Correction: Systems and trans-system level analysis identifies conserved iron deficiency responses in the plant lineage (Plant Cell, (2012) 24, (3921-3948), 10.1105/tpc.112.102491);Systems and Trans-system level analysis identifies conserved iron deficiency responses in the plant lineage

Plant Cell

Volumn 24, Issue 10, 2012, Pages 3921-3948

  Urzica, Eugen I ^a   Casero, David ^a,b   Yamasaki, Hiroaki ^a,b   Hsieh, Scott I ^a   Adler, Lital N ^a   Karpowicz, Steven J ^a,c   Blaby Haas, Crysten E ^a   Clarke, Steven G ^a   Loo, Joseph A ^a,b   Pellegrini, Matteo ^a,b   Merchanta, Sabeeha S ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CENTRAL OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84870706076     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.19.00217     Document Type: Erratum

References (143)

1. Allen, A.E., Laroche, J., Maheswari, U., Lommer, M., Schauer, N., Lopez, P.J., Finazzi, G., Fernie, A.R., and Bowler, C. (2008). Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl. Acad. Sci. USA 105: 10438-10443.
2. Allen, M.D., del Campo, J.A., Kropat, J., and Merchant, S.S. (2007a). FEA1, FEA2, and FRE1, encoding two homologous secreted proteins and a candidate ferrireductase, are expressed coordinately with FOX1 and FTR1 in iron-deficient Chlamydomonas reinhardtii. Eukaryot. Cell 6: 1841-1852.
3. Allen, M.D., Kropat, J., Tottey, S., Del Campo, J.A., and Merchant, S.S. (2007b). Manganese deficiency in Chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol. 143: 263-277.
4. Allmer, J., Naumann, B., Markert, C., Zhang, M., and Hippler, M. (2006). Mass spectrometric genomic data mining: Novel insights into bioenergetic pathways in Chlamydomonas reinhardtii. Proteomics 6: 6207-6220.
5. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11: R106.
6. Andrews, N.C. (2000). Iron homeostasis: Insights from genetics and animal models. Nat. Rev. Genet. 1: 208-217.
7. Atteia, A., et al. (2009). A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the alpha-proteobacterial mitochondrial ancestor. Mol. Biol. Evol. 26: 1533-1548.
8. Bauer, P., Ling, H.Q., and Guerinot, M.L. (2007). FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis. Plant Physiol. Biochem. 45: 260-261.
9. Behrenfeld, M.J., et al. (2009). Satellite-detected fluorescence reveals global physiology of ocean phytoplankton. Biogeosciences 6: 779.
10. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B. Methodol. 57: 289-300.
11. Bernal, M., Casero, D., Singh, V., Wilson, G.T., Grande, A., Yang, H., Dodani, S.C., Pellegrini, M., Huijser, P., Connolly, E.L., Merchant, S.S., and Krämer, U. (2012). Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24: 738-761.
12. Blaby-Haas, C.E., and Merchant, S.S. (2012). The ins and outs of algal metal transport. Biochim. Biophys. Acta 1823: 1531-1552.
13. Briat, J.-F., and Lobréaux, S. (1997). Iron transport and storage in plants. Trends Plant Sci. 2: 187-193.
14. Briat, J.F., Lobréaux, S., Grignon, N., and Vansuyt, G. (1999). Regulation of plant ferritin synthesis: How and why. Cell. Mol. Life Sci. 56: 155-166.
15. Brumbarova, T., and Bauer, P. (2005). Iron-mediated control of the basic helix-loop-helix protein FER, a regulator of iron uptake in tomato. Plant Physiol. 137: 1018-1026.
16. Buckhout, T.J., Yang, T.J., and Schmidt, W. (2009). Early irondeficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genomics 10: 147.
17. Busch, A., Rimbauld, B., Naumann, B., Rensch, S., and Hippler, M. (2008). Ferritin is required for rapid remodeling of the photosynthetic apparatus and minimizes photo-oxidative stress in response to iron availability in Chlamydomonas reinhardtii. Plant J. 55: 201-211.
