title: Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution.
abstract: WUS and WOX5, which are expressed, respectively, in the organizing center (OC) and the quiescent center (QC), are essential for shoot/root apical stem-cell maintenance in flowering plants. However, little is known about how these stem-cell factors evolved their functions in flowering plants. Here, we show that the WUS/WOX5 proteins acquired two distinct capabilities by a two-step functional innovation process in the course of plant evolution. The first-step is the apical stem-cell maintenance activity of WUS/WOX5, which originated in the common ancestor of ferns and seed plants, as evidenced by the interspecies complementation experiments, showing that ectopic expression of fern Ceratopteris richardii WUS-like (CrWUL) surrounding OC/QC, or exclusive OC-/QC-expressed gymnosperms/angiosperms WUS/WOX5 in Arabidopsis wus-1 and wox5-1 mutants, could rescue their phenotypes. The second-step is the intercellular mobility that emerged in the common ancestor of seed plants after divergence from the ferns. Evidence for this includes confocal imaging of GFP fusion proteins, showing that WUS/WOX5 from seed plants, rather than from the fern CrWUL, can migrate into cells adjacent to the OC/QC. Evolutionary analysis showed that the WUS-like gene was duplicated into two copies prior to the divergence of gymnosperms/angiosperms. Then the two gene copies (WUS and WOX5) have undergone similar levels of purifying selection, which is consistent with their conserved functions in angiosperm shoot/root stem-cell maintenance and floral organ formation. Our results highlight the critical roles and the essential prerequisites that the two-step functional innovation of these genes performs and represents in the origin of flowering plants.
authors.affiliation: Institute for Advanced Studies, Wuhan University, Wuhan, China.
authors.forename: Yuzhou
authors.initials: Y
authors.lastname: Zhang
authors.affiliation: Development Center for Science and Technology, Ministry of Agriculture, Beijing, China.
authors.forename: Yue
authors.initials: Y
authors.lastname: Jiao
authors.affiliation: Department of Ecology and Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, China.
authors.forename: Hengwu
authors.initials: H
authors.lastname: Jiao
authors.affiliation: Department of Ecology and Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, China.
authors.forename: Huabin
authors.initials: H
authors.lastname: Zhao
authors.affiliation: Institute for Advanced Studies, Wuhan University, Wuhan, China.|Department of Plant Sciences, College of Life Sciences, Wuhan University, Wuhan, China.
authors.forename: Yu-Xian
authors.initials: YX
authors.lastname: Zhu
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D005075:Biological Evolution; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D055786:Gene Knockout Techniques; D017343:Genes, Plant; D018398:Homeodomain Proteins / Q000235:genetics* / Q000378:metabolism; D018519:Meristem / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D010940:Plant Proteins / Q000235:genetics; D018517:Plant Roots / Q000235:genetics; D019089:Stem Cell Factor / Q000378:metabolism; D013234:Stem Cells / Q000378:metabolism / Q000502:physiology*
chemical_list: D029681:Arabidopsis Proteins; D018398:Homeodomain Proteins; D010940:Plant Proteins; D019089:Stem Cell Factor; C116421:WUSCHEL protein, Arabidopsis
keywords: developmental biology; experimental evolution; plant molecular evolution; plant stem cells.