Van Leeuwen Thomas, Vanholme Bartel, Van Pottelberge Steven, Van Nieuwenhuyse Pieter, Nauen Ralf, Tirry Luc, Denholm Ian
Faculty of Bioscience Engineering, Ghent University, Coupure links 653, B9000 Ghent, Belgium.
Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):5980-5. doi: 10.1073/pnas.0802224105. Epub 2008 Apr 11.
Genes encoded by mitochondrial DNA (mtDNA) exist in large numbers per cell but can be selected very rapidly as a result of unequal partitioning of mtDNA between germ cells during embryogenesis. However, empirical studies of this "bottlenecking" effect are rare because of the apparent scarcity of heteroplasmic individuals possessing more than one mtDNA haplotype. Here, we report an example of insecticide resistance in an arthropod pest (Tetranychus urticae) being controlled by mtDNA and on its inheritance in a heteroplasmic mite strain. Resistance to the insecticide bifenazate is highly correlated with remarkable mutations in cytochrome b, a mitochondrially encoded protein in the respiratory pathway. Four sites in the Q(o) site that are absolutely conserved across fungi, protozoa, plants, and animals are mutated in resistant mite strains. Despite the unusual nature of these mutations, resistant mites showed no fitness costs in the absence of insecticide. Partially resistant strains, consisting of heteroplasmic individuals, transmit their resistant and susceptible haplotypes to progeny in highly variable ratios consistent with a sampling bottleneck of approximately 180 copies. Insecticide selection on heteroplasmic individuals favors those carrying resistant haplotypes at a frequency of 60% or more. This combination of factors enables very rapid evolution and accounts for mutations being fixed in most field-collected resistant strains. The results provide a rare insight into non-Mendelian mechanisms of mitochondrial inheritance and evolution, relevant to anticipating and understanding the development of other mitochondrially encoded adaptations in arthropods. They also provide strong evidence of cytochrome b being the target site for bifenazate in spider mites.
线粒体DNA（mtDNA）编码的基因在每个细胞中大量存在，但在胚胎发育过程中，由于生殖细胞间mtDNA分配不均，这些基因可能会被快速筛选。然而，由于明显缺乏拥有不止一种mtDNA单倍型的异质性个体，对这种“瓶颈效应”的实证研究很少见。在此，我们报告了一个节肢动物害虫（二斑叶螨）中由mtDNA控制的抗杀虫剂现象及其在异质性螨株中的遗传情况。对杀虫剂联苯肼酯的抗性与呼吸途径中线粒体编码蛋白细胞色素b的显著突变高度相关。在抗性螨株中，Q(o)位点上在真菌、原生动物、植物和动物中绝对保守的四个位点发生了突变。尽管这些突变性质异常，但在没有杀虫剂的情况下，抗性螨并未表现出适合度代价。由异质性个体组成的部分抗性株系，以与约180个拷贝的抽样瓶颈一致的高度可变比例，将其抗性和敏感单倍型传递给后代。对异质性个体进行杀虫剂选择时，会青睐携带抗性单倍型频率达到60%或更高的个体。这些因素共同作用使得进化非常迅速，并解释了大多数田间采集的抗性株系中突变得以固定的原因。这些结果为线粒体遗传和进化的非孟德尔机制提供了难得的见解，有助于预测和理解节肢动物中其他线粒体编码适应性的发展。它们还为细胞色素b是联苯肼酯在叶螨中的靶位点提供了有力证据。
