Hybrid embryos of Vicia faba develop enhanced sink strength, which is established during early development

Plant Journal

Volumn 65, Issue 4, 2011, Pages 517-531

  Meitzel, Tobias ^a   Radchuk, Ruslana ^a   Nunes Nesi, Adriano ^c   Fernie, Alisdair R ^c   Link, Wolfgang ^b   Weschke, Winfriede ^a   Weber, Hans ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

cell proliferation; heterosis; hybrid embryo; seed development; storage capacity

Indexed keywords

HETEROSIS; HYBRID EMBRYOS; MEAN WEIGHT; METABOLIC FLUX; METABOLIC SHIFT; METABOLITE PROFILES; MID-PARENT HETEROSIS; MOLECULAR MECHANISM; MOTHER PLANT; SEED DEVELOPMENT; SINK STRENGTH; STORAGE CAPACITY; TRANSCRIPT LEVEL; TRANSCRIPT PROFILING; UPTAKE CAPACITY; VICIA FABA;

CELL PROLIFERATION; FORESTRY; LAKES; METABOLISM; METABOLITES; PHYSIOLOGICAL MODELS; PLANTS (BOTANY); TRANSCRIPTION FACTORS;

SEED;

PLANT RNA;

ARTICLE; CELL PROLIFERATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROSIS; HYBRIDIZATION; METABOLISM; PLANT SEED; PRENATAL DEVELOPMENT; VICIA FABA;

CELL PROLIFERATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HYBRID VIGOR; HYBRIDIZATION, GENETIC; RNA, PLANT; SEEDS; VICIA FABA;

VICIA FABA;

EID: 79551622802     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04450.x     Document Type: Article

References (83)

