Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.

In cucumber seedlings, gravitropism interferes with hydrotropism, which results in the nearly complete inhibition of hydrotropism under stationary conditions. However, hydrotropic responses are induced when the gravitropic response in the root is nullified by clinorotation. Columella cells in the ro...

Full description

Bibliographic Details
Main Authors: Nobuharu Fujii, Sachiko Miyabayashi, Tomoki Sugita, Akie Kobayashi, Chiaki Yamazaki, Yutaka Miyazawa, Motoshi Kamada, Haruo Kasahara, Ikuko Osada, Toru Shimazu, Yasuo Fusejima, Akira Higashibata, Takashi Yamazaki, Noriaki Ishioka, Hideyuki Takahashi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC5764274?pdf=render
_version_ 1819062674064932864
author Nobuharu Fujii
Sachiko Miyabayashi
Tomoki Sugita
Akie Kobayashi
Chiaki Yamazaki
Yutaka Miyazawa
Motoshi Kamada
Haruo Kasahara
Ikuko Osada
Toru Shimazu
Yasuo Fusejima
Akira Higashibata
Takashi Yamazaki
Noriaki Ishioka
Hideyuki Takahashi
author_facet Nobuharu Fujii
Sachiko Miyabayashi
Tomoki Sugita
Akie Kobayashi
Chiaki Yamazaki
Yutaka Miyazawa
Motoshi Kamada
Haruo Kasahara
Ikuko Osada
Toru Shimazu
Yasuo Fusejima
Akira Higashibata
Takashi Yamazaki
Noriaki Ishioka
Hideyuki Takahashi
author_sort Nobuharu Fujii
collection DOAJ
description In cucumber seedlings, gravitropism interferes with hydrotropism, which results in the nearly complete inhibition of hydrotropism under stationary conditions. However, hydrotropic responses are induced when the gravitropic response in the root is nullified by clinorotation. Columella cells in the root cap sense gravity, which induces the gravitropic response. In this study, we found that removing the root tip induced hydrotropism in cucumber roots under stationary conditions. The application of auxin transport inhibitors to cucumber seedlings under stationary conditions suppressed the hydrotropic response induced by the removal of the root tip. To investigate the expression of genes related to hydrotropism in de-tipped cucumber roots, we conducted transcriptome analysis of gene expression by RNA-Seq using seedlings exhibiting hydrotropic and gravitropic responses. Of the 21 and 45 genes asymmetrically expressed during hydrotropic and gravitropic responses, respectively, five genes were identical. Gene ontology (GO) analysis indicated that the category auxin-inducible genes was significantly enriched among genes that were more highly expressed in the concave side of the root than the convex side during hydrotropic or gravitropic responses. Reverse transcription followed by quantitative polymerase chain reaction (RT-qPCR) analysis revealed that root hydrotropism induced under stationary conditions (by removing the root tip) was accompanied by the asymmetric expression of several auxin-inducible genes. However, intact roots did not exhibit the asymmetric expression patterns of auxin-inducible genes under stationary conditions, even in the presence of a moisture gradient. These results suggest that the root tip inhibits hydrotropism by suppressing the induction of asymmetric auxin distribution. Auxin transport and distribution not mediated by the root tip might play a role in hydrotropism in cucumber roots.
first_indexed 2024-12-21T15:02:32Z
format Article
id doaj.art-7f2ab9aa2f84422b9a379b9fa7531a91
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-21T15:02:32Z
publishDate 2018-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-7f2ab9aa2f84422b9a379b9fa7531a912022-12-21T18:59:33ZengPublic Library of Science (PLoS)PLoS ONE1932-62032018-01-01131e018982710.1371/journal.pone.0189827Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.Nobuharu FujiiSachiko MiyabayashiTomoki SugitaAkie KobayashiChiaki YamazakiYutaka MiyazawaMotoshi KamadaHaruo KasaharaIkuko OsadaToru ShimazuYasuo FusejimaAkira HigashibataTakashi YamazakiNoriaki IshiokaHideyuki TakahashiIn cucumber seedlings, gravitropism interferes with hydrotropism, which results in the nearly complete inhibition of hydrotropism under stationary conditions. However, hydrotropic responses are induced when the gravitropic response in the root is nullified by clinorotation. Columella cells in the root cap sense gravity, which induces the gravitropic response. In this study, we found that removing the root tip induced hydrotropism in cucumber roots under stationary conditions. The application of auxin transport inhibitors to cucumber seedlings under stationary conditions suppressed the hydrotropic response induced by the removal of the root tip. To investigate the expression of genes related to hydrotropism in de-tipped cucumber roots, we conducted transcriptome analysis of gene expression by RNA-Seq using seedlings exhibiting hydrotropic and gravitropic responses. Of the 21 and 45 genes asymmetrically expressed during hydrotropic and gravitropic responses, respectively, five genes were identical. Gene ontology (GO) analysis indicated that the category auxin-inducible genes was significantly enriched among genes that were more highly expressed in the concave side of the root than the convex side during hydrotropic or gravitropic responses. Reverse transcription followed by quantitative polymerase chain reaction (RT-qPCR) analysis revealed that root hydrotropism induced under stationary conditions (by removing the root tip) was accompanied by the asymmetric expression of several auxin-inducible genes. However, intact roots did not exhibit the asymmetric expression patterns of auxin-inducible genes under stationary conditions, even in the presence of a moisture gradient. These results suggest that the root tip inhibits hydrotropism by suppressing the induction of asymmetric auxin distribution. Auxin transport and distribution not mediated by the root tip might play a role in hydrotropism in cucumber roots.http://europepmc.org/articles/PMC5764274?pdf=render
spellingShingle Nobuharu Fujii
Sachiko Miyabayashi
Tomoki Sugita
Akie Kobayashi
Chiaki Yamazaki
Yutaka Miyazawa
Motoshi Kamada
Haruo Kasahara
Ikuko Osada
Toru Shimazu
Yasuo Fusejima
Akira Higashibata
Takashi Yamazaki
Noriaki Ishioka
Hideyuki Takahashi
Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.
PLoS ONE
title Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.
title_full Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.
title_fullStr Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.
title_full_unstemmed Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.
title_short Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots.
title_sort root tip mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin inducible genes in response to moisture gradients in cucumber roots
url http://europepmc.org/articles/PMC5764274?pdf=render
work_keys_str_mv AT nobuharufujii roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT sachikomiyabayashi roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT tomokisugita roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT akiekobayashi roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT chiakiyamazaki roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT yutakamiyazawa roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT motoshikamada roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT haruokasahara roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT ikukoosada roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT torushimazu roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT yasuofusejima roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT akirahigashibata roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT takashiyamazaki roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT noriakiishioka roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots
AT hideyukitakahashi roottipmediatedinhibitionofhydrotropismisaccompaniedwiththesuppressionofasymmetricexpressionofauxininduciblegenesinresponsetomoisturegradientsincucumberroots