Plant J. 2022 Jan;109(1):196-214. doi: 10.1111/tpj.15566. Epub 2021 Nov 22.

The Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase is required during normal seed development and germination.

The Plant journal : for cell and molecular biology

Paula da Fonseca-Pereira, Phuong Anh Pham, João Henrique F Cavalcanti, Rebeca P Omena-Garcia, Jessica A S Barros, Laise Rosado-Souza, José G Vallarino, Marek Mutwil, Tamar Avin-Wittenberg, Adriano Nunes-Nesi, Alisdair R Fernie, Wagner L Araújo

PMID: 34741366 DOI: 10.1111/tpj.15566

Abstract

The importance of the alternative donation of electrons to the ubiquinol pool via the electron-transfer flavoprotein/electron-transfer flavoprotein:ubiquinone oxidoreductase (ETF/ETFQO) complex has been demonstrated. However, the functional significance of this pathway during seed development and germination remains to be elucidated. To assess the function of this pathway, we performed a detailed metabolic and transcriptomic analysis of Arabidopsis mutants to test the molecular consequences of a dysfunctional ETF/ETFQO pathway. We demonstrate that the disruption of this pathway compromises seed germination in the absence of an external carbon source and also impacts seed size and yield. Total protein and storage protein content is reduced in dry seeds, whilst sucrose levels remain invariant. Seeds of ETFQO and related mutants were also characterized by an altered fatty acid composition. During seed development, lower levels of fatty acids and proteins accumulated in the etfqo-1 mutant as well as in mutants in the alternative electron donors isovaleryl-CoA dehydrogenase (ivdh-1) and d-2-hydroxyglutarate dehydrogenase (d2hgdh1-2). Furthermore, the content of several amino acids was increased in etfqo-1 mutants during seed development, indicating that these mutants are not using such amino acids as alternative energy source for respiration. Transcriptome analysis revealed alterations in the expression levels of several genes involved in energy and hormonal metabolism. Our findings demonstrated that the alternative pathway of respiration mediated by the ETF/ETFQO complex affects seed germination and development by directly adjusting carbon storage during seed filling. These results indicate a role for the pathway in the normal plant life cycle to complement its previously defined roles in the response to abiotic stress.

© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.

Keywords: ETF/electron-transfer flavoprotein:ubiquinone oxidoreductase pathway; amino acid metabolism; carbon partition; germination; primary metabolism; seed development

