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...
Guardado en:
Autores principales: | , , , , , , , , |
---|---|
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 |