Molybdenum and iron mutually impact their homeostasis in cucumber (Cucumis sativus) plants

New Phytologist

Volumn 213, Issue 3, 2017, Pages 1222-1241

  Vigani, Gianpiero ^a   Di Silvestre, Dario ^b   Agresta, Anna Maria ^b   Donnini, Silvia ^a   Mauri, Pierluigi ^b   Gehl, Christian ^c   Bittner, Florian ^d   Murgia, Irene ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Cucumis sativus (cucumber); ionomics; iron (Fe); micronutrient homeostasis; mitochondria; molybdenum (Mo); molybdo enzymes

Indexed keywords

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; HOMEOSTASIS; IRON; METABOLISM; MITOCHONDRION; MOLECULAR ANALYSIS; MOLYBDENUM; STARVATION; TRACE ELEMENT; VINE;

CUCUMIS SATIVUS;

FORMATE DEHYDROGENASE; IRON; METALLOPROTEIN; MITOCHONDRIAL PROTEIN; MOLYBDENUM; MOLYBDENUM COFACTOR; OXIDOREDUCTASE; PROTEOME; PTERIDINE DERIVATIVE;

BIOLOGICAL MODEL; CLUSTER ANALYSIS; COENZYME; CUCUMBER; DRUG EFFECTS; HOMEOSTASIS; METABOLISM; METABOLOME; MITOCHONDRION; PLANT LEAF; PLANT ROOT;

CLUSTER ANALYSIS; COENZYMES; CUCUMIS SATIVUS; FORMATE DEHYDROGENASES; HOMEOSTASIS; IRON; METABOLOME; METALLOPROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MOLYBDENUM; OXIDOREDUCTASES; PLANT LEAVES; PLANT ROOTS; PROTEOME; PTERIDINES;

EID: 84992428192     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14214     Document Type: Article

References (109)

