Nutrient homeostasis within the plant circadian network

Frontiers in Plant Science

Volumn 6, Issue APR, 2015, Pages

  Haydon, Michael J ^a   Román, Ángela ^a   Arshad, Waheed ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Arabidopsis; Carbohydrate; Circadian clocks; Ion; Metal; Micronutrient; Nutrient; Plants

Indexed keywords

ARABIDOPSIS;

EID: 84934873958     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00299     Document Type: Review

References (68)

1. Amtmann, A., and Blatt, M. R. (2009). Regulation of macronutrient transport. New Phytol. 181, 35-52. doi: 10. 1111/j. 1469-8137. 2008. 02666. x.
2. Andrés-Colás, N., Perea-García, A., Puig, S., and Peñarrubia, L. (2010). Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles. Plant Physiol. 153, 170-184. doi: 10. 1104/pp. 110. 153676.
3. Blaby-Haas, C. E., and Merchant, S. S. (2013). Iron sparing and recycling in a compartmentalized cell. Curr. Opin. Microbiol. 16, 677-685. doi: 10. 1016/j. mib. 2013. 07. 019.
4. Bläsing, O. E., Gibon, Y., Günther, M., Höhne, M., Morcuende, R., Osuna, D., et al. (2005). Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17, 3257-3281. doi: 10. 1105/tpc. 105. 035261.
5. Caldeira, C. F., Jeanguenin, L., Chaumont, F., and Tardieu, F. (2014). Circadian rhythms of hydraulic conductance and growth are enhanced by drought and improve plant performance. Nat. Commun. 5, 5365. doi: 10. 1038/ncomms6365.
6. Cao, M. J., Wang, Z., Wirtz, M., Hell, R., Oliver, D. J., and Xiang, C. B. (2013). SULTR3; 1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J. 73, 607-616. doi: 10. 1111/tpj. 12059.
7. Chen, Y.-Y., Wang, Y., Shin, L.-J., Wu, J.-F., Shanmugam, V., Tsednee, M., et al. (2013). Iron is involved in the maintenance of circadian period length in Arabidopsis. Plant Physiol. 161, 1409-1420. doi: 10. 1104/pp. 112. 212068.
8. Chiasson, D. M., Loughlin, P. C., Mazurkiewicz, D., Mohammadidehcheshmeh, M., Fedorova, E. E., Okamoto, M., et al. (2014). Soybean SAT1 (Symbiotic Ammonium Transporter 1) encodes a bHLH transcription factor involved in nodule growth and NH4+ transport. Proc. Natl. Acad. Sci. U. S. A. 111, 4814-4819. doi: 10. 1073/pnas. 1312801111.
9. Clemens, S., Palmgren, M. G., and Krämer, U. (2002). A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7, 309-315. doi: 10. 1016/S1360-1385(02)02295-1.
10. Covington, M. F., Maloof, J. N., Straume, M., Kay, S. A., and Harmer, S. L. (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130. doi: 10. 1186/gb-2008-9-8-r130.
11. Dalchau, N., Baek, S. J., Briggs, H. M., Robertson, F. C., Dodd, A. N., Gardner, M. J., et al. (2011). The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc. Natl. Acad. Sci. U. S. A. 108, 5104-5109. doi: 10. 1073/pnas. 1015452108.
12. Ding, Z., Millar, A. J., Davis, A. M., and Davis, S. J. (2007). TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell 19, 1522-1536. doi: 10. 1105/tpc. 106. 047241.
13. Dodd, A. N., Gardner, M. J., Hotta, C. T., Hubbard, K. E., Dalchau, N., Love, J., et al. (2007). TheArabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318, 1789-1792. doi: 10. 1126/science. 1146757.
14. Dodd, A. N., Kudla, J., and Sanders, D. (2010). The language of calcium signaling. Annu. Rev. Plant Biol. 61, 593-620. doi: 10. 1146/annurev-arplant-070109-104628.
15. Dodd, A. N., Parkinson, K., and Webb, A. A. R. (2004). Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol. 162, 63-70. doi: 10. 1111/j. 1469-8137. 2004. 01005. x.
