Pearl Stephanie A, Welch Mark E, McCauley David E
Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA.
Mol Biol Evol. 2009 Mar;26(3):537-45. doi: 10.1093/molbev/msn273. Epub 2008 Nov 24.
It is currently thought that most angiosperms transmit their mitochondrial genomes maternally. Maternal transmission limits opportunities for genetic heterogeneity (heteroplasmy) of the mitochondrial genome within individuals. Recent studies of the gynodioecious species Silene vulgaris and Silene acaulis, however, document both direct and indirect evidence of mitochondrial heteroplasmy, suggesting that the mitochondrial genome is at times transmitted via paternal leakage. This heteroplasmy allows the generation of multi-locus recombinants, as documented in recent studies of both species. A prior study that employed quantitative PCR (q-PCR) on a limited sample provided direct evidence of heteroplasmy in the mitochondrial gene atp1 in S. vulgaris. Here, we apply the q-PCR methods to a much larger sample and extend them to incorporate the study of an additional atp1 haplotype along with two other haplotypes of the mitochondrial gene cox1 to evaluate the origin, extent, and transmission of mitochondrial genome heteroplasmy in S. vulgaris. We first calibrate our q-PCR methods experimentally and then use them to quantify heteroplasmy in 408 S. vulgaris individuals sampled from 22 natural populations located in Virginia, New York, and Tennessee. Sixty-one individuals exhibit heteroplasmy, including five that exhibited the joint heteroplasmy at both loci that is a prerequisite for effective recombination. The heteroplasmic individuals were distributed among 18 of the populations studied, demonstrating that heteroplasmy is a widespread phenomenon in this species. Further, we compare mother and offspring from 71 families to determine the rate of heteroplasmy gained and lost via paternal leakage and vegetative sorting across generations. Of 17 sibships exhibiting cox1 heteroplasmy and 14 sibships exhibiting atp1 heteroplasmy, more than half of the observations of heteroplasmy are generated via paternal leakage at the time of fertilization, with the rest being inherited from a heteroplasmic mother. Moreover, we show that the average paternal contribution during paternal leakage is about 12%. These findings are surprising, given that the current understanding of gynodioecy assumes that mitochondrial cytoplasmic male sterility elements are strictly maternally inherited. Knowledge of the dynamics of mitochondrial populations within individuals plays an important role in understanding the evolution of gynodioecy, and we discuss our findings within this context.
目前认为，大多数被子植物的线粒体基因组是通过母系遗传的。母系遗传限制了个体线粒体内基因组遗传异质性（异质性）的产生机会。然而，最近对雌雄异株物种普通麦瓶草和矮生麦瓶草的研究记录了线粒体异质性的直接和间接证据，表明线粒体基因组有时会通过父系渗漏进行传递。这种异质性使得多位点重组体得以产生，这在最近对这两个物种的研究中都有记录。一项先前的研究对有限的样本进行了定量PCR（q-PCR），提供了普通麦瓶草线粒体基因atp1中异质性的直接证据。在这里，我们将q-PCR方法应用于更大的样本，并将其扩展到纳入对另一种atp1单倍型以及线粒体基因cox1的另外两种单倍型的研究，以评估普通麦瓶草线粒体基因组异质性的起源、程度和传递情况。我们首先通过实验校准我们的q-PCR方法，然后用它们来量化从弗吉尼亚、纽约和田纳西州的22个自然种群中采集的408株普通麦瓶草个体的异质性。61个个体表现出异质性，其中5个个体在两个位点都表现出联合异质性，这是有效重组的先决条件。异质个体分布在所研究的18个种群中，表明异质性在该物种中是一种普遍现象。此外，我们比较了71个家庭的母亲和后代，以确定通过父系渗漏和跨代营养分选获得和丧失异质性的速率。在17个表现出cox1异质性的同胞关系和14个表现出atp1异质性的同胞关系中，超过一半的异质性观察结果是在受精时通过父系渗漏产生的，其余的则是从异质母亲那里遗传而来的。此外，我们表明父系渗漏期间的平均父系贡献约为12%。鉴于目前对雌雄异株的理解假设线粒体细胞质雄性不育元件严格通过母系遗传，这些发现令人惊讶。了解个体线粒体内群体的动态对于理解雌雄异株的进化起着重要作用，我们在此背景下讨论我们的发现。
