Evolution of plastid FAX (fatty acid export) proteins and the plants' conquest of land - molecular and metabolic adaptation

淡水藻类后代对土地的殖民是地球历史上的一个分水岭时刻。植物在征服这片土地的过程中遇到了许多环境挑战，如干燥、高强度光照、紫外线辐射、养分缺乏、机械破坏和病原体感染。因此，在祖先从早期的链藻进化到今天的种子植物的过程中，代谢和形态发生了连续的适应。在陆地植物代谢对陆地环境的多种调节中，脂质的生物合成、分布和动态平衡的变化是应对应激生活的关键步骤。在模式生物拟南芥(种子植物)和衣藻(绿藻)中，叶绿体内膜中FAX(脂肪酸输出)蛋白的脂肪酸运输功能在正常和胁迫条件下对细胞脂平衡至关重要。然而，与植物陆地化第一步相关的生物体中的传真蛋白却一无所知。为了缩小这一差距，并评估FAX蛋白进化对陆地生物新陈代谢的调节，我们的目标是精确定位叶绿体FAX蛋白在苔藓植物中的分子适应，即在苔藓植物中。随着在叶绿体FAX的N-末端出现显著的载脂蛋白α-螺旋束的出现，我们已经可以确定一个关键的分子元件。有趣的是，FAX的载脂蛋白结构域被预测为连接叶绿体内膜和外膜的脂肪酸和脂类运输的桥梁。此外，该结构域可能在磷酸盐饥饿胁迫下介导叶绿体-线粒体的接触以进行脂质交换。在这项研究项目中，我们现在的目标是确定准确的膜拓扑结构，异源低聚复合体的形成以及apoFAX和FAX蛋白在植物中的功能。人们关注的焦点是脂肪代谢在应对冷应激和矿物质缺乏(即磷和钾饥饿)方面的适应作用。

The colonization of land by descendants of freshwater algae was a watershed moment in earths’ history. Plants encountered many environmental challenges during the conquest of the land, such as desiccation, high intensity light, UV-radiation, lack of nutrient availability, mechanical damage, and pathogen infections. In consequence, a consecutive adaptation of metabolism and morphology took place during evolution of ancestors from early Streptophyte algae to todays seed plants. Among these versatile adjustments of land plant metabolism to terrestrial environments, changes in biosynthesis, distribution and homeostasis of lipids represent crucial steps to cope with stressful life. Fatty acid transport function of FAX (fatty acid export) proteins in the inner envelope membrane of chloroplasts has been shown to be crucial for cellular lipid homeostasis under normal and stress conditions such as cold acclimation in the model organisms Arabidopsis thaliana (seed plant) and Chlamydomonas reinhardtii (green micro alga). However, nothing is known about FAX proteins in the organisms relevant for first steps in plant terrestrialization. In order to close this gap and evaluate FAX protein evolution towards adjustment of metabolism to life on land, we aim to pinpoint molecular adaptation of plastid FAX proteins in bryophytes, i.e. in Physcomitrium patens and Marchantia polymorpha. With the emergence of the prominent apo-lipoprotein α-helix bundle at the N-terminus of plastid FAX that is conserved throughout evolution of monophyletic Phragmoplastophyta, we could already identify a crucial molecular element. Interestingly, the FAX apo domain is predicted to bridge the inner and outer envelope membrane of chloroplasts for fatty acid and lipid transport. Moreover, this domain is likely to mediate chloroplast-mitochondrium contacts for lipid exchange at phosphate starvation stress. Within the research project, we now aim to identify exact membrane topology, formation of hetero-oligomeric complexes as well as in planta function of apoFAX and FAX proteins in Physcomitrium patens and Marchantia polymorpha. In the spotlight is the role in adaptation of lipid metabolism in response to cold stress and mineral deficiency, namely phosphate and potassium starvation.