1. +-dependent formate dehydrogenase from plants. Acta Naturae 3: 38–54.
2. Anbar AD. 2008. Oceans. Elements and evolution. Science 322: 1481–1483.
3. Andalus S, Lopez-Millan AF, De las Rivas J, Aro EM, Abadia J, Abadia A. 2006. Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynthesis Research 89: 141–155.
4. Araulo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA et al. 2010. Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenase as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22: 1549–1563.
5. Balk J, Leaver CJ. 2001. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13: 1803–1818.
6. Balk J, Schaedler TA. 2014. Iron cofactor assembly in plants. Annual Review of Plant Physiology 65: 125–153.
7. Bashir K, Ishimaru Y, Shimo H, Nagasaka S, Fujimoto M, Takanashi H, Tsutsumi N, An G, Nakanishi H, Nishizawa NK. 2011. The rice mitochondrial iron transporter is essential for plant growth. Nature Communications 2: 322.
8. Baxter I. 2009. Ionomics: studying the social network of mineral nutrients. Current Opinion in Plant Biology 12: 381–386.
9. Baxter I, Muthukumar B, Park HC, Buchner P, Lahner B, Danku J, Zhao K, Lee J, Hawkesford MJ, Guerinot ML et al. 2008b. Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial Molybdenum Transporter (MOT1). PLoS Genetics 4: e1000004.
10. Baxter I, Vitek O, Lahner B, Muthukumar B, Borghi M, Morrissey J, Guerinot ML, Salt DE. 2008a. The leaf ionome as a multivariable system to detect a plant's physiological status. Proceedings of the National Academy of Sciences, USA 105: 12081–12086.
11. Bittner F. 2014. Molybdenum metabolism in plants and crosstalks to iron. Frontiers in Plant Science 5: 28.
12. Bittner F, Mendel RR. 2010. Cell biology of molybdenum. In: Hell R, Mendel RR, eds. Cell biology of metals and nutrients. Plant Cell Monogr, 17. Berlin, Heidelberg: Springer-Verlag, 119–143.
13. Borlotti A, Vigani G, Zocchi G. 2012. Iron deficiency affects nitrogen metabolism in cucumber (Cucumis sativus L.) plants. BMC Plant Biology 12: 189.
14. Briat JF, Dubos C, Gaymard F. 2015a. Iron nutrition, biomass production and plant product quality. Trends in Plant Science 20: 33–40.
15. Briat JF, Rouached H, Tissot N, Gaymard F, Dubos C. 2015b. Integration of P, S, Fe and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Frontiers in Plant Science 6: 290.
16. Brychkova G, Alikulov Z, Fluhr R, Sagi M. 2008. A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. Plant Journal 54: 496–509.
17. Carr S, Aebersold R, Baldwin M, Burlingame A, Clauser K, Nesvizhskii A. 2004. The need for guidelines in publication of peptide and protein identification data: working group on publication guidelines for peptide and protein identification data. Molecular & Cellular Proteomics: MCP 3: 531–533.
18. Carvalho PC, Fischer JSG, Chen EI, Yates JR 3rd, Barbosa VC. 2008. PatternLab for proteomics: a tool for differential shotgun proteomics. BMC Bioinformatics 9: 316.
19. Chamizo-Ampudia A, Galvan A, Fernandez E, Llamas A. 2011. The Chlamydomonas reinhardtii molybdenum cofactor enzyme crARC has a Zn-dependent activity and protein partners similar to those of its human homologue. Eukaryotic Cell 10: 1270–1282.
20. Ciaffi M, Paolacci AR, Celletti S, Catarcione G, Kopriva S, Astolfi S. 2013. Transcriptional and physiological changes in the S assimilation pathway due to single or combined S and Fe deprivation in durum wheat (Triticum durum L.) seedlings. Journal of Experimental Botany 64: 1663–1675.
21. Colangelo EP, Guerinot ML. 2004. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400–3412.
22. Colinas M, Fitzpatrick TB. 2015. Natures balancing act: examining biosynthesis de novo, recycling and processing damaged vitamin B metabolytes. Current Opinion in Plant Biology 25: 98–106.
23. Cosentino C, Di Silvestre D, Fischer-Schliebs E, Homann U, De Palma A, Comunian C, Mauri PL, Thiel G. 2013. Proteomic analysis of Mesembryanthemum crystallinum leaf microsomal fractions finds an imbalance in V-ATPase stoichiometry during the salt-induced transition from C3 to CAM. Biochemical Journal. 450: 407–415.