18. de Benoist, B., McLean, E., Egli, I., and Cogswell, M., eds. (2008). Worldwide Prevalence of Anaemia 1993-2005: WHO Global Database on Anaemia. (WHO Press: Geneva, Switzerland).
19. Cardol, P., González-Halphen, D., Reyes-Prieto, A., Baurain, D., Matagne, R.F., and Remacle, C. (2005). The mitochondrial oxidative phosphorylation proteome of Chlamydomonas reinhardtii deduced from the Genome Sequencing Project. Plant Physiol. 137: 447-459.
20. Cardol, P., Vanrobaeys, F., Devreese, B., Van Beeumen, J., Matagne, R.F., and Remacle, C. (2004). Higher plant-like subunit composition of mitochondrial complex I from Chlamydomonas reinhardtii: 31 conserved components among eukaryotes. Biochim. Biophys. Acta 1658: 212-224.
21. Castruita, M., Casero, D., Karpowicz, S.J., Kropat, J., Vieler, A., Hsieh, S.I., Yan, W., Cokus, S., Loo, J.A., Benning, C., Pellegrini, M., and Merchant, S.S. (2011). Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23: 1273-1292.
22. Chen, J.C., Hsieh, S.I., Kropat, J., and Merchant, S.S. (2008). A ferroxidase encoded by FOX1 contributes to iron assimilation under conditions of poor iron nutrition in Chlamydomonas. Eukaryot. Cell 7: 541-545.
23. Chen, Y.H., Wu, X.M., Ling, H.Q., and Yang, W.C. (2006). Transgenic expression of DwMYB2 impairs iron transport from root to shoot in Arabidopsis thaliana. Cell Res. 16: 830-840.
24. Clemens, S. (2006). Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707-1719.
25. Clemens, S., Naumann, B., and Hippler, M. (2009). Proteomics of metal mediated protein dynamics in plants-Iron and cadmium in the focus. Front. Biosci. 14: 1955-1969.
26. Colangelo, E.P., and Guerinot, M.L. (2004). The essential basic helixloop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400-3412.
27. 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.
28. Conte, S., Stevenson, D., Furner, I., and Lloyd, A. (2009). Multiple antibiotic resistance in Arabidopsis is conferred by mutations in a chloroplastlocalized transport protein. Plant Physiol. 151: 559-573.
29. Courville, P., Chaloupka, R., and Cellier, M.F. (2006). Recent progress in structure-function analyses of Nramp proton-dependent metal-ion transporters. Biochem. Cell Biol. 84: 960-978.
30. De Domenico, I., McVey Ward, D., and Kaplan, J. (2008). Regulation of iron acquisition and storage: Consequences for iron-linked disorders. Nat. Rev. Mol. Cell Biol. 9: 72-81.
31. Deng, X., and Eriksson, M. (2007). Two iron-responsive promoter elements control expression of FOX1 in Chlamydomonas reinhardtii. Eukaryot. Cell 6: 2163-2167.
32. Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J., and Benfey, P.N. (2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320: 942-945.
33. Dorn, K.V., Willmund, F., Schwarz, C., Henselmann, C., Pohl, T., Hess, B., Veyel, D., Usadel, B., Friedrich, T., Nickelsen, J., and Schroda, M. (2010). Chloroplast DnaJ-like proteins 3 and 4 (CDJ3/4) from Chlamydomonas reinhardtii contain redox-active Fe-S clusters and interact with stromal HSP70B. Biochem. J. 427: 205-215.
34. Douglas, S.E., and Penny, S.L. (1999). The plastid genome of the cryptophyte alga, Guillardia theta: Complete sequence and conserved synteny groups confirm its common ancestry with red algae. J. Mol. Evol. 48: 236-244.
35. 2-concentrating mechanism regulator CIA5/CCM1. Plant Cell 24: 1876-1893.
