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Mitochondrial Zea mays Brittle1-1 Is a Major Determinant of the Metabolic Fate of Incoming Sucrose and Mitochondrial Function in Developing Maize Endosperms

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Mitochondrial Zea mays Brittle1-1 Is a Major Determinant of the Metabolic Fate of Incoming Sucrose and Mitochondrial Function in Developing Maize Endosperms

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dc.contributor.author Bahaji, Abdellatif es_ES
dc.contributor.author Muñoz, Francisco José es_ES
dc.contributor.author Seguí-Simarro, Jose M. es_ES
dc.contributor.author Camacho-Fernández, Carolina es_ES
dc.contributor.author Rivas-Sendra, Alba es_ES
dc.contributor.author Parra Vega, Verónica es_ES
dc.contributor.author Ovecka, Miroslav es_ES
dc.contributor.author Li, Jun es_ES
dc.contributor.author Sánchez-López, Ángela María es_ES
dc.contributor.author Almagro, Goizeder es_ES
dc.contributor.author Baroja-Fernández, Edurne es_ES
dc.contributor.author POZUETA-ROMERO, JAVIER es_ES
dc.date.accessioned 2020-05-20T03:01:40Z
dc.date.available 2020-05-20T03:01:40Z
dc.date.issued 2019-03-12 es_ES
dc.identifier.uri http://hdl.handle.net/10251/143785
dc.description.abstract [EN] Zea mays Brittle1-1 (ZmBT1-1) is an essential component of the starch biosynthetic machinery in maize endosperms, enabling ADPglucose transport from cytosol to amyloplast in exchange for AMP or ADP. Although ZmBT1-1 has been long considered to be an amyloplast-specific marker, evidence has been provided that ZmBT1-1 is dually localized to plastids and mitochondria (Bahaji et al., 2011b). The mitochondrial localization of ZmBT1-1 suggested that this protein may have as-yet unidentified function(s). To understand the mitochondrial ZmBT1-1 function(s), we produced and characterized transgenic Zmbt1-1 plants expressing ZmBT1-1 delivered specifically to mitochondria. Metabolic and differential proteomic analyses showed down-regulation of sucrose synthase (SuSy)-mediated channeling of sucrose into starch metabolism, and up-regulation of the conversion of sucrose breakdown products generated by cell wall invertase (CWI) into ethanol and alanine, in Zmbt1-1 endosperms compared to wild-type. Electron microscopic analyses of Zmbt1-1 endosperm cells showed gross alterations in the mitochondrial ultrastructure. Notably, the protein expression pattern, metabolic profile, and aberrant mitochondrial ultrastructure of Zmbt1-1 endosperms were rescued by delivering ZmBT1-1 specifically to mitochondria. Results presented here provide evidence that the reduced starch content in Zmbt1-1 endosperms is at least partly due to (i) mitochondrial dysfunction, (ii) enhanced CWI-mediated channeling of sucrose into ethanol and alanine metabolism, and (iii) reduced SuSy-mediated channeling of sucrose into starch metabolism due to the lack of mitochondrial ZmBT1-1. Our results also strongly indicate that (a) mitochondrial ZmBT1-1 is an important determinant of the metabolic fate of sucrose entering the endosperm cells, and (b) plastidic ZmBT1-1 is not the sole ADPglucose transporter in maize endosperm amyloplasts. The possible involvement of mitochondrial ZmBT1-1 in exchange between intramitochondrial AMP and cytosolic ADP is discussed. es_ES
dc.description.sponsorship This research was partially supported by the grants BIO2010-18239, BI2013-49125-C2-2-P and BIO2016-78747-P from the Comisión Interministerial de Ciencia y Tecnología and Fondo Europeo de Desarrollo Regional (Spain) and by the ERDF project Plants as a tool for sustainable global development (No. CZ.02.1.01/0.0/0.0/16_019/0000827). es_ES
dc.language Inglés es_ES
dc.publisher Frontiers Media SA es_ES
dc.relation.ispartof Frontiers in Plant Science es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject ADP glucose es_ES
