A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots

When plants suffer from Fe deficiency, they develop morphological and physiological responses, mainly in their roots, aimed to facilitate Fe mobilization and uptake. Once Fe has been acquired in sufficient quantity, the responses need to be switched off to avoid Fe toxicity and to conserve energy. S...

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Main Authors: María José García, Macarena Angulo, Francisco Javier Romera, Carlos Lucena, Rafael Pérez-Vicente
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.971773/full
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author María José García
Macarena Angulo
Francisco Javier Romera
Carlos Lucena
Rafael Pérez-Vicente
author_facet María José García
Macarena Angulo
Francisco Javier Romera
Carlos Lucena
Rafael Pérez-Vicente
author_sort María José García
collection DOAJ
description When plants suffer from Fe deficiency, they develop morphological and physiological responses, mainly in their roots, aimed to facilitate Fe mobilization and uptake. Once Fe has been acquired in sufficient quantity, the responses need to be switched off to avoid Fe toxicity and to conserve energy. Several hormones and signaling molecules, such as ethylene, auxin and nitric oxide, have been involved in the activation of Fe deficiency responses in Strategy I plants. These hormones and signaling molecules have almost no effect when applied to plants grown under Fe-sufficient conditions, which suggests the existence of a repressive signal related to the internal Fe content. The nature of this repressive signal is not known yet many experimental results suggest that is not related to the whole root Fe content but to some kind of Fe compound moving from leaves to roots through the phloem. After that, this signal has been named LOng-Distance Iron Signal (LODIS). Very recently, a novel family of small peptides, “IRON MAN” (IMA), has been identified as key components of the induction of Fe deficiency responses. However, the relationship between LODIS and IMA peptides is not known. The main objective of this work has been to clarify the relationship between both signals. For this, we have used Arabidopsis wild type (WT) Columbia and two of its mutants, opt3 and frd3, affected, either directly or indirectly, in the transport of Fe (LODIS) through the phloem. Both mutants present constitutive activation of Fe acquisition genes when grown in a Fe-sufficient medium despite the high accumulation of Fe in their roots. Arabidopsis WT Columbia plants and both mutants were treated with foliar application of Fe, and later on the expression of IMA and Fe acquisition genes was analyzed. The results obtained suggest that LODIS may act upstream of IMA peptides in the regulation of Fe deficiency responses in roots. The possible regulation of IMA peptides by ethylene has also been studied. Results obtained with ethylene precursors and inhibitors, and occurrence of ethylene-responsive cis-acting elements in the promoters of IMA genes, suggest that IMA peptides could also be regulated by ethylene.
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spelling doaj.art-1b2931aa5b5a4f74898b67e906c001cb2022-12-22T03:07:44ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-08-011310.3389/fpls.2022.971773971773A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana rootsMaría José García0Macarena Angulo1Francisco Javier Romera2Carlos Lucena3Rafael Pérez-Vicente4Department of Agronomy (DAUCO-María de Maeztu Unit of Excellence), Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, Córdoba, SpainDepartment of Agronomy (DAUCO-María de Maeztu Unit of Excellence), Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, Córdoba, SpainDepartment of Agronomy (DAUCO-María de Maeztu Unit of Excellence), Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, Córdoba, SpainDepartment of Botany, Ecology and Plant Physiology, Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, Córdoba, SpainDepartment of Botany, Ecology and Plant Physiology, Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, Córdoba, SpainWhen plants suffer from Fe deficiency, they develop morphological and physiological responses, mainly in their roots, aimed to facilitate Fe mobilization and uptake. Once Fe has been acquired in sufficient quantity, the responses need to be switched off to avoid Fe toxicity and to conserve energy. Several hormones and signaling molecules, such as ethylene, auxin and nitric oxide, have been involved in the activation of Fe deficiency responses in Strategy I plants. These hormones and signaling molecules have almost no effect when applied to plants grown under Fe-sufficient conditions, which suggests the existence of a repressive signal related to the internal Fe content. The nature of this repressive signal is not known yet many experimental results suggest that is not related to the whole root Fe content but to some kind of Fe compound moving from leaves to roots through the phloem. After that, this signal has been named LOng-Distance Iron Signal (LODIS). Very recently, a novel family of small peptides, “IRON MAN” (IMA), has been identified as key components of the induction of Fe deficiency responses. However, the relationship between LODIS and IMA peptides is not known. The main objective of this work has been to clarify the relationship between both signals. For this, we have used Arabidopsis wild type (WT) Columbia and two of its mutants, opt3 and frd3, affected, either directly or indirectly, in the transport of Fe (LODIS) through the phloem. Both mutants present constitutive activation of Fe acquisition genes when grown in a Fe-sufficient medium despite the high accumulation of Fe in their roots. Arabidopsis WT Columbia plants and both mutants were treated with foliar application of Fe, and later on the expression of IMA and Fe acquisition genes was analyzed. The results obtained suggest that LODIS may act upstream of IMA peptides in the regulation of Fe deficiency responses in roots. The possible regulation of IMA peptides by ethylene has also been studied. Results obtained with ethylene precursors and inhibitors, and occurrence of ethylene-responsive cis-acting elements in the promoters of IMA genes, suggest that IMA peptides could also be regulated by ethylene.https://www.frontiersin.org/articles/10.3389/fpls.2022.971773/fulldicotyledonousethyleneFe deficiency responsesIMA peptidesLong Distance Iron Signal (LODIS)Strategy I plants
spellingShingle María José García
Macarena Angulo
Francisco Javier Romera
Carlos Lucena
Rafael Pérez-Vicente
A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots
Frontiers in Plant Science
dicotyledonous
ethylene
Fe deficiency responses
IMA peptides
Long Distance Iron Signal (LODIS)
Strategy I plants
title A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots
title_full A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots
title_fullStr A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots
title_full_unstemmed A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots
title_short A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots
title_sort shoot derived long distance iron signal may act upstream of the ima peptides in the regulation of fe deficiency responses in arabidopsis thaliana roots
topic dicotyledonous
ethylene
Fe deficiency responses
IMA peptides
Long Distance Iron Signal (LODIS)
Strategy I plants
url https://www.frontiersin.org/articles/10.3389/fpls.2022.971773/full
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