References

1. Andalo, C., Godelle, B., Lefranc, M., Mousseau, M. & Till-Bottraud, I. (1996) Elevated CO2 decreases seed germination in Arabidopsis thaliana. Global Change Biology, 2, 129-135. - PubMed
2. Angelovici, R., Fait, A., Fernie, A.R. & Galili, G. (2011) A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytologist, 189, 148-159. - PubMed
3. Angelovici, R., Galili, G., Fernie, A.R. & Fait, A. (2010) Seed desiccation: a bridge between maturation and germination. Trends in Plant Science, 15, 211-218. - PubMed
4. Angelovici, R., Lipka, A.E., Deason, N., Gonzalez-Jorge, S., Lin, H., Cepela, J. et al. (2013) Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. The Plant Cell, 25, 4827-4843. - PubMed
5. Araújo, W.L., Ishizaki, K., Nunes-Nesi, A., Larson, T.R., Tohge, T., Krahnert, I. et al. (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. The Plant Cell, 22, 1549-1563. - PubMed
6. Araújo, W.L., Nunes-Nesi, A. & Fernie, A.R. (2014) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynthesis Research, 119, 141-156. - PubMed
7. Araújo, W.L., Tohge, T., Ishizaki, K., Leaver, C.J. & Fernie, A.R. (2011) Protein degradation - an alternative respiratory substrate for stressed plants. Trends in Plant Science, 16, 489-498. - PubMed
8. Atkin, O.K. & Macherel, D. (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Annals of Botany, 103, 581-597. - PubMed
9. Baena-González, E., Rolland, F., Thevelein, J.M. & Sheen, J. (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature, 448, 938-942. - PubMed
10. Balazadeh, S., Schildhauer, J., Araújo, W.L., Munné-Bosch, S., Fernie, A.R., Proost, S. et al. (2014) Reversal of senescence by N resupply to N starved Arabidopsis thaliana: Transcriptomic and metabolomic consequences. Journal of Experimental Botany, 65, 3975-3992. - PubMed
11. Barreto, P., Counago, R.M. & Arruda, P. (2020) Mitochondrial uncoupling protein-dependent signaling in plant bioenergetics and stress response. Mitochondrion, 52, 109-120. - PubMed
12. Barros, J.A.S., Cavalcanti, J.H.F., Medeiros, D.B., Nunes-Nesi, A., Avin- Wittenberg, T., Fernie, A.R. et al. (2017) Autophagy deficiency compromises alternative pathway of respiration following energy deprivation. Plant Physiology, 175, 62-76. - PubMed
13. Baud, S., Wuilleme, S., Lemoine, R., Kronenberger, J., Caboche, M., Lepiniec, L. et al. (2005) The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. The Plant Journal, 43, 824-836. - PubMed
14. Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57, 289-300. - PubMed
15. Bewley, J.D. (1997) Seed germination and dormancy. The Plant Cell, 9, 1055. - PubMed
16. Braun, H.-P. (2020) The oxidative phosphorylation system of the mitochondria in plants. Mitochondrion, 53, 66-75. - PubMed
17. Brown, P.D., Tokuhisa, J.G., Reichelt, M. & Gershenzon, J. (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry, 62, 471-481. - PubMed
18. Browse, J., McCourt, P.J. & Somerville, C.R. (1986) Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. Analytical Biochemistry, 152, 141-145. - PubMed
19. 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. The Plant Journal, 42, 567-585. - PubMed
20. Cavalcanti, J.H.F., Quinhones, C.G.S., Schertl, P., Brito, D.S., Eubel, H., Hildebrandt, T. et al. (2017) The differential impact of amino acids on OXPHOS system activity following carbohydrate starvation in Arabidopsis cell suspensions. Physiologia Plantarum, 161(4), 451-467. - PubMed
21. Chen, Z., Zhao, N., Li, S., Grover, C.E., Nie, H., Wendel, J.F. et al. (2017) Plant mitochondrial genome evolution and cytoplasmic male sterility. Critical Reviews in Plant Sciences, 36, 55-69. - PubMed
22. Clifton, R., Millar, A.H. & Whelan, J. (2006) Alternative oxidases in Arabidopsis: A comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochimica Et Biophysica Acta, 1757, 730-741. - PubMed
23. Curien, G., Ravanel, S. & Dumas, R. (2003) A kinetic model of the branch-point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana. European Journal of Biochemistry, 270, 4615-4627. - PubMed
