ABI5 is a regulator of seed maturation and longevity in legumes

Plant Cell

Volumn 28, Issue 11, 2016, Pages 2735-2754

  Zinsmeister, Julia ^a   Lalanne, David ^a   Terrasson, Emmanuel ^a,e   Chatelain, Emilie ^a   Vandecasteele, Céline ^a,f   Ly Vu, Benoit ^a   Dubois Laurent, Cécile ^a   Geoffriau, Emmanuel ^a   Le Signor, Christine ^b   Dalmais, Marion ^c   Gutbrod, Katharina ^d   Dörmann, Peter ^d   Gallardo, Karine ^b   Bendahmane, Abdelhafid ^c   Buitink, Julia ^a   Leprince, Olivier ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^c CNRS   (France)

^d UNIVERSITY OF BONN   (Germany)

^e ILLUMINA INC   (United States)

^f UMR1388 GenPhySE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; CHLOROPHYLL; PLANT PROTEIN; TRANSCRIPTION FACTOR;

BARREL MEDIC; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PEA; PHYSIOLOGY; PLANT SEED;

CAROTENOIDS; CHLOROPHYLL; GENE EXPRESSION REGULATION, PLANT; MEDICAGO TRUNCATULA; PEAS; PLANT PROTEINS; SEEDS; TRANSCRIPTION FACTORS;

EID: 85006263047     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.16.00470     Document Type: Article

References (74)

