Browse > Article
http://dx.doi.org/10.14348/molcells.2022.2029

E3 ligase BRUTUS Is a Negative Regulator for the Cellular Energy Level and the Expression of Energy Metabolism-Related Genes Encoded by Two Organellar Genomes in Leaf Tissues  

Choi, Bongsoo (Department of Life Science, Pohang University of Science and Technology)
Hyeon, Do Young (School of Biological Sciences, Seoul National University)
Lee, Juhun (Department of Life Science, Pohang University of Science and Technology)
Long, Terri A. (Department of Plant and Microbial Biology, North Carolina State University)
Hwang, Daehee (School of Biological Sciences, Seoul National University)
Hwang, Inhwan (Department of Life Science, Pohang University of Science and Technology)
Abstract
E3 ligase BRUTUS (BTS), a putative iron sensor, is expressed in both root and shoot tissues in seedlings of Arabidopsis thaliana. The role of BTS in root tissues has been well established. However, its role in shoot tissues has been scarcely studied. Comparative transcriptome analysis with shoot and root tissues revealed that BTS is involved in regulating energy metabolism by modulating expression of mitochondrial and chloroplast genes in shoot tissues. Moreover, in shoot tissues of bts-1 plants, levels of ADP and ATP and the ratio of ADP/ATP were greatly increased with a concomitant decrease in levels of soluble sugar and starch. The decreased starch level in bts-1 shoot tissues was restored to the level of shoot tissues of wild-type plants upon vanadate treatment. Through this study, we expand the role of BTS to regulation of energy metabolism in the shoot in addition to its role of iron deficiency response in roots.
Keywords
Arabidopsis thaliana; BRUTUS; energy metabolism; shoot tissues;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Bolstad, B.M., Irizarry, R.A., Astrand, M., and Speed, T.P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193.   DOI
2 Clough, S.J. and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.   DOI
3 Duby, G. and Boutry, M. (2009). The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflugers Arch. 457, 645-655.   DOI
4 Falhof, J., Pedersen, J.T., Fuglsang, A.T., and Palmgren, M. (2016). Plasma membrane H(+)-ATPase regulation in the center of plant physiology. Mol. Plant 9, 323-337.   DOI
5 Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.   DOI
6 Kaplan, J. and Ward, D.M. (2013). The essential nature of iron usage and regulation. Curr. Biol. 23, R642-R646.   DOI
7 Kobayashi, T. and Nishizawa, N.K. (2014). Iron sensors and signals in response to iron deficiency. Plant Sci. 224, 36-43.   DOI
8 Kobayashi, T., Nozoye, T., and Nishizawa, N.K. (2019). Iron transport and its regulation in plants. Free Radic. Biol. Med. 133, 11-20.   DOI
9 Kroh, G.E. and Pilon, M. (2019). Connecting the negatives and positives of plant iron homeostasis. New Phytol. 223, 1052-1055.   DOI
10 Lee, C.P., Eubel, H., Solheim, C., and Millar, A.H. (2012a). Mitochondrial proteome heterogeneity between tissues from the vegetative and reproductive stages of Arabidopsis thaliana development. J. Proteome Res. 11, 3326-3343.   DOI
11 Hindt, M.N., Akmakjian, G.Z., Pivarski, K.L., Punshon, T., Baxter, I., Salt, D.E., and Guerinot, M.L. (2017). BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana. Metallomics 9, 876-890.   DOI
12 Hossain, M.A., Kamiya, T., Burritt, D.J., Phan Tran, L.S., and Fujiwara, T. (2018). Plant Micronutrient Use Efficiency: Molecular and Genomic Perspectives in Crop Plants (San Diego: Elsevier Science & Technology).
