Natural Variation at the MATE Transporter Locus Reveals Cross-Talk between Fe Homeostasis and Zn Tolerance in

English version České info

Zinc (Zn) is essential for the optimal growth of plants but is toxic if present in excess, so Zn homeostasis needs to be finely tuned. Understanding Zn homeostasis mechanisms in plants will help in the development of innovative approaches for the phytoremediation of Zn-contaminated sites. In this study, Zn tolerance quantitative trait loci (QTL) were identified by analyzing differences in the Bay-0 and Shahdara accessions of Arabidopsis thaliana. Fine-scale mapping showed that a variant of the Fe homeostasis-related FERRIC REDUCTASE DEFECTIVE3 (FRD3) gene, which encodes a multidrug and toxin efflux (MATE) transporter, is responsible for reduced Zn tolerance in A. thaliana. Allelic variation in FRD3 revealed which amino acids are necessary for FRD3 function. In addition, the results of allele-specific expression assays in F1 individuals provide evidence for the existence of at least one putative metal-responsive cis-regulatory element. Our results suggest that FRD3 works as a multimer and is involved in loading Zn into xylem. Cross-homeostasis between Fe and Zn therefore appears to be important for Zn tolerance in A. thaliana with FRD3 acting as an essential regulator.

Vyšlo v časopise: Natural Variation at the MATE Transporter Locus Reveals Cross-Talk between Fe Homeostasis and Zn Tolerance in. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003120
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003120

Souhrn

Zdroje

1. BroadleyMR, WhitePJ, HammondJP, ZelkoI, LuxA (2007) Zinc in plants. New Phytol 73 : 677–702.

2. KramerU (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61 : 517–34.

3. HanikenneM, NouetC (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14 : 252–259.

4. MarquèsL, OomenR (2011) On the way to unravel zinc hyperaccumulation in plants: a mini review. Metallomics 3 : 1265–1270.

5. DeinleinU, WeberM, SchmidtH, RenschS, TrampczynskA, et al. (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24 : 708–723.

6. WillemsG, DragerDB, CourbotM, GodeC, VerbruggenN, et al. (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.

7. RyanPR, TyermanSD, SasakiT, FuruichiT, YamamotoY, et al. (2011) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62 : 9–20.

8. KobayashiY, KurodaK, KimuraK, Southron-FrancisJL, FuruzawaA, et al. (2008) Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis. Plant Physiol 148 : 969–980.

9. BuescherE, AchbergerT, AmusanI, GianniniA, OchsenfeldC, et al. (2010) Natural genetic variation in selected populations of Arabidopsis thaliana is associated with ionomic differences. PLoS ONE 5: e11081 doi:10.1371/journal.pone.0011081.

10. BaxterI, HermansC, LahnerB, YakubovaE, TikhonovaM, et al. (2012) Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana. PLoS ONE 7: e35121 doi:10.1371/journal.pone.0035121.

11. GhandilyanA, BarbozaL, TisnéS, GranierC, ReymondM, et al. (2009a) Genetic analysis identifies quantitative trait loci controlling rosette mineral concentrations in Arabidopsis thaliana under drought. New Phytol 184 : 180–192.

12. GhandilyanA, IlkN, HanhartC, MbengueM, BarbozaL, et al. (2009b) A strong effect of growth medium and organ type on the identification of QTLs for phytate and mineral concentrations in three Arabidopsis thaliana RIL populations. J Exp Bot 60 : 1409–1425.

13. VreugdenhilD, AartsMGM, KoornneefM, NelissenH, ErnstWHO (2004) Natural variation and QTL analysis for cationic mineral content in seeds of Arabidopsis thaliana. Plant Cell Environ 27 : 828–839.

14. WatersBM, GrusakMA (2008) Quantitative trait locus mapping for seed mineral concentrations in two Arabidopsis thaliana recombinant inbred populations. New Phytol 179 : 1033–1047.

15. PrinzenbergAE, BarbierH, SaltDE, StichB, ReymondM (2010) Relationships between growth, growth response to nutrient supply, and ion content using a recombinant inbred line population in Arabidopsis. Plant Physiol 154 : 1361–1371.

16. RichardO, PineauC, LoubetS, ChaliesC, VileD, et al. (2011) Diversity analysis of the response to Zn within the Arabidopsis thaliana species revealed a low contribution of Zn translocation to Zn tolerance and a new role for Zn in lateral root development. Plant Cell Environ 34 : 1065–1078.

17. ShanmugamV, LoJC, WuCL, WangSL, LaiCC, et al. (2011) Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana –⁠ the role in zinc tolerance. New Phytol 190 : 125–137.

18. ShanmugamV, TsedneeM, YehKC (2012) ZINC TOLERANCE INDUCED BY IRON1 reveals the importance of glutathione in the cross-homeostasis between zinc and iron in Arabidopsis thaliana. Plant J 69 : 1006–1017.

19. RogersEE, GuerinotML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14 : 1787–1799.

20. LoudetO, ChaillouS, CamilleriC, BouchezD, Daniel-VedeleF (2002) Bay-0×Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor Appl Genet 104 : 1173–1184.

21. GreenLS, RogersEE (2004) FRD3 controls iron localization in Arabidopsis. Plant Physiol 136 : 2523–2531.

22. DurrettTP, GassmannW, RogersEE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144 : 197–205.

23. RoschzttardtzH, Séguéla-ArnaudM, BriatJF, VertG, CurieC (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23 : 2725–2737.

24. Alonso-BlancoC, AartsMGM, BentsinkL, KeurentkesJJB, ReymondM, et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21 : 1877–1896.

25. SteinRJ, WatersBM (2012) Use of natural variation reveals core genes in the transcriptome of iron-deficient Arabidopsis thaliana roots. J Exp Bot 63 : 1039–1055.

26. OmoteH, HiasaM, MatsumotoT, OtsukaM, MoriyamaY (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27 : 587–593.

27. DelaizeE (1996) A metal-accumulator mutant of Arabidopsis thaliana. Plant Physiol 111 : 849–855.

28. HanikenneM, TalkeIN, HaydonMJ, LanzC, NolteA, et al. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453 : 391–395.

29. VerretF, GravotA, AuroyP, LeonhardtN, DavidP, et al. (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Letters 576 : 306–312.

30. HussainD, HaydonMJ, WangY, WongE, ShersonSM, et al. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16 : 1327–1339.

31. 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.

32. LobreauxS, BriatJF (1991) Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem J 274 : 601–606.

33. HellensRP, EdwardsEA, LeylandNR, BeanS, MullineauxPM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42 : 819–832.

34. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 : 735–743.

35. CharrierB, ChampionA, HenryY, KreisM (2002) Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction. Plant Physiol 130 : 577–590.

36. SéguélaM, BriatJF, VertG, CurieC (2008) Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. Plant J 55 : 289–300.

37. CzechowskiT, StittM, AltmannT, UdvardiMK, ScheibleWR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139 : 5–17.

38. WittkoppPJ, HaerumBK, ClarkAG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430 : 85–88.

39. ZhangX, RichardsEJ, BorevitzJO (2007) Genetic and epigenetic dissection of cis regulatory variation. Curr Opin Plant Biol 10 : 142–148.

40. KroukG, LacombeB, BielachA, Perrine-WalkerF, MalinskaK (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18 : 927–937.

41. HedgesLV, GurevitchJ, CurtisPS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80 : 1150–1156.