36. Fei, X., and Deng, X. (2007). A novel Fe deficiency-responsive element (FeRE) regulates the expression of atx1 in Chlamydomonas reinharditii. Plant Cell Physiol. 48: 1496-1503.
37. Fei, X., Eriksson, M., Li, Y., and Deng, X. (2010). A novel negative Fedeficiency-responsive element and a TGGCA-type-like FeRE control the expression of FTR1 in Chlamydomonas reinhardtii. J. Biomed. Biotechnol. 2010: 790247.
38. Fei, X., Eriksson, M., Yang, J., and Deng, X. (2009). An Fe deficiency responsive element with a core sequence of TGGCA regulates the expression of FEA1 in Chlamydomonas reinharditii. J. Biochem. 146: 157-166.
39. Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
40. Fleming, M.D., Trenor, C.C., IIISu, M.A., Foernzler, D., Beier, D.R., Dietrich, W.F., and Andrews, N.C. (1997). Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 16: 383-386.
41. 561, ascorbic acid, and transmembrane electron transfer. Am. J. Clin. Nutr. 54(6, Suppl) 1173S-1178S.
42. Foyer, C.H., and Noctor, G. (2011). Ascorbate and glutathione: The heart of the redox hub. Plant Physiol. 155: 2-18.
43. Geromanos, S.J., Vissers, J.P., Silva, J.C., Dorschel, C.A., Li, G.Z., Gorenstein, M.V., Bateman, R.H., and Langridge, J.I. (2009). The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS/MS. Proteomics 9: 1683-1695.
44. Gill, S.S., and Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48: 909-930.
45. Guerinot, M.L., and Yi, Y. (1994). Iron: Nutritious, noxious, and not readily available. Plant Physiol. 104: 815-820.
46. Harris, E.H. (2009). The Chlamydomonas Sourcebook, 2nd ed. (San Diego, CA: Academic Press).
47. Hell, R., and Stephan, U.W. (2003). Iron uptake, trafficking and homeostasis in plants. Planta 216: 541-551.
48. Hellman, N.E., and Gitlin, J.D. (2002). Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 22: 439-458.
49. Howe, G., and Merchant, S. (1992). Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol. 98: 127-136.
50. 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.
51. Jeong, J., Cohu, C., Kerkeb, L., Pilon, M., Connolly, E.L., and Guerinot, M.L. (2008). Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc. Natl. Acad. Sci. USA 105: 10619-10624.
52. Jeong, J., and Guerinot, M.L. (2009). Homing in on iron homeostasis in plants. Trends Plant Sci. 14: 280-285.
53. Karpowicz, S.J., Prochnik, S.E., Grossman, A.R., and Merchant, S.S. (2011). The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J. Biol. Chem. 286: 21427-21439.
54. 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.
55. Kosman, D.J. (2010). Redox cycling in iron uptake, efflux, and trafficking. J. Biol. Chem. 285: 26729-26735.
56. Kourmpetis, Y.A., van Dijk, A.D., Bink, M.C., van Ham, R.C., and ter Braak, C.J. (2010). Bayesian Markov Random Field analysis for protein function prediction based on network data. PLoS ONE 5: e9293.
57. Kropat, J., Tottey, S., Birkenbihl, R.P., Depège, N., Huijser, P., and Merchant, S. (2005). A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc. Natl. Acad. Sci. USA 102: 18730-18735.
58. La Fontaine, S., Quinn, J.M., Nakamoto, S.S., Page, M.D., Göhre, V., Moseley, J.L., Kropat, J., and Merchant, S. (2002). Copperdependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot. Cell 1: 736-757.
59. Lanquar, V., Lelièvre, F., Bolte, S., Hamès, C., Alcon, C., Neumann, D., Vansuyt, G., Curie, C., Schröder, A., Krämer, U., Barbier-Brygoo, H., and Thomine, S. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24: 4041-4051.
