Discovery of new group I-D introns leads to creation of subtypes and link to an adaptive response of the mitochondrial genome in fungi

Group I catalytic introns are widespread in bacterial, archaeal, viral, organellar, and some eukaryotic genomes, where they are reported to provide regulatory functions. The group I introns are currently divided into five types (A-E), which are themselves distributed into several subtypes, with the exception of group I type D intron (GI-D). GI-D introns belong to the rarest group with only 17 described to date, including only one with a putative role reported in fungi, where it would interfere with an adaptive response in the cytochrome b (COB) gene to quinone outside inhibitor (QoI) fungicide resistance. Using homology search methods taking into account both conserved sequences and RNA secondary structures, we analysed the mitochondrial genomes or COB genes of 169 fungal species, including some frequently under QoI selection pressure. These analyses have led to the identification of 216 novel GI-D introns, and the definition of three distinct subtypes, one of which being linked with a functional activity. We have further uncovered a homing site for this GI-D intron type, which helps refine the accepted model of quinone outside inhibitor resistance, whereby mobility of the intron across fungal mitochondrial genomes, would influence a fungus ability to develop resistance to QoIs.

第I类催化型内含子（Group I catalytic intron）广泛分布于细菌、古菌、病毒、细胞器及部分真核生物基因组中，据报道其可发挥调控功能。目前第I类内含子可分为A至E共5个类型，除第I类D型内含子（group I type D intron, GI-D）外，其余类型均进一步划分为若干亚型。GI-D内含子属于目前已报道数量最少的一类，截至目前仅发现17例，其中仅1例在真菌中被报道具备推定功能：该内含子会干扰细胞色素b（cytochrome b, COB）基因针对醌类体外抑制剂（quinone outside inhibitor, QoI）杀菌剂抗性的适应性应答过程。本研究结合保守序列与RNA二级结构特征，采用同源搜索方法，对169种真菌的线粒体基因组或COB基因开展分析，其中部分真菌长期处于QoI选择压力之下。通过本次分析，本研究共鉴定出216个全新的GI-D内含子，并明确了3个独立亚型，其中一个亚型具备功能活性。本研究还进一步发现了该类GI-D内含子的归巢位点，这一发现有助于完善现有QoI抗性模型——内含子在真菌线粒体基因组中的移动性，会影响真菌获得QoI抗性的能力。