dc.subject Dual targeting es_ES
dc.subject Mitochondrial carrier family es_ES
dc.subject Mitochondrial retrograde signaling es_ES
dc.subject Starch es_ES
dc.subject Sucrose synthase es_ES
dc.subject Zea mays es_ES
dc.subject.classification GENETICA es_ES
dc.title Mitochondrial Zea mays Brittle1-1 Is a Major Determinant of the Metabolic Fate of Incoming Sucrose and Mitochondrial Function in Developing Maize Endosperms es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.3389/fpls.2019.00242 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//BIO2010-18239/ES/ASPECTOS FUNDAMENTALES DE MIVOISAP (MICROBIAL VOLATILES INDUCED STARCH ACCUMULATION PROCESS)/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MSMT//CZ.02.1.01%2F0.0%2F0.0%2F16_019%2F0000827/CZ/Plants as a tool for sustainable global development/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BIO2013-49125-C2-2-P/ES/ASPECTOS BASICOS DEL METABOLISMO DEL ALMIDON Y APLICACIONES BIOTECNOLOGICAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BIO2016-78747-P/ES/MECANISMOS DE REGULACION DEL CRECIMIENTO Y METABOLISMO EN PLANTAS EXPUESTAS A SUSTANCIAS BIOESTIMULANTES EMITIDAS POR MICROORGANISMOS Y APLICACIONES BIOTECNOLOGICAS/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia es_ES
dc.description.bibliographicCitation Bahaji, A.; Muñoz, FJ.; Seguí-Simarro, JM.; Camacho-Fernández, C.; Rivas-Sendra, A.; Parra Vega, V.; Ovecka, M.... (2019). Mitochondrial Zea mays Brittle1-1 Is a Major Determinant of the Metabolic Fate of Incoming Sucrose and Mitochondrial Function in Developing Maize Endosperms. Frontiers in Plant Science. 10:1-16. https://doi.org/10.3389/fpls.2019.00242 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.3389/fpls.2019.00242 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 16 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 10 es_ES
dc.identifier.eissn 1664-462X es_ES
dc.identifier.pmid 30915089 es_ES
dc.identifier.pmcid PMC6423154 es_ES
dc.relation.pasarela S\384606 es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.contributor.funder Ministry of Education, Youth and Sports, República Checa es_ES
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.description.references Almagro, G., Viale, A. M., Montero, M., Muñoz, F. J., Baroja-Fernández, E., Mori, H., & Pozueta-Romero, J. (2018). A cAMP/CRP-controlled mechanism for the incorporation of extracellular ADP-glucose in Escherichia coli involving NupC and NupG nucleoside transporters. Scientific Reports, 8(1). doi:10.1038/s41598-018-33647-w es_ES
dc.description.references Atkins, C. A., Smith, P., & Storer, P. J. (1997). Reexamination of the Intracellular Localization of de Novo Purine Synthesis in Cowpea Nodules. Plant Physiology, 113(1), 127-135. doi:10.1104/pp.113.1.127 es_ES
dc.description.references Bahaji, A., Li, J., Sánchez-López, Á. M., Baroja-Fernández, E., Muñoz, F. J., Ovecka, M., … Pozueta-Romero, J. (2014). Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnology Advances, 32(1), 87-106. doi:10.1016/j.biotechadv.2013.06.006 es_ES
dc.description.references Bahaji, A., Muñoz, F. J., Ovecka, M., Baroja-Fernández, E., Montero, M., Li, J., … Pozueta-Romero, J. (2011). Specific delivery of AtBT1 to mitochondria complements the aberrant growth and sterility phenotype of homozygous Atbt1 Arabidopsis mutants. The Plant Journal, 68(6), 1115-1121. doi:10.1111/j.1365-313x.2011.04767.x es_ES
dc.description.references Bahaji, A., Ovecka, M., Bárány, I., Risueño, M. C., Muñoz, F. J., Baroja-Fernández, E., … Pozueta-Romero, J. (2011). Dual Targeting to Mitochondria and Plastids of AtBT1 and ZmBT1, Two Members of the Mitochondrial Carrier Family. Plant and Cell Physiology, 52(4), 597-609. doi:10.1093/pcp/pcr019 es_ES