60. Li, G.Z., Vissers, J.P., Silva, J.C., Golick, D., Gorenstein, M.V., and Geromanos, S.J. (2009). Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Proteomics 9: 1696-1719.
61. Li, J., Wu, X.D., Hao, S.T., Wang, X.J., and Ling, H.Q. (2008). Proteomic response to iron deficiency in tomato root. Proteomics 8: 2299-2311.
62. Li, L., Chen, O.S., McVey Ward, D., and Kaplan, J. (2001). CCC1 is a transporter that mediates vacuolar iron storage in yeast. J. Biol. Chem. 276: 29515-29519.
63. Lill, R., and Mühlenhoff, U. (2008). Maturation of iron-sulfur proteins in eukaryotes: Mechanisms, connected processes, and diseases. Annu. Rev. Biochem. 77: 669-700.
64. 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.
65. Linster, C.L., Gomez, T.A., Christensen, K.C., Adler, L.N., Young, B.D., Brenner, C., and Clarke, S.G. (2007). Arabidopsis VTC2 encodes a GDP-L-galactose phosphorylase, the last unknown enzyme in the Smirnoff-Wheeler pathway to ascorbic acid in plants. J. Biol. Chem. 282: 18879-18885.
66. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25: 402-408.
67. Lohr, M., Im, C.S., and Grossman, A.R. (2005). Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiol. 138: 490-515.
68. Lohr, M., Schwender, J., and Polle, J.E. (2012). Isoprenoid biosynthesis in eukaryotic phototrophs: A spotlight on algae. Plant Sci. 185-186: 9-22.
69. Long, J.C., Sommer, F., Allen, M.D., Lu, S.F., and Merchant, S.S. (2008). FER1 and FER2 encoding two ferritin complexes in Chlamydomonas reinhardtii chloroplasts are regulated by iron. Genetics 179: 137-147.
70. 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.
71. MacDiarmid, C.W., Milanick, M.A., and Eide, D.J. (2003). Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. J. Biol. Chem. 278: 15065-15072.
72. McKie, A.T. (2008). The role of Dcytb in iron metabolism: An update. Biochem. Soc. Trans. 36: 1239-1241.
73. McKie, A.T., et al. (2001). An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291: 1755-1759.
74. Merchant, S.S., Allen, M.D., Kropat, J., Moseley, J.L., Long, J.C., Tottey, S., and Terauchi, A.M. (2006). Between a rock and a hard place: Trace element nutrition in Chlamydomonas. Biochim. Biophys. Acta 1763: 578-594.
75. Merchant, S.S., and Helmann, J.D. (2012). Elemental economy: Microbial strategies for optimizing growth in the face of nutrient limitation. Adv. Microb. Physiol. 60: 91-210.
76. Miyake, C., and Asada, K. (1992). Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol. 33: 541-553.
77. Morel, F.M.M., Hudson, R.J.M., and Price, N.M. (1991). Limitation of productivity by trace metals in the sea. Limnol. Oceanogr. 36: 1742.
78. Morrissey, J., Baxter, I.R., Lee, J., Li, L., Lahner, B., Grotz, N., Kaplan, J., Salt, D.E., and Guerinot, M.L. (2009). The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21: 3326-3338.
79. Morrissey, J., and Guerinot, M.L. (2009). Iron uptake and transport in plants: The good, the bad, and the ionome. Chem. Rev. 109: 4553-4567.
80. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5: 621-628.
81. Moseley, J.L., Allinger, T., Herzog, S., Hoerth, P., Wehinger, E., Merchant, S., and Hippler, M. (2002). Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J. 21: 6709-6720.
82. Naumann, B., Busch, A., Allmer, J., Ostendorf, E., Zeller, M., Kirchhoff, H., and Hippler, M. (2007). Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7: 3964-3979.
83. Naumann, B., Stauber, E.J., Busch, A., Sommer, F., and Hippler, M. (2005). N-terminal processing of Lhca3 Is a key step in remodeling of the photosystem I-light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii. J. Biol. Chem. 280: 20431-20441.
