The Arabidopsis Mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25

Plant Journal

Volumn 77, Issue 6, 2014, Pages 838-851

  Yang, Yan ^a   Ou, Bin ^a   Zhang, Jinzhe ^a   Si, Wen ^a   Gu, Hongya ^a,b   Qin, Genji ^a   Qu, Li Jia ^a,b  

^a PEKING UNIVERSITY   (China)

^b The National Plant Gene Research Center Beijing   (China)

Author keywords

MED16; MED25; Mediator complex; plant iron homeostasis; yid1

Indexed keywords

ETHYLENE; IRON; PHYSIOLOGY;

IRON HOMEOSTASIS; MED16; MED25; MEDIATOR COMPLEX; YID1;

IRON COMPOUNDS;

ANIMALIA; ARABIDOPSIS;

ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; EIL1 PROTEIN, ARABIDOPSIS; EIN3 PROTEIN, ARABIDOPSIS; IRON; MEDIATOR COMPLEX; NUCLEAR PROTEIN; PFT1 PROTEIN, ARABIDOPSIS; SFR6 PROTEIN, ARABIDOPSIS; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; MED16; MED25; METABOLISM; PLANT IRON HOMEOSTASIS; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; TWO HYBRID SYSTEM; YID1;

MED16; MED25; MEDIATOR COMPLEX; PLANT IRON HOMEOSTASIS; YID1;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; IRON; MODELS, BIOLOGICAL; MUTAGENESIS, INSERTIONAL; NUCLEAR PROTEINS; PLANTS, GENETICALLY MODIFIED; SEEDLING; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84895929144     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12440     Document Type: Article

References (80)