13 Lee, J., Choi, B., Yun, A., Son, N., Ahn, G., Cha, J.Y., Kim, W.Y., and Hwang, I. (2021). Long-term abscisic acid promotes golden2-like1 degradation through constitutive photomorphogenic 1 in a light intensity-dependent manner to suppress chloroplast development. Plant Cell Environ. 44, 3034-3048.   DOI
14 Lemoine, R., La Camera, S., Atanassova, R., Dedaldechamp, F., Allario, T., Pourtau, N., Bonnemain, J.L., Laloi, M., Coutos-Thevenot, P., Maurousset, L., et al. (2013). Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci. 4, 272.   DOI
15 Lin, A., Shen, S., Wang, G., Yi, Q., Qiao, H., Niu, J., and Pan, G. (2011). Comparison of chlorophyll and photosynthesis parameters of floating and attached Ulva prolifera. J. Integr. Plant Biol. 53, 25-34.   DOI
16 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.   DOI
17 O'Neill, S.D. and Spanswick, R.M. (1984). Effects of vanadate on the plasma membrane ATPase of red beet and corn. Plant Physiol. 75, 586-591.   DOI
18 Tzafrir, I., Pena-Muralla, R., Dickerman, A., Berg, M., Rogers, R., Hutchens, S., Sweeney, T.C., McElver, J., Aux, G., Patton, D., et al. (2004). Identification of genes required for embryo development in Arabidopsis. Plant Physiol. 135, 1206-1220.   DOI
19 Mendoza-Cozatl, D.G., Xie, Q., Akmakjian, G.Z., Jobe, T.O., Patel, A., Stacey, M.G., Song, L., Demoin, D.W., Jurisson, S.S., Stacey, G., et al. (2014). OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol. Plant 7, 1455-1469.   DOI
20 Niittyla, T., Fuglsang, A.T., Palmgren, M.G., Frommer, W.B., and Schulze, W.X. (2007). Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol. Cell. Proteomics 6, 1711-1726.   DOI
21 Okumura, M., Inoue, S.I., Kuwata, K., and Kinoshita, T. (2016). Photosynthesis activates plasma membrane H+-ATPase via sugar accumulation. Plant Physiol. 171, 580-589.   DOI
22 Palmgren, M.G. (2001). Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 817-845.   DOI
23 Santi, S. and Schmidt, W. (2009). Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol. 183, 1072-1084.   DOI
24 Vert, G.G.A., Briat, J.F.O., and Curie, C. (2003). Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol. 132, 796-804.   DOI
25 Selote, D., Samira, R., Matthiadis, A., Gillikin, J.W., and Long, T.A. (2015). Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiol. 167, 273-286.   DOI
26 Shevtsov, S., Nevo-Dinur, K., Faigon, L., Sultan, L.D., Zmudjak, M., Markovits, M., and Ostersetzer-Biran, O. (2018). Control of organelle gene expression by the mitochondrial transcription termination factor mTERF22 in Arabidopsis thaliana plants. PLoS One 13, e0201631.   DOI
27 Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.   DOI
28 Wang, M., Lee, J., Choi, B., Park, Y., Sim, H.J., Kim, H., and Hwang, I. (2018). Physiological and molecular processes associated with long duration of ABA treatment. Front. Plant Sci. 9, 176.   DOI
29 Zhang, C., Romheld, V., and Marschner, H. (1996). Remobilization of iron from primary leaves of bean plants grown at various iron levels. J. Plant Nutr. 19, 1017-1028.   DOI
30 Zhang, Y., Zhang, A., Li, X., and Lu, C. (2020). The role of chloroplast gene expression in plant responses to environmental stress. Int. J. Mol. Sci. 21, 6082.   DOI
31 Li, Z., Wu, Y., Xing, D., Zhang, K., Xie, J., Yu, R., Chen, T., and Duan, R. (2021). Effects of foliage spraying with sodium bisulfite on the photosynthesis of Orychophragmus violaceus. Horticulturae 7, 137.   DOI
32 Garcia, M.J., Romera, F.J., Stacey, M.G., Stacey, G., Villar, E., Alcantara, E., and Perez-Vicente, R. (2013). Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants. Planta 237, 65-75.   DOI
33 Kroh, G.E. and Pilon, M. (2020). Regulation of iron homeostasis and use in chloroplasts. Int. J. Mol. Sci. 21, 3395.   DOI
34 McElver, J., Tzafrir, I., Aux, G., Rogers, R., Ashby, C., Smith, K., Thomas, C., Schetter, A., Zhou, Q., Cushman, M.A., et al. (2001). Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics 159, 1751-1763.   DOI
35 Leister, D. (2005). Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354, 110-116.   DOI
36 Narsai, R., Law, S.R., Carrie, C., Xu, L., and Whelan, J. (2011). In-depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiol. 157, 1342-1362.   DOI
37 Kobayashi, T. and Nishizawa, N.K. (2012). Iron uptake, translocation, and regulation in higher plants. Annu. Rev. Plant Biol. 63, 131-152.   DOI
38 Kramer, D.M., Johnson, G., Kiirats, O., and Edwards, G.E. (2004). New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth. Res. 79, 209.   DOI
