The Five Zinc Transporters Undergo Different Evolutionary Fates towards Adaptive Evolution to Zinc Tolerance in

English version České info

Gene duplication is a major mechanism facilitating adaptation to changing environments. From recent genomic analyses, the acquisition of zinc hypertolerance and hyperaccumulation characters discriminating Arabidopsis halleri from its zinc sensitive/non-accumulator closest relatives Arabidopsis lyrata and Arabidopsis thaliana was proposed to rely on duplication of genes controlling zinc transport or zinc tolerance. Metal Tolerance Protein 1 (MTP1) is one of these genes. It encodes a Zn²⁺/H⁺ antiporter involved in cytoplasmic zinc detoxification and thus in zinc tolerance. MTP1 was proposed to be triplicated in A. halleri, while it is present in single copy in A. thaliana and A. lyrata. Two of the three AhMTP1 paralogues were shown to co-segregate with zinc tolerance in a BC1 progeny from a cross between A. halleri and A. lyrata. In this work, the MTP1 family was characterized at both the genomic and functional levels in A. halleri. Five MTP1 paralogues were found to be present in A. halleri, AhMTP1-A1, -A2, -B, -C, and -D. Interestingly, one of the two newly identified AhMTP1 paralogues was not fixed at least in one A. halleri population. All MTP1s were expressed, but transcript accumulation of the paralogues co-segregating with zinc tolerance in the A. halleri X A. lyrata BC1 progeny was markedly higher than that of the other paralogues. All MTP1s displayed the ability to functionally complement a Saccharomyces cerevisiæ zinc hypersensitive mutant. However, the paralogue showing the least complementation of the yeast mutant phenotype was one of the paralogues co-segregating with zinc tolerance. From our results, the hypothesis that pentaplication of MTP1 could be a major basis of the zinc tolerance character in A. halleri is strongly counter-balanced by the fact that members of the MTP1 family are likely to experience different evolutionary fates, some of which not concurring to increase zinc tolerance.

Vyšlo v časopise: The Five Zinc Transporters Undergo Different Evolutionary Fates towards Adaptive Evolution to Zinc Tolerance in. PLoS Genet 6(4): e32767. doi:10.1371/journal.pgen.1000911
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000911

Souhrn

Zdroje

1. OhnoS

1970 Evolution by gene duplication. New York Springer-Verlag. ISBN 0-04-575015-7

2. ZhangJZ

2003 Evolution by gene duplication: an update. Trends Ecol Evol 18 292 298

3. VelascoR

ZharkikhA

TroggioM

CartwrightDA

CestaroA

2007 A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2 e1326 doi:10.1371/journal.pone.0001326

4. MingR

HouS

FengY

YuQ

Dionne-LaporteA

2008 The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452 991 996

5. RensingSA

LangD

ZimmerAD

TerryA

SalamovA

2008 The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319 64 69

6. FlagelLE

WendelJF

2009 Gene duplication and evolutionary novelty in plants. New Phytol 183 557 564

7. HurlesM

2004 Gene Duplication: The Genomic Trade in Spare Parts. PLoS Biol 2 e206 doi:10.1371/journal.pbio.0020206

8. AntonovicsJ

BradshawAD

TurnerRG

1971 Heavy metal tolerance in plants. Adv Ecol Res 7 1 85

9. Pilon-SmitsE

2005 Phytoremediation. Annu Rev Plant Biol 56 15 39

10. BertV

MacnairMR

Saumitou-LapradeP

De LaguerieP

PetitD

2000 Zinc Tolerance and Accumulation in metallicolous and non-metallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol 146 225 233

11. PauwelsM

FrerotH

BonninI

Saumitou-LapradeP

2006 A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). J Evol Biol 19 1838 1850

12. KochMA

MatschingerM

2007 Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc Natl Acad Sci USA 104 6272 6277

13. PauwelsM

WillemsG

RoosensNCJ

FrérotH

Saumitou-LapradeP

2008 Merging methods in molecular and ecological genetics to study the adaptation of plants to anthropogenic metal-pollutedsites: implication for phytoremediation. Mol Ecol 17 108 119

14. DrägerDB

Desbrosses-FonrougeAG

KrachC

ChardonnensAN

MeyerRC

2004 Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39 425 439

15. HanikenneM

TalkeIN

HaydonMJ

LanzC

NolteA

2008 Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453 391 396

16. TalkeIN

HanikenneM

KrämerU

2006 Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142 148 167

17. Desbrosses-FonrougeAG

VoigtK

SchröderA

ArrivaultS

ThomineS

2005 Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579 4165 4174

18. KawachiM

KobaeY

MimuraT

MaeshimaM

2008 Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn2+/H+ antiporter of Arabidopsis thaliana, stimulates the transport activity. J Biol Chem 283 8374 8383

19. Van der ZaalBJ

NeuteboomLW

PinasJE

ChardonnensAN

SchatH

1999 Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119 1047 1055

20. WillemsG

DrägerDB

CourbotM

GodéC

VerbruggenN

2007 The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176 659 674

21. LacombeE

CossegalM

MirouzeM

AdamT

VaroquauxF

2008 Construction and characterisation of a BAC library from Arabidopsis halleri: Evaluation of physical mapping based on conserved syntheny with Arabidopsis thaliana. Plant Sci 174 634 640

22. SchranzME

LysakMA

Mitchell-OldsT

2006 The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11 535 542

23. KoizumiS

SuzukiK

OgraY

YamadaH

OtsukaF

1999 Transcriptional activity and regulatory protein binding of metal-responsive elements of the human metallothionein-IIA gene. Eur J Biochem 259 635 642

24. MacDiarmidCW

GaitherAL

EideD

2000 Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19 2845 2855

25. MirouzeM

SelsJ

RichardO

CzernicP

LoubetS

2006 A putative novel role for plant defensins: a defensin from the zinc hyperaccumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J 47 329 342

26. LinYF

LiangHM

YangSY

BochA

ClemensS

2009 Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182 392 404

27. PersansMW

NiemanK

SaltDE

2001 Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98 9995 10000

28. ForceA

LynchM

PickettFB

AmoresA

YanY-L

PostlethwaitJ

1999 Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 1531 1545

29. ChurchGM

GilbertW

1984 Genomic sequencing. Proc Natl Acad Sci USA 81 1991 1995

30. RoosensNCJ

WillemsG

GodéC

CourseauxA

Saumitou-LapradeP

2008 The use of comparative genome analysis and syntenic relationships allows extrapolating the position of Zn tolerance QTL regions from Arabidopsis halleri into Arabidopsis thaliana. Plant Soil 306 105 116

31. Van OoijenJW

VoorripsRE

2001 JoinMap® version 3.0: software for the calculation of genetic linkage maps. Wageningen Plant Research International

32. KosambiDD

1944 The estimation of map distances from recombination values. Ann Eugen 12 172 175

33. GietzRD

WoodsRA

2002 Transformation of yeast by the LiAc/SS carrier DNA/PEG method. Methods Enzymol 350 87 96

34. KroghA

LarssonB

von HeijneG

SonnhammerEL