24. Delahunty CM, Yates JR III. 2007. MudPIT: multidimensional protein identification technology. BioTechniques 43: 563, 565, 567
25. +-ATPase in Fe-deficient cucumber roots by immunodetection. Plant and Soil 241: 11–17.
26. Donnini S, Prinsi B, Negri AS, Vigani G, Espen L, Zocchi G. 2010. Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots. BMC Plant Biology 10: 268.
27. Ducret A, Van Oostveen I, Eng JK, Yates J III, Aebersold R. 1998. High throughput protein characterization by automated reverse-phase chromatography/electrospray tandem mass spectrometry. Protein Science 7: 706–719.
28. Fitzpatrick KL, Tyerman SD, Kaiser BN. 2008. Molybdate transport through the plant sulfate transporter SHST1. FEBS Letters 582: 1508–1513.
29. Forieri I, Wirtz M, Hell R. 2013. Toward new perspectives on the interaction of iron and sulfur metabolism. Frontiers in Plant Science 4: 357.
30. Gasber A, Klaumann S, Trentmann O, Trampczynska A, Clemens S, Schneider S, Sauer N, Feifer I, Bittner F, Mendel RR et al. 2011. Identification of an Arabidopsis solute carrier critical for intracellular transport and inter-organ allocation of molybdate. Plant Biology 13: 710–718.
31. Gerdes S, Lerma-Ortiz C, Frelin O, Seaver SMD, Henry CS, de Crécy-Lagard V, Hanson AD. 2012. Plant B vitamin pathways and their compartmentation: a guide for the perplexed. Journal of Experimental Botany 63: 695–709.
32. Grimm S. 2012. The ER-mitochondria interface: the social network of cell death. Biochimica et Biophysica Acta 1823: 327–334.
33. Gruenewald S, Wahl B, Bittner F, Hungeling H, Kanzow S, Kotthaus J, Schwering U, Mendel RR, Clement B. 2008. The fourth molybdenum containing enzyme mARC: cloning and involvement in the activation of N-hydroxylated prodrugs. Journal of Medicinal Chemistry 51: 8173–8177.
34. Haferkamp I, Schmitz-Esser S. 2012. The plant mitochondrial carrier family: functional and evolutionary aspects. Frontiers in Plant Science 3: 2.
35. Havelund JF, Thelen JJ, Moller IM. 2013. Biochemistry, proteomics and phosphoproteomics of plant mitochondria from non-photosynthetic cells. Frontiers in Plant Science 4: 51.
36. Herbik A, Ciritch A, Horstmann C, Becker R, Balzer HJ, Baumlein H, Udo WS. 1996. Iron and copper nutrition-dependent changes in protein expression in a tomato wild type and the nicotianamine-free mutant chloronerva. Plant Physiology 11: 533–540.
37. Hesberg C, Haensch R, Mendel RR, Bittner F. 2004. Tandem orientation of duplicated xanthine dehydrogenase genes from Arabidopsis thaliana: differential gene expression and enzyme activities. Journal of Biological Chemistry 279: 13547–13554.
38. Hilario M, Kalousis A. 2008. Approaches to dimensionality reduction in proteomic biomarker studies. Briefings in Bioinformatics 9: 102–118.
39. Ide Y, Kusano M, Oikawa A, Fukushima A, Tomatsu H, Saito K, Hirai MY, Fujiwara T. 2011. Effects of molybdenum deficiency and defects in molybdate transporter MOT1 on transcript accumulation and nitrogen/sulphur metabolism in Arabidopsis thaliana. Journal of Experimental Botany 62: 1483–1497.
40. Itai RN, Ogo Y, Kobayashi T, Nakanishi H, Nishizawa NK. 2013. Rice genes involved in phytosiderophore biosynthesis are synchronously regulated during the early stages of iron deficiency in roots. Rice 6: 16.
41. Ivanov R, Brumbarova T, Bauer P. 2012. Fitting into the harsh reality: regulation of iron deficiency responses in dicotyledonous plants. Molecular Plant 5: 27–42.
42. Jain AK, Murty MN, Flynn PJ. 1999. Data clustering: a review. ACM Computing Surveys 31: 264–323.
43. Jeong J, Guerinot ML. 2009. Homing in on iron homeostasis in plants. Trends in Plant Science 14: 280–285.
44. Kaiser BN, Gridley KL, Brady JN, Phillips T, Tyerman SD. 2005. The role of molybdenum in agricultural plant production. Annals of Botany 96: 745–754.
45. Kobayashi T, Nishizawa NK. 2012. Iron uptake, translocation and regulation in higher plants. Annual Review of Plant Biology 63: 131–152.
46. Kobayashi T, Nishizawa NK. 2014. Iron sensors and signals in response to iron deficiency. Plant Science 224: 36–43.
