Lin Xiaofei, Li Ningning, Kudo Hiromi, Zhang Zhe, Li Jinyu, Wang Li, Zhang Wenbo, Takechi Katsuaki, Takano Hiroyoshi
College of Life Sciences, Inner Mongolia University, Hohhot 010021, China.
Graduate School of Science and Technology, Kumamoto University, Kumamoto, 860-8555 Japan.
Plant Cell Physiol. 2017 Mar 1;58(3):587-597. doi: 10.1093/pcp/pcx005.
The endosymbiotic theory states that plastids are derived from a single cyanobacterial ancestor that possessed a cell wall. Peptidoglycan (PG), the main component of the bacteria cell wall, gradually degraded during plastid evolution. PG-synthesizing Mur genes have been found to be retained in the genomes of basal streptophyte plants, although many of them have been lost from the genomes of angiosperms. The enzyme encoded by bacterial MurE genes catalyzes the formation of the UDP-N-acetylmuramic acid (UDP-MurNAc) tripeptide in bacterial PG biosynthesis. Knockout of the MurE gene in the moss Physcomitrella patens resulted in defects of chloroplast division, whereas T-DNA-tagged mutants of Arabidopsis thaliana for MurE revealed inhibition of chloroplast development but not of plastid division, suggesting that AtMurE is functionally divergent from the bacterial and moss MurE proteins. Here, we could identify 10 homologs of bacterial Mur genes, including MurE, in the recently sequenced genomes of Picea abies and Pinus taeda, suggesting the retention of the plastid PG system in gymnosperms. To investigate the function of gymnosperm MurE, we isolated an ortholog of MurE from the larch, Larix gmelinii (LgMurE) and confirmed its presence as a single copy per genome, as well as its abundant expression in the leaves of larch seedlings. Analysis with a fusion protein combining green fluorescent protein and LgMurE suggested that it localizes in chloroplasts. Cross-species complementation assay with MurE mutants of A. thaliana and P. patens showed that the expression of LgMurE cDNA completely rescued the albefaction defects in A. thaliana but did not rescue the macrochloroplast phenotype in P. patens. The evolution of plastid PG and the mechanism behind the functional divergence of MurE genes are discussed in the context of information about plant genomes at different evolutionary stages.
内共生理论认为，质体起源于一个具有细胞壁的单一蓝细菌祖先。肽聚糖（PG）作为细菌细胞壁的主要成分，在质体进化过程中逐渐降解。尽管被子植物基因组中许多参与PG合成的Mur基因已经丢失，但在基部链型植物基因组中仍保留着这些基因。细菌MurE基因编码的酶在细菌PG生物合成中催化UDP-N-乙酰胞壁酸（UDP-MurNAc）三肽的形成。苔藓小立碗藓中MurE基因的敲除导致叶绿体分裂缺陷，而拟南芥中MurE基因的T-DNA标签突变体显示叶绿体发育受到抑制，但质体分裂未受影响，这表明拟南芥AtMurE在功能上与细菌和苔藓的MurE蛋白不同。在这里，我们在最近测序的欧洲云杉和火炬松基因组中鉴定出包括MurE在内的10个细菌Mur基因的同源物，这表明裸子植物中保留了质体PG系统。为了研究裸子植物MurE的功能，我们从落叶松中分离出MurE的一个直系同源基因（LgMurE），并证实其在每个基因组中以单拷贝形式存在，且在落叶松幼苗叶片中大量表达。对绿色荧光蛋白与LgMurE融合蛋白的分析表明，它定位于叶绿体中。用拟南芥和小立碗藓的MurE突变体进行的跨物种互补试验表明，LgMurE cDNA的表达完全挽救了拟南芥的白化缺陷，但没有挽救小立碗藓的大叶绿体表型。本文结合不同进化阶段植物基因组的信息，讨论了质体PG的进化以及MurE基因功能分化背后的机制。