dc.description.references Baroja-Fernández, E., Muñoz, F. J., Montero, M., Etxeberria, E., Sesma, M. T., Ovecka, M., … Pozueta-Romero, J. (2009). Enhancing Sucrose Synthase Activity in Transgenic Potato (Solanum tuberosum L.) Tubers Results in Increased Levels of Starch, ADPglucose and UDPglucose and Total Yield. Plant and Cell Physiology, 50(9), 1651-1662. doi:10.1093/pcp/pcp108 es_ES
dc.description.references Bedhomme, M., Hoffmann, M., McCarthy, E. A., Gambonnet, B., Moran, R. G., Rébeillé, F., & Ravanel, S. (2005). Folate Metabolism in Plants. Journal of Biological Chemistry, 280(41), 34823-34831. doi:10.1074/jbc.m506045200 es_ES
dc.description.references Bhave, M. R., Lawrence, S., Barton, C., & Hannah, L. C. (1990). Identification and molecular characterization of shrunken-2 cDNA clones of maize. The Plant Cell, 2(6), 581-588. doi:10.1105/tpc.2.6.581 es_ES
dc.description.references Boehlein, S. K., Shaw, J. R., Boehlein, T. J., Boehlein, E. C., & Hannah, L. C. (2018). Fundamental differences in starch synthesis in the maize leaf, embryo, ovary and endosperm. The Plant Journal, 96(3), 595-606. doi:10.1111/tpj.14053 es_ES
dc.description.references Bowsher, C. G., Scrase-Field, E. F. A. L., Esposito, S., Emes, M. J., & Tetlow, I. J. (2007). Characterization of ADP-glucose transport across the cereal endosperm amyloplast envelope. Journal of Experimental Botany, 58(6), 1321-1332. doi:10.1093/jxb/erl297 es_ES
dc.description.references Busi, M. V., Gomez-Lobato, M. E., Rius, S. P., Turowski, V. R., Casati, P., Zabaleta, E. J., … Araya, A. (2011). Effect of Mitochondrial Dysfunction on Carbon Metabolism and Gene Expression in Flower Tissues of Arabidopsis thaliana. Molecular Plant, 4(1), 127-143. doi:10.1093/mp/ssq065 es_ES
dc.description.references Cakir, B., Shiraishi, S., Tuncel, A., Matsusaka, H., Satoh, R., Singh, S., … Okita, T. W. (2016). Analysis of the rice ADPglucose transporter (OsBT1) indicates the presence of regulatory processes in the amyloplast stroma that control ADPglucose flux into starch. Plant Physiology, pp.01911.2015. doi:10.1104/pp.15.01911 es_ES
dc.description.references Cao, H., & Shannon, J. C. (1996). BT1, a protein critical for in vivo starch accumulation in maize endosperm, is not detected in maize endosperm suspension cultures. Physiologia Plantarum, 97(4), 665-673. doi:10.1111/j.1399-3054.1996.tb00530.x es_ES
dc.description.references Cao, H., Sullivan, T. D., Boyer, C. D., & Shannon, J. C. (1995). Btl, a structural gene for the major 39-44 kDa amyloplast membrane polypeptides. Physiologia Plantarum, 95(2), 176-186. doi:10.1111/j.1399-3054.1995.tb00825.x es_ES
dc.description.references Chandel, N. S. (2014). Mitochondria as signaling organelles. BMC Biology, 12(1). doi:10.1186/1741-7007-12-34 es_ES
dc.description.references Cheng, W. H., Taliercio, E. W., & Chourey, P. S. (1996). The Miniature1 Seed Locus of Maize Encodes a Cell Wall Invertase Required for Normal Development of Endosperm and Maternal Cells in the Pedicel. The Plant Cell, 971-983. doi:10.1105/tpc.8.6.971 es_ES
dc.description.references Chourey, P. S., Taliercio, E. W., Carlson, S. J., & Ruan, Y.-L. (1998). Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Molecular and General Genetics MGG, 259(1), 88-96. doi:10.1007/s004380050792 es_ES
dc.description.references Christensen, A. C., Lyznik, A., Mohammed, S., Elowsky, C. G., Elo, A., Yule, R., & Mackenzie, S. A. (2005). Dual-Domain, Dual-Targeting Organellar Protein Presequences in Arabidopsis Can Use Non-AUG Start Codons. The Plant Cell, 17(10), 2805-2816. doi:10.1105/tpc.105.035287 es_ES
dc.description.references Christensen, A. H., & Quail, P. H. (1996). Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Research, 5(3), 213-218. doi:10.1007/bf01969712 es_ES