1. Alonso, J.M., Stepanova, A.N., Solano, R., Wisman, E., Ferrari, S., Ausubel, F.M., and, Ecker, J.R., (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc. Natl Acad. Sci. USA, 100, 2992-2997.
2. Asturias, F.J., Jiang, Y.W., Myers, L.C., Gustafsson, C.M., and, Kornberg, R.D., (1999) Conserved structures of mediator and RNA polymerase II holoenzyme. Science, 283, 985-987.
3. Autran, D., Jonak, C., Belcram, K., Beemster, G.T.S., Kronenberger, J., Grandjean, O., Inzé, D., and, Traas, J., (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J. 21, 6036-6049.
4. Bäckström, S., Elfving, N., Nilsson, R., Wingsle, G., and, Björklund, S., (2007) Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the MED25 subunit. Mol. Cell, 26, 717-729.
5. Bonawitz, N.D., Soltau, W.L., Blatchley, M.R., Powers, B.L., Hurlock, A.K., Seals, L.A., Weng, J.K., Stout, J., and, Chapple, C., (2012) REF4 and RFR1, subunits of the transcriptional coregulatory complex mediator, are required for phenylpropanoid homeostasis in Arabidopsis. J. Biol. Chem. 287, 5434-5445.
6. Bourbon, H.M., (2008) Comparative genomics supports a deep evolutionary origin for the large, four-module transcriptional mediator complex. Nucleic Acids Res. 36, 3993-4008.
7. Boyce, J.M., Knight, H., Deyholos, M., Openshaw, M.R., Galbraith, D.W., Warren, G., and, Knight, M.R., (2003) The sfr6 mutant of Arabidopsis is defective in transcriptional activation via CBF/DREB1 and DREB2 and shows sensitivity to osmotic stress. Plant J. 34, 395-406.
8. Briat, J.F., Curie, C., and, Gaymard, F., (2007) Iron utilization and metabolism in plants. Curr. Opin. Plant Biol. 10, 276-282.
9. Casamassimi, A., and, Napoli, C., (2007) Mediator complexes and eukaryotic transcription regulation: an overview. Biochimie, 89, 1439-1446.
10. Cerdán, P.D., and, Chory, J., (2003) Regulation of flowering time by light quality. Nature, 423, 881-885.
11. Çevik, V., Kidd, B.N., Zhang, P., Hill, C., Kiddle, S., Denby, K.J., Holub, E.B., Cahill, D.M., Manners, J.M., and, Schenk, P.M., (2012) MED25 acts as an integrative hub for the regulation of jasmonate-responsive gene expression in Arabidopsis. Plant Physiol. 160, 541-555.
12. Chadick, J.Z., and, Asturias, F.J., (2005) Structure of eukaryotic mediator complexes. Trends Biochem. Sci. 30, 264-271.
13. Chen, Y., Yang, X., He, K., et al. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol. Biol. 60, 107-124.
14. Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R., Tang, X., and, Zhou, J.-M., (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146, 368-376.
15. Chen, R., Jiang, H., Li, L., et al. (2012) The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell, 24, 2898-2916.
16. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
17. Colangelo, E.P., and, Guerinot, M.L., (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell, 16, 3400-3412.
18. Connolly, E.L., Fett, J.P., and, Guerinot, M.L., (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell, 14, 1347-1357.
19. Connolly, E.L., Campbell, N.H., Grotz, N., Prichard, C.L., and, Guerinot, M.L., (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol. 133, 1102-1110.
20. Curie, C., Alonso, J.M., Le Jean, M., Ecker, J.R., and, Briat, J.F., (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochemical J. 347, 749-755.
21. Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Le Jean, M., Misson, J., Schikora, A., Czernic, P., and, Mari, S., (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot. 103, 1-11.
22. Dolan, L., (2001) The role of ethylene in root hair growth in Arabidopsis. J. Plant Nutr. Soil Sci. 164, 141-145.
23. Eide, D., Broderius, M., Fett, J., and, Guerinot, M.L., (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl Acad. Sci. USA, 93, 5624-5628.
24. Elfving, N., Davoine, C., Benlloch, R., et al. (2011) The Arabidopsis thaliana MED25 mediator subunit integrates environmental cues to control plant development. Proc. Natl Acad. Sci. USA, 108, 8245-8250.
25. Guglielmi, B., Van Berkum, N.L., Klapholz, B., Bijma, T., Boube, M., Boschiero, C., Bourbon, H.M., Holstege, F.C.P., and, Werner, M., (2004) A high resolution protein interaction map of the yeast mediator complex. Nucl. Acids Res. 32, 5379-5391.
26. EBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell, 115, 667-677.
27. Guo, Y., Qin, G., Gu, H., and, Qu, L.-J., (2009) HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell, 21, 3518-3534.
