Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, 611-0011 Japan.
Laboratoire Physiologie Cellulaire & Vegetale, University of Grenoble Alpes, IRIG, INRA, CNRS, CEA, F-38054, Grenoble 9, France.
Plant Cell Physiol. 2022 May 16;63(5):635-648. doi: 10.1093/pcp/pcac025.
Phosphatidylinositol 4-phosphate 5-kinase (PIP5K) is involved in regulating various cellular processes through the signaling function of its product, phosphatidylinositol (4,5)-bisphosphate. Higher plants encode a large number of PIP5Ks forming distinct clades in their molecular phylogenetic tree. Although biological functions of PIP5K genes have been analyzed intensively in Arabidopsis thaliana, it remains unclear how those functions differ across clades of paralogs. We performed comparative functional analysis of the Arabidopsis genes encoding PIP5K1, PIP5K2 and PIP5K3, of which the first two and the last belong to closely related but distinct clades, to clarify their conserved and/or differentiated functions. Genetic analysis with their single and multiple mutants revealed that PIP5K1 and PIP5K3 have non-overlapping functions, with the former in total plant growth and the latter in root hair elongation, whereas PIP5K2 redundantly functions in both phenomena. This pattern of functional redundancy is explainable in terms of the overlapping pattern of their promoter activities. In transformation rescue experiments, PIP5K3 promoter-directed PIP5K1-YFP completely rescued the short-root-hair phenotype of pip5k3. However, PIP5K3-YFP could substitute for PIP5K1-YFP only partially in rescuing the severe dwarfism of pip5k1pip5k2 when directed by the PIP5K1 promoter. Phylogenetic analysis of angiosperm PIP5Ks revealed that PIP5K3 orthologs have a faster rate of diversification in their amino-acid sequences compared with PIP5K1/2 orthologs after they arose through a eudicot-specific duplication event. These findings suggest that PIP5K3 specialized to promote root hair elongation and lost some of the protein-encoded functions retained by PIP5K1 and PIP5K2, whereas PIP5K1 differentiated from PIP5K2 only in its promoter-directed expression pattern.
磷脂酰肌醇 4-磷酸 5-激酶 (PIP5K) 通过其产物磷脂酰肌醇 (4,5)-二磷酸的信号功能参与调节各种细胞过程。高等植物编码大量的 PIP5K，在其分子系统发育树中形成不同的分支。虽然已经在拟南芥中对 PIP5K 基因的生物学功能进行了深入分析，但不同分支的旁系同源物的功能差异仍不清楚。我们对编码 PIP5K1、PIP5K2 和 PIP5K3 的拟南芥基因进行了比较功能分析，其中前两个和最后一个属于密切相关但不同的分支，以阐明它们的保守和/或分化功能。对其单个和多个突变体的遗传分析表明，PIP5K1 和 PIP5K3 具有非重叠的功能，前者在整个植物生长中起作用，后者在根毛伸长中起作用，而 PIP5K2 在这两种现象中冗余起作用。这种功能冗余模式可以用它们启动子活性的重叠模式来解释。在转化拯救实验中，PIP5K3 启动子指导的 PIP5K1-YFP 完全拯救了 pip5k3 的短根毛表型。然而，当由 PIP5K1 启动子时，PIP5K3-YFP 只能部分替代 PIP5K1-YFP 来拯救 pip5k1pip5k2 的严重矮化。被子植物 PIP5K 的系统发育分析表明，PIP5K3 直系同源物在其氨基酸序列中的多样化速度比 PIP5K1/2 直系同源物快，因为它们是在一个被子植物特异性的重复事件后产生的。这些发现表明，PIP5K3 特化促进根毛伸长，并失去了 PIP5K1 和 PIP5K2 保留的一些蛋白质编码功能，而 PIP5K1 仅在其启动子指导的表达模式上从 PIP5K2 分化出来。