dc.description.references Doehlert, D. C., Kuo, T. M., & Felker, F. C. (1988). Enzymes of Sucrose and Hexose Metabolism in Developing Kernels of Two Inbreds of Maize. Plant Physiology, 86(4), 1013-1019. doi:10.1104/pp.86.4.1013 es_ES
dc.description.references Duchene, A.-M., Giritch, A., Hoffmann, B., Cognat, V., Lancelin, D., Peeters, N. M., … Small, I. D. (2005). Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 102(45), 16484-16489. doi:10.1073/pnas.0504682102 es_ES
dc.description.references Emanuelsson, O., Nielsen, H., Brunak, S., & von Heijne, G. (2000). Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence. Journal of Molecular Biology, 300(4), 1005-1016. doi:10.1006/jmbi.2000.3903 es_ES
dc.description.references Fiermonte, G., De Leonardis, F., Todisco, S., Palmieri, L., Lasorsa, F. M., & Palmieri, F. (2004). Identification of the Mitochondrial ATP-Mg/PiTransporter. Journal of Biological Chemistry, 279(29), 30722-30730. doi:10.1074/jbc.m400445200 es_ES
dc.description.references Fukao, Y., Hayashi, Y., Mano, S., Hayashi, M., & Nishimura, M. (2001). Developmental Analysis of a Putative ATP/ADP Carrier Protein Localized on Glyoxysomal Membranes During the Peroxisome Transition in Pumpkin Cotyledons. Plant and Cell Physiology, 42(8), 835-841. doi:10.1093/pcp/pce108 es_ES
dc.description.references Goggin, D. E., Lipscombe, R., Fedorova, E., Millar, A. H., Mann, A., Atkins, C. A., & Smith, P. M. C. (2003). Dual Intracellular Localization and Targeting of Aminoimidazole Ribonucleotide Synthetase in Cowpea. Plant Physiology, 131(3), 1033-1041. doi:10.1104/pp.102.015081 es_ES
dc.description.references Haferkamp, I., & Schmitz-Esser, S. (2012). The Plant Mitochondrial Carrier Family: Functional and Evolutionary Aspects. Frontiers in Plant Science, 3. doi:10.3389/fpls.2012.00002 es_ES
dc.description.references Huang, S., Taylor, N. L., Narsai, R., Eubel, H., Whelan, J., & Millar, A. H. (2008). Experimental Analysis of the Rice Mitochondrial Proteome, Its Biogenesis, and Heterogeneity. Plant Physiology, 149(2), 719-734. doi:10.1104/pp.108.131300 es_ES
dc.description.references Igamberdiev, A. U. (2006). Equilibration of adenylates in the mitochondrial intermembrane space maintains respiration and regulates cytosolic metabolism. Journal of Experimental Botany, 57(10), 2133-2141. doi:10.1093/jxb/erl006 es_ES
dc.description.references Kirchberger, S., Leroch, M., Huynen, M. A., Wahl, M., Neuhaus, H. E., & Tjaden, J. (2007). Molecular and Biochemical Analysis of the Plastidic ADP-glucose Transporter (ZmBT1) fromZea mays. Journal of Biological Chemistry, 282(31), 22481-22491. doi:10.1074/jbc.m702484200 es_ES
dc.description.references Kleczkowski, L. (1996). Back to the drawing board: redefining starch synthesis in cereals. Trends in Plant Science, 1(11), 363-364. doi:10.1016/1360-1385(96)83884-2 es_ES
dc.description.references Kmiec, B., Teixeira, P. F., & Glaser, E. (2014). Shredding the signal: targeting peptide degradation in mitochondria and chloroplasts. Trends in Plant Science, 19(12), 771-778. doi:10.1016/j.tplants.2014.09.004 es_ES
dc.description.references Krath, B. N., & Hove-Jensen, B. (1999). Organellar and Cytosolic Localization of Four Phosphoribosyl Diphosphate Synthase Isozymes in Spinach. Plant Physiology, 119(2), 497-506. doi:10.1104/pp.119.2.497 es_ES
dc.description.references Lee, C. P., Taylor, N. L., & Millar, A. H. (2013). Recent Advances in the Composition and Heterogeneity of the Arabidopsis Mitochondrial Proteome. Frontiers in Plant Science, 4. doi:10.3389/fpls.2013.00004 es_ES
dc.description.references Li, J., Baroja-Fernández, E., Bahaji, A., Muñoz, F. J., Ovecka, M., Montero, M., … Pozueta-Romero, J. (2013). Enhancing Sucrose Synthase Activity Results in Increased Levels of Starch and ADP-Glucose in Maize (Zea mays L.) Seed Endosperms. Plant and Cell Physiology, 54(2), 282-294. doi:10.1093/pcp/pcs180 es_ES