28. Henriques, R., Jásik, J., Klein, M., Martinoia, E., Feller, U., Schell, J., Pais, M.S., and, Koncz, C., (2002) Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol. Biol. 50, 587-597.
29. Jakoby, M., Wang, H.Y., Reidt, W., Weisshaar, B., and, Bauer, P., (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett. 577, 528-534.
30. Janody, F., Martirosyan, Z., Benlali, A., and, Treisman, J.E., (2003) Two subunits of the Drosophila mediator complex act together to control cell affinity. Development, 130, 3691-3701.
31. Jeong, J., and, Guerinot, M.L., (2009) Homing in on iron homeostasis in plants. Trends Plant Sci. 14, 280-285.
32. Kidd, B.N., Edgar, C.I., Kumar, K.K., Aitken, E.A., Schenk, P.M., Manners, J.M., and, Kazan, K., (2009) The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell, 21, 2237-2252.
33. Kim, S.A., and, Guerinot, M.L., (2007) Mining iron: iron uptake and transport in plants. FEBS Lett. 581, 2273-2280.
34. Kim, T.W., Kwon, Y.-J., Kim, J.M., Song, Y.-H., Kim, S.N., and, Kim, Y.-J., (2004) MED16 and MED23 of Mediator are coactivators of lipopolysaccharide-and heat-shock-induced transcriptional activators. Proc. Natl Acad. Sci. USA, 101, 12153-12158.
35. Kim, S.A., Punshon, T., Lanzirotti, A., Li, L., Alonso, J.M., Ecker, J.R., Kaplan, J., and, Guerinot, M.L., (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science, 314, 1295-1298.
36. Kim, Y.J., Zheng, B., Yu, Y., Won, S.Y., Mo, B., and, Chen, X., (2011) The role of mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J. 30, 814-822.
37. Knight, H., Veale, E.L., Warren, G.J., and, Knight, M.R., (1999) The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell, 11, 875-886.
38. Knight, H., Thomson, A.J.W., and, McWatters, H.G., (2008) SENSITIVE TO FREEZING 6 integrates cellular and environmental inputs to the plant circadian clock. Plant Physiol. 148, 293-303.
39. Knight, H., Mugford, S.G., Ülker, B., Gao, D., Thorlby, G., and, Knight, M.R., (2009) Identification of SFR6, a key component in cold acclimation acting post-translationally on CBF function. Plant J. 58, 97-108.
40. Korshunova, Y.O., Eide, D., Gregg Clark, W., Lou Guerinot, M., and, Pakrasi, H.B., (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40, 37-44.
41. Ling, H.-Q., Bauer, P., Bereczky, Z., Keller, B., and, Ganal, M., (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc. Natl Acad. Sci. USA, 99, 13938-13943.
42. Lingam, S., Mohrbacher, J., Brumbarova, T., Potuschak, T., Fink-Straube, C., Blondet, E., Genschik, P., and, Bauer, P., (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell, 23, 1815-1829.
43. Liu, J., Zhang, Y., Qin, G., et al. (2008) Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell, 20, 1538-1554.
44. Liu, J., Zhong, S., Guo, X., et al. (2013) Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr. Biol. 23, 993-998.
45. -ΔΔCT method. Methods, 25, 402-408.
46. Long, T.A., Tsukagoshi, H., Busch, W., Lahner, B., Salt, D.E., and, Benfey, P.N., (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell, 22, 2219-2236.
47. Marsh, H. Jr, Evans, H., and, Matrone, G., (1963) Investigations of the role of iron in chlorophyll metabolism. II. Effect of iron deficiency on chlorophyll synthesis. Plant Physiol. 38, 638-642.
48. Meyer, P.A., and, Fu, J., (2012) Mutual remodeling and conformation grid: a mediator code? Structure, 20, 755-757.
49. Mittler, G., Stühler, T., Santolin, L., Uhlmann, T., Kremmer, E., Lottspeich, F., Berti, L., and, Meisterernst, M., (2003) A novel docking site on Mediator is critical for activation by VP16 in mammalian cells. EMBO J. 22, 6494-6504.
50. Myers, L.C., and, Kornberg, R.D., (2000) Mediator of transcriptional regulation. Annu. Rev. Biochem. 69, 729-749.
51. Ogawara, T., Higashi, K., Kamada, H., and, Ezura, H., (2003) Ethylene advances the transition from vegetative growth to flowering in Arabidopsis thaliana. J. Plant Physiol. 160, 1335-1340.
52. Ou, B., Yin, K.Q., Liu, S.N., et al. (2011) A high-throughput screening system for Arabidopsis transcription factors and its application to MED25-dependent transcriptional regulation. Mol. Plant, 4, 546-555.
53. Pauwels, L., Barbero, G.F., Geerinck, J., Tilleman, S., Grunewald, W., Pérez, A.C., Chico, J.M., Bossche, R.V., Sewell, J., and, Gil, E., (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature, 464, 788-791.
