体, M型mtDNA的精细胞呼吸代谢率更低, 磷酸化系统也受到更强的限制, OXPHOS的耦合能力也更低[27]。此外, 研究显示M型线粒体DNA受放松选择(relaxed selection)[30], 这些结果表明DUI贝类精子除了OXPHOS产能外可能还可以依靠其他途径如糖酵解来产生ATP。多产能途径意味着DUI精子在低氧情况下可能有更强的适应性, 然而该推测仍需要更多的结果支撑。DUI贝类独有的两套线粒体OXPHOS基因让其成为研究线粒体生物学和呼吸代谢的理想模型, 对研究生殖细胞能量供给模式有重要参考价值。
6 展望自双单亲遗传首次发现至今已经过30多年的研究, 新发现的DUI贝类的数量也已有100多种, 涵盖双壳贝类的主要科目, 随着高通量测序技术尤其是线粒体测序技术的进步, 我们相信这一数量将进一步增加, DUI起源的面纱将会被慢慢揭开。贝类双单亲遗传现象的发现丰富了母系遗传外的线粒体遗传机制研究, 为线粒体生物学、核质冲突等研究提供了宝贵材料。DUI贝类独有的两套线粒体OXPHOS系统是揭示贝类低氧耐受机制, 线粒体与核OXPHOS互作调控的理想模型。DUI贝类mtDNA所呈现的与性别相关的传递模式和子代的性别比例呈现出与植物雄性不育系高度相似的遗传特征, 如能从分子水平验证这一猜想的正确性, 这将是动物学研究的重大发现。
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