1. Aukerman, M.J., Lee, I., Weigel, D., and, Amasino, R.M., (1999) The Arabidopsis flowering-time gene LUMINIDEPENDENS is expressed primarily in regions of cell proliferation and encodes a nuclear protein that regulates LEAFY expression. Plant J. 18, 195-203.
2. Becker, H.C., and, Link, W., (2000) Heterosis and hybrid breeding. Vortraege Pflanzenzuechtung, 48, 319-327.
3. Bialek, K., and, Cohen, J.D., (1992) Amide-linked indoleacetic acid conjugates may control levels of indoleacetic acid in germinating seedlings of Phaseolus vulgaris. Plant Physiol. 100, 2002-2007.
4. Birchler, J.A., Auger, D.L., and, Riddle, N.C., (2003) In search of the molecular basis of heterosis. Plant Cell, 15, 2236-2239.
5. Borisjuk, L., Weber, H., Panitz, R., Manteuffel, R., and, Wobus, U., (1995) Embryogenesis of Vicia faba L.: histodifferentiation in relation to starch and storage protein synthesis. J. Plant Physiol. 147, 203-218.
6. Borisjuk, L., Walenta, S., Weber, H., Mueller-Klieser, W., and, Wobus, U., (1998) High resolution histographical mapping of glucose concentration in developing cotyledons of V. faba in relation to mitotic activity and starch accumulation: glucose as a possible developmental trigger. Plant J. 15, 583-591.
7. Brady, S.M., Sarkar, S.F., Bonetta, D., and, McCourt, P., (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J. 34, 67-75.
8. Busov, V.B., Brunner, A.M., and, Strauss, S.H., (2008) Genes for control of plant stature and form. New Phytol. 177, 589-607.
9. Casson, S.A., and, Lindsey, K., (2006) The turnip mutant of Arabidopsis reveals that LEAFY COTYLEDON1 expression mediates the effects of auxin and sugars to promote embryonic cell identity. Plant Physiol. 142, 526-541.
10. Chapman, E.J., and, Estelle, M., (2009) Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 43, 265-285.
11. Chen, R., Ni, Z., Qin, Y., Nie, X., Lin, Z., Dong, G., and, Sun, Q., (2005) Isolation and characterization of TaDof1 transcription factor in wheat (Triticum aestivum L). DNA Seq. 16, 358-363.
12. Delgado-Alvarado, A., Walker, R.P., and, Leegood, R.C., (2007) Phosphoenolpyruvate carboxykinase in developing pea seeds is associated with tissues involved in solute transport and is nitrogen-responsive. Plant Cell Environ. 30, 225-235.
13. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., and, Friml, J., (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520-527.
14. Dieckmann, S., and, Link, W., (2010) Quantitative genetic analysis of embryo heterosis in faba bean (Vicia faba L.). Theor. Appl. Genet. 120, 261-270.
15. DiGiacomo, E., Sestili, F., Iannelli, M.A., Testone, G., Mariotti, D., and, Frugis, G., (2008) Characterization of KNOX genes in Medicago truncatula. Plant Mol. Biol. 67, 135-150.
16. Duc, G., Moessner, A., Moussy, F., and, Mousset-Déclas, C., (2001) A xenia effect on number and volume of cotyledon cells and on seed weight in faba bean (Vicia faba L.). Euphytica, 117, 169-174.
17. Falkenberg, B., Witt, I., Zanor, M.I., Steinhauser, D., Mueller-Roeber, B., Hesse, H., and, Hoefgen, R., (2008) Transcription factors relevant to auxin signalling coordinate broad-spectrum metabolic shifts including sulphur metabolism. J. Exp. Bot. 59, 2831-2846.
18. Funck, D., Stadelhofer, B., and, Koch, W., (2008) Ornithine-delta- aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biol. 8, 40.
19. Genuario, R.R., and, Perry, R.P., (1996) The GA-binding protein can serve as both an activator and repressor of ribosomal protein gene transcription. J. Biol. Chem. 271, 4388-4395.
20. Gregis, V., Sessa, A., Colombo, L., and, Kater, M.M., (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell, 18, 1373-1382.
21. Harashima, H., and, Schnittger, A., (2010) The integration of cell division, growth and differentiation. Curr. Opin. Plant Biol. 13, 66-74.
22. Hatton, D., and, Gray, J.C., (1999) Two MAR DNA-binding proteins of the pea nuclear matrix identify a new class of DNA-binding proteins. Plant J. 18, 417-429.
23. Hecht, V., Foucher, F., Ferrándiz, C., et al. (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137, 1420-1434.
24. Hoecker, N., Keller, B., Piepho, H.-P., and, Hochholdinger, F., (2006) Manifestation of heterosis during early maize (Zea mays L.) root development. Theor. Appl. Genet. 112, 421-429.
25. Hoyos, M.E., Palmieri, L., Wertin, T., Arrigoni, R., Polacco, J.C., and, Palmieri, F., (2003) Identification of a mitochondrial transporter for basic amino acids in Arabidopsis thaliana by functional reconstitution into liposomes and complementation in yeast. Plant J. 33, 1027-1035.
26. Ishizaki, K., Larson, T.R., Schauer, N., Fernie, A.R., Graham, I.A., and, Leaver, C.J., (2005) The critical role of Arabidopsis electron transfer flavoprotein: ubiquinone oxidoreductase during dark induced starvation. Plant Cell, 17, 2587-2600.
27. Jenner, C.F., Uglade, T.D., and, Aspinall, D., (1991) The physiology of starch and protein deposition in the endosperm of wheat. Aust. J. Plant Physiol. 18, 211-226.
28. JÃrgensen, J.E., GrÃnlund, M., Pallisgaard, N., Larsen, K., Marcker, K.A., and, Jensen, E.O., (1999) A new class of plant homeobox genes is expressed in specific regions of determinate symbiotic root nodules. Plant Mol. Biol. 40, 65-77.