24. Dietrich, K., Weltmeier, F., Ehlert, A., Weiste, C., Stahl, M., Harter, K. et al. (2011) Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. The Plant Cell, 23, 381-395. - PubMed
25. Eastmond, P.J. & Graham, I.A. (2001) Re-examining the role of the glyoxylate cycle in oilseeds. Trends in Plant Science, 6, 72-78. - PubMed
26. Engqvist, M., Drincovich, M.F., Flugge, U.I. & Maurino, V.G. (2009) Two D-2-hydroxy-acid dehydrogenases in Arabidopsis thaliana with catalytic capacities to participate in the last reactions of the methylglyoxal and beta-oxidation pathways. Journal of Biological Chemistry, 284, 25026-25037. - PubMed
27. Fait, A., Angelovici, R., Less, H., Ohad, I., Urbanczyk-Wochniak, E., Fernie, A.R. et al. (2006) Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiology, 142, 839-854. - PubMed
28. Fait, A., Yellin, A. & Fromm, H. (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Letters, 579, 415-420. - PubMed
29. Fernie, A.R., Aharoni, A., Willmitzer, L., Stitt, M., Tohge, T., Kopka, J. et al. (2011) Recommendations for reporting metabolite data. The Plant Cell, 23, 2477-2482. - PubMed
30. Fernie, A.R., Roscher, A., Ratcliffe, R.G. & Kruger, N.J. (2001) Fructose 2,6-bisphosphate activates pyrophosphate: Fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta, 212, 250-263. - PubMed
31. Focks, N. & Benning, C. (1998) wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiology, 118, 91-101. - PubMed
32. Galili, G., Avin-wittenberg, T., Angelovici, R. & Fernie, A.R. (2014) The role of photosynthesis and amino acid metabolism in the energy status during seed development. Frontiers in Plant Science, 5, 447. - PubMed
33. Garapati, P., Feil, R., Lunn, J.E., Van Dijck, P., Balazadeh, S. & Mueller-Roeber, B. (2015) Transcription factor Arabidopsis activating factor1 integrates carbon starvation responses with trehalose metabolism. Plant Physiology, 169, 379-390. - PubMed
34. Geisler, D.A., Päpke, C., Obata, T., Nunes-Nesi, A., Matthes, A., Schneitz, K. et al. (2012) Downregulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis. The Plant Cell, 24, 2792-2811. - PubMed
35. Giraud, E., Ho, L.H., Clifton, R., Carroll, A., Estavillo, G., Tan, Y.F. et al. (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiology, 147, 595-610. - PubMed
36. Girke, T., Todd, J., Ruuska, S., Benning, C. & Ohlrogge, J. (2000) Microarray analysis of developing Arabidopsis seeds. Plant Physiology, 124, 1570-1581. - PubMed
37. Graham, I.A. (2008) Seed storage oil mobilization. Annual Review of Plant Biology, 59, 115-142. - PubMed
38. Gu, L., Jones, A.D. & Last, R.L. (2010) Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. The Plant Journal, 61, 579-590. - PubMed
39. Guo, Y., Cai, Z. & Gan, S. (2004) Transcriptome of Arabidopsis leaf senescence. Plant, Cell and Environment, 27, 521-549. - PubMed
40. Hildebrandt, T.M., Nunes Nesi, A., Araújo, W.L. & Braun, H.P. (2015) Amino acid catabolism in plants. Molecular Plant, 8, 1563-1579. - PubMed
41. Hong, F., Breitling, R., McEntee, C.W., Wittner, B.S., Nemhauser, J.L. & Chory, J. (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics, 22, 2825-2827. - PubMed
42. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherfe, U., et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-64. https://doi.org/10.1093/biostatistics/4.2.249 - PubMed
43. Ishizaki, K., Larson, T.R., Schauer, N., Fernie, A.R., Graham, I.A. & Leaver, C.J. (2005) The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. The Plant Cell, 17, 2587-2600. - PubMed
44. Ishizaki, K., Schauer, N., Larson, T.R., Graham, I.A., Fernie, A.R. & Leaver, C.J. (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. The Plant Journal, 47, 751-760. - PubMed
45. Jeong, E.Y., Seo, P.J., Woo, J.C. & Park, C.M. (2015) AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis. BMC Plant Biology, 15, 1-13. - PubMed
46. Kakkar, R.K. & Sawhney, V.K. (2002) Polyamine research in plants-a changing perspective. Physiologia Plantarum, 116, 281-292. - PubMed
