and Are Required for Growth under Iron-Limiting Conditions

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Iron is essential for photosynthesis and is often a limiting nutrient for plant productivity. Plants respond to conditions of iron deficiency by increasing transcript abundance of key genes involved in iron homeostasis, but only a few regulators of these genes have been identified. Using genome-wide expression analysis, we searched for transcription factors that are induced within 24 hours after transferring plants to iron-deficient growth conditions. Out of nearly 100 transcription factors shown to be up-regulated, we identified MYB10 and MYB72 as the most highly induced transcription factors. Here, we show that MYB10 and MYB72 are functionally redundant and are required for plant survival in alkaline soil where iron availability is greatly restricted. myb10myb72 double mutants fail to induce transcript accumulation of the nicotianamine synthase gene NAS4. Both myb10myb72 mutants and nas4-1 mutants have reduced iron concentrations, chlorophyll levels, and shoot mass under iron-limiting conditions, indicating that these genes are essential for proper plant growth. The double myb10myb72 mutant also showed nickel and zinc sensitivity, similar to the nas4 mutant. Ectopic expression of NAS4 rescues myb10myb72 plants, suggesting that loss of NAS4 is the primary defect in these plants and emphasizes the importance of nicotianamine, an iron chelator, in iron homeostasis. Overall, our results provide evidence that MYB10 and MYB72 act early in the iron-deficiency regulatory cascade to drive gene expression of NAS4 and are essential for plant survival under iron deficiency.

Vyšlo v časopise: and Are Required for Growth under Iron-Limiting Conditions. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003953
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003953

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Zdroje

1. PalmerC, GuerinotML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nature Chem Biol 5: 333–340.

2. GuerinotML, YiY (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104: 815–820.

3. CurieC, PanavieneZ, LoulergueC, DellaportaSL, BriatJ-F, et al. (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409: 346–349.

4. LeeS, ChieckoJC, KimSA, WalkerEL, LeeY, et al. (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150: 786–800.

5. SantiS, SchmidtW (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183 (4) 1072–84.

6. RobinsonNJ, ProcterCM, ConnollyEL, GuerinotML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397: 694–697.

7. EideD, BroderiusM, FettJ, GuerinotML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93: 5624–5628.

8. VertG, GrotzN, DedaldechampF, GaymardF, GuerinotML, et al. (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and plant growth. Plant Cell 14: 1223–1233.

9. MorrisseyJ, BaxterIR, LeeJ, LiL, LahnerB, et al. (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21: 3326–3338.

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

11. CurieC, CassinG, CounchD, DivolF, KH, et al. (2009) Metal movement within the plant: contribution of nictotianamine and yellow stripe 1-like transporters. Ann Bot 103: 1–11.

12. BauerP, SchulerM (2011) Heavy metals need assistance: The contribution of nicotianamine to metal circulation throughout the plant and the Arabidopsis NAS gene family. Frontiers in Plant Science 2: 69.

13. WatersBM, ChuHH, DidonatoRJ, RobertsLA, EisleyRB, et al. (2006) Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141: 1446–1458.

14. SchulerM, Rellan-AlverezR, Fink-StraubeC, AbadiaJ, BauerP (2012) Nictoianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24: 2380–2400.

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

16. HaydonMJ, KawachiM, WirtzM, HillmerS, HellR, et al. (2012) Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell 24: 724–737.

17. MasudaH, UsudaK, KobayashiT, IshimaruY, KakeiY, et al. (2009) Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2: 155–166.

18. LeeS, JeonUS, LeeSJ, KimYK, PerssonDP, et al. (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc Natl Acad Sci USA 106: 14–19.

19. JohnsonAA, KyriacouB, CallahanDL, CarruthersL, StangoulisJ, et al. (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLoS One 6 (9) e24476 doi: 10.1371/journal.pone.0024476

20. MasudaH, IshimaruY, AungMS, KobayashiT, KakeiY, et al. (2012) Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci Rep 2: 543.

21. BuckhoutTJ, YangTJ, SchmidtW (2009) Early iron-deficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genomics 10: 147.

22. DinnenyJR, LongTA, WangJY, JungJW, MaceD, et al. (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320: 942–945.

23. ColangeloEP, GuerinotML (2004) The essential bHLH protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400–3412.

24. JakobyM, WangHY, ReidtW, WeisshaarB, BauerP (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577: 528–534.

25. YuanYX, ZhangJ, WangDW, LingHQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15: 613–621.

26. YuanY, WuH, WangN, KLiJ, ZhaoW, et al. (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18: 385–397.

27. WangN, CuiY, FanH, DuJ, HuangZ, et al. (2012) Requirement and functional redundancy of 1b subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6 (2) 503–13.

