Autophagy as a possible mechanism for micronutrient remobilization from leaves to seeds

Frontiers in Plant Science

Volumn 5, Issue JAN, 2014, Pages

  Pottier, Mathieu ^a   Masclaux Daubresse, Céline ^b,c   Yoshimoto, Kohki ^b,c   Thomine, Sébastien ^a  

^a CEA SACLAY   (France)

^b CEMAGREF   (France)

^c INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Atg; Fe; Isotopic labeling; Leaf senescence; Nutrient fluxes; Nutrient use efficiency; Transition metal; Zn

Indexed keywords

EID: 84901041391     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00011     Document Type: Review

References (109)

1. Aggarwal, A., Sharma, I., Tripathi, B. N., Munjal, A. K., Baunthiyal, M., and Sharma, V. (2012). "Metal toxicity and photosynthesis, " in Photosynthesis: Overviews on Recent Progress and Future Perspectives, eds S. Itoh, P. Mohanty, and K. N. Guruprasad (New Delhi: IK International Publishing House (Pvt) Limited).
2. Alloway, B. J. (2009). Soil factors associated with zinc deficiency in crops and humans. Environ. Geochem. Health31, 537-548. doi: 10.1007/s10653-009-9255-4
3. Andersson, A., Keskitalo, J., Sjodin, A., Bhalerao, R., Sterky, F., Wissel, K., et al. (2004). A transcriptional timetable of autumn senescence. Genome Biol. 5, R24. doi: 10.1186/gb-2004-5-4-r24
4. Badger, M. R., and Price, G. D. (1994). The role of carbonic anhydrase in photosynthesis. Annu. Rev. Plant Biol. 45, 369-392. doi: 10.1146/annurev.pp.45.060194.002101
5. Bassham, D. C. (2007). Plant autophagy-more than a starvation response. Curr. Opin. Plant Biol. 10, 587-593. doi: 10.1016/j.pbi.2007.06.006
6. Bhalerao, R., Keskitalo, J., Sterky, F., Erlandsson, R., Björkbacka, H., Birve, S. J., et al. (2003). Gene expression in autumn leaves. Plant Physiol. 131, 430-442. doi: 10.1104/pp.012732
7. Bleackley, M. R., and Macgillivray, R. T. A. (2011). Transition metal homeostasis: from yeast to human disease. Biometals 24, 785-809. doi: 10.1007/s10534-011-9451-4
8. Breeze, E., Harrison, E., Mchattie, S., Hughes, L., Hickman, R., Hill, C., et al. (2011). High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23, 873-894. doi: 10.1105/tpc.111.083345
9. Buchanan-Wollaston, V. (1994). Isolation of cDNA clones for genes that are expressed during leaf senescence inBrassica napus (identification of a gene encoding a senescence-specific metallothionein-like protein). Plant Physiol. 105, 839-846. doi: 10.1104/pp.105.3.839
10. Buchanan-Wollaston, V. (1997). The molecular biology of leaf senescence. J. Exp. Bot. 48, 181-199. doi: 10.1093/jxb/48.2.181
11. Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Lim, P. O., Nam, H. G., et al. (2005). Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42, 567-585. doi: 10.1111/j.1365-313X.2005.02399.x
12. Chen, Y., and Barak, P. (1982). Iron nutrition of plants in calcareous soils. Adv. Agron. 35, 217-240. doi: 10.1016/S0065-2113(08)60326-0
13. Chiba, A., Ishida, H., Nishizawa, N. K., Makino, A., and Mae, T. (2003). Exclusion of ribulose-1, 5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol. 44, 914-921. doi: 10.1093/pcp/pcg118
14. Chung, T., Phillips, A. R., and Vierstra, R. D. (2010). ATG8 lipidation and ATG8-mediated autophagy in Arabidopsisrequire ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci. Plant J. 62, 483-493. doi: 10.1111/j.1365-313X.2010.04166.x
15. Crafts-Brandner, S. J., and Egli, D. B. (1987). Sink removal and leaf senescence in soybean: cultivar effects. Plant Physiol. 85, 662-666. doi: 10.1104/pp.85.3.662
16. del Rìo, L. A., Pastori, G. M., Palma, J. M., Sandalio, L. M., Sevilla, F., Corpas, F. J., et al. (1998). The activated oxygen role of peroxisomes in senescence. Plant Physiol. 116, 1195-1200. doi: 10.1104/pp.116.4.1195
17. Diaz-Troya, S., Pérez-Pérez, M. E., Florencio, F. J., and Crespo, J. L. (2008). The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4, 851-865.