39 Kumar, R., Pandey, S., and Pandey, A. (2006). Plant roots and carbon sequestration. Curr. Sci. 91, 885-890.
40 Lee, S., Kim, Y.S., Jeon, U.S., Kim, Y.K., Schjoerring, J.K., and An, G. (2012b). Activation of rice nicotianamine synthase 2 (OsNAS2) enhances iron availability for biofortification. Mol. Cells 33, 269-275.   DOI
41 Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10-12.   DOI
42 Oh, Y.J., Kim, H., Seo, S.H., Hwang, B.G., Chang, Y.S., Lee, J., Lee, D.W., Sohn, E.J., Lee, S.J., Lee, Y., et al. (2016). Cytochrome b 5 reductase 1 triggers serial reactions that lead to iron uptake in plants. Mol. Plant 9, 501-513.   DOI
43 Gratani, L., Pesoli, P., and Crescente, M.F. (1998). Relationship between photosynthetic activity and chlorophyll content in an isolated Quercus ilex L. tree during the year. Photosynthetica 35, 445-451.   DOI
44 Rodriguez-Celma, J., Connorton, J.M., Kruse, I., Green, R.T., Franceschetti, M., Chen, Y.T., Cui, Y., Ling, H.Q., Yeh, K.C., and Balk, J. (2019). Arabidopsis BRUTUS-LIKE E3 ligases negatively regulate iron uptake by targeting transcription factor FIT for recycling. Proc. Natl. Acad. Sci. U. S. A. 116, 17584-17591.   DOI
45 Shameer, S., Baghalian, K., Cheung, C.Y.M., Ratcliffe, R.G., and Sweetlove, L.J. (2018). Computational analysis of the productivity potential of CAM. Nat. Plants 4, 165-171.   DOI
46 Hennion, N., Durand, M., Vriet, C., Doidy, J., Maurousset, L., Lemoine, R., and Pourtau, N. (2019). Sugars en route to the roots. Transport, metabolism and storage within plant roots and towards microorganisms of the rhizosphere. Physiol. Plant. 165, 44-57.   DOI
47 Yan, F., Zhu, Y., Muller, C., Zorb, C., and Schubert, S. (2002). Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol. 129, 50-63.   DOI
48 Allen, J.F. (2015). Why chloroplasts and mitochondria retain their own genomes and genetic systems: colocation for redox regulation of gene expression. Proc. Natl. Acad. Sci. U. S. A. 112, 10231-10238.   DOI
49 Chiu, W.L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. (1996). Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325-330.   DOI
50 Enomoto, Y., Hodoshima, H., Shimada, H., Shoji, K., Yoshihara, T., and Goto, F. (2007). Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots. Planta 227, 81-89.   DOI
51 Grillet, L., Lan, P., Li, W., Mokkapati, G., and Schmidt, W. (2018). IRON MAN is a ubiquitous family of peptides that control iron transport in plants. Nat. Plants 4, 953-963.   DOI
52 Anders, S., Pyl, P.T., and Huber, W. (2015). HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169.   DOI