84. Nevo, Y., and Nelson, N. (2006). The NRAMP family of metal-ion transporters. Biochim. Biophys. Acta 1763: 609-620.
85. 561. Ann. N. Y. Acad. Sci. 493: 108-119.
86. Obayashi, T., Kinoshita, K., Nakai, K., Shibaoka, M., Hayashi, S., Saeki, M., Shibata, D., Saito, K., and Ohta, H. (2007). ATTED-II: A database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res. 35 (Database issue): D863-D869.
87. Obayashi, T., Nishida, K., Kasahara, K., and Kinoshita, K. (2011). ATTED-II updates: Condition-specific gene coexpression to extend coexpression analyses and applications to a broad range of flowering plants. Plant Cell Physiol. 52: 213-219.
88. Ogo, Y., Itai, R.N., Nakanishi, H., Inoue, H., Kobayashi, T., Suzuki, M., Takahashi, M., Mori, S., and Nishizawa, N.K. (2006). Isolation and characterization of IRO2, a novel iron-regulated bHLH transcription factor in graminaceous plants. J. Exp. Bot. 57: 2867-2878.
89. Page, M.D., Allen, M.D., Kropat, J., Urzica, E.I., Karpowicz, S.J., Hsieh, S.I., Loo, J.A., and Merchant, S.S. (2012). Fe sparing and Fe recycling contribute to increased superoxide dismutase capacity in iron-starved Chlamydomonas reinhardtii. Plant Cell 24: 2649-2665.
90. Philpott, C.C. (2006). Iron uptake in fungi: A system for every source. Biochim. Biophys. Acta 1763: 636-645.
91. Philpott, C.C., and Protchenko, O. (2008). Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot. Cell 7: 20-27.
92. Portnoy, M.E., Liu, X.F., and Culotta, V.C. (2000). Saccharomyces cerevisiae expresses three functionally distinct homologues of the nramp family of metal transporters. Mol. Cell. Biol. 20: 7893-7902.
93. Quinn, J.M., and Merchant, S. (1998). Copper-responsive gene expression during adaptation to copper deficiency. Methods Enzymol. 297: 263-279.
94. Rampey, R.A., Woodward, A.W., Hobbs, B.N., Tierney, M.P., Lahner, B., Salt, D.E., and Bartel, B. (2006). An Arabidopsis basic helix-loop-helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness. Genetics 174: 1841-1857.
95. Reinhardt, I., Haebel, S., Herbik, A., and Buckhout, T.J. (2006). Proteomic studies under iron stress: Iron deficiency-induced regulation of protein synthesis in the green alga Chlamydomonas reinhardtii. In Iron Nutrition in Plants and Rhizospheric Microorganisms, L.L. Barton and J. Abadia, eds (Dordrecht, The Netherlands: Springer), pp. 371-393.
96. Riedel, H.D., Remus, A.J., Fitscher, B.A., and Stremmel, W. (1995). Characterization and partial purification of a ferrireductase from human duodenal microvillus membranes. Biochem. J. 309: 745-748.
97. Rubio, V., Linhares, F., Solano, R., Martín, A.C., Iglesias, J., Leyva, A., and Paz-Ares, J. (2001). A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15: 2122-2133.
98. Ruiz, F.A., Marchesini, N., Seufferheld, M., Govindjee, Docampo, R. (2001). The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J. Biol. Chem. 276: 46196-46203.
99. Salahudeen, A.A., Thompson, J.W., Ruiz, J.C., Ma, H.W., Kinch, L.N., Li, Q., Grishin, N.V., and Bruick, R.K. (2009). An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326: 722-726.
100. Santi, S., and Schmidt, W. (2009). Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol. 183: 1072-1084.
101. Schaaf, G., Honsbein, A., Meda, A.R., Kirchner, S., Wipf, D., and von Wirén, N. (2006). AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J. Biol. Chem. 281: 25532-25540.