18. Doelling, J. H., Walker, J. M., Friedman, E. M., Thompson, A. R., and Vierstra, R. D. (2002). The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277, 33105-33114. doi: 10.1074/jbc.M204630200
19. Erenoglu, E. B., Kutman, U. B., Ceylan, Y., Yildiz, B., and Cakmak, I. (2011). Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytol. 189, 438-448. doi: 10.1111/j.1469-8137.2010.03488.x
20. Etienne, P., Desclos, M., Le Gou, L., Gombert, J., Bonnefoy, J., Maurel, K., et al. (2007). N-protein mobilisation associated with the leaf senescence process in oilseed rape is concomitant with the disappearance of trypsin inhibitor activity. Funct. Plant Biol. 34, 895-906. doi: 10.1071/FP07088
21. Finney, L. A., and O'Halloran, T. V. (2003). Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Sci. Signal. 300, 931. doi: 10.1126/science.1085049
22. Gan, S., and Amasino, R. M. (1997). Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiol. 113, 313.
23. Gomez-Galera, S., Rojas, E., Sudhakar, D., Zhu, C., Pelacho, A. M., Capell, T., et al. (2010). Critical evaluation of strategies for mineral fortification of staple food crops. Transgenic Res. 19, 165-180. doi: 10.1007/s11248-009-019311-y
24. Graham R. D. (1988). "Genotypic diferences in tolerance to manganese deficiency, " in Manganese in Soils and Plants, eds R. D. Graham, R. J. Hannam, and N. C. Uren (Dordrecht: Kluwer Academic Publishers), 261-276.
25. Grusak, M. A. (1994). Iron transport to developing ovules of Pisum sativum (I. Seed import characteristics and phloem iron-loading capacity of source regions). Plant Physiol. 104, 649-655. doi: 10.1104/pp.104.2.649
26. Guiboileau, A., Yoshimoto, K., Soulay, F., Bataillé, M.-P., Avice, J.-C., et al. (2012). Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol. 194, 732-740. doi: 10.1111/j.1469-8137.2012.04084.x
27. Guo, Y., Cai, Z., and Gan, S. (2004). Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 27, 521-549. doi: 10.1111/j.1365-3040.2003.01158.x
28. Guo, Y., and Gan, S. (2006). AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612. doi: 10.1111/j.1365-313X.2006.02723.x
29. Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., et al. (2002). Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129, 1181-1193. doi: 10.1104/pp.011024
30. Hegelund, J. N., Pedas, P., Husted, S., Schiller, M., and Schjoerring, J. K. (2012). Zinc fluxes into developing barley grains: use of stable Zn isotopes to separate root uptake from remobilization in plants with contrasting Zn status. Plant Soil 361, 241-250. doi: 10.1007/s11104-012-1272-x
31. Hensel, L. L., Grbic, V., Baumgarten, D. A., and Bleecker, A. B. (1993). Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5, 553-564. doi: 10.1105/tpc.5.5.553
32. Himelblau, E., and Amasino, R. M. (2001). Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158, 1317-1323. doi: 10.1078/0176-1617-00608
33. Horsburgh, M. J., Wharton, S. J., Karavolos, M., and Foster, S. J. (2002). Manganese: elemental defence for a life with oxygen. Trends Microbiol. 10, 496-501. doi: 10.1016/S0966-842X(02)02462-9
34. Hörtensteiner, S., and Feller, U. (2002). Nitrogen metabolism and remobilization during senescence. J. Exp. Bot.53, 927-937. doi: 10.1093/jexbot/53.370.927
35. Hörtensteiner, S., Vicentini, F., and Matile, P. (1995). Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L: enzymatic cleavage of pheophorbide a in vitro. New Phytol. 129, 237-246. doi: 10.1111/j.1469-8137.1995.tb04293.x
36. Htwe, N. M. P. S., Yuasa, T., Ishibashi, Y., Tanigawa, H., Okuda, M., Zheng, S.-H., et al. (2011). Leaf senescence of soybean at reproductive stage is associated with induction of autophagy-related genes, GmATG8c, GmATG8i and GmATG4. Plant Prod. Sci. 14, 141-147. doi: 10.1626/pps.14.141
37. Ishida, H., Izumi, M., Wada, S., and Makino, A. (2013). Roles of autophagy in chloroplast recycling. Biochim. Biophys. Acta doi: 10.1016/j.bbabio.2013.11.009 [Epub ahead of print].