dc.description.references Licausi, F., Van Dongen, J. T., Giuntoli, B., Novi, G., Santaniello, A., Geigenberger, P., & Perata, P. (2010). HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. The Plant Journal, 62(2), 302-315. doi:10.1111/j.1365-313x.2010.04149.x es_ES
dc.description.references Loiret, F. G., Grimm, B., Hajirezaei, M. R., Kleiner, D., & Ortega, E. (2009). Inoculation of sugarcane with Pantoea sp. increases amino acid contents in shoot tissues; serine, alanine, glutamine and asparagine permit concomitantly ammonium excretion and nitrogenase activity of the bacterium. Journal of Plant Physiology, 166(11), 1152-1161. doi:10.1016/j.jplph.2009.01.002 es_ES
dc.description.references Méchin, V., Thévenot, C., Le Guilloux, M., Prioul, J.-L., & Damerval, C. (2007). Developmental Analysis of Maize Endosperm Proteome Suggests a Pivotal Role for Pyruvate Orthophosphate Dikinase. Plant Physiology, 143(3), 1203-1219. doi:10.1104/pp.106.092148 es_ES
dc.description.references Miyashita, Y., & Good, A. G. (2008). Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant and Cell Physiology, 49(1), 92-102. doi:10.1093/pcp/pcm171 es_ES
dc.description.references Naeem, M., Tetlow, I. J., & Emes, M. J. (1997). Starch synthesis in amyloplasts purified from developing potato tubers. The Plant Journal, 11(5), 1095-1103. doi:10.1046/j.1365-313x.1997.11051095.x es_ES
dc.description.references Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M., & Kobayashi, H. (1999). Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. The Plant Journal, 18(4), 455-463. doi:10.1046/j.1365-313x.1999.00464.x es_ES
dc.description.references Palmieri, L., Arrigoni, R., Blanco, E., Carrari, F., Zanor, M. I., Studart-Guimaraes, C., … Palmieri, F. (2006). Molecular Identification of an Arabidopsis S-Adenosylmethionine Transporter. Analysis of Organ Distribution, Bacterial Expression, Reconstitution into Liposomes, and Functional Characterization. Plant Physiology, 142(3), 855-865. doi:10.1104/pp.106.086975 es_ES
dc.description.references Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D. M., … Velours, J. (2002). The ATP synthase is involved in generating mitochondrial cristae morphology. The EMBO Journal, 21(3), 221-230. doi:10.1093/emboj/21.3.221 es_ES
dc.description.references Peeters, N., & Small, I. (2001). Dual targeting to mitochondria and chloroplasts. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1541(1-2), 54-63. doi:10.1016/s0167-4889(01)00146-x es_ES
dc.description.references Pozueta-Romero, J., Ardila, F., & Akazawa, T. (1991). ADP-Glucose Transport by the Chloroplast Adenylate Translocator Is Linked to Starch Biosynthesis. Plant Physiology, 97(4), 1565-1572. doi:10.1104/pp.97.4.1565 es_ES
dc.description.references Prioul, J. L., Méchin, V., Lessard, P., Thévenot, C., Grimmer, M., Chateau-Joubert, S., … Edwards, K. J. (2008). A joint transcriptomic, proteomic and metabolic analysis of maize endosperm development and starch filling. Plant Biotechnology Journal, 6(9), 855-869. doi:10.1111/j.1467-7652.2008.00368.x es_ES
dc.description.references Reynolds, E. S. (1963). THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY. Journal of Cell Biology, 17(1), 208-212. doi:10.1083/jcb.17.1.208 es_ES
dc.description.references Rhoads, D. M., & Subbaiah, C. C. (2007). Mitochondrial retrograde regulation in plants. Mitochondrion, 7(3), 177-194. doi:10.1016/j.mito.2007.01.002 es_ES
dc.description.references Sánchez-López, Á. M., Bahaji, A., De Diego, N., Baslam, M., Li, J., Muñoz, F. J., … Pozueta-Romero, J. (2016). Arabidopsis Responds to Alternaria alternata Volatiles by Triggering Plastid Phosphoglucose Isomerase-Independent Mechanisms. Plant Physiology, 172(3), 1989-2001. doi:10.1104/pp.16.00945 es_ES