28. LongTA, TsukagoshiH, BuschW, LahnerB, SaltDE, et al. (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22: 2219–2236.

29. van de MortelJE, SchatH, ModerlandPD, van ThemaatE, van der EntS, et al. (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31: 301–324.

30. DubosC, StrackeR, GrotewoldE, WeisshaarB, MartinC, et al. (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573–581.

31. Van der EntS, VerhagenBWM, Van DoornR, BakkerD, VerlaanMG, et al. (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146: 1293–1304.

32. SegarraG, Van der EntS, TrillasI, PieterseC (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11: 90–96.

33. MatusJT, AqueaF, Arce-JohnsonP (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8: 83.

34. StrackeR, WerberM, WeisshaarB (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447–456.

35. AlonsoJM, StephanovaAN, LeisseTJ, KCJ, ChenH, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

36. Marschner H (2012) Mineral Nutrition of Higher Plants. Boston: Academic Press. 651 p.

37. BaxterI, VitekO, LahnerB, MuthukumarB, BorghiM, et al. (2008) The leaf ionome as a multivariable system to detect a plant's physiological status. Proc Natl Acad Sci U S A 105: 12081–12086.

38. GhasemiR, GhaderianSM, KramerU (2009) Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytol 184: 566–580.

39. SchmidM, DavisonTS, HenzSR, PapeUJ, DemarM, et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501–506.

40. ZimmermannP, Hirsch-HoffmannM, HennigL, GruissemW (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621–2632.

41. RomeroI, FuertesA, BenitoMJ, MalpicaJM, LeyvaA, et al. (1998) More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14: 273–284.

42. KlatteM, SchulerM, WirtzM, Fink-StraubeC, HellR, et al. (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150: 257–271.

43. PianelliK, MariS, MarquesL, LebrunM, CzernicP (2005) Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res 14: 739–748.

44. KimS, TakahashiM, HiguchiK, TsunodaK, NakanishiH, et al. (2005) Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants. Plant Cell Physiol 46: 1809–1818.

45. MariS, GendreD, PianelliK, OuerdaneL, LobinskiR, et al. (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57: 4111–4122.

46. SivitzAB, HermandV, CurieC, VertG (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS One 7: e44843.

47. LingHQ, KochG, BauleinH, GanalMW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96: 7098–7103.

48. TakahashiM, TeradaY, NakaiI, NakanishiH, YoshimuraE, et al. (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15: 1263–1280.

49. BauerP, ThielT, KlatteM, BereczkyZ, BrumbarovaT, et al. (2004) Analysis of sequence, map position, and gene expression reveals conserved essential genes for iron uptake in Arabidopsis and tomato. Plant Physiol 136: 4169–4183.

50. KoenE, Besson-BardA, DucC, AstierJ, GravotA, et al. (2013) Arabidopsis thaliana nicotianamine synthase 4 is required for proper response to iron deficiency and to cadmium exposure. Plant Sci 209: 1–11.

51. KramerU, TalkeIN, HanikenneM (2007) Transition metal transport. FEBS Lett 581: 2263–2272.

52. MarschnerH, RömheldV, Ossenberg-NeuhausH (1982) Rapid method for measuring changes in pH and reducing processes along roots of intact plants. Z Pflanzenphysiol 105: 407–416.

53. KrysanPJ, YoungJC, SussmanMR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11: 2283–2290.

54. NishalB, TantikanjanaT, SundaresanV (2005) An inducible targeted tagging system for localized saturation mutagenesis in Arabidopsis. Plant Physiol 137: 3–12.

55. JeffersonRA, KavanaghTA, BevanMW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907.

56. LichtenthalerHK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148: 350–382.

57. SmythGK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3.

58. LahnerB, GongJ, MahmoudianM, SmithEL, AbidKB, et al. (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechnol 21: 1215–1221.

59. CurtisMD, GrossniklausU (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469.

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

61. EarleyKW, HaagJR, PontesO, OpperK, JuehneT, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616–629.

62. DeplanckeB, VermeirssenV, ArdaHE, MartinezNJ, WalhoutAJ (2006) Gateway-compatible yeast one-hybrid screens. CSH Protoc 2006 doi: 10.1101/pdb.prot4590

63. BowlerC, BenvenutoG, LaflammeP, MolinoD, ProbstA, et al. (2004) Chromatin techniques for plant cells. Plant J 39: 776–789.

64. SchmidtH, BöttcherC, TrampczynskaA, ClemensS (2011) Use of recombinantly produced 15N3-labelled nicotianamine for fast and sensitive stable isotope dilution ultra-performance liquid chromatography/electrospray ionization time-of-flight mass spectrometry. Anal Bioanal Chem 399: 1355–1361.