47. Krüßel, L., Junemann, J., Wirtz, M., Birke, H., Thornton, J.D., Browning, L.W. et al. (2014) The mitochondrial sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 is required for amino acid catabolism during carbohydrate starvation and embryo development in Arabidopsis. Plant Physiology, 165, 92-104. - PubMed
48. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature, 227, 680-685. - PubMed
49. Li, L.-Q., Huang, L.-P., Pan, G., Liu, L., Wang, X.-Y. & Lu, L.-M. (2017) Identifying the genes regulated by AtWRKY6 using comparative transcript and proteomic analysis under phosphorus deficiency. International Journal of Molecular Sciences, 18, 1046. - PubMed
50. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1(387-789), 396. - PubMed
51. Lohse, M., Bolger, A.M., Nagel, A., Fernie, A.R., Lunn, J.E., Stitt, M. et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Research, 40, W622-W627. - PubMed
52. Lüdemann, A., Strassburg, K., Erban, A. & Kopka, J. (2008) TagFinder for thequantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics, 24, 732-737. - PubMed
53. Ma, J., Hanssen, M., Lundgren, K., Hernández, L., Delatte, T., Ehlert, A. et al. (2011) The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. New Phytologist, 191, 733-745. - PubMed
54. Macherel, D., Benamar, A., Avelange-Macherel, M.H. & Tolleter, D. (2007) Function and stress tolerance of seed mitochondria. Physiologia Plantarum, 129, 233-241. - PubMed
55. Mair, A., Pedrotti, L., Wurzinger, B., Anrather, D., Simeunovic, A., Weiste, C. et al. (2015) SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife, 4, e05828. - PubMed
56. Millar, A.H., Whelan, J., Soole, K.L. & Day, D.A. (2011) Organization and regulation of mitochondrial respiration in plants. Annual Review of Plant Biology, 62, 79-104. - PubMed
57. Narsai, R., Law, S.R., Carrie, C., Xu, L. & 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 Physiology, 157, 1342-1362. - PubMed
58. Nour-Eldin, H.H., Andersen, T.G., Burow, M., Madsen, S.R., Jorgensen, M.E., Olsen, C.E. et al. (2012) NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature, 488, 531-534. - PubMed
59. Nunes-Nesi, A., Carrari, F., Lytovchenko, A., Smith, A.M.O., Ehlers Loureiro, M., Ratcliffe, R.G. et al. (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiology, 137, 611-622. - PubMed
60. Nunes-Nesi, A., Santos Brito, D., Inostroza-Blancheteau, C., Fernie, A.R. & Araújo, W.L. (2014) The complex role of mitochondrial metabolism in plant aluminum resistance. Trends in Plant Science, 19, 399-407. - PubMed
61. Pastore, D., Trono, D., Laus, M.N., Di Fonzo, N. & Flagella, Z. (2007) Possible plant mitochondria involvement in cell adaptation to drought stress. A case study: durum wheat mitochondria. Journal of Experimental Botany, 58, 195-210. - PubMed
62. Peng, C., Uygun, S., Shiu, S.H. & Last, R.L. (2015) The impact of the branched-chain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiology, 169, 1807-1820. - PubMed
63. Pires, M.V., Junior, A.A., Medeiros, D.B., Daloso, D.M., Pham, P.A., Barros, K.A. et al. (2015) The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis. Plant, Cell and Environment, 39, 1304-1319. - PubMed
64. Plaxton, W.C. & Podestá, F.E. (2006) The functional organization and control of plant respiration. Critical Reviews in Plant Sciences, 25(2), 159-198. - PubMed
65. Pracharoenwattana, I., Cornah, J.E. & Smith, S.M. (2005) Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination. The Plant Cell, 17, 2037-2048. - PubMed
66. Rasmusson, A.G., Geisler, D.A. & Møller, I.M. (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion, 8, 47-60. - PubMed
67. Ribas-Carbo, M., Taylor, N.L., Giles, L., Busquets, S., Finnegan, P.M., Day, D.A. et al. (2005) Effects of water stress on respiration in soybean leaves. Plant Physiology, 139, 466-473. - PubMed
68. Rolletschek, H., Weber, H. & Borisjuk, L. (2003) Energy status and its control on embryogenesis of legumes. Embryo photosynthesis contributes to oxygen supply and is coupled to biosynthetic fluxes. Plant Physiology, 132, 1196-1206. - PubMed
