Cargando…

Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution

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, w...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Yuzhou, Jiao, Yue, Jiao, Hengwu, Zhao, Huabin, Zhu, Yu-Xian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5400392/
https://www.ncbi.nlm.nih.gov/pubmed/28053005
http://dx.doi.org/10.1093/molbev/msw263
_version_ 1783230827322146816
author Zhang, Yuzhou
Jiao, Yue
Jiao, Hengwu
Zhao, Huabin
Zhu, Yu-Xian
author_facet Zhang, Yuzhou
Jiao, Yue
Jiao, Hengwu
Zhao, Huabin
Zhu, Yu-Xian
author_sort Zhang, Yuzhou
collection PubMed
description 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.
format Online
Article
Text
id pubmed-5400392
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-54003922017-04-28 Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution Zhang, Yuzhou Jiao, Yue Jiao, Hengwu Zhao, Huabin Zhu, Yu-Xian Mol Biol Evol Discoveries 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. Oxford University Press 2017-03 2016-12-24 /pmc/articles/PMC5400392/ /pubmed/28053005 http://dx.doi.org/10.1093/molbev/msw263 Text en © The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Zhang, Yuzhou
Jiao, Yue
Jiao, Hengwu
Zhao, Huabin
Zhu, Yu-Xian
Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution
title Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution
title_full Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution
title_fullStr Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution
title_full_unstemmed Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution
title_short Two-Step Functional Innovation of the Stem-Cell Factors WUS/WOX5 during Plant Evolution
title_sort two-step functional innovation of the stem-cell factors wus/wox5 during plant evolution
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5400392/
https://www.ncbi.nlm.nih.gov/pubmed/28053005
http://dx.doi.org/10.1093/molbev/msw263
work_keys_str_mv AT zhangyuzhou twostepfunctionalinnovationofthestemcellfactorswuswox5duringplantevolution
AT jiaoyue twostepfunctionalinnovationofthestemcellfactorswuswox5duringplantevolution
AT jiaohengwu twostepfunctionalinnovationofthestemcellfactorswuswox5duringplantevolution
AT zhaohuabin twostepfunctionalinnovationofthestemcellfactorswuswox5duringplantevolution
AT zhuyuxian twostepfunctionalinnovationofthestemcellfactorswuswox5duringplantevolution