47. Kobayashi T, Suzuki M, Inoue H, Nakanishi Itai R, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2005. Expression of iron-acquisition-related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements. Journal of Experimental Botany 56: 1305–1316.
48. Koshiba T, Saito E, Ono N, Yamamoto N, Sato M. 1996. Purification and properties of flavin- and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiology 110: 781–789.
49. Kotthaus J, Wahl B, Havemeyer A, Kotthaus J, Schade D, Garbe-Schoenberg D, Mendel R, Bittner F, Clement C. 2011. Reduction of Nω-hydroxy-l-arginine by the mitochondrial amidoxime reducing component (mARC). Biochemical Journal 433: 383–391.
50. Kumar R, Phan Tran LS, Neelakandar AK, Nguyen HT. 2012. Higher plant cytochrome b5 polypetides modulate fatty acid desaturation. PLoS ONE 7: e31370.
51. Laganowsky A, Gomez SM, Whitelegge JP, Nishio JN. 2009. Hydroponics on a chip. Analysis of the Fe deficient Arabidopsis thylakoid membrane proteome. Journal of Proteomics 72: 397–415.
52. Lan P, Li W, Wen TN, Shiau JY, Wu YC, Lin W, Schmidt W. 2011. iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for Fe homeostasis. Plant Physiology 155: 821–834.
53. Li J, Hao ST, Wang XJ, Ling HQ. 2008. Proteomic response to iron deficiency in tomato root. Proteomics 8: 2299–2311.
54. Li Y, Wang N, Zhao F, Song X, Yin Z, Huang R, Zhang C. 2014. Changes in the transcriptomic profiles of maize roots in response to iron-deficiency stress. Plant Molecular Biology 85: 349–363.
55. Lima MRM, Diaz SO, Lamego I, Grusak MA, Vasconcelos MV, Gil AM. 2014. Nuclear magnetic resonance metabolomics of iron deficiency in soybean leaves. Journal of Proteome Research 13: 3075–3087.
56. Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, 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.
57. Llamas A, Tejada-Jimenez M, Fernandez E, Galvan A. 2011. Molybdenum metabolism in the alga Chlamydomonas stands at the cross road of those in Arabidopsis and humans. Metallomics 3: 578–590.
58. Lopez-Millan AF, Grusak MA, Abadia A, Abadia J. 2013. Iron deficiency in plants: an insight from proteomic approaches. Frontiers in Plant Science 4: 254.
59. Mauri P, Dehò G. 2008. A proteomic approach to the analysis of RNA degradosome composition in Escherichia coli. Methods in Enzymology 447: 99–117.
60. Mauri P, Scarpa A, Nascimbeni AC, Benazzi L, Parmagnani E, Mafficini A, Della Peruta M, Bassi C, Miyazaki K, Sorio C. 2005. Identification of proteins released by pancreatic cancer cells by multidimensional protein identification technology: a strategy for identification of novel cancer markers. FASEB Journal 19: 1125–1127.
61. Meiser J, Lingam S, Bauer P. 2011. Posttranslational regulation of the iron deficiency basic helix-loop-helix transcription factor FIT is affected by iron and nitric oxide. Plant Physiology 157: 2154–2166.
62. Millar AH, Liddell A, Leaver CL. 2007. Isolation and subfractionation of mitochondria from plants. Methods in Cell Biology 80: 65–90.
63. Miyazaki JH, Yang SF. 1987. The methionine salvage pathway in relation to ethylene and polyamine biosynthesis. Physiologia Plantarum 69: 366–370.
64. Moran Lauter AN, Peiffer GA, Yin T, Whitham SA, Cook D, Shoemaker RC, Graham MA. 2014. Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves. BMC Genomics 15: 702.
65. Muller-Taubenberger A, Lupas AN, Li H, Ecke M, Simmeth E, Gerisch G. 2001. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO Journal 20: 6772–6782.
66. Murgia I, Vigani G. 2015. Analysis of Arabidopsis thaliana atfer4-1, atfh and atfer4-1/atfh mutants uncovers frataxin and ferritin contributions to leaf ionome homeostasis. Plant Physiology and Biochemistry 94: 65–72.
67. Nakagawa A, Sakamoto S, Takahashi M, Morikawa H, Sakamoto A. 2007. The RNAi-mediated silencing of xanthine dehydrogenase impairs growth and fertility and accelerates leaf senescence in transgenic Arabidopsis plants. Plant and Cell Physiology 48: 1484–1495.
68. Nziengui H, Bouhidel K, Der C, Marty F, Schoefs BI. 2007. Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Letters 581: 3356–3362.
69. Ott G, Havemeyer A, Clement B. 2015. The mammalian molybdenum enzymes of mARC. JBIC Journal of Biological Inorganic Chemistry 20: 265–275.
