An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.

In plants, the effective mobilization of seed nutrient reserves is crucial during germination and for seedling establishment. The Arabidopsis H+-PPase-loss-of-function fugu5 mutants exhibit a reduced number of cells in the cotyledons. This leads to enhanced post-mitotic cell expansion, also known as...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Hiromitsu Tabeta, Shunsuke Watanabe, Keita Fukuda, Shizuka Gunji, Mariko Asaoka, Masami Yokota Hirai, Mitsunori Seo, Hirokazu Tsukaya, Ali Ferjani
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2021
Materias:
Acceso en línea:https://doaj.org/article/ab3bfa8490d0447380fbbf166fcef9b5
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:ab3bfa8490d0447380fbbf166fcef9b5
record_format dspace
spelling oai:doaj.org-article:ab3bfa8490d0447380fbbf166fcef9b52021-12-02T20:03:24ZAn auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.1553-73901553-740410.1371/journal.pgen.1009674https://doaj.org/article/ab3bfa8490d0447380fbbf166fcef9b52021-08-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009674https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404In plants, the effective mobilization of seed nutrient reserves is crucial during germination and for seedling establishment. The Arabidopsis H+-PPase-loss-of-function fugu5 mutants exhibit a reduced number of cells in the cotyledons. This leads to enhanced post-mitotic cell expansion, also known as compensated cell enlargement (CCE). While decreased cell numbers have been ascribed to reduced gluconeogenesis from triacylglycerol, the molecular mechanisms underlying CCE remain ill-known. Given the role of indole 3-butyric acid (IBA) in cotyledon development, and because CCE in fugu5 is specifically and completely cancelled by ech2, which shows defective IBA-to-indoleacetic acid (IAA) conversion, IBA has emerged as a potential regulator of CCE. Here, to further illuminate the regulatory role of IBA in CCE, we used a series of high-order mutants that harbored a specific defect in IBA-to-IAA conversion, IBA efflux, IAA signaling, or vacuolar type H+-ATPase (V-ATPase) activity and analyzed the genetic interaction with fugu5-1. We found that while CCE in fugu5 was promoted by IBA, defects in IBA-to-IAA conversion, IAA response, or the V-ATPase activity alone cancelled CCE. Consistently, endogenous IAA in fugu5 reached a level 2.2-fold higher than the WT in 1-week-old seedlings. Finally, the above findings were validated in icl-2, mls-2, pck1-2 and ibr10 mutants, in which CCE was triggered by low sugar contents. This provides a scenario in which following seed germination, the low-sugar-state triggers IAA synthesis, leading to CCE through the activation of the V-ATPase. These findings illustrate how fine-tuning cell and organ size regulation depend on interplays between metabolism and IAA levels in plants.Hiromitsu TabetaShunsuke WatanabeKeita FukudaShizuka GunjiMariko AsaokaMasami Yokota HiraiMitsunori SeoHirokazu TsukayaAli FerjaniPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 8, p e1009674 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Hiromitsu Tabeta
Shunsuke Watanabe
Keita Fukuda
Shizuka Gunji
Mariko Asaoka
Masami Yokota Hirai
Mitsunori Seo
Hirokazu Tsukaya
Ali Ferjani
An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
description In plants, the effective mobilization of seed nutrient reserves is crucial during germination and for seedling establishment. The Arabidopsis H+-PPase-loss-of-function fugu5 mutants exhibit a reduced number of cells in the cotyledons. This leads to enhanced post-mitotic cell expansion, also known as compensated cell enlargement (CCE). While decreased cell numbers have been ascribed to reduced gluconeogenesis from triacylglycerol, the molecular mechanisms underlying CCE remain ill-known. Given the role of indole 3-butyric acid (IBA) in cotyledon development, and because CCE in fugu5 is specifically and completely cancelled by ech2, which shows defective IBA-to-indoleacetic acid (IAA) conversion, IBA has emerged as a potential regulator of CCE. Here, to further illuminate the regulatory role of IBA in CCE, we used a series of high-order mutants that harbored a specific defect in IBA-to-IAA conversion, IBA efflux, IAA signaling, or vacuolar type H+-ATPase (V-ATPase) activity and analyzed the genetic interaction with fugu5-1. We found that while CCE in fugu5 was promoted by IBA, defects in IBA-to-IAA conversion, IAA response, or the V-ATPase activity alone cancelled CCE. Consistently, endogenous IAA in fugu5 reached a level 2.2-fold higher than the WT in 1-week-old seedlings. Finally, the above findings were validated in icl-2, mls-2, pck1-2 and ibr10 mutants, in which CCE was triggered by low sugar contents. This provides a scenario in which following seed germination, the low-sugar-state triggers IAA synthesis, leading to CCE through the activation of the V-ATPase. These findings illustrate how fine-tuning cell and organ size regulation depend on interplays between metabolism and IAA levels in plants.
format article
author Hiromitsu Tabeta
Shunsuke Watanabe
Keita Fukuda
Shizuka Gunji
Mariko Asaoka
Masami Yokota Hirai
Mitsunori Seo
Hirokazu Tsukaya
Ali Ferjani
author_facet Hiromitsu Tabeta
Shunsuke Watanabe
Keita Fukuda
Shizuka Gunji
Mariko Asaoka
Masami Yokota Hirai
Mitsunori Seo
Hirokazu Tsukaya
Ali Ferjani
author_sort Hiromitsu Tabeta
title An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
title_short An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
title_full An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
title_fullStr An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
title_full_unstemmed An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
title_sort auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/ab3bfa8490d0447380fbbf166fcef9b5
work_keys_str_mv AT hiromitsutabeta anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT shunsukewatanabe anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT keitafukuda anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT shizukagunji anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT marikoasaoka anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT masamiyokotahirai anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT mitsunoriseo anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT hirokazutsukaya anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT aliferjani anauxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT hiromitsutabeta auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT shunsukewatanabe auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT keitafukuda auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT shizukagunji auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT marikoasaoka auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT masamiyokotahirai auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT mitsunoriseo auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT hirokazutsukaya auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
AT aliferjani auxinsignalingnetworktranslateslowsugarstateinputintocompensatedcellenlargementinthefugu5cotyledon
_version_ 1718375678657691648