Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana

Exposure of plants to different biotic and abiotic stress condition instigates significant change in the cellular redox status; resulting in the elevation of reactive nitrogen species that play signaling role in mediating defense responses. Heavy metal associated (HMA) domain containing genes are re...

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Main Authors: Qari Muhammad Imran, Noreen Falak, Adil Hussain, Bong-Gyu Mun, SangUK Lee, Byung-Wook Yun, Kyung-Min Kim, Arti Sharma
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01712/full
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spelling doaj-0f0bc182544747b0ad867a1c90d888d02020-11-24T23:55:31ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-11-01710.3389/fpls.2016.01712232346Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thalianaQari Muhammad Imran0Noreen Falak1Adil Hussain2Bong-Gyu Mun3SangUK Lee4Byung-Wook Yun5Kyung-Min Kim6Arti Sharma7Kyungpook national universityKyungpook national universityKyungpook national universityKyungpook national universityKyungpook national universityKyungpook national universityKyungpook national universityKyungpook national universityExposure of plants to different biotic and abiotic stress condition instigates significant change in the cellular redox status; resulting in the elevation of reactive nitrogen species that play signaling role in mediating defense responses. Heavy metal associated (HMA) domain containing genes are required for spatio-temporal transportation of metal ions that bind with various enzymes and co-factors within the cell. To uncover the underlying mechanisms mediated by AtHMA genes, we identified 14 Arabidopsis HMA genes that were differentially expressed in response to nitrosative stress through RNA-seq analysis. Of those 14 genes, the expression of eight HMA genes was significantly increased, whereas that of six genes was significantly reduced. We further validated the RNA-seq results through quantitative real-time PCR analysis. Gene ontology analysis revealed the involvement of these genes in biological processes such as hemostasis and transport. The majority of these nitric oxide (NO)-responsive AtHMA gene products are carrier/transport proteins. AtHMAD1 (At1g51090) showed the highest fold change to S-nitrosocystein. We therefore, further investigated its role in oxidative and nitrosative mediated stress conditions and found that AtHMAD1 has antagonistic role in shoot and root growth. Characterization of AtHMAD1 through functional genomics showed that the knock out mutant athmad1 plants were resistant to virulent Pseudomonas syringae (DC3000) and showed early induction and high transcript accumulation of pathogenesis related gene. Furthermore, inoculation of athamd1 with avirulent strain of the same bacteria showed negative regulation of R-gene mediated resistance. These results were supported by hypersensitive cell death response and cell death induced electrolyte leakage. AtHMAD1 was also observed to negatively regulate systemic acquired resistance SAR as the KO mutant showed induction of SAR marker genes. Overall, these results imply that NO-responsive AtHMA domain containing genes may play an important role in plant development and immunity.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01712/fullArabidopsis thaliananitrosative stressHR responseBasal defenseR-gene mediated resistanceRNA-seq profile
collection DOAJ
language English
format Article
sources DOAJ
author Qari Muhammad Imran
Noreen Falak
Adil Hussain
Bong-Gyu Mun
SangUK Lee
Byung-Wook Yun
Kyung-Min Kim
Arti Sharma
spellingShingle Qari Muhammad Imran
Noreen Falak
Adil Hussain
Bong-Gyu Mun
SangUK Lee
Byung-Wook Yun
Kyung-Min Kim
Arti Sharma
Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana
Frontiers in Plant Science
Arabidopsis thaliana
nitrosative stress
HR response
Basal defense
R-gene mediated resistance
RNA-seq profile
author_facet Qari Muhammad Imran
Noreen Falak
Adil Hussain
Bong-Gyu Mun
SangUK Lee
Byung-Wook Yun
Kyung-Min Kim
Arti Sharma
author_sort Qari Muhammad Imran
title Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana
title_short Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana
title_full Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana
title_fullStr Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana
title_full_unstemmed Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana
title_sort nitric oxide responsive heavy metal-associated gene athmad1 contributes to development and disease resistance in arabidopsis thaliana
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2016-11-01
description Exposure of plants to different biotic and abiotic stress condition instigates significant change in the cellular redox status; resulting in the elevation of reactive nitrogen species that play signaling role in mediating defense responses. Heavy metal associated (HMA) domain containing genes are required for spatio-temporal transportation of metal ions that bind with various enzymes and co-factors within the cell. To uncover the underlying mechanisms mediated by AtHMA genes, we identified 14 Arabidopsis HMA genes that were differentially expressed in response to nitrosative stress through RNA-seq analysis. Of those 14 genes, the expression of eight HMA genes was significantly increased, whereas that of six genes was significantly reduced. We further validated the RNA-seq results through quantitative real-time PCR analysis. Gene ontology analysis revealed the involvement of these genes in biological processes such as hemostasis and transport. The majority of these nitric oxide (NO)-responsive AtHMA gene products are carrier/transport proteins. AtHMAD1 (At1g51090) showed the highest fold change to S-nitrosocystein. We therefore, further investigated its role in oxidative and nitrosative mediated stress conditions and found that AtHMAD1 has antagonistic role in shoot and root growth. Characterization of AtHMAD1 through functional genomics showed that the knock out mutant athmad1 plants were resistant to virulent Pseudomonas syringae (DC3000) and showed early induction and high transcript accumulation of pathogenesis related gene. Furthermore, inoculation of athamd1 with avirulent strain of the same bacteria showed negative regulation of R-gene mediated resistance. These results were supported by hypersensitive cell death response and cell death induced electrolyte leakage. AtHMAD1 was also observed to negatively regulate systemic acquired resistance SAR as the KO mutant showed induction of SAR marker genes. Overall, these results imply that NO-responsive AtHMA domain containing genes may play an important role in plant development and immunity.
topic Arabidopsis thaliana
nitrosative stress
HR response
Basal defense
R-gene mediated resistance
RNA-seq profile
url http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01712/full
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