38. Ishida, H., Yoshimoto, K., Izumi, M., Reisen, D., Yano, Y., Makino, A., et al. (2008). Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol. 148, 142-155. doi: 10.1104/pp.108.122770
39. Juliano, B. O. (1993). Rice in Human Nutrition. Rome: International Rice Research Institute & FAO.
40. Kamada, Y., Funakoshi, T., Shintani, T., Nagano, K., Ohsumi, M., and Ohsumi, Y. (2000). Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150, 1507-1513. doi: 10.1083/jcb.150.6.1507
41. Karamanos, R. E., Kruger, G. A., and Stewart, J. W. B. (1986). Copper deficiency in cereal and oilseed crops in northern Canadian prairie soils. Agron. J. 78, 317-323. doi: 10.2134/agronj1986.00021962007800020021x
42. Kennedy, G., Nantel, G., and Shetty, P. (2003). The scourge of "hidden hunger": global dimensions of micronutrient deficiencies. Food Nutr. Agric. 8-16.
43. Kume, T., Matsuhashi, S., Shimazu, M., Ito, H., Fujimura, T., Adachi, K., et al. (1997). Uptake and transport of positron-emitting tracer (18 F) in plants. Appl. Radiat. Isot. 48, 1035-1043. doi: 10.1016/S0969-8043(97)00117-6
44. Kurepa, J., Hérouart, D., Van Montagu, M., and Inzé, D. (1997). Differential expression of CuZn-and Fe-superoxide dismutase genes of tobacco during development, oxidative stress, and hormonal treatments. Plant Cell Physiol. 38, 463-470. doi: 10.1093/oxfordjournals.pcp.a029190
45. Lanquar, V., Lelievre, F., Bolte, S., Hames, C., Alcon, C., Neumann, D., et al. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041-4051. doi: 10.1038/sj.emboj.7600864
46. Lanquar, V., Ramos, M. S., Lelièvre, F., Barbier-Brygoo, H., Krieger-Liszkay, A., Kramer, U., et al. (2010). Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol. 152, 1986-1999. doi: 10.1104/pp.109.150946
47. Lemaître, T., Gaufichon, L., Boutet-Mercey, S., Christ, A., and Masclaux-Daubresse, C. (2008). Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant Cell Physiol. 49, 1056-1065. doi: 10.1093/pcp/pcn081
48. Li, F., and Vierstra, R. D. (2012). Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci. 17, 526-537. doi: 10.1016/j.tplants.2012.05.006
49. Lu, Y., Hall, D. A., and Last, R. L. (2011). A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. Plant Cell 23, 1861-1875. doi: 10.1105/tpc.111.085456
50. Luk, E. E. C., and Culotta, V. C. (2001). Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J. Biol. Chem. 276, 47556-47562. doi: 10.1074/jbc.M108923200
51. Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., and Suzuki, A. (2010). Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105, 1141-1157. doi: 10.1093/aob/mcq028
52. Masclaux-Daubresse, C. L., and Chardon, F. (2011). Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. J. Exp. Bot. 62, 2131-2142. doi: 10.1093/jxb/erq405
53. Masclaux, C., Quilleré, I., Gallais, A., and Hirel, B. (2001). The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Ann. Appl. Biol. 138, 69-81. doi: 10.1111/j.1744-7348.2001.tb00086.x
54. Masclaux, C., Valadier, M.-H., Brugière, N., Morot-Gaudry, J.-F., and Hirel, B. (2000). Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211, 510-518. doi: 10.1007/s004250000310
55. Masuda, H., Ishimaru, Y., Aung, M. S., Kobayashi, T., Kakei, Y., Takahashi, M., et al. (2012). Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci. Rep. 2, 543. doi:10.1038/srep00543