70. Palmer C, Guerinot ML. 2009. A question of balance: facing the challenges of Cu, Fe and Zn homeostasis. Nature Chemical Biology 5: 333–340.
71. Paolacci AR, Celletti S, Catarcione G, Hawkesford MJ, Astolfi S, Ciaffi M. 2014. Iron deprivation results in a rapid but not sustained increase of the expression of genes involved in iron metabolism and sulfate uptake in tomato (Solanum lycopersicum L.) seedlings. Journal of Integrative Plant Biology 56: 88–100.
72. Peng C, Uygun S, Shiu SH, Last RL. 2015. The impact of the branched-chain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiology 169: 1807–1820.
73. Ravet K, Pilon M. 2013. Copper and iron homeostasis in plants: the challenges of oxidative stress. Antioxidants & Redox Signaling 19: 919–932.
74. Regonesi ME, Del Favero M, Basilico F, Briani F, Benazzi L, Tortora P, Mauri P, Dehò G. 2006. Analysis of the Escherichia coli RNA degradosome composition by a proteomic approach. Biochimie 88: 151–161.
75. Rellán-Álvarez R, Andaluz S, Rodríguez-Celma J, Wohlgemuth G, Zocchi G, Álvarez- Fernández A, Fiehn O, López-Millán AF, Abadía J. 2010. Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply. BMC Plant Biology 10: 120–134.
76. Rellán-Álvarez R, El-Jendoubi H, Wohlgemuth G, Abadía A, Fiehn O, Abadía J, Álvarez-Fernández A. 2011. Metabolite profile changes in xylem sap and leaf extracts of strategy I plants in response to iron deficiency and resupply. Frontiers in Plant Science 2: 66.
77. Ro DK, Mah N, Ellis BE, Douglas CJ. 2001. Functional characterization and subcellular localization of poplar (Populus trichocarpa × Populus deltoides) cinnamate 4-hydroxylase. Plant Physiology 126: 317–329.
78. Rödiger A, Baudisch B, Klösgen EB. 2010. Simultaneous isolation of intact mitochondria and chloroplasts from a single pulping of plant tissue. Journal of Plant Physiology 167: 620–624.
79. Rodriguez-Celma J, Pan IC, Li W, Lan P, Buckhout TJ, Schmidt W. 2013. The transcriptional response of Arabidopsis leaves to Fe deficiency. Frontiers in Plant Science 4: 276.
80. Santi S, Schmidt W. 2009. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytologist 183: 1072–1084.
81. Schaedler TA, Thornton JD, Kruse I, Schwarzländer M, Meyer AJ, van Veen HW, Balk J. 2014. A conserved mitochondrial ATP-binding cassette transporter exports gluthatione polysulfide for cytosolic metal cofactor assembly. Journal of Biological Chemistry 289: 23264–23274.
82. Schinmachi F, Buchner P, Stroud J, Parmar S, Zhao FJ, McGrath SP, Hawkesford MJ. 2010. Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium and molybdenum in wheat. Plant Physiology 153: 327–336.
83. Schmidt H, Günther C, Weber M, Spörlein C, Loscher S, Böttcher C, Schobert R, Clemens S. 2014. Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLoS ONE 9: e102444.
84. Schuler M, Keller A, Backes C, Philippar K, Lenhof HP, Bauer P. 2011. Transcriptome analysis by GeneTrail revealed regulation of functional categories in response to alterations of iron homeostasis in Arabidopsis thaliana. BMC Plant Biology 11: 87.
85. Shinmachi F, Buchner P, Stroud JL, Parmar S, Zhao FJ, McGrath SP, Hawkesford MJ. 2010. Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium, and molybdenum in wheat. Plant Physiology 153: 327–336.
86. 24- reductase (DIMINUTO/DWARF1) show multiple subcellular localization in Arabidopsis thaliana (Heynh) L. PLoS ONE 8: e56429.
87. Sudre D, Gutierrez-Carbonell E, Lattanzio G, Rellan-Alvarez R, Gaymard F, Wohlgemuth G, Fiehn O, Alvarez-Fernandez A, Zamarreño AG, Bacaicoa E et al. 2013. Iron-dependent modifications of the flower transcriptome, proteome, metabolome, and hormonal content in an Arabidopsis ferritin mutant. Journal of Experimental Botany 64: 2665–2688.
88. Suzuki K, Itai R, Suzuki K, Nakanishi H, Nishizawa NK, Yoshimura E, Mori S. 1998. Formate dehydrogenase, an enzyme of anaerobic metabolism, is induced by iron deficiency in barley roots. Plant Physiology 116: 725–732.
89. Tan YF, O'Toole N, Taylor NL, Millar AH. 2010. Divalent metal ions in plant mitochondria and their role in interaction with proteins and oxidative stress-induced damage to respiratory function. Plant Physiology 152: 747–761.
