Signaling mechanisms integrating carbon and nitrogen utilization in plants
Received date: 03 Sep 2012
Accepted date: 09 Oct 2012
Published date: 01 Dec 2012
Copyright
Carbon (C) and nitrogen (N) are two essential nutrients affecting plant growth and development. Plants are non-motile organisms and have evolved highly sophisticated and complex sensing and signaling mechanisms to respond to the dynamic changes of C and N nutrients in their surroundings. C and N metabolism are tightly coordinated to maintain intracellular C/N homeostasis. However, the regulatory mechanism underlying C/N coordination and balancing in plants remains to be elucidated. It has been suggested that C and N metabolism are modulated by the interaction of C signaling with N signaling or by C/N ratio signaling. This review focuses on cell signaling studies that provide insight into the regulation mechanism of C/N balancing in plants.
Key words: carbon; nitrogen; balancing; coordination; signaling
Yuying SANG , Wenfeng SUN , Zhenbiao YANG . Signaling mechanisms integrating carbon and nitrogen utilization in plants[J]. Frontiers in Biology, 2012 , 7(6) : 548 -556 . DOI: 10.1007/s11515-012-1249-4
1 |
Baena-Gonzalez E, Rolland F, Thevelein J M, Sheen J (2007). A central integrator of transcription networks in plant stress and energy signalling. Nature, 448(7156): 938–942
|
2 |
Barbosa J M, Singh N K, Cherry J H, Locy R D (2010). Nitrate uptake and utilization is modulated by exogenous γ-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiol Biochem, 48(6): 443–450
|
3 |
Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H (1996). Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J, 15(12): 2988–2996
|
4 |
Beuve N, Rispail N, Laine P, Cliquet J B, Ourry A, Le Deunff E (2004). Putative role of γ-amino- butyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ, 27(8): 1035–1046
|
5 |
Bi Y M, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S (2005). Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. Plant J, 44(4): 680–692
|
6 |
Bouche N, Fromm H (2004). GABA in plants: just a metabolite? Trends Plant Sci, 9(3): 110–115
|
7 |
Bown A W, Shelp B J (1997). The metabolism and functions of γ-aminobutyric acid. Plant Physiol, 115(1): 1–5
|
8 |
Chen Y M, Ferrar T S, Lohmeier-Vogel E M, Morrice N, Mizuno Y, Berenger B, Ng K K, Muench D G, Moorhead G B (2006). The PII signal transduction protein of Arabidopsis thaliana forms an arginine-regulated complex with plastid N-acetyl glutamate kinase. J Biol Chem, 281(9): 5726–5733
|
9 |
Chiang Y H, Zubo Y O, Tapken W, Kim H J, Lavanway A M, Howard L, Pilon M, Kieber J J, Schaller G E (2012). Functional characterization of the GATA transcription factors GNC and CGA1 reveals their key role in chloroplast development, growth, and division in Arabidopsis. Plant Physiol, 160(1): 332–348
|
10 |
Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolaï M, Bedu M, Robaglia C, Meyer C (2007). The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep, 8(9): 864–870
|
11 |
Diaz C, Kusano M, Sulpice R, Araki M, Redestig H, Saito K, Stitt M, Shin R (2011). Determining novel functions of Arabidopsis 14-3-3 proteins in central metabolic processes. BMC Syst Biol, 5(1): 192–201
|
12 |
Fait A, Nesi A N, Angelovici R, Lehmann M, Pham P A, Song L, Haslam R P, Napier J A, Galili G, Fernie A R (2011). Targeted enhancement of glutamate-to-γ-aminobutyrate conversion in Arabidopsis seeds affects carbon-nitrogen balance and storage reserves in a development-dependent manner. Plant Physiol, 157(3): 1026–1042
|
13 |
Faix B, Radchuk V, Nerlich A, Hümmer C, Radchuk R, Emery R J, Keller H, Götz K P, Weschke W, Geigenberger P, Weber H (2012). Barley grains, deficient in cytosolic small subunit of ADP-glucose pyrophosphorylase, reveal coordinate adjustment of C:N metabolism mediated by an overlapping metabolic-hormonal control. Plant J, 69(6): 1077–1093
|
14 |
Ferl R J, Chung H J, Sehnke P C (1999). The 14–3-3 proteins: cellular regulators of plant metabolism.