1. Allorent, G., Osorio, S., Vu, J.L., Falconet, D., Jouhet, J., Kuntz,M., Fernie, A.R., Lerbs-Mache, S., Macherel, D., Courtois, F., and Finazzi, G. (2015). Adjustments of embryonic photosynthetic activity modulate seed fitness in Arabidopsis thaliana. New Phytol. 205: 707-719.
2. Almoguera, C., Prieto-Dapena, P., Díaz-Martín, J., Espinosa, J.M., Carranco, R., and Jordano, J. (2009). The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biol. 9: 75.
3. Bensmihen, S., Rippa, S., Lambert, G., Jublot, D., Pautot, V., Granier, F., Giraudat, J., and Parcy, F. (2002). The homologous ABI5 and EEL transcription factors function antagonistically to finetune gene expression during late embryogenesis. Plant Cell 14: 1391-1403.
4. Bentsink, L., Jowett, J., Hanhart, C.J., and Koornneef, M. (2006). Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc. Natl. Acad. Sci. USA 103: 17042-17047.
5. Bolingue, W., Ly Vu, B., Leprince, O., and Buitink, J. (2010). Characterization of dormancy behaviour in seeds of the model legume Medicago truncatula. Seed Sci. Res. 20: 97-107.
6. Boucher, V., Buitink, J., Lin, X., Boudet, J., Hoekstra, F.A., Hundertmark, M., Renard, D., and Leprince, O. (2010). MtPM25 is an atypical hydrophobic late embryogenesis-abundant protein that dissociates cold and desiccation-aggregated proteins. Plant Cell Environ. 33: 418-430.
7. Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larré, C., Satour, P., and Leprince, O. (2006). Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol. 140: 1418-1436.
8. Buitink, J., Hemminga, M.A., and Hoekstra, F.A. (2000). Is there a role for oligosaccharides in seed longevity? An assessment of intracellular glass stability. Plant Physiol. 122: 1217-1224.
9. Buitink, J., and Leprince, O. (2004). Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48: 215-228.
10. Canfield, M.R., Guiamét, J.J., and Noodén, L.D. (1995). Alteration of soybean seedling development in darkness and light by the staygreen mutation cytG and Gd1d2. Ann. Bot. (Lond.) 75: 143-150.
11. Carles, C., Bies-Etheve, N., Aspart, L., Léon-Kloosterziel, K.M., Koornneef, M., Echeverria, M., and Delseny, M. (2002). Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J. 30: 373-383.
12. Chatelain, E., Hundertmark, M., Leprince, O., Le Gall, S., Satour, P., Deligny-Penninck, S., Rogniaux, H., and Buitink, J. (2012). Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity. Plant Cell Environ. 35: 1440-1455.
13. Châtelain, E., Satour, P., Laugier, E., Ly Vu, B., Payet, N., Rey, P., and Montrichard, F. (2013). Evidence for participation of the methionine sulfoxide reductase repair system in plant seed longevity. Proc. Natl. Acad. Sci. USA 110: 3633-3638.
14. Christ, B., and Hörtensteiner, S. (2014). Mechanism and significance of chlorophyll breakdown. J. Plant Growth Regul. 33: 4-20.
15. Chung, D.W., Pruzinská, A., Hörtensteiner, S., and Ort, D.R. (2006). The role of pheophorbide a oxygenase expression and activity in the canola green seed problem. Plant Physiol. 142: 88-97.
16. Clerkx, E.J.M., Vries, H.B., Ruys, G.J., Groot, S.P.C., and Koornneef, M. (2003). Characterization of green seed, an enhancer of abi3-1 in Arabidopsis that affects seed longevity. Plant Physiol. 132: 1077-1084.
17. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R. (2010). Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61: 651-679.
18. Dalmais, M., Schmidt, J., Le Signor, C., Moussy, F., Burstin, J., Savois, V., Aubert, G., Brunaud, V., de Oliveira, Y., Guichard, C., Thompson, R., and Bendahmane, A. (2008). UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biol. 9: R43.
19. De Giorgi, J., Piskurewicz, U., Loubery, S., Utz-Pugin, A., Bailly, C., Mène-Saffrané, L., and Lopez-Molina, L. (2015). An endospermassociated cuticle is required for Arabidopsis seed viability, dormancy and early control of germination. PLoS Genet. 11: e1005708.
20. Debeaujon, I., Léon-Kloosterziel, K.M., and Koornneef, M. (2000). Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122: 403-414.
21. Dekkers, B.J.W., He, H., Hanson, J., Willems, L.A.J., Jamar, D.C.L., Cueff, G., Rajjou, L., Hilhorst, H.W.M., and Bentsink, L. (2016). The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. Plant J. 85: 451-465.
22. Delahaie, J., Hundertmark, M., Bove, J., Leprince, O., Rogniaux, H., and Buitink, J. (2013). LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance. J. Exp. Bot. 64: 4559-4573.
23. Delmas, F., Sankaranarayanan, S., Deb, S., Widdup, E., Bournonville, C., Bollier, N., Northey, J.G.B., McCourt, P., and Samuel, M.A. (2013). ABI3 controls embryo degreening through Mendel’s I locus. Proc. Natl. Acad. Sci. USA 110: E3888-E3894.
24. de Souza Vidigal, D., Willems, L., van Arkel, J., Dekkers, B.J., Hilhorst, H.W., and Bentsink, L. (2016). Galactinol as marker for seed longevity. Plant Sci. 246: 112-118.