16. Dodd, A. N., Salathia, N., Hall, A., Kévei, E., Tóth, R., Nagy, F., et al. (2005). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633. doi: 10. 1126/science. 1115581.
17. Duc, C., Cellier, F., Lobréaux, S., Briat, J. F., and Gaymard, F. (2009). Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee. J. Biol. Chem. 284, 36271-36281. doi: 10. 1074/jbc. M109. 059873.
18. Endo, M., Shimizu, H., Nohales, M. A., Araki, T., and Kay, S. A. (2014). Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515, 419-422. doi: 10. 1038/nature13919.
19. Fan, S.-C., Lin, C.-S., Hsu, P.-K., Lin, S.-H., and Tsay, Y.-F. (2009). The Arabidopsis nitrate transporter NRT1. 7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell 21, 2750-2761. doi: 10. 1105/tpc. 109. 067603.
20. Gazzarrini, S., Lejay, L., Gojon, A., Ninnemann, O., Frommer, W. B., and Von Wirén, N. (1999). Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11, 937-947. doi: 10. 1105/tpc. 11. 5. 937.
21. Gilliham, M., Dayod, M., Hocking, B. J., Xu, B., Conn, S. J., Kaiser, B. N., et al. (2011). Calcium delivery and storage in plant leaves: exploring the link with water flow. J. Exp. Bot. 62, 2233-2250. doi: 10. 1093/jxb/err111.
22. Graf, A., Schlereth, A., Stitt, M., and Smith, A. M. (2010). Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc. Natl. Acad. Sci. U. S. A. 107, 9458-9463. doi: 10. 1073/pnas. 0914299107.
23. Grossmann, G., Guo, W.-J., Ehrhardt, D. W., Frommer, W. B., Sit, R. V., Quake, S. R., et al. (2011). The RootChip: an integrated microfluidic chip for plant science. Plant Cell 23, 4234-4240. doi: 10. 1105/tpc. 111. 092577.
24. Gutiérrez, R. A., Stokes, T. L., Thum, K., Xu, X., Obertello, M., Katari, M. S., et al. (2008). Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc. Natl. Acad. Sci. U. S. A. 105, 4939-4944. doi: 10. 1073/pnas. 0800211105.
25. Harmer, S. L., Hogenesch, J. B., Straume, M., Chang, H., Han, B., Zhu, T., et al. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113. doi: 10. 1126/science. 290. 5499. 2110.
26. Haydon, M. J. (2014). Getting a sense for zinc in plants. New Phytol. 202, 10-12. doi: 10. 1111/nph. 12736.
27. Haydon, M. J., Bell, L. J., and Webb, A. A. R. (2011). Interactions between plant circadian clocks and solute transport. J. Exp. Bot. 62, 2333-2348. doi: 10. 1093/jxb/err040.
28. Haydon, M. J., Hearn, T. J., Bell, L. J., Hannah, M. A., and Webb, A. A. R. (2013a). Metabolic regulation of circadian clocks. Semin. Cell Dev. Biol. 24, 414-421. doi: 10. 1016/j. semcdb. 2013. 03. 007.
29. Haydon, M. J., Mielzcarek, O., Robertson, F. C., Hubbard, K. E., and Webb, A. A. R. (2013b). Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502, 689-692. doi: 10. 1038/nature12603.
30. Hermans, C., Hammond, J. P., White, P. J., and Verbruggen, N. (2006). How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 11, 610-617. doi: 10. 1016/j. tplants. 2006. 10. 007.
31. Hermans, C., Vuylsteke, M., Coppens, F., Craciun, A., Inzé, D., and Verbruggen, N. (2010a). Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol. 187, 119-131. doi: 10. 1111/j. 1469-8137. 2010. 03258. x.
32. Hermans, C., Vuylsteke, M., Coppens, F., Cristescu, S. M., Harren, F. J. M., Inzé, D., et al. (2010b). Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol. 187, 132-144. doi: 10. 1111/j. 1469-8137. 2010. 03257. x.
33. Ho, C.-H., Lin, S.-H., Hu, H.-C., and Tsay, Y.-F. (2009). CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194. doi: 10. 1016/j. cell. 2009. 07. 004.