|
15 |
Ferrario-Mery S, Meyer C, Hodges M (2008). Chloroplast nitrite uptake is enhanced in Arabidopsis PII mutants. FEBS Lett, 582(7): 1061–1066
|
16 |
Foyer C H, Noctor G, Hodges M (2011). Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot, 62(4): 1467–1482
|
17 |
Gao P, Xin Z, Zheng Z L (2008). The OSU1/QUA2/TSD2-encoded putative methyltransferase is a critical modulator of carbon and nitrogen nutrient balance response in Arabidopsis. PLoS ONE, 3(1): e1387
|
18 |
Gutierrez R A, Stokes T L, Thum K, Xu X, Obertello M, Katari M S, Tanurdzic M, Dean A, Nero D C, McClung C R, Coruzzi G M (2008). Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA, 105(12): 4939–4944
|
19 |
Halford N G, Hey S, Jhurreea D, Laurie S, McKibbin R S, Paul M, Zhang Y (2003). Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J Exp Bot, 54(382): 467–475
|
20 |
Hanning I, Heldt H W (1993). On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L). leaves: Partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products. Plant Physiol, 103(4): 1147–1154
|
21 |
Hershko A, Ciechanover A (1998). The ubiquitin system. Annu Rev Biochem, 67(1): 425–479
|
22 |
Hey S J, Byrne E, Halford N G (2010). The interface between metabolic and stress signaling. Ann Bot (Lond), 105(2): 197–203
|
23 |
Hsieh M H, Lam H M, van de Loo F J, Coruzzi G (1998). A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc Natl Acad Sci USA, 95(23): 13965–13970
|
24 |
Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001). Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature, 409(6823): 1060–1063
|
25 |
Jacinto E, Loewith R, Schmidt A, Lin S, Rüegg M A, Hall A, Hall M N (2004). Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol, 6(11): 1122–1128
|
26 |
Jang J C, León P, Zhou L, Sheen J (1997). Hexokinase as a sugar sensor in higher plants. Plant Cell, 9(1): 5–19
|
27 |
Joy K W (1988). Ammonia, glutamine, and asparagine: a carbon-nitrogen interface. Can J Bot, 66: 2103–2109
|
28 |
Kang J, Mehta S, Turano F J (2004). The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signaling to control development and water loss. Plant Cell Physiol, 45(10): 1380–1389
|
29 |
Kang J, Turano F J (2003). The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc Natl Acad Sci USA, 100(11): 6872–6877
|
30 |
Kiba T, Kudo T, Kojima M, Sakakibara H (2011). Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot, 62(4): 1399–1409
|
31 |
Kinnersley A M, Lin F (2000). Receptor modifiers indicate that γ-aminobutyric acid (GABA) is a potential modulator of ion transport in plants. Plant Growth Regul, 32(1): 65–76
|
32 |
Krouk G, Crawford N M, Coruzzi G M, Tsay Y F (2010). Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol, 13(3): 266–273
|
33 |
Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R (2011). Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnol J, 9(8): 826–837
|
34 |
Laurie S, McKibbin R S, Halford N G (2003). Antisense SNF1-related (SnRK1) protein kinase gene represses transient activity of an alpha-amylase (alpha-Amy2) gene promoter in cultured wheat embryos. J Exp Bot, 54(383): 739–747
|
35 |
Li J Y, Liu X H, Cai Q S, Gu H, Zhang S S, Wu Y Y, Wang C J (2008). Effects of elevated CO2 on growth, carbon assimilation, photosynthate accumulation and related enzymes in rice leaves during sink-source transition. J Integr Plant Biol, 50(6): 723–732
|
36 |
Longstreth D J, Nobel P S (1980). Nutrient Influences on Leaf Photosynthesis: effects of nitrogen, phosphorus, and potassium for Gossypium hirsutum L. Plant Physiol, 65(3): 541–543
|
37 |
Maekawa S, Sato T, Asada Y, Yasuda S, Yoshida M, Chiba Y, Yamaguchi J (2012). The Arabidopsis ubiquitin ligases ATL31 and ATL6 control the defense response as well as the carbon/nitrogen response. Plant Mol Biol, 79(3): 217–227
|
38 |
Malamy J E, Ryan K S (2001). Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol, 127(3): 899–909
|
39 |
Masumoto C, Miyazawa S, Ohkawa H, Fukuda T, Taniguchi Y, Murayama S, Kusano M, Saito K, Fukayama H, Miyao M (2010). Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc Natl Acad Sci USA, 107(11): 5226–5231
|
40 |
McKibbin R S, Muttucumaru N, Paul M J, Powers S J, Burrell M M, Coates S, Purcell P C, Tiessen A, Geigenberger P, Halford N G (2006). Production of high-starch, low-glucose potatoes through over-expression of the metabolic regulator SnRK1. Plant Biotechnol J, 4(4): 409–418
|
41 |
Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002). Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA, 99(9): 6422–6427
|
42 |
Naito T, Kiba T, Koizumi N, Yamashino T, Mizuno T (2007). Characterization of a unique GATA family gene that responds to both light and cytokinin in Arabidopsis thaliana. Biosci Biotechnol Biochem, 71(6): 1557–1560
|
43 |