dc.description.references Seguí-Simarro, J. M. (2015). High-Pressure Freezing and Freeze Substitution of In Vivo and In Vitro Cultured Plant Samples. Plant Microtechniques and Protocols, 117-134. doi:10.1007/978-3-319-19944-3_7 es_ES
dc.description.references Shannon, J. C., Pien, F. M., & Liu, K. C. (1996). Nucleotides and Nucleotide Sugars in Developing Maize Endosperms (Synthesis of ADP-Glucose in brittle-1). Plant Physiology, 110(3), 835-843. doi:10.1104/pp.110.3.835 es_ES
dc.description.references Shannon, J. C., Pien, F.-M., Cao, H., & Liu, K.-C. (1998). Brittle-1, an Adenylate Translocator, Facilitates Transfer of Extraplastidial Synthesized ADP-Glucose into Amyloplasts of Maize Endosperms. Plant Physiology, 117(4), 1235-1252. doi:10.1104/pp.117.4.1235 es_ES
dc.description.references SHINGAKI-WELLS, R., MILLAR, A. H., WHELAN, J., & NARSAI, R. (2014). What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation. Plant, Cell & Environment, n/a-n/a. doi:10.1111/pce.12312 es_ES
dc.description.references Shockey, J. M., Fulda, M. S., & Browse, J. (2003). Arabidopsis Contains a Large Superfamily of Acyl-Activating Enzymes. Phylogenetic and Biochemical Analysis Reveals a New Class of Acyl-Coenzyme A Synthetases. Plant Physiology, 132(2), 1065-1076. doi:10.1104/pp.103.020552 es_ES
dc.description.references Smith, P. M. C., Mann, A. J., Goggin, D. E., & Atkins, C. A. (1998). Plant Molecular Biology, 36(6), 811-820. doi:10.1023/a:1005969830314 es_ES
dc.description.references Sullivan, T., & Kaneko, Y. (1995). The maize brittle1 gene encodes amyloplast membrane polypeptides. Planta, 196(3). doi:10.1007/bf00203647 es_ES
dc.description.references Sullivan, T. D., Strelow, L. I., Illingworth, C. A., Phillips, R. L., & Nelson, O. E. (1991). Analysis of maize brittle-1 alleles and a defective Suppressor-mutator-induced mutable allele. The Plant Cell, 3(12), 1337-1348. doi:10.1105/tpc.3.12.1337 es_ES
dc.description.references Tarasenko, V. I., Katyshev, A. I., Yakovleva, T. V., Garnik, E. Y., Chernikova, V. V., Konstantinov, Y. M., & Koulintchenko, M. V. (2016). RPOTmp, an Arabidopsis RNA polymerase with dual targeting, plays an important role in mitochondria, but not in chloroplasts. Journal of Experimental Botany, 67(19), 5657-5669. doi:10.1093/jxb/erw327 es_ES
dc.description.references Taylor, E. B. (2017). Functional Properties of the Mitochondrial Carrier System. Trends in Cell Biology, 27(9), 633-644. doi:10.1016/j.tcb.2017.04.004 es_ES
dc.description.references Thevenot, C. (2005). QTLs for enzyme activities and soluble carbohydrates involved in starch accumulation during grain filling in maize. Journal of Experimental Botany, 56(413), 945-958. doi:10.1093/jxb/eri087 es_ES
dc.description.references Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., … Stitt, M. (2004). mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal, 37(6), 914-939. doi:10.1111/j.1365-313x.2004.02016.x es_ES
dc.description.references Todisco, S., Agrimi, G., Castegna, A., & Palmieri, F. (2005). Identification of the Mitochondrial NAD+Transporter inSaccharomyces cerevisiae. Journal of Biological Chemistry, 281(3), 1524-1531. doi:10.1074/jbc.m510425200 es_ES
dc.description.references Wang, K., & Frame, B. (2009). Biolistic Gun-Mediated Maize Genetic Transformation. Transgenic Maize, 29-45. doi:10.1007/978-1-59745-494-0_3 es_ES
dc.description.references Wiseman, A., Gillham, N. W., & Boynton, J. E. (1977). Nuclear mutations affecting mitochondrial structure and function in Chlamydomonas. Journal of Cell Biology, 73(1), 56-77. doi:10.1083/jcb.73.1.56 es_ES
dc.description.references Zrenner, R., Stitt, M., Sonnewald, U., & Boldt, R. (2006). PYRIMIDINE AND PURINE BIOSYNTHESIS AND DEGRADATION IN PLANTS. Annual Review of Plant Biology, 57(1), 805-836. doi:10.1146/annurev.arplant.57.032905.105421 es_ES


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