25. Finkelstein, R., Gampala, S.S.L., Lynch, T.J., Thomas, T.L., and Rock, C.D. (2005). Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol. Biol. 59: 253-267.
26. Finkelstein, R.R. (1994). Maternal effects govern variable dominance of two abscisic acid response mutations in Arabidopsis thaliana. Plant Physiol. 105: 1203-1208.
27. Finkelstein, R.R., and Lynch, T.J. (2000). The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609.
28. Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M.M., Seki, M., Hiratsu, K., Ohme-Takagi, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2005). AREB1 is a transcription activator of novel ABREdependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488.
29. Fujita, Y., Fujita, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2011). ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 124: 509-525.
30. Goldovsky, L., Cases, I., Enright, A.J., and Ouzounis, C.A. (2005). BioLayout(Java): versatile network visualisation of structural and functional relationships. Appl. Bioinformatics 4: 71-74.
31. Gonzalez-Jorge, S., et al. (2013). Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene content in Arabidopsis seeds. Plant Cell 25: 4812-4826.
32. Havaux, M., Eymery, F., Porfirova, S., Rey, P., and Dörmann, P. (2005). Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17: 3451-3469.
33. Hundertmark, M., Buitink, J., Leprince, O., and Hincha, D.K. (2011). The reduction of seed-specific dehydrins reduces seed longevity in Arabidopsis thaliana. Seed Sci. Res. 21: 165-173.
34. Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., and Parcy, F.; bZIP Research Group (2002). bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7: 106-111.
35. Jalink, H., van der Schoor, R., Frandas, A., van Pijlen, J.G., and Bino, R.J. (1998). Chlorophyll fluorescence of Brassica oleracea seeds as a non-destructive marker for seed maturity and seed performance. Seed Sci. Res. 8: 437-443.
36. Jourjon, M.-F., Jasson, S., Marcel, J., Ngom, B., and Mangin, B. (2005). MCQTL: multi-allelic QTL mapping in multi-cross design. Bioinformatics 21: 128-130.
37. Kranner, I., Birtić, S., Anderson, K.M., and Pritchard, H.W. (2006). Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radic. Biol. Med. 40: 2155-2165.
38. Lee, K.P., Piskurewicz, U., Turečková, V., Carat, S., Chappuis, R., Strnad, M., Fankhauser, C., and Lopez-Molina, L. (2012). Spatially and genetically distinct control of seed germination by phytochromes A and B. Genes Dev. 26: 1984-1996.
39. Lopez-Molina, L., Mongrand, S., and Chua, N.-H. (2001). A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl. Acad. Sci. USA 98: 4782-4787.
40. Maia, J., Dekkers, B.J.W., Dolle, M.J., Ligterink, W., and Hilhorst, H.W.M. (2014). Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. New Phytol. 203: 81-93.
41. Mène-Saffrané, L., Jones, A.D., and DellaPenna, D. (2010). Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proc. Natl. Acad. Sci. USA 107: 17815-17820.
42. Monma, M., Ito, M., Saito, M., and Chikuni, K. (1994). Carotenoid components in soybean seeds varying with seed color and maturation stage. Biosci. Biotechnol. Biochem. 58: 926-930.
43. Moran, R. (1982). Formulae for determination of chlorophyllous pigments extracted with n,n-dimethylformamide. Plant Physiol. 69: 1376-1381.
44. Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y., and Nambara, E. (2005). Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41: 697-709.
45. Nakajima, S., Ito, H., Tanaka, R., and Tanaka, A. (2012). Chlorophyll b reductase plays an essential role in maturation and storability of Arabidopsis seeds. Plant Physiol. 160: 261-273.
46. Nambara, E., Keith, K., McCourt, P., and Naito, S. (1994). Isolation of an internal deletion mutant of the Arabidopsis thaliana ABI3 gene. Plant Cell Physiol. 35: 509-513.
47. Nishizawa, A., Yabuta, Y., and Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147: 1251-1263.
48. Ogé, L., Bourdais, G., Bove, J., Collet, B., Godin, B., Granier, F., Boutin, J.-P., Job, D., Jullien, M., and Grappin, P. (2008). Protein repair L-isoaspartyl methyltransferase 1 is involved in both seed longevity and germination vigor in Arabidopsis. Plant Cell 20: 3022-3037.
49. Ooms, J., Leon-Kloosterziel, K.M., Bartels, D., Koornneef, M., and Karssen, C.M. (1993). Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana (a comparative study using abscisic acid-insensitive abi3 mutants). Plant Physiol. 102: 1185-1191.
50. Perrin, F., Brahem, M., Dubois-Laurent, C., Huet, S., Jourdan, M., Geoffriau, E., Peltier, D., and Gagné, S. (2016). Differential pigment accumulation in carrot leaves and roots during two growing periods. J. Agric. Food Chem. 64: 906-912.