29. Ju, C., Zhang, F., Gao, Y., Zhang, W., Yan, J., Dai, J., and, Li, J., (2006) Cloning, chromosome mapping and expression analysis of an R2R3-MYB gene under-expressed in maize hybrid. Mol. Biol. Rep. 33, 103-110.
30. Kalamaki, M.S., Merkouropoulos, G., and, Kanellis, A.K., (2009) Can ornithine accumulation modulate abiotic stress tolerance in Arabidopsis? Plant Signal. Behav. 4, 1099-10101.
31. Kamauchi, S., Nakatani, H., Nakano, C., and, Urade, R., (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 272, 3461-3476.
32. Kleine-Vehn, J., and, Friml, J., (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu. Rev. Cell Dev. Biol. 24, 447-473.
33. Kopka, J., Schauer, N., Krueger, S., et al. (2005) gmd@csb.db: the Golm Metabolome database. Bioinformatics, 21, 1635-1638.
34. Kosugi, S., and, Ohashi, Y., (2003) Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiol. 132, 2012-2022.
35. Liao, Y., Zou, H.F., Wang, H.W., Zhang, W.K., Ma, B., Zhang, J.S., and, Chen, S.Y., (2008) Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants. Cell Res. 18, 1047-1060.
36. Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K., and, Hake, S., (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell, 6, 1859-1876.
37. Link, W., (1990) Autofertility and rate of cross-fertilization: crucial characters for breeding synthetic varieties in faba beans (Vicia faba L.). Theor. Appl. Genet. 79, 713-717.
38. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and, Fernie, A.R., (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396.
39. Ljun, K., Hul, A.K., Kowalczyk, M., Marchant, A., Celenza, J., Cohen, J.D., and, Sandberg, G., (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol. Biol. 50, 309-332.
40. Luedemann, A., Strassburg, K., Erban, A., and, Kopka, J., (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS) based metabolite profiling experiments. Bioinformatics, 24, 732-737.
41. Malone, S., Chen, Z.H., Bahrami, A.R., Walker, R.P., Gray, J.E., and, Leegood, R.C., (2007) Phosphoenolpyruvate carboxykinase in Arabidopsis: changes in gene expression, protein and activity during vegetative and reproductive development. Plant Cell Physiol. 48, 441-450.
42. Meyer, R.C., Torjek, O., Becher, M., and, Altmann, T., (2004) Heterosis of biomass production in Arabidopsis. Establishment during early development. Plant Physiol. 134, 1813-1823.
43. Meyer, R.C., Steinfath, M., Lisec, J., et al. (2007a) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 104, 4759-4764.
44. Meyer, S., Pospisil, H., and, Scholten, S., (2007b) Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol. Biol. 63, 381-391.
45. Miranda, M., Borisjuk, L., Tewes, A., Heim, U., Sauer, N., Wobus, U., and, Weber, H., (2001) Amino acid permeases in developing seeds of Vicia faba L.: expression precedes storage protein synthesis and is regulated by amino acid supply. Plant J. 28, 61-71.
46. Molendijk, A.J., Ruperti, B., and, Palme, K., (2004) Small GTPases in vesicle trafficking. Curr. Opin. Plant Biol. 7, 694-700.
47. Nagano, Y., Furuhashi, H., Inaba, T., and, Sasaki, Y., (2002) A novel class of plant-specific zinc-dependent DNA-binding protein that binds to A/T-rich DNA sequences. Nucleic Acids Res. 29, 4097-4105.
48. Navarro, C., Efremova, N., Golz, J.F., Rubiera, R., Kuckenberg, M., Castillo, R., Tietz, O., Saedler, H., and, Schwarz-Sommer, Z., (2004) Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development. Development, 131, 3649-3659.
49. Nelissen, H., Fleury, D., Bruno, L., Robles, P., De Veylder, L., Traas, J., Micol, J.L., Van Montagu, M., Inzé, D., and, Van Lijsebettens, M., (2005) The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc. Natl. Acad. Sci. USA, 102, 7754-7759.
50. Paciorek, T., and, Friml, J., (2006) Auxin signaling. J. Cell Sci. 119, 1199-1202.
51. Patrick, J.W., and, Offler, C.E., (2001) Compartmentation of transport and transfer events in developing seeds. J. Exp. Bot. 52, 551-564.
52. Quittenden, L.J., Davies, N.W., Smith, J.A., Molesworth, P.P., Tivendale, N.D., and, Ross, J.J., (2009) Auxin biosynthesis in pea: characterization of the tryptamine pathway. Plant Physiol. 151, 1130-1138.
53. Radchuk, R., Radchuk, V., Weschke, W., Borisjuk, L., and, Weber, H., (2006) Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiol. 140, 263-278.
54. Radchuk, R., Emery, R.J.N., Weier, D., Vigeolas, H., Geigenberger, P., Lunn, J.E., Feil, R., Weschke, W., and, Weber, H., (2010) Sucrose non-fermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. Plant J. 61, 324-338.
55. Radwanski, E.R., and, Last, R.L., (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell, 7, 921-934.
56. Rampey, R.A., LeClere, S., Kowalczyk, M., Ljung, K., Sandberg, G., and, Bartel, B., (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 135, 978-988.
57. Rampey, R.A., Woodward, A.W., Hobbs, B.N., Tierney, M.P., Lahner, B., Salt, D.E., and, Bartel, B., (2006) An Arabidopsis basic helix-loop-helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness. Genetics, 174, 1841-1857.
58. Riebeseel, E., Häusler, R.E., Radchuk, R., et al. (2010) The 2-oxoglutarate/malate translocator mediates amino acid and storage protein biosynthesis in pea embryos. Plant J. 61, 350-363.
59. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., and, Fernie, A.R., (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell, 13, 11-29.
60. Rolletschek, H., Hajirezaei, M., Wobus, U., and, Weber, H., (2002) Antisense-inhibition of ADP-glucose pyrophosphorylase in Vicia narbonensis seeds increases soluble sugars, causes higher uptake of water and amino acids which leads to higher protein content. Planta, 214, 954-964.
61. Rolletschek, H., Nguyen, T.H., Häusler, R.E., et al. (2007) Antisense inhibition of the plastidial glucose-6-phosphate/phosphate translocator in Vicia seeds shifts cellular differentiation and promotes protein storage. Plant J. 51, 468-484.
62. Rozhon, W., Mayerhofer, J., Petutschnig, E., Fujioka, S., and, Jonak, C., (2010) ASKtheta, a group-III Arabidopsis GSK3, functions in the brassinosteroid signalling pathway. Plant J. 62, 215-223.
63. Sassa, N., Matsushita, Y., Nakamura, T., and, Nyunoya, H., (2001) The molecular characterization and in situ expression pattern of pea SCARECROW gene. Plant Cell Physiol. 42, 385-394.
64. Sato, N., Ohshima, K., Watanabe, A., Ohta, N., Nishiyama, Y., Joyard, J., and, Douce, R., (1998) Molecular characterization of the PEND protein, a novel bZIP protein present in the envelope membrane that is the site of nucleoid replication in developing plastids. Plant Cell, 10, 859-872.
65. Schwender, J., Shachar-Hill, Y., and, Ohlrogge, J.B., (2006) Mitochondrial metabolism in developing embryos of Brassica napus. J. Biol. Chem. 281, 34040-34047.
66. Singh, D.K., Islam, M.N., Choudhury, N.R., Karjee, S., and, Mukherjee, S.K., (2007) The 32 kDa subunit of replication protein A (RPA) participates in the DNA replication of mung bean yellow mosaic India virus (MYMIV) by interacting with the viral Rep protein. Nucleic Acids Res. 35, 755-770.
67. Staswick, P.E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M.T., Maldonado, M.C., and, Suza, W., (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell, 17, 616-627.
68. Steinkamp, T., Hill, K., Hinnah, S.C., Wagner, R., Röhl, T., Pohlmeyer, K., and, Soll, J., (2000) Identification of the pore-forming region of the outer chloroplast envelope protein OEP16. J. Biol. Chem. 275, 11758-11764.
69. Stone, S.L., and, Callis, J., (2007) Ubiquitin ligases mediate growth and development by promoting protein death. Curr. Opin. Plant Biol. 10, 624-632.
70. Stuurman, J., Jäggi, F., and, Kuhlemeier, C., (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev. 16, 2213-2218.
71. Tang, Z., Sadka, A., Morishige, D.T., and, Mullet, J.E., (2001) Homeodomain leucine zipper proteins bind to the phosphate response domain of the soybean VspB tripartite promoter. Plant Physiol. 125, 797-809.
72. Thiel, J., Müller, M., Weschke, W., and, Weber, H., (2009) Amino acid metabolism at the maternal-filial boundary of young barley seeds: a microdissection-based study. Planta, 230, 205-213.
73. Tsukagoshi, H., Morikami, A., and, Nakamura, K., (2007) Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings. Proc. Natl. Acad. Sci. USA, 104, 2543-2547.
74. Wang, H., Caruso, L.V., Downie, A.B., and, Perry, S.E., (2004) The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell, 16, 1206-1219.
75. Weber, H., Borisjuk, L., Heim, U., Buchner, P., and, Wobus, U., (1995) Seed coat-associated invertases of Fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. Plant Cell, 7, 1835-1846.
76. Weber, H., Borisjuk, L., and, Wobus, U., (1996) Controlling seed development and seed size in Vicia faba: a role for seed coat-associated invertases and carbohydrate state. Comparative analysis of a small and a large-seeded genotype. Plant J. 10, 823-824.
77. Weber, H., Borisjuk, L., Heim, U., Sauer, N., and, Wobus, U., (1997) A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in faba bean seeds. Plant Cell, 9, 895-908.
78. Weber, H., Borisjuk, L., and, Wobus, U., (2005) Molecular physiology of legume seed development. Annu. Rev. Plant Biol. 56, 253-279.
79. Weber, H., Radchuk, R., Weigelt, K., and, Saalbach, I., (2009) Changing metabolic pathways to manipulate legume seed maturation and composition. In Modification of Seed Composition to Promote Health and Nutrition. Agronomy Monograph 51 (, Krishnan, H.B., ed.). Madison, WI, USA: American Society of Agronomy, Crop Science Society of America and Soil Science Society of America, pp. 55-78.
80. Weber, H., Sreenivasulu, N., and, Weschke, W., (2010) Molecular Physiology of Seed Maturation and Seed Storage Protein Biosynthesis. Plant Developmental Biology-Biotechnological Perspectives, Vol. 2 (, Pua, E.C., and, Davey, M.R., eds). Heidelberg, Berlin: Springer-Verlag, pp. 83-104.
81. Yanagisawa, S., Akiyama, A., Kisaka, H., Uchimiya, H., and, 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, 7833-7838.
82. Zheng, Y., Ren, N., Wang, H., Stromberg, A.J., and, Perry, S.E., (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell, 21, 2563-2577.
83. Zhou, Y., Chan, K., Wang, T.L., Hedley, C.L., Offler, C.E., and, Patrick, J.W., (2009) Intracellular sucrose communicates metabolic demand to sucrose transporters in developing pea cotyledons. J. Exp. Bot. 60, 71-85.