102. Schloss, J.A. (1990). A Chlamydomonas gene encodes a G protein beta subunit-like polypeptide. Mol. Gen. Genet. 221: 443-452.
103. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501-506.
104. Schuler, M., Keller, A., Backes, C., Philippar, K., Lenhof, H.P., and Bauer, P. (2011). Transcriptome analysis by GeneTrail revealed regulation of functional categories in response to alterations of iron homeostasis in Arabidopsis thaliana. BMC Plant Biol. 11: 87.
105. Schultz, I.J., Chen, C., Paw, B.H., and Hamza, I. (2010). Iron and porphyrin trafficking in heme biogenesis. J. Biol. Chem. 285: 26753-26759.
106. Shen, J., Xu, X., Li, T., Cao, D., and Han, Z. (2008). An MYB transcription factor from Malus xiaojinensis has a potential role in iron nutrition. J. Integr. Plant Biol. 50: 1300-1306.
107. Silva, J.C., Denny, R., Dorschel, C.A., Gorenstein, M., Kass, I.J., Li, G.Z., McKenna, T., Nold, M.J., Richardson, K., Young, P., and Geromanos, S. (2005). Quantitative proteomic analysis by accurate mass retention time pairs. Anal. Chem. 77: 2187-2200.
108. Silva, J.C., Denny, R., Dorschel, C., Gorenstein, M.V., Li, G.Z., Richardson, K., Wall, D., and Geromanos, S.J. (2006a). Simultaneous qualitative and quantitative analysis of the Escherichia coli proteome: A sweet tale. Mol. Cell Proteomics 5: 589-607.
109. Silva, J.C., Gorenstein, M.V., Li, G.Z., Vissers, J.P., and Geromanos, S.J. (2006b). Absolute quantification of proteins by LCMSE: A virtue of parallel MS acquisition. Mol. Cell. Proteomics 5: 144-156.
110. Singh, A., Kaur, N., and Kosman, D.J. (2007). The metalloreductase Fre6p in Fe-efflux from the yeast vacuole. J. Biol. Chem. 282: 28619-28626.
111. Sonnhammer, E.L., von Heijne, G., and Krogh, A. (1998). A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6: 175-182.
112. Sperotto, R.A., Boff, T., Duarte, G.L., and Fett, J.P. (2008). Increased senescence-associated gene expression and lipid peroxidation induced by iron deficiency in rice roots. Plant Cell Rep. 27: 183-195.
113. Spiller, S.C., Castelfranco, A.M., and Castelfranco, P.A. (1982). Effects of iron and oxygen on chlorophyll biosynthesis: I. In vivo observations on iron and oxygen-deficient plants. Plant Physiol. 69: 107-111.
114. Spreitzer, R.J., and Mets, L. (1981). Photosynthesis-deficient mutants of Chlamydomonas reinhardtii with associated light-sensitive phenotypes. Plant Physiol. 67: 565-569.
115. Staiger, D. (2002). Chemical strategies for iron acquisition in plants. Angew. Chem. Int. Ed. Engl. 41: 2259-2264.
116. Stanke, M., Diekhans, M., Baertsch, R., and Haussler, D. (2008). Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637-644.
117. Stein, R.J., and Waters, B.M. (2012). Use of natural variation reveals core genes in the transcriptome of iron-deficient Arabidopsis thaliana roots. J. Exp. Bot. 63: 1039-1055.
118. 561 are ascorbate-dependent ferrireductases. FEBS J. 273: 3722-3734.
119. 561 from bovine chromaffin vesicles studied by EPR, resonance Raman, and ascorbate reduction assay. J. Biochem. 135: 53-64.
120. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
121. Terauchi, A.M., Lu, S.F., Zaffagnini, M., Tappa, S., Hirasawa, M., Tripathy, J.N., Knaff, D.B., Farmer, P.J., Lemaire, S.D., Hase, T., and Merchant, S.S. (2009). Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J. Biol. Chem. 284: 25867-25878.
