Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens

Pauliina Halimaa*, Daniel Blande, Erol Baltzi, Mark G.M. Aarts, Lars Granlund, Markku Keinänen, Sirpa O. Kärenlampi, Anna D. Kozhevnikova, Sirpa Peräniemi, Henk Schat, Ilya V. Seregin, Marjo Tuomainen, Arja I. Tervahauta

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

1 Citation (Scopus)

Abstract

Calamine accessions of the zinc/cadmium/nickel hyperaccumulator, Noccaea caerulescens, exhibit striking variation in foliar cadmium accumulation in nature. The Ganges accession (GA) from Southern France displays foliar cadmium hyperaccumulation (>1000 μg g−1 DW), whereas the accession La Calamine (LC) from Belgium, with similar local soil metal composition, does not (<100 μg g−1 DW). All calamine accessions are cadmium hypertolerant. To find out the differences between LC and GA in their basic adaptation mechanisms, we bypassed the cadmium excluding phenotype of LC by exposing the plants to 50 μm cadmium in hydroponics, achieving equal cadmium accumulation in the shoots. The iron content increased in the roots of both accessions. GA exhibited significant decreases in manganese and zinc contents in the roots and shoots, approaching those in LC. Altogether 702 genes responded differently to cadmium exposure between the accessions, 157 and 545 in the roots and shoots, respectively. Cadmium-exposed LC showed a stress response and had decreased levels of a wide range of photosynthesis-related transcripts. GA showed less changes, mainly exhibiting an iron deficiency-like response. This included increased expression of genes encoding five iron deficiency-regulated bHLH transcription factors, ferric reduction oxidase FRO2, iron transporters IRT1 and OPT3, and nicotianamine synthase NAS1, and decreased expression of genes encoding ferritins and NEET (a NEET family iron-sulfur protein), which is possibly involved in iron transfer, distribution and/or management. The function of the IRT1 gene in the accessions was compared. We conclude that the major difference between the two accessions is in the way they cope with iron under cadmium exposure.

Original languageEnglish
Pages (from-to)306-320
JournalPlant Journal
Volume97
Issue number2
Early online date4 Oct 2018
DOIs
Publication statusPublished - Jan 2019

Fingerprint

Cadmium
cadmium
homeostasis
Homeostasis
Iron
iron
shoots
Zinc
zinc
Noccaea caerulescens
smithsonite
sulfur proteins
Iron-Sulfur Proteins
Hydroponics
Basic Helix-Loop-Helix Transcription Factors
Gene Expression
gene expression
hyperaccumulators
Belgium
Photosynthesis

Keywords

  • cadmium
  • Illumina
  • iron deficiency
  • IRT1
  • Noccaea caerulescens
  • RNA-seq
  • spectral imaging
  • Thlaspi caerulescens
  • transcriptome

Cite this

Halimaa, P., Blande, D., Baltzi, E., Aarts, M. G. M., Granlund, L., Keinänen, M., ... Tervahauta, A. I. (2019). Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. Plant Journal, 97(2), 306-320. https://doi.org/10.1111/tpj.14121
Halimaa, Pauliina ; Blande, Daniel ; Baltzi, Erol ; Aarts, Mark G.M. ; Granlund, Lars ; Keinänen, Markku ; Kärenlampi, Sirpa O. ; Kozhevnikova, Anna D. ; Peräniemi, Sirpa ; Schat, Henk ; Seregin, Ilya V. ; Tuomainen, Marjo ; Tervahauta, Arja I. / Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. In: Plant Journal. 2019 ; Vol. 97, No. 2. pp. 306-320.
@article{9143d17ce27346dc842ffdee490e3a46,
title = "Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens",
abstract = "Calamine accessions of the zinc/cadmium/nickel hyperaccumulator, Noccaea caerulescens, exhibit striking variation in foliar cadmium accumulation in nature. The Ganges accession (GA) from Southern France displays foliar cadmium hyperaccumulation (>1000 μg g−1 DW), whereas the accession La Calamine (LC) from Belgium, with similar local soil metal composition, does not (<100 μg g−1 DW). All calamine accessions are cadmium hypertolerant. To find out the differences between LC and GA in their basic adaptation mechanisms, we bypassed the cadmium excluding phenotype of LC by exposing the plants to 50 μm cadmium in hydroponics, achieving equal cadmium accumulation in the shoots. The iron content increased in the roots of both accessions. GA exhibited significant decreases in manganese and zinc contents in the roots and shoots, approaching those in LC. Altogether 702 genes responded differently to cadmium exposure between the accessions, 157 and 545 in the roots and shoots, respectively. Cadmium-exposed LC showed a stress response and had decreased levels of a wide range of photosynthesis-related transcripts. GA showed less changes, mainly exhibiting an iron deficiency-like response. This included increased expression of genes encoding five iron deficiency-regulated bHLH transcription factors, ferric reduction oxidase FRO2, iron transporters IRT1 and OPT3, and nicotianamine synthase NAS1, and decreased expression of genes encoding ferritins and NEET (a NEET family iron-sulfur protein), which is possibly involved in iron transfer, distribution and/or management. The function of the IRT1 gene in the accessions was compared. We conclude that the major difference between the two accessions is in the way they cope with iron under cadmium exposure.",
keywords = "cadmium, Illumina, iron deficiency, IRT1, Noccaea caerulescens, RNA-seq, spectral imaging, Thlaspi caerulescens, transcriptome",
author = "Pauliina Halimaa and Daniel Blande and Erol Baltzi and Aarts, {Mark G.M.} and Lars Granlund and Markku Kein{\"a}nen and K{\"a}renlampi, {Sirpa O.} and Kozhevnikova, {Anna D.} and Sirpa Per{\"a}niemi and Henk Schat and Seregin, {Ilya V.} and Marjo Tuomainen and Tervahauta, {Arja I.}",
year = "2019",
month = "1",
doi = "10.1111/tpj.14121",
language = "English",
volume = "97",
pages = "306--320",
journal = "The Plant Journal",
issn = "0960-7412",
publisher = "Wiley",
number = "2",