51. Personat, J.-M., Tejedor-Cano, J., Prieto-Dapena, P., Almoguera, C., and Jordano, J. (2014). Co-overexpression of two Heat Shock Factors results in enhanced seed longevity and in synergistic effects on seedling tolerance to severe dehydration and oxidative stress. BMC Plant Biol. 14: 56.
52. Prieto-Dapena, P., Castaño, R., Almoguera, C., and Jordano, J. (2006). Improved resistance to controlled deterioration in transgenic seeds. Plant Physiol. 142: 1102-1112.
53. Probert, R., Adams, J., Coneybeer, J., Crawford, A., and Hay, F. (2007). Seed quality for conservation is critically affected by prestorage factors. Aust. J. Bot. 55: 326-335.
54. Righetti, K., Vu, J.L., Pelletier, S., Vu, B.L., Glaab, E., Lalanne, D., Pasha, A., Patel, R.V., Provart, N.J., Verdier, J., Leprince, O., and Buitink, J. (2015). Inference of longevity-related genes from a robust co-expression network of seed maturation identifies regulators linking seed storability to biotic defense-related pathways. Plant Cell 27: 2692-2708.
55. Rosnoblet, C., Aubry, C., Leprince, O., Vu, B.L., Rogniaux, H., and Buitink, J. (2007). The regulatory gamma subunit SNF4b of the sucrose non-fermenting-related kinase complex is involved in longevity and stachyose accumulation during maturation of Medicago truncatula seeds. Plant J. 51: 47-59.
56. Sakuraba, Y., Jeong, J., Kang, M.-Y., Kim, J., Paek, N.-C., and Choi, G. (2014). Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat. Commun. 5: 4636.
57. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101-1108.
58. Schneider, T., and Keller, F. (2009). Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant Cell Physiol. 50: 2174-2182.
59. Sinniah, U.R., Ellis, R.H., and John, P. (1998). Irrigation and seed quality development in rapid-cycling Brassica: soluble carbohydrates and heat-stable proteins. Ann. Bot. (Lond.) 82: 647-655.
60. Sugliani, M., Rajjou, L., Clerkx, E.J.M., Koornneef, M., and Soppe, W.J.J. (2009). Natural modifiers of seed longevity in the Arabidopsis mutants abscisic acid insensitive3-5 (abi3-5) and leafy cotyledon1-3 (lec1-3). New Phytol. 184: 898-908.
61. Tang, W., Ji, Q., Huang, Y., Jiang, Z., Bao, M., Wang, H., and Lin, R. (2013). FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol. 163: 857-866.
62. Teixeira, R.N., Ligterink, W., França-Neto, J.B., Hilhorst, H.W., and da Silva, E.A. (2016). Gene expression profiling of the green seed problem in soybean. BMC Plant Biol. 16: 37.
63. Terrasson, E., Buitink, J., Righetti, K., Ly Vu, B., Pelletier, S., Zinsmeister, J., Lalanne, D., and Leprince, O. (2013). An emerging picture of the seed desiccome: confirmed regulators and newcomers identified using transcriptome comparison. Front. Plant Sci. 4: 497.
64. Thayer, S.S., and Björkman, O. (1990). Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth. Res. 23: 331-343.
65. Tunnacliffe, A., Hincha, D.K., Leprince, O., and Macherel, D. (2010). LEA proteins: versatility of form and function. In Dormancy and Resistance in Harsh Environments: Topics in Current Genetics 21, E. Lubzens, J. Cerda, and M. Clark, eds (Berlin, Heidelberg: Springer-Verlag), pp. 91-108.
66. Vandecasteele, C., et al. (2011). Quantitative trait loci analysis reveals a correlation between the ratio of sucrose/raffinose family oligosaccharides and seed vigour in Medicago truncatula. Plant Cell Environ. 34: 1473-1487.
67. Verdier, J., et al. (2013). A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiol. 163: 757-774.
68. Vom Dorp, K., Hölzl, G., Plohmann, C., Eisenhut, M., Abraham, M., Weber, A.P.M., Hanson, A.D., and Dörmann, P. (2015). Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis. Plant Cell 27: 2846-2859.
69. Voorrips, R.E. (2002). MapChart: software for the graphical presentation of linkage maps and QTLs. J. Hered. 93: 77-78.
70. Wang, Z., Cheng, K., Wan, L., Yan, L., Jiang, H., Liu, S., Lei, Y., and Liao, B. (2015). Genome-wide analysis of the basic leucine zipper (bZIP) transcription factor gene family in six legume genomes. BMC Genomics 16: 1053.
71. Waterworth, W.M., Masnavi, G., Bhardwaj, R.M., Jiang, Q., Bray, C.M., and West, C.E. (2010). A plant DNA ligase is an important determinant of seed longevity. Plant J. 63: 848-860.
72. Yamburenko, M.V., Zubo, Y.O., Vanková, R., Kusnetsov, V.V., Kulaeva, O.N., and Börner, T. (2013). Abscisic acid represses the transcription of chloroplast genes. J. Exp. Bot. 64: 4491-4502.
73. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61: 672-685.
74. Zbierzak, A.M., Kanwischer, M., Wille, C., Vidi, P.-A., Giavalisco, P., Lohmann, A., Briesen, I., Porfirova, S., Bréhélin, C., Kessler, F., and Dörmann, P. (2009). Intersection of the tocopherol and plastoquinol metabolic pathways at the plastoglobule. Biochem. J. 425: 389-399.