56. Matsuura, A., Tsukada, M., Wada, Y., and Ohsumi, Y. (1997). Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192, 245-250. doi: 10.1016/S0378-1119(97)00084-X
57. 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. doiI: 10.1021/cr900112r
58. Noda, T., and Ohsumi, Y. (1998). Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273, 3963-3966. doi: 10.1074/jbc.273.7.3963
59. Nooden, L. D., Guiamet, J. J., and John, I. (1997). Senescence mechanisms. Physiol. Plant. 101, 746-753. doi: 10.1111/j.1399-3054.1997.tb01059.x
60. Nooden, L. D., Hillsberg, J. W., and Schneider, M. J. (1996). Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect. Physiol. Plant. 96, 491-495. doi: 10.1111/j.1399-3054.1996.tb00463.x
61. Noquet, C., Avice, J.-C., Rossato, L., Beauclair, P., Henry, M.-P., and Ourry, A. (2004). Effects of altered source-sink relationships on N allocation and vegetative storage protein accumulation in Brassica napus L. Plant Sci. 166, 1007-1018. doi: 10.1016/j.plantsci.2003.12.014
62. Nouet, C., Motte, P., and Hanikenne, M. (2011). Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci. 16, 395-404. doi: 10.1016/j.tplants.2011.03.005
63. Olmos, S., Distelfeld, A., Chicaiza, O., Schlatter, A. R., Fahima, T., Echenique, V., et al. (2003). Precise mapping of a locus affecting grain protein content in durum wheat. Theor. Appl. Genet. 107, 1243-1251. doi: 10.1007/s00122-003-1377-y
64. Palmgren, M. G., Clemens, S., Williams, L. E., Kramer, U., Borg, S., Schjorring, J. K., et al. (2008). Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 13, 464-473. doi: 10.1016/j.tplants.2008.06.005
65. Park, S.-Y., Yu, J.-W., Park, J.-S., Li, J., Yoo, S.-C., Lee, N.-Y., et al. (2007). The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19, 1649-1664. doi: 10.1105/tpc.106.044891
66. Patrick, J. W., and Offler, C. E. (2001). Compartmentation of transport and transfer events in developing seeds. J. Exp. Bot. 52, 551-564. doi: 10.1093/jexbot/52.356.551
67. Patterson, T. G., and Brun, W. A. (1980). Influence of sink removal in the senescence pattern of wheat. Crop Sci. 20, 19-23. doi: 10.2135/cropsci1980.0011183X002000010006x
68. Phillips, A. R., Suttangkakul, A., and Vierstra, R. D. (2008). The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178, 1339-1353. doi: 10.1534/genetics.107.086199
69. Pierre, J. L., and Fontecave, M. (1999). Iron and activated oxygen species in biology: the basic chemistry. Biometals 12, 195-199. doi: 10.1023/A:1009252919854
70. Pilon, M. (2011). Moving copper in plants. New Phytol. 192, 305-307. doi: 10.1111/j.1469-8137.2011.03869.x
71. Pittman, J. K. (2005). Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol. 167, 733-742. doi: 10.1111/j.1469-8137.2005.01453.x
72. Puig, S., and Peñarrubia, L. (2009). Placing metal micronutrients in context: transport and distribution in plants. Curr. Opin. Plant Biol 12, 299-306. doi: 10.1016/j.pbi.2009.04.008
73. Salon, C., Avice, J. C., Alain, O., Prudent, M., and Voisin, A.-S. (2011). "Plant N fluxes and modulation by nitrogen, heat, and water stresses: a review based on comparison of legumes and non legume plants, " in Abiotic Stress in Plants-Mechanisms and Adaptations, eds A. Shanker and B. Venkateswarlu (Rijeka: InTech), 78-118.