69. Rosental, L., Nonogaki, H. & Fait, A. (2014) Activation and regulation of primary metabolism during seed germination. Seed Science Research, 24, 1-15. - PubMed
70. Ruuska, S.A., Girke, T., Benning, C. & Ohlrogge, J.B. (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. The Plant Cell, 14, 1191-1206. - PubMed
71. Ruuska, S.A. & Ohlrogge, J.B. (2001) Protocol for small-scale RNA isolation and transcriptional profiling of developing Arabidopsis seeds. BioTechniques, 31, 752-758. - PubMed
72. Schertl, P. & Braun, H.P. (2014) Respiratory electron transfer pathways in plant mitochondria. Frontiers in Plant Science, 5, 163. - PubMed
73. Schertl, P., Danne, L. & Braun, H.P. (2017) 3-Hydroxyisobutyrate dehydrogenase is involved in both, valine and isoleucine degradation in Arabidopsis thaliana. Plant Physiology, 841(175), 51-61. - PubMed
74. Sew, Y.S., Ströher, E., Fenske, R. & Millar, A.H. (2016) Loss of mitochondrial malate dehydrogenase activity alters seed metabolism impairing seed maturation and post-germination growth in Arabidopsis. Plant Physiology, 171, 849-863. - PubMed
75. Shrestha, P., Callahan, D.L., Singh, S.P. & Petrie, J.R. (2016) Reduced triacylglycerol mobilization during seed germination and early seedling growth in Arabidopsis containing nutritionally important polyunsaturated fatty acids. Frontiers in Plant Science, 7, 1-15. - PubMed
76. Studart-Guimarães, C., Fait, A., Nunes-Nesi, A., Carrari, F., Usadel, B. & Fernie, A.R. (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by upregulation of the γ-aminobutyrate shunt in illuminated tomato leaves. Plant Physiology, 145, 626-639. - PubMed
77. Sweetlove, L.J., Fait, A., Nunes-Nesi, A., Williams, T. & Fernie, A.R. (2007) The mitochondrion: an integration point of cellular metabolism and signalling. Critical Reviews in Plant Sciences, 26, 17-43. - PubMed
78. Szecowka, M., Heise, R., Tohge, T., Nunes-Nesi, A., Vosloh, D., Huege, J. et al. (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. The Plant Cell, 25, 694-714. - PubMed
79. Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P. et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal, 37, 914-939. - PubMed
80. Tsai, A.-Y.-L. & Gazzarrini, S. (2012) AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis. The Plant Journal, 69, 809-821. - PubMed
81. Usadel, B., Nagel, A., Steinhauser, D., Gibon, Y., Bläsing, O.E., Redestig, H. et al. (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics, 7, 535. - PubMed
82. van Dongen, J.T., Roeb, G.W., Dautzenberg, M., Froehlich, A., Vigeolas, H., Minchin, P.E. et al. (2004) Phloem import and storage metabolism are highly coordinated by the low oxygen concentrations within developing wheat seeds. Plant Physiology, 135, 1809-1821. - PubMed
83. Wang, T., Harp, T., Hammond, E.G., Burrisa, J.S. & Fehr, W.R. (2001) Seed physiological performance of soybeans with altered saturated fatty acid contents. Seed Science Research, 11, 93-97. - PubMed
84. Watanabe, M., Balazadeh, S., Tohge, T., Erban, A., Giavalisco, P., Kopka, J. et al. (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiology, 162, 1290-1310. - PubMed
85. Watmough, N.J. & Frerman, F.E. (2010) The electron transfer flavoprotein: ubiquinone oxidoreductases. Biochimica Et Biophysica Acta, 1797, 1910-1916. - PubMed
86. Weber, H., Borisjuk, L. & Wobus, U. (2005) Molecular physiology of legume seed development. Annual Review of Plant Biology, 56, 253-279. - PubMed
87. Weigelt, K., Küster, H., Rutten, T., Fait, A., Fernie, A.R., Miersch, O. et al. (2009) ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses. Plant Physiology, 149, 395-411. - PubMed
88. Weiste, C., Pedrotti, L., Selvanayagam, J., Muralidhara, P., Fröschel, C., Novák, O. et al. (2017) The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth. PLoS Genetics, 13, e1006607. - PubMed
89. Weitbrecht, K., Müller, K. & Leubner-Metzger, G. (2011) First off the mark: early seed germination. Journal of Experimental Botany, 62, 3289-3309. - PubMed

Publication Types

• Journal Article

Grant support

• 402511/2016-6/CNPq-Brazil
• APQ-01171-17/FAPEMIG-Brazil
• RED-00053-16/FAPEMIG-Brazil