34. Hong, S., Kim, S. A., Guerinot, M. L., and McClung, C. R. (2013). Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. Plant Physiol. 161, 893-903. doi: 10. 1104/pp. 112. 208603.
35. Hsu, P. Y., and Harmer, S. L. (2014). Wheels within wheels: the plant circadian system. Trends Plant Sci. 19, 240-249. doi: 10. 1016/j. tplants. 2013. 11. 007.
36. James, A. B., Monreal, J. A., Nimmo, G. A., Kelly, C. L., Herzyk, P., Jenkins, G. I., et al. (2008). The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322, 1832-1835. doi: 10. 1126/science. 1161403.
37. Johnson, C. H., Knight, M. R., Kondo, T., Masson, P., Sedbrook, J., Haley, A., et al. (1995). Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269, 1863-1865. doi: 10. 1126/science. 7569925.
38. Kaasik, K., and Lee, C. C. (2004). Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430, 467-471. doi: 10. 1038/nature02724.
39. Kim, W.-Y., Fujiwara, S., Suh, S.-S., Kim, J., Kim, Y., Han, L., et al. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356-360. doi: 10. 1038/nature06132.
40. Knight, H., Thomson, A. J. W., and McWatters, H. G. (2008). SENSITIVE TO FREEZING6 integrates cellular and environmental inputs to the plant circadian clock. Plant Physiol. 148, 293-303. doi: 10. 1104/pp. 108. 123901.
41. Koussevitzky, S., Nott, A., Mockler, T. C., Hong, F., Sachetto-Martins, G., Surpin, M., et al. (2007). Signals from chloroplasts converge to regulate nuclear gene expression. Science 316, 715-719. doi: 10. 1126/science. 1140516.
42. Krebs, M., Held, K., Binder, A., Hashimoto, K., Den Herder, G., Parniske, M., et al. (2012). FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics. Plant J. 69, 181-192. doi: 10. 1111/j. 1365-313X. 2011. 04780. x.
43. Lanquar, V., Grossmann, G., Vinkenborg, J. L., Merkx, M., Thomine, S., and Frommer, W. B. (2014). Dynamic imaging of cytosolic zinc in Arabidopsis roots combining FRET sensors and RootChip technology. New Phytol. 202, 198-208. doi: 10. 1111/nph. 12652.
44. Lebaudy, A., Vavasseur, A., Hosy, E., Dreyer, I., Leonhardt, N., Thibaud, J.-B., et al. (2008). Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels. Proc. Natl. Acad. Sci. U. S. A. 105, 5271-5276. doi: 10. 1073/pnas. 0709732105.
45. Liu, T., Carlsson, J., Takeuchi, T., Newton, L., and Farré, E. M. (2013). Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J. 76, 101-114. doi: 10. 1111/tpj. 12276.
46. Love, J., Dodd, A. N., and Webb, A. A. R. (2004). Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16, 956-966. doi: 10. 1105/tpc. 020214.
47. Malapeira, J., Khaitova, L. C., and Mas, P. (2012). Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc. Natl. Acad. Sci. U. S. A. 109, 21540-21545. doi: 10. 1073/pnas. 1217022110.
48. Martí, M. C., Stancombe, M. A., and Webb, A. A. R. (2013). Cell-and stimulus type-specific intracellular free Ca2+ signals in Arabidopsis. Plant Physiol. 163, 625-634. doi: 10. 1104/pp. 113. 222901.
49. Noordally, Z. B., Ishii, K., Atkins, K. A., Wetherill, S. J., Kusakina, J., Walton, E. J., et al. (2013). Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339, 1316-1319. doi: 10. 1126/science. 1230397.
50. Perea-García, A., Andrés-Colás, N., and Peñarrubia, L. (2010). Copper homeostasis influences the circadian clock in Arabidopsis. Plant Signal. Behav. 5, 1237-1240. doi: 10. 4161/psb. 5. 10. 12920.