90. Tarantino D, Casagrande F, Soave C, Murgia I. 2010. Knocking out of the mitochondrial AtFer4 ferritin does not alter response of Arabidopsis plants to abiotic stresses. Journal of Plant Physiology 167: 453–460.
91. Tarantino D, Morandini P, Ramirez L, Soave C, Murgia I. 2011. Identification of an Arabidopsis mitoferrinlike carrier protein involved in Fe metabolism. Plant Physiology and Biochemistry 49: 520–529.
92. Tarantino D, Vannini C, Bracale M, Campa M, Soave C, Murgia I. 2005. Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances Paraquat-induced photooxidative stress and nitric oxide-induced cell death. Planta 221: 757–765.
93. Teschner J, Lachmann N, Schulze J, Geisler M, Selbach K, Santamaria-Araujo J, Balk J, Mendel RR, Bittner F. 2010. A novel role for Arabidopsis mitochondrial ABC transporter ATM3 in molybdenum cofactor biosynthesis. Plant Cell 22: 468–480.
94. Timperio AM, D'Amici GM, Barta C, Loreto F, Zolla L. 2007. Proteomics, pigment composition and organization of thylakoid membranes in iron-deficient spinach leaves. Journal of Experimental Botany 58: 3695–3710.
95. Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T. 2007. An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proceedings of the National Academy of Sciences, USA 104: 18807–18812.
96. Vigani G. 2012. Discovering the role of mitochondria in the iron deficiency-induced metabolic responses of plants. Journal of Plant Physiology 169: 1–11.
97. Vigani G, Bashir K, Ishimaru Y, Lehmann M, Casiraghi FM, Nakanishi H, Seki M, Geigenberger P, Zocchi G, Nishizawa NK. 2016. Knocking down mitochondrial iron transporter (MIT) reprograms primary and secondary metabolism in rice plants. Journal of Experimental Botany 67: 1357–1368.
98. Vigani G, Maffi D, Zocchi G. 2009. Iron availability affects the function of mitochondria in cucumber roots. New Phytologist 182: 127–136.
99. Vigani G, Zocchi G. 2010. Effect of Fe deficiency on mitochondrial alternative NAD(P)H dehydrogenases in cucumber roots. Journal of Plant Physiology 167: 666–669.
100. Vigani G, Morandini P, Murgia I. 2013a. Searching iron sensors in plants by exploring the link among 2′-OG-dependent dioxygenases, the iron deficiency response and metabolic adjustments occurring under iron deficiency. Frontiers in Plant Science 4: 169.
101. Vigani G, Tarantino D, Murgia I. 2013b. Mitochondrial ferritin is a functional iron storage protein in cucumber (Cucumis sativus) roots. Frontiers in Plant Science 4: 316.
102. Vigani G, Zocchi G, Bashir K, Philippar K, Briat JF. 2013c. Signal for chloroplast and mitochondria for iron homeostasis regulation. Trends in Plant Science 18: 305–311.
103. Wang G, Wu WW, Zhang Z, Masilamani S, Shen RF. 2009. Decoy methods for assessing false positives and false discovery rates in shotgun proteomics. Analytical Chemistry 81: 146–159.
104. Witte CP, Igeño MI, Mendel R, Schwarz G, Fernandez E. 1998. The Chlamydomonas reinhardtii MoCo carrier protein is multimeric and stabilizes molybdopterin cofactor in a molybdate charged form. FEBS Letters 431: 205–209.
105. Yamaguchi J, Nishimura M. 1984. Purification of glyoxysomal catalase and immunochemical comparison of glyoxysomal and leaf peroxisomal catalase in germinating pumpkin cotyledons. Plant Physiology 74: 261–267.
106. Yang J, Giles LJ, Ruppelt C, Mendel RR, Bittner F, Kirk ML. 2015. Oxyl and hydroxyl radical transfer in mitochondrial amidoxime reducing component-catalyzed nitrite reduction. Journal of the American Chemical Society 137: 5276–5279.
107. Yokoyama K, Leimkühler S. 2015. The role of FeS clusters for molybdenum cofactor biosynthesis and molybdoenzymes in bacteria. Biochimica et Biophysica Acta 1853: 1335–1349.
108. Zhao Y, Karypis G. 2005. Data clustering in life sciences. Molecular Biotechnology 31: 55–80.
109. Zuchi S, Watanabe M, Hubberten HM, Bromke M, Osorio S, Fernie AR, Celletti S, Paolacci AR, Catarcione G, Ciaffi M et al. 2015. The interplay between sulfur and iron nutrition in tomato. Plant Physiology 169: 2624–2639.