EARLY NODULIN 93 (ENOD93) has been genetically associated with biological nitrogen fixation in legumes and nitrogen use efficiency in cereals, but its precise function is unknown. We show that hidden Markov models define ENOD93 as a homolog of the N-terminal domain of RESPIRATORY SUPERCOMPLEX FACTOR 2 (RCF2). RCF2 regulates cytochrome oxidase (CIV), influencing the generation of a mitochondrial proton motive force in yeast (Saccharomyces cerevisiae). Knockout of ENOD93 in Arabidopsis (Arabidopsis thaliana) causes a short root phenotype and early flowering. ENOD93 is associated with a protein complex the size of CIV in mitochondria, but neither CIV abundance nor its activity changed in ruptured organelles of enod93. However, a progressive loss of ADP-dependent respiration rate was observed in intact enod93 mitochondria, which could be recovered in complemented lines. Mitochondrial membrane potential was higher in enod93 in a CIV-dependent manner, but ATP synthesis and ADP depletion rates progressively decreased. The respiration rate of whole enod93 seedlings was elevated, and root ADP content was nearly double that in wild type without a change in ATP content. We propose that ENOD93 and HYPOXIA-INDUCED GENE DOMAIN 2 (HIGD2) are the functional equivalent of yeast RCF2 but have remained undiscovered in many eukaryotic lineages because they are encoded by 2 distinct genes.

中文翻译：

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EARLY NODULIN93 通过细胞色素 c 氧化酶改变植物呼吸 ATP 的产生和根系生长


早期根瘤蛋白 93 （ENOD93） 在遗传上与豆科植物中的生物固氮和谷物中的氮利用效率有关，但其确切功能尚不清楚。我们表明，隐马尔可夫模型将 ENOD93 定义为呼吸超复杂因子 2 （RCF2） 的 N 末端结构域的同源物。RCF2 调节细胞色素氧化酶 （CIV），影响酵母 （酿酒酵母） 中线粒体质子驱动力的产生。拟南芥 （Arabidopsis thaliana） 中 ENOD93 的敲除导致根表型短和早开花。ENOD93 与线粒体中 CIV 大小的蛋白质复合物相关，但在 enod93 破裂的细胞器中，CIV 丰度及其活性都没有变化。然而，在完整的 enod93 线粒体中观察到 ADP 依赖性呼吸率的进行性丧失，这可以在互补系中恢复。enod93 的线粒体膜电位以 CIV 依赖性方式较高，但 ATP 合成和 ADP 耗竭率逐渐降低。全 enod93 幼苗的呼吸速率升高，根 ADP 含量几乎是野生型的两倍，而 ATP 含量没有变化。我们提出 ENOD93 和缺氧诱导的基因结构域 2 （HIGD2） 是酵母 RCF2 的功能等价物，但在许多真核生物谱系中仍未被发现，因为它们由 2 个不同的基因编码。