74. Schjoerring, J. K., Bock, J. G. H., Gammelvind, L., Jensen, C. R., and Mogensen, V. O. (1995). Nitrogen incorporation and remobilization in different shoot components of field-grown winter oilseed rape (Brassica napusL.) as affected by rate of nitrogen application and irrigation. Plant Soil 177, 255-264. doi: 10.1007/BF00010132
75. Smart, C. M., Hosken, S. E., Thomas, H., Greaves, J. A., Blair, B. G., and Schuch, W. (1995). The timing of maize leaf senescence and characterisation of senescence-related cDNAs. Physiol. Plant. 93, 673-682. doi: 10.1111/j.1399-3054.1995.tb05116.x
76. Sondergaard, T. E., Schulz, A., and Palmgren, M. G. (2004). Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol. 136, 2475-2482. doi: 10.1104/pp.104.048231
77. Sperotto, R. A., Boff, T., Duarte, G. L., Santos, L. S., Grusak, M. A., and Fett, J. P. (2010). Identification of putative target genes to manipulate Fe and Zn concentrations in rice grains. J. Plant Physiol. 167, 1500-1506. doi: 10.1016/j.jplph.2010.05.003
78. Sperotto, R. A., Ricachenevsky, F. K., Duarte, G. L., Boff, T., Lopes, K. L., Sperb, E. R., et al. (2009). Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230, 985-1002. doi: 10.1007/s00425-009-1000-9
79. Sperotto, R. A., Ricachenevsky, F. K., Waldow, V. D. A., and Fett, J. P. (2012a). Iron biofortification in rice: it's a long way to the top. Plant Sci. 190, 24-39. doi: 10.1016/j.plantsci.2012.03.004
80. Sperotto, R. A., Vasconcelos, M. W., Grusak, M. A., and Fett, J. P. (2012b). Effects of different Fe supplies on mineral partitioning and remobilization during the reproductive development of rice (Oryza sativa L.). Rice 5, 1-11. doi: 10.1186/1939-8433-5-27
81. Suttangkakul, A., Li, F., Chung, T., and Vierstra, R. D. (2011). The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23, 3761-3779. doi: 10.1105/tpc.111.090993
82. Tanaka, M., Wallace, I. S., Takano, J., Roberts, D. M., and Fujiwara, T. (2008). NIP6; 1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 20, 2860-2875. doi: 10.1105/tpc.108.058628
83. 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. doi: 10.1046/j.1365-313X.2003.01760.x
84. Thomine, S., and Vert, G. (2013). Iron transport in plants: better be safe than sorry. Curr. Opin. Plant Biol 16, 322-327. doi: 10.1016/j.pbi.2013.01.003
85. Thompson, A. R., and Vierstra, R. D. (2005). Autophagic recycling: lessons from yeast help define the process in plants. Curr. Opin. Plant Biol 8, 165-173. doi: 10.1016/j.pbi.2005.01.013
86. Tommos, C., Hoganson, C. W., Di Valentin, M., Lydakis-Simantiris, N., Dorlet, P., Westphal, K., et al. (1998). Manganese and tyrosyl radical function in photosynthetic oxygen evolution. Curr. Opin. Chem. Biol 2, 244-252. doi: 10.1016/S1367-5931(98)80066-5
87. Tsukamoto, T., Nakanishi, H., Kiyomiya, S., Watanabe, S., Matsuhashi, S., Nishizawa, N. K., et al. (2006). 52Mn translocation in barley monitored using a positron-emitting tracer imaging system. Soil Sci. Plant Nutr. 52, 717-725. doi:10.1111/j.1747-0765.2006.00096.x
88. Tsukamoto, T., Nakanishi, H., Uchida, H., Watanabe, S., Matsuhashi, S., Mori, S., et al. (2009). 52Fe Translocation in barley as monitored by a positron-emitting tracer imaging system (PETIS): evidence for the direct translocation of Fe from roots to young leaves via phloem. Plant Cell Physiol. 50, 48-57. doi: 10.1093/pcp/pcn192
89. Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., and Dubcovsky, J. (2006). A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298-1301. doi: 10.1126/science.1133649
90. van der Graaff, E., Schwacke, R., Schneider, A., Desimone, M., Flugge, U.-I., and Kunze, R. (2006). Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 141, 776-792. doi: 10.1104/pp.106.079293
91. Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T., et al. (2009). Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol. 149, 885-893. doi: 10.1104/pp.108.130013
92. Wang, Y. X., Specht, A., and Horst, W. J. (2010). Stable isotope labelling and zinc distribution in grains studied by laser ablation ICP-MS in an ear culture system reveals zinc transport barriers during grain filling in wheat. New Phytol. 189, 428-437. doi: 10.1111/j.1469-8137.2010.03489.x
93. Watanabe, M., Balazadeh, S., Tohge, T., Erban, A., Giavalisco, P., Kopka, J., et al. (2013). Comprehensive dissection of spatio-temporal metabolic shifts in primary, secondary and lipid metabolism during developmental senescence in Arabidopsis thaliana. Plant Physiol. 162, 1290-1310. doi:10.1104/pp.113.217380
94. Waters, B. M., and Sankaran, R. P. (2011). Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci. 180, 562-574. doi: 10.1016/j.plantsci.2010.12.003
95. Waters, B. M., Uauy, C., Dubcovsky, J., and Grusak, M. A. (2009). Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J. Exp. Bot. 60, 4263-4274. doi: 10.1093/jxb/erp257
96. White, P. J., and Broadley, M. R. (2009). Biofortification of crops with seven mineral elements often lacking in human diets-iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 182, 49-84. doi: 10.1111/j.1469-8137.2008.02738.x
97. WHO. (2002). World Health Report 2002: World Health Report: Reducing Risks to Health Noncommunicable Diseases. Geneva: World Health Organization.
98. Wu, C.-Y., Lu, L.-L., Yang, X.-E., Feng, Y., Wei, Y.-Y., Hao, H.-L., et al. (2010). Uptake, translocation, and remobilization of zinc absorbed at different growth stages by rice genotypes of different Zn densities. J. Agric. Food Chem. 58, 6767-6773. doi: 10.1021/jf100017e
99. Xiao, W., Sheen, J., and Jang, J.-C. (2000). The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol. Biol. 44, 451-461. doi: 10.1023/A:1026501430422
100. Yamaji, N., and Ma, J. F. (2009). A transporter at the node responsible for intervascular transfer of silicon in rice. Plant Cell 21, 2878-2883. doi: 10.1105/tpc.109.069831
101. Yoshida, S. (2003). Molecular regulation of leaf senescence. Curr. Opin. Plant Biol 6, 79-84. doi: 10.1016/S1369526602000092
102. Yoshimoto, K. (2012). Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol. 53, 1355-1365. doi: 10.1093/pcp/pcs099
103. Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T., et al. (2004). Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16, 2967-2983. doi: 10.1105/tpc.104.025395
104. Yoshimoto, K., Jikumaru, Y., Kamiya, Y., Kusano, M., Consonni, C., Panstruga, R., et al. (2009). Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21, 2914-2927. doi: 10.1105/tpc.109.068635
105. Yruela, I. (2009). Copper in plants: acquisition, transport and interactions. Funct. Plant Biol. 36, 409-430. doi: 10.1071/FP08288
106. Yruela, I. (2013). Transition metals in plant photosynthesis. Metallomics 5, 1090-1109. doi: 10.1039/C3MT00086A
107. Zavaleta-Mancera, H., Franklin, K., Ougham, H., Thomas, H., and Scott, I. (1999). Regreening of senescentNicotiana leaves. II. Redifferenciation of plastids. J. Exp. Biol. 50, 1683-1689. doi: 10.1093/jxb/50.340.1683
108. Zelisko, A., Garcia-Lorenzo, M., Jackowski, G., Jansson, S., and Funk, C. (2005). AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc. Natl. Acad. Sci. U.S.A. 102, 13699-13704. doi: 10.1073/pnas.0503472102
109. Zheng, L., Yamaji, N., Yokosho, K., and Ma, J. F. (2012). YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. Plant Cell 24, 3767-3782. doi: 10.1105/tpc.112.103820