}

Halimaa, P, Blande, D, Baltzi, E, Aarts, MGM, Granlund, L, Keinänen, M, Kärenlampi, SO, Kozhevnikova, AD, Peräniemi, S, Schat, H, Seregin, IV, Tuomainen, M & Tervahauta, AI 2019, 'Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens', Plant Journal, vol. 97, no. 2, pp. 306-320. https://doi.org/10.1111/tpj.14121

Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. / Halimaa, Pauliina; Blande, Daniel; Baltzi, Erol; Aarts, Mark G.M.; Granlund, Lars; Keinänen, Markku; Kärenlampi, Sirpa O.; Kozhevnikova, Anna D.; Peräniemi, Sirpa; Schat, Henk; Seregin, Ilya V.; Tuomainen, Marjo; Tervahauta, Arja I.

In: Plant Journal, Vol. 97, No. 2, 01.2019, p. 306-320.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens

AU - Halimaa, Pauliina

AU - Blande, Daniel

AU - Baltzi, Erol

AU - Aarts, Mark G.M.

AU - Granlund, Lars

AU - Keinänen, Markku

AU - Kärenlampi, Sirpa O.

AU - Kozhevnikova, Anna D.

AU - Peräniemi, Sirpa

AU - Schat, Henk

AU - Seregin, Ilya V.

AU - Tuomainen, Marjo

AU - Tervahauta, Arja I.

PY - 2019/1

Y1 - 2019/1

N2 - Calamine accessions of the zinc/cadmium/nickel hyperaccumulator, Noccaea caerulescens, exhibit striking variation in foliar cadmium accumulation in nature. The Ganges accession (GA) from Southern France displays foliar cadmium hyperaccumulation (>1000 μg g−1 DW), whereas the accession La Calamine (LC) from Belgium, with similar local soil metal composition, does not (<100 μg g−1 DW). All calamine accessions are cadmium hypertolerant. To find out the differences between LC and GA in their basic adaptation mechanisms, we bypassed the cadmium excluding phenotype of LC by exposing the plants to 50 μm cadmium in hydroponics, achieving equal cadmium accumulation in the shoots. The iron content increased in the roots of both accessions. GA exhibited significant decreases in manganese and zinc contents in the roots and shoots, approaching those in LC. Altogether 702 genes responded differently to cadmium exposure between the accessions, 157 and 545 in the roots and shoots, respectively. Cadmium-exposed LC showed a stress response and had decreased levels of a wide range of photosynthesis-related transcripts. GA showed less changes, mainly exhibiting an iron deficiency-like response. This included increased expression of genes encoding five iron deficiency-regulated bHLH transcription factors, ferric reduction oxidase FRO2, iron transporters IRT1 and OPT3, and nicotianamine synthase NAS1, and decreased expression of genes encoding ferritins and NEET (a NEET family iron-sulfur protein), which is possibly involved in iron transfer, distribution and/or management. The function of the IRT1 gene in the accessions was compared. We conclude that the major difference between the two accessions is in the way they cope with iron under cadmium exposure.

AB - Calamine accessions of the zinc/cadmium/nickel hyperaccumulator, Noccaea caerulescens, exhibit striking variation in foliar cadmium accumulation in nature. The Ganges accession (GA) from Southern France displays foliar cadmium hyperaccumulation (>1000 μg g−1 DW), whereas the accession La Calamine (LC) from Belgium, with similar local soil metal composition, does not (<100 μg g−1 DW). All calamine accessions are cadmium hypertolerant. To find out the differences between LC and GA in their basic adaptation mechanisms, we bypassed the cadmium excluding phenotype of LC by exposing the plants to 50 μm cadmium in hydroponics, achieving equal cadmium accumulation in the shoots. The iron content increased in the roots of both accessions. GA exhibited significant decreases in manganese and zinc contents in the roots and shoots, approaching those in LC. Altogether 702 genes responded differently to cadmium exposure between the accessions, 157 and 545 in the roots and shoots, respectively. Cadmium-exposed LC showed a stress response and had decreased levels of a wide range of photosynthesis-related transcripts. GA showed less changes, mainly exhibiting an iron deficiency-like response. This included increased expression of genes encoding five iron deficiency-regulated bHLH transcription factors, ferric reduction oxidase FRO2, iron transporters IRT1 and OPT3, and nicotianamine synthase NAS1, and decreased expression of genes encoding ferritins and NEET (a NEET family iron-sulfur protein), which is possibly involved in iron transfer, distribution and/or management. The function of the IRT1 gene in the accessions was compared. We conclude that the major difference between the two accessions is in the way they cope with iron under cadmium exposure.

KW - cadmium

KW - Illumina

KW - iron deficiency

KW - IRT1

KW - Noccaea caerulescens

KW - RNA-seq

KW - spectral imaging

KW - Thlaspi caerulescens

KW - transcriptome

U2 - 10.1111/tpj.14121

DO - 10.1111/tpj.14121

M3 - Article

VL - 97

SP - 306

EP - 320

JO - The Plant Journal

JF - The Plant Journal

SN - 0960-7412

IS - 2

ER -