51. Ravet, K., Touraine, B., Boucherez, J., Briat, J. F., Gaymard, F., and Cellier, F. (2009). Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J. 57, 400-412. doi: 10. 1111/j. 1365-313X. 2008. 03698. x.
52. Salomé, P. A., Oliva, M., Weigel, D., and Krämer, U. (2013). Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function. EMBO J. 32, 511-523. doi: 10. 1038/emboj. 2012. 330.
53. Sanchez-Villarreal, A., Shin, J., Bujdoso, N., Obata, T., Neumann, U., Du, S. X., et al. (2013). TIME FOR COFFEE is an essential component in the maintenance of metabolic homeostasis in Arabidopsis thaliana. Plant J. 76, 188-200. doi: 10. 1111/tpj. 12292.
54. Shcolnick, S., and Keren, N. (2006). Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiol. 141, 805-810. doi: 10. 1104/pp. 106. 079251.
55. Shikanai, T., Müller-Moulé, P., Munekage, Y., Niyogi, K. K., and Pilon, M. (2003). PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15, 1333-1346. doi: 10. 1105/tpc. 011817.
56. Smith, A. M., and Stitt, M. (2007). Coordination of carbon supply and plant growth. Plant Cell Environ. 30, 1126-1149. doi: 10. 1111/j. 1365-3040. 2007. 01708. x.
57. Song, Y. H., Ito, S., and Imaizumi, T. (2010). Similarities in the circadian clock and photoperiodism in plants. Curr. Opin. Plant Biol. 13, 594-603. doi: 10. 1016/j. pbi. 2010. 05. 004.
58. Sweeney, B. M., and Folli, S. I. (1984). Nitrate deficiency shortens the circadian period in Gonyaulax. Plant Physiol. 75, 242-245. doi: 10. 1104/pp. 75. 1. 242.
59. Takase, T., Ishikawa, H., Murakami, H., Kikuchi, J., Sato-Nara, K., and Suzuki, H. (2011). The circadian clock modulates water dynamics and aquaporin expression in Arabidopsis roots. Plant Cell Physiol. 52, 373-383. doi: 10. 1093/pcp/pcq198.
60. 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. doi: 10. 1046/j. 1365-313X. 2002. 01381. x.
61. Versaw, W. K., Harrison, M. J., Samuel, T., Noble, R., and Parkway, S. N. (2002). A chloroplast phosphate transporter, PHT2; 1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14, 1751-1766. doi: 10. 1105/tpc. 002220.
62. Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, L., Briat, J., et al. (2002). IRT1, anArabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223-1233. doi: 10. 1105/tpc. 001388.
63. Wang, G. Y., Shi, J. L., Ng, G., Battle, S. L., Zhang, C., and Lu, H. (2011). Circadian clock-regulated phosphate transporter PHT4; 1 plays an important role in Arabidopsis defense. Mol. Plant 4, 516-526. doi: 10. 1093/mp/ssr016.
64. Wang, Y., and Wu, W.-H. (2013). Potassium transport and signaling in higher plants. Annu. Rev. Plant Biol. 64, 451-476. doi: 10. 1146/annurev-arplant-050312-120153.
65. Wenden, B., Toner, D. L. K., Hodge, S. K., Grima, R., and Millar, A. J. (2012). Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf. Proc. Natl. Acad. Sci. U. S. A. 109, 6757-6762. doi: 10. 1073/pnas. 1118814109.
66. Woodson, J. D., Perez-ruiz, J. M., and Chory, J. (2011). Heme synthesis by plastid Ferrochelatase I regulates nuclear gene expression in plants. Curr. Biol. 21, 897-903. doi: 10. 1016/j. cub. 2011. 04. 004.
67. Yin, L., Wu, N., Curtin, J. C., Qatanani, M., Szwergold, N. R., Reid, R. A., et al. (2007). Rev-erbα, a heme sensor that coordinates metabolic and circadian pathways. Science 318, 1786-1789. doi: 10. 1126/science. 1150179.
68. Zhang, H., Zhao, X., Li, J., Cai, H., Deng, X. W., and Li, L. (2014). MicroRNA408 is critical for theHY5-SPL7 gene network that mediates the coordinated response to light and copper. Plant Cell 26, 4933-4953. doi: 10. 1105/tpc. 114. 127340.