122. Terauchi, A.M., Peers, G., Kobayashi, M.C., Niyogi, K.K., and Merchant, S.S. (2010). Trophic status of Chlamydomonas reinhardtii influences the impact of iron deficiency on photosynthesis. Photosynth. Res. 105: 39-49.
123. Thamatrakoln, K., Korenovska, O., Niheu, A.K., and Bidle, K.D. (2012). Whole-genome expression analysis reveals a role for deathrelated genes in stress acclimation of the diatom Thalassiosira pseudonana. Environ. Microbiol. 14: 67-81.
124. Theil, E.C. (2004). Iron, ferritin, and nutrition. Annu. Rev. Nutr. 24: 327-343.
125. Thomine, S., Lelièvre, F., Debarbieux, E., Schroeder, J.I., and Barbier-Brygoo, H. (2003). AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34: 685-695.
126. Thomine, S., Wang, R., Ward, J.M., Crawford, N.M., and Schroeder, J.I. (2000). Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. USA 97: 4991-4996.
127. 561 from bean hypocotyls plasma membrane. Evidence for the presence of two heme centers. Biochim. Biophys. Acta 1468: 1-5.
128. Urzica, E.I., Adler, L.N., Page, M.D., Linster, C.L., Arbing, M.A., Casero, D., Pellegrini, M., Merchant, S.S., and Clarke, S.G. (2012). Impact of oxidative stress on ascorbate biosynthesis in Chlamydomonas via regulation of the VTC2 gene encoding a GDPL-galactose phosphorylase. J. Biol. Chem. 287: 14234-14245.
129. 561 are functional ferric reductases. Biochim. Biophys. Acta 1651: 116-123.
130. Vashisht, A.A., et al. (2009). Control of iron homeostasis by an ironregulated ubiquitin ligase. Science 326: 718-721.
131. 2 recapture. Photosynth. Res. 109: 115-122.
132. Whelan, S., and Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18: 691-699.
133. Wykoff, D.D., Grossman, A.R., Weeks, D.P., Usuda, H., and Shimogawara, K. (1999). Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc. Natl. Acad. Sci. USA 96: 15336-15341.
134. Yadavalli, V., Jolley, C.C., Malleda, C., Thangaraj, B., Fromme, P., and Subramanyam, R. (2012). Alteration of proteins and pigments influence the function of photosystem I under iron deficiency from Chlamydomonas reinhardtii. PLoS ONE 7: e35084.
135. Yagisawa, F., Nishida, K., Yoshida, M., Ohnuma, M., Shimada, T., Fujiwara, T., Yoshida, Y., Misumi, O., Kuroiwa, H., and Kuroiwa, T. (2009). Identification of novel proteins in isolated polyphosphate vacuoles in the primitive red alga Cyanidioschyzon merolae. Plant J. 60: 882-893.
136. Yamano, T., and Fukuzawa, H. (2009). Carbon-concentrating mechanism in a green alga, Chlamydomonas reinhardtii, revealed by transcriptome analyses. J. Basic Microbiol. 49: 42-51.
137. Yamasaki, H., Hayashi, M., Fukazawa, M., Kobayashi, Y., and Shikanai, T. (2009). SQUAMOSA Promoter Binding Protein-Like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21: 347-361.
138. Yang, T.J., Lin, W.D., and Schmidt, W. (2010). Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiol. 152: 2130-2141.
139. 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.
140. Yuan, Y.X., 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.
141. Zaharieva, T.B., and Abadía, J. (2003). Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221: 269-275.
142. 561 is localized in macrophage lysosomes. Biochim. Biophys. Acta 1760: 1903-1913.
143. Zheng, L., Huang, F., Narsai, R., Wu, J., Giraud, E., He, F., Cheng, L., Wang, F., Wu, P., Whelan, J., and Shou, H. (2009). Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol. 151: 262-274.