Nero D, Krouk G, Tranchina D, Coruzzi G M (2009). A system biology approach highlights a hormonal enhancer effect on regulation of genes in a nitrate responsive “biomodule”. BMC Syst Biol, 3(1): 59
|
44 |
Ninfa A J, Atkinson M R (2000). PII signal transduction proteins. Trends Microbiol, 8(4): 172–179
|
45 |
Ninfa A J, Jiang P (2005). PII signal transduction proteins: sensors of α-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol, 8(2): 168–173
|
46 |
Nunes-Nesi A, Fernie A R, Stitt M (2010). Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant, 3(6): 973–996
|
47 |
Oka M, Shimoda Y, Sato N, Inoue J, Yamazaki T, Shimomura N, Fujiyama H (2012). Abscisic acid substantially inhibits senescence of cucumber plants (Cucumis sativus) grown under low nitrogen conditions. J Plant Physiol, 169(8): 789–796
|
48 |
Paul M J, Primavesi L F, Jhurreea D, Zhang Y (2008). Trehalose metabolism and signaling. Annu Rev Plant Biol, 59(1): 417–441
|
49 |
Price J, Laxmi A, St Martin S K, Jang J C (2004). Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell, 16(8): 2128–2150
|
50 |
Rahayu Y S, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F (2005). Root-derived cytokinins as long-distance signals for NO3—induced stimulation of leaf growth. J Exp Bot, 56(414): 1143–1152
|
51 |
Rolland F, Baena-Gonzalez E, Sheen J (2006). Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol, 57(1): 675–709
|
52 |
Saci A, Cantley L C, Carpenter C L (2011). Rac1 regulates the activity of mTORC1 and mTORC2 and controls cellular size. Mol Cell, 42(1): 50–61
|
53 |
Sanchez S, Demain A L (2002). Metabolic regulation of fermentation processes. Enzyme Microb Technol, 31(7): 895–906
|
54 |
Sato T, Maekawa S, Yasuda S, Domeki Y, Sueyoshi K, Fujiwara M, Fukao Y, Goto D B, Yamaguchi J (2011a). Identification of 14-3-3 proteins as a target of ATL31 ubiquitin ligase, a regulator of the C/N response in Arabidopsis. Plant J, 68(1): 137–146
|
55 |
Sato T, Maekawa S, Yasuda S, Yamaguchi J (2011b). Carbon and nitrogen metabolism regulated by the ubiquitin-proteasome system. Plant Signal Behav, 6(10): 1465–1468
|
56 |
Schmelzle T, Hall M N (2000). TOR, a central controller of cell growth. Cell, 103(2): 253–262
|
57 |
Smeekens S, Ma J, Hanson J, Rolland F (2010). Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol, 13(3): 274–279
|
58 |
Sreenivasulu N, Radchuk V, Alawady A, Borisjuk L, Weier D, Staroske N, Fuchs J, Miersch O, Strickert M, Usadel B, Wobus U, Grimm B, Weber H, Weschke W (2010). De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8. Plant J, 64(4): 589–603
|
59 |
Stitt M (1999). Nitrate regulation of metabolism and growth. Curr Opin Plant Biol, 2(3): 178–186
|
60 |
Stitt M, Krapp A (1999). The molecular physiological basis for the interaction between elevated carbon dioxide and nutrients. Plant Cell Environ, 22: 583–622
|
61 |
Storm-Mathisen J (1974). GABA as a transmitter in the central nervous system of vertebrates. J Neural Transm, 11: 227–253
|
62 |
Sugiyama K, Hayakawa T, Kudo T, Ito T, Yamaya T (2004). Interaction of N-acetylglutamate kinase with a PII-like protein in rice. Plant Cell Physiol, 45(12): 1768–1778
|
63 |
Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004). AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol, 45(8): 1053–1062
|
64 |
Toroser D, Plaut Z, Huber S C (2000). Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiol, 123(1): 403–412
|
65 |
Uhrig R G, Ng K K, Moorhead G B (2009). PII in higher plants: a modern role for an ancient protein. Trends Plant Sci, 14(9): 505–511
|
66 |
Vidal E A, Gutierrez R A (2008). A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol, 11(5): 521–529
|
67 |
Walch-Liu P, Neumann G, Bangerth F, Engels C (2000). Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot, 51(343): 227–237
|
68 |
Xiong Y, Sheen J (2012). Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J Biol Chem, 287(4): 2836–2842
|
69 |
Xu G, Fan X, Miller A J (2012). Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol, 63(1): 153–182
|
70 |
Yanagisawa S (2000). Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J, 21(3): 281–288
|
71 |
Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004). Metabolic engineering with Dof1 transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA, 101(20): 7833–7838
|
72 |
Zhang Y, Primavesi L F, Jhurreea D, Andralojc P J, Mitchell R A, Powers S J, Schluepmann H, Delatte T, Wingler A, Paul M J (2009). Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol, 149(4): 1860–1871
|
73 |
Zheng Z L (2009). Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav, 4(7): 584–591
|
74 |
Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini D M (2011). mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science, 334(6056): 678–683
|
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