Laboratory of Molecular Biology, Department of Plant Science, Wageningen University, Droevendaalsesteeg 1, 6703PB, Wageningen, The Netherlands.
Department of Ecological Science. Faculty of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1085, 1081HV, Amsterdam, The Netherlands.
BMC Plant Biol. 2022 Apr 30;22(1):225. doi: 10.1186/s12870-022-03606-9.
Nodule symbiosis with diazotrophic Frankia or rhizobium occurs in plant species belonging to ten taxonomic lineages within the related orders Fabales, Fagales, Cucurbitales, and Rosales. Phylogenomic studies indicate that this nitrogen-fixing nodulation trait has a single evolutionary origin. In legume model plants, the molecular interaction between plant and rhizobium microsymbiont is mapped to a significant degree. A specific LysM-type receptor kinase, LjEPR3 in Lotus japonicus and MtLYK10 in Medicago truncatula, was found to act in a secondary identity-based mechanism, controlling intracellular rhizobium infection. Furthermore, LjEPR3 showed to bind surface exopolysaccharides of Mesorhizobium loti, the diazotrophic microsymbiont of L. japonicus. EPR3 orthologous genes are not unique to legumes. Surprisingly, however, its ortholog EXOPOLYSACCHARIDE RECEPTOR (EPR) is pseudogenized in Parasponia, the only lineage of non-legume plants that nodulate also with rhizobium.
Analysis of genome sequences showed that EPR3 orthologous genes are highly conserved in nodulating plants. We identified a conserved retrotransposon insertion in the EPR promoter region in three Parasponia species, which associates with defected transcriptional regulation of this gene. Subsequently, we studied the EPR gene of two Trema species as they represent the sister genus of Parasponia for which it is assumed it lost the nitrogen-fixing nodulation trait. Both Trema species possess apparently functional EPR genes that have a nodulation-specific expression profile when introduced into a Parasponia background. This indicates the EPR gene functioned in nodulation in the Parasponia-Trema ancestor.
We conclude that nodule-specific expression of EPR3 orthologous genes is shared between the legume and Parasponia-Trema lineage, suggesting an ancestral function in the nitrogen-fixing nodulation trait. Pseudogenization of EPR in Parasponia is an exceptional case in nodulating plants. We speculate that this may have been instrumental to the microsymbiont switch -from Frankia to rhizobium- that has occurred in the Parasponia lineage and the evolution of a novel crack entry infection mechanism.
与固氮弗兰克氏菌或根瘤菌共生的结瘤现象发生在属于相关目豆目、壳斗目、葫芦目和蔷薇目的十个分类群的植物物种中。系统基因组学研究表明，这种固氮结瘤特性具有单一的进化起源。在豆科模式植物中，植物与根瘤菌微共生体的分子相互作用在很大程度上被映射到。在豆科植物中，一种特定的 LysM 型受体激酶 LjEPR3 和 Medicago truncatula 中的 MtLYK10 被发现作用于一种基于二次身份的机制中，控制细胞内根瘤菌的感染。此外，LjEPR3 被发现与豆科植物的共生固氮菌 Mesorhizobium loti 的表面胞外多糖结合。EPR3 同源基因不仅存在于豆科植物中。然而，令人惊讶的是，其同源物 EXOPOLYSACCHARIDE RECEPTOR (EPR) 在 Parasponia 中是假基因化的，Parasponia 是唯一与根瘤菌共生的非豆科植物谱系。
对基因组序列的分析表明，EPR3 同源基因在结瘤植物中高度保守。我们在三个 Parasponia 物种的 EPR 启动子区域发现了一个保守的逆转座子插入，这与该基因转录调控的缺陷有关。随后，我们研究了两个 Trema 物种的 EPR 基因，因为它们代表了与 Parasponia 具有姐妹关系的属，据推测，它失去了固氮结瘤特性。这两个 Trema 物种都拥有明显功能的 EPR 基因，当引入 Parasponia 背景时，它们具有结瘤特异性的表达谱。这表明 EPR 基因在 Parasponia-Trema 祖先的结瘤中起作用。
我们的结论是，EPR3 同源基因的结瘤特异性表达在豆科植物和 Parasponia-Trema 谱系中是共有的，这表明其在固氮结瘤特性中有一个祖先功能。EPR 在 Parasponia 中的假基因化是结瘤植物中的一个特殊情况。我们推测，这可能是 Parasponia 谱系中从弗兰克氏菌到根瘤菌的微共生体转变以及一种新的裂缝进入感染机制的进化的关键。
