Wang Gang, Wang Yongyan, Ni Jiacheng, Li Rongrong, Zhu Fengling, Wang Ruyin, Tian Qiuzhen, Shen Qingwen, Yang Qinghua, Tang Jihua, Murcha Monika W, Wang Guifeng
School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China.
National Key Laboratory of Wheat and Maize Crops Science, CIMMYT--China Joint Center of Wheat and Maize, Center for Crop Genome Engineering, College of Agronomy, Henan Agricultural University, Zhengzhou 450046, China.
Mol Plant. 2022 Sep 5;15(9):1470-1487. doi: 10.1016/j.molp.2022.08.001. Epub 2022 Aug 11.
During adaptive radiation, mitochondria have co-evolved with their hosts, leading to gain or loss of subunits and assembly factors of respiratory complexes. Plant mitochondrial complex I harbors ∼40 nuclear- and 9 mitochondrial-encoded subunits, and is formed by stepwise assembly during which different intermediates are integrated via various assembly factors. In mammals, the mitochondrial complex I intermediate assembly (MCIA) complex is required for building the membrane arm module. However, plants have lost almost all of the MCIA complex components, giving rise to the hypothesis that plants follow an ancestral pathway to assemble the membrane arm subunits. Here, we characterize a maize crumpled seed mutant, crk1, and reveal by map-based cloning that CRK1 encodes an ortholog of human complex I assembly factor 1, zNDUFAF1, the only evolutionarily conserved MCIA subunit in plants. zNDUFAF1 is localized in the mitochondria and accumulates in two intermediate complexes that contain complex I membrane arm subunits. Disruption of zNDUFAF1 results in severe defects in complex I assembly and activity, a cellular bioenergetic shift to aerobic glycolysis, and mitochondrial vacuolation. Moreover, we found that zNDUFAF1, the putative mitochondrial import inner membrane translocase ZmTIM17-1, and the isovaleryl-coenzyme A dehydrogenase ZmIVD1 interact each other, and could be co-precipitated from the mitochondria and co-migrate in the same assembly intermediates. Knockout of either ZmTIM17-1 or ZmIVD1 could lead to the significantly reduced complex I stability and activity as well as defective seeds. These results suggest that zNDUFAF1, ZmTIM17-1 and ZmIVD1 probably form an MCIA-like complex that is essential for the biogenesis of mitochondrial complex I and seed development in maize. Our findings also imply that plants and mammals recruit MCIA subunits independently for mitochondrial complex I assembly, highlighting the importance of parallel evolution in mitochondria adaptation to their hosts.
在适应性辐射过程中，线粒体与其宿主共同进化，导致呼吸复合体的亚基和组装因子的获得或丧失。植物线粒体复合体I含有约40个核编码亚基和9个线粒体编码亚基，通过逐步组装形成，在此过程中不同的中间体通过各种组装因子整合。在哺乳动物中，线粒体复合体I中间组装（MCIA）复合体是构建膜臂模块所必需的。然而，植物几乎失去了所有的MCIA复合体成分，由此产生了一种假说，即植物遵循祖先的途径来组装膜臂亚基。在这里，我们对一个玉米皱缩种子突变体crk1进行了表征，并通过图位克隆揭示CRK1编码人类复合体I组装因子1的直系同源物zNDUFAF1，它是植物中唯一进化保守的MCIA亚基。zNDUFAF1定位于线粒体中，并在两个包含复合体I膜臂亚基的中间复合体中积累。zNDUFAF1的破坏导致复合体I组装和活性的严重缺陷，细胞生物能量向有氧糖酵解转变，以及线粒体空泡化。此外，我们发现zNDUFAF1、假定的线粒体输入内膜转位酶ZmTIM17-1和异戊酰辅酶A脱氢酶ZmIVD1相互作用，并且可以从线粒体中共同沉淀出来，并在相同的组装中间体中共同迁移。敲除ZmTIM17-1或ZmIVD1都会导致复合体I稳定性和活性显著降低以及种子缺陷。这些结果表明，zNDUFAF1、ZmTIM17-1和ZmIVD1可能形成一个类似MCIA的复合体，这对玉米线粒体复合体I的生物发生和种子发育至关重要。我们的发现还意味着植物和哺乳动物独立招募MCIA亚基用于线粒体复合体I的组装