54. Pitts, R.J., Cernac, A., and, Estelle, M., (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J. 16, 553-560.
55. Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C., and, Genschik, P., (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F-box proteins: EBF1 and EBF2. Cell, 115, 679-689.
56. Qin, G., Kang, D., Dong, Y., et al. (2003) Obtaining and analysis of flanking sequences from T-DNA transformants of Arabidopsis. Plant Sci. 165, 941-949.
57. Qu, L.-J., and, Zhu, X.Y., (2006) Transcription factor families in Arabidopsis: major progress and outstanding issues for future research. Curr. Opin. Plant Biol. 9, 544-549.
58. Robinson, N.J., Procter, C.M., Connolly, E.L., and, Guerinot, M.L., (1999) A ferric-chelate reductase for iron uptake from soils. Nature, 397, 694-697.
59. Römheld, V., (1987) Different strategies for iron acquisition in higher plants. Physiol. Plant. 70, 231-234.
60. Schmidt, W., (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci. 8, 188-193.
61. Shanmugam, V., Lo, J.C., Wu, C.L., Wang, S.L., Lai, C.C., Connolly, E.L., Huang, J.L., and, Yeh, K.C., (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.
62. Sivitz, A., Grinvalds, C., Barberon, M., Curie, C., and, Vert, G., (2011) Proteasome-mediated turnover of the transcriptional activator FIT is required for plant iron-deficiency responses. Plant J. 66, 1044-1052.
63. Stephan, U.W., and, Scholz, G., (1993) Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiol. Plant. 88, 522-529.
64. Sundaravelpandian, K., Chandrika, N.N.P., and, Schmidt, W., (2013) PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytol. 197, 151-161.
65. Tóth-Petróczy, Á., Oldfield, C.J., Simon, I., Takagi, Y., Dunker, A.K., Uversky, V.N., and, Fuxreiter, M., (2008) Malleable machines in transcription regulation: the mediator complex. PLoS Comput. Biol. 4, e1000243.
66. Varotto, C., Maiwald, D., Pesaresi, P., Jahns, P., Salamini, F., and, Leister, D., (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J. 31, 589-599.
67. Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F., and, Curie, C., (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell, 14, 1223-1233.
68. Walker, E.L., and, Connolly, E.L., (2008) Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Curr. Opin. Plant Biol. 11, 530-535.
69. Wang, N., Cui, Y., Liu, Y., Fan, H., Du, J., Huang, Z., Yuan, Y., Wu, H., and, Ling, H.Q., (2012) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol. Plant, 2, 503-513.
70. Weigel, D., Ahn, J.H., Blázquez, M.A., Borevitz, J.O., Christensen, S.K., Fankhauser, C., Ferrándiz, C., Kardailsky, I., Malancharuvil, E.J., and, Neff, M.M., (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003-1014.
71. Wu, R., Li, S., He, S., Wassmann, F., Yu, C., Qin, G., Schreiber, L., Qu, L.-J., and, Gu, H., (2011) CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Plant Cell, 23, 3392-3411.
72. Xu, R., and, Li, Y., (2011) Control of final organ size by Mediator complex subunit 25 in Arabidopsis thaliana. Development, 138, 4545-4554.
73. Xu, R., and, Li, Y., (2012) The Mediator complex subunit 8 regulates organ size in Arabidopsis thaliana. Plant Signal. Behav. 7, 182-183.
74. Yang, F., Vought, B.W., Satterlee, J.S., Walker, A.K., Sun, Z.-Y.J., Watts, J.L., DeBeaumont, R., Saito, R.M., Hyberts, S.G., and, Yang, S., (2006) An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature, 442, 700-704.
75. Yuan, Y., Zhang, J., Wang, D.W., and, Ling, H.Q., (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.
76. Yuan, Y., Wu, H., Wang, N., Li, J., Zhao, W., Du, J., Wang, D., and, Ling, H.Q., (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res. 18, 385-397.
77. Zhang, Y., Wu, R., Qin, G., Chen, Z., Gu, H., and, Qu, L.-J., (2011) Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis. J. Integr. Plant Biol. 53, 493-506.
78. Zhang, X., Wang, C., Zhang, Y., Sun, Y., and, Mou, Z., (2012) The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell, 24, 4294-4309.
79. Zhu, Z., An, F., Feng, Y., Li, P., Xue, L., Mu, A., Jiang, Z., Kim, J.-M., To, T.K., and, Li, W., (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl Acad. Sci. USA, 108, 12539-12544.
80. Zhu, D., Wu, Z., Cao, G., Li, J., Wei, J., Tsuge, T., Gu, H., Aoyama, T., and, Qu, L.-J., (2013) TRANSLUCENT GREEN, an ERF family transcription factor, controls water balance in Arabidopsis by activating the expression of aquaporin genes. Mol. Plant. DOI: 10.1093/mp/sst152