Cargando…

A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism

A continuum from stem to transit-amplifying to a differentiated cell state is a common theme in multicellular organisms. In the plant root apical meristem (RAM), transit-amplifying cells are organized into two domains: cells from the proliferation domain (PD) are displaced to the transition domain (...

Descripción completa

Detalles Bibliográficos
Autores principales: García-Gómez, Monica L., Reyes-Hernández, Blanca J., Sahoo, Debee P., Napsucialy-Mendivil, Selene, Quintana-Armas, Aranza X., Pedroza-García, José A., Shishkova, Svetlana, Torres-Martínez, Héctor H., Pacheco-Escobedo, Mario A., Dubrovsky, Joseph G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9796171/
https://www.ncbi.nlm.nih.gov/pubmed/36278862
http://dx.doi.org/10.1242/dev.200899
_version_ 1784860421924061184
author García-Gómez, Monica L.
Reyes-Hernández, Blanca J.
Sahoo, Debee P.
Napsucialy-Mendivil, Selene
Quintana-Armas, Aranza X.
Pedroza-García, José A.
Shishkova, Svetlana
Torres-Martínez, Héctor H.
Pacheco-Escobedo, Mario A.
Dubrovsky, Joseph G.
author_facet García-Gómez, Monica L.
Reyes-Hernández, Blanca J.
Sahoo, Debee P.
Napsucialy-Mendivil, Selene
Quintana-Armas, Aranza X.
Pedroza-García, José A.
Shishkova, Svetlana
Torres-Martínez, Héctor H.
Pacheco-Escobedo, Mario A.
Dubrovsky, Joseph G.
author_sort García-Gómez, Monica L.
collection PubMed
description A continuum from stem to transit-amplifying to a differentiated cell state is a common theme in multicellular organisms. In the plant root apical meristem (RAM), transit-amplifying cells are organized into two domains: cells from the proliferation domain (PD) are displaced to the transition domain (TD), suggesting that both domains are necessarily coupled. Here, we show that in the Arabidopsis thaliana mto2-2 mutant, in which threonine (Thr) synthesis is affected, the RAM lacks the PD. Through a combination of cell length profile analysis, mathematical modeling and molecular markers, we establish that the PD and TD can be uncoupled. Remarkably, although the RAM of mto2-2 is represented solely by the TD, the known factors of RAM maintenance and auxin signaling are expressed in the mutant. Mathematical modeling predicts that the stem cell niche depends on Thr metabolism and that, when disturbed, the normal continuum of cell states becomes aborted.
format Online
Article
Text
id pubmed-9796171
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher The Company of Biologists Ltd
record_format MEDLINE/PubMed
spelling pubmed-97961712023-01-17 A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism García-Gómez, Monica L. Reyes-Hernández, Blanca J. Sahoo, Debee P. Napsucialy-Mendivil, Selene Quintana-Armas, Aranza X. Pedroza-García, José A. Shishkova, Svetlana Torres-Martínez, Héctor H. Pacheco-Escobedo, Mario A. Dubrovsky, Joseph G. Development Research Article A continuum from stem to transit-amplifying to a differentiated cell state is a common theme in multicellular organisms. In the plant root apical meristem (RAM), transit-amplifying cells are organized into two domains: cells from the proliferation domain (PD) are displaced to the transition domain (TD), suggesting that both domains are necessarily coupled. Here, we show that in the Arabidopsis thaliana mto2-2 mutant, in which threonine (Thr) synthesis is affected, the RAM lacks the PD. Through a combination of cell length profile analysis, mathematical modeling and molecular markers, we establish that the PD and TD can be uncoupled. Remarkably, although the RAM of mto2-2 is represented solely by the TD, the known factors of RAM maintenance and auxin signaling are expressed in the mutant. Mathematical modeling predicts that the stem cell niche depends on Thr metabolism and that, when disturbed, the normal continuum of cell states becomes aborted. The Company of Biologists Ltd 2022-11-09 /pmc/articles/PMC9796171/ /pubmed/36278862 http://dx.doi.org/10.1242/dev.200899 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
García-Gómez, Monica L.
Reyes-Hernández, Blanca J.
Sahoo, Debee P.
Napsucialy-Mendivil, Selene
Quintana-Armas, Aranza X.
Pedroza-García, José A.
Shishkova, Svetlana
Torres-Martínez, Héctor H.
Pacheco-Escobedo, Mario A.
Dubrovsky, Joseph G.
A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
title A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
title_full A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
title_fullStr A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
title_full_unstemmed A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
title_short A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
title_sort mutation in threonine synthase 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9796171/
https://www.ncbi.nlm.nih.gov/pubmed/36278862
http://dx.doi.org/10.1242/dev.200899
work_keys_str_mv AT garciagomezmonical amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT reyeshernandezblancaj amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT sahoodebeep amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT napsucialymendivilselene amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT quintanaarmasaranzax amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT pedrozagarciajosea amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT shishkovasvetlana amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT torresmartinezhectorh amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT pachecoescobedomarioa amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT dubrovskyjosephg amutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT garciagomezmonical mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT reyeshernandezblancaj mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT sahoodebeep mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT napsucialymendivilselene mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT quintanaarmasaranzax mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT pedrozagarciajosea mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT shishkovasvetlana mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT torresmartinezhectorh mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT pachecoescobedomarioa mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism
AT dubrovskyjosephg mutationinthreoninesynthase1uncouplesproliferationandtransitiondomainsoftherootapicalmeristemexperimentalevidenceandinsilicoproposedmechanism