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Control of seed coat rupture by ABA-INSENSITIVE 5 in Arabidopsis thaliana

Published online by Cambridge University Press:  12 April 2019

Thiago Barros-Galvão ,
Fabián E. Vaistij  and
Ian A. Graham Open the ORCID record for Ian A. Graham [Opens in a new window]
Thiago Barros-Galvão
Affiliation:
Centre for Novel Agricultural Products, Department of Biology, University of York, York YO10 5DD, UK
Fabián E. Vaistij
Affiliation:
Centre for Novel Agricultural Products, Department of Biology, University of York, York YO10 5DD, UK
Ian A. Graham*
Affiliation:
Centre for Novel Agricultural Products, Department of Biology, University of York, York YO10 5DD, UK
*
Author for correspondence: Ian A. Graham, E-mail: ian.graham@york.ac.uk
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Abstract

In Arabidopsis, seed germination is a biphasic process involving rupture of the seed coat followed by emergence of the radicle through the micropylar endosperm. Embryo expansion results in seed coat rupture and removal of seed coat imposed dormancy with DELLA proteins blocking embryo expansion in the absence of gibberellins. Exogenous abscisic acid (ABA) treatment does not block seed coat rupture but does block radicle emergence. We used this limited effect of exogenous ABA to further investigate the mechanism by which it blocks the onset of germination marked by seed coat rupture. We show that physical nicking of the seed coat results in exogenous ABA treatment blocking both seed coat and endosperm rupture and this block requires the transcription factors ABI3 and ABI5, but not ABI4. Furthermore, we show that the repression of expression of several EXPANSIN genes (EXPA1, EXPA2, EXPA3, EXPA9 and EXPA20) by exogenous ABA requires ABI5. We conclude that ABI5 plays an important role in the ABA-mediated repression of germination through prevention of seed coat rupture and propose that this involves EXPANSIN related control of cell wall loosening.

Keywords

ABAABI5EXPANSINnickingtesta rupture
Type
Short Communication
Information
Seed Science Research , Volume 29 , Issue 2 , June 2019 , pp. 143 - 148
Copyright
Copyright © Cambridge University Press 2019 

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References

Beisson, F, Li, Y, Bonaventure, G, Pollard, M and Ohlrogge, JB (2007) The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19, 351–368.Google Scholar
Bewley, JD (1997) Breaking down the walls – A role for endo-b-mannanase in release from seed dormancy? Trends in Plant Science 12, 464–469.Google Scholar
Bies-Etheve, N, da Silva Conceicao, A, Giraudat, J, Koornneef, M, Léon-Kloosterziel, K, Valon, C and Delseny, M (1999) Importance of the B2 domain of the Arabidopsis ABI3 protein for Em and 2S albumin gene regulation. Plant Molecular Biology 40, 1045–1054.Google Scholar
Bossi, F, Cordoba, E, Dupré, P, Mendoza, MS, Román, CS and León, P (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. Plant Journal 59, 359–374.Google Scholar
Cao, D, Hussain, A, Cheng, H and Peng, J (2005) Loss of function of four DELLA genes leads to light- and gibberellin- independent seed germination in Arabidopsis. Planta 223, 105–113.Google Scholar
Chen, F and Bradford, KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiology 124, 1265–1274.Google Scholar
Chen, F, Dahal, P and Bradford, KJ (2001) Two tomato expansin genes show divergent expression and localization in embryos during seed development and germination. Plant Physiology 127, 928–936.Google Scholar
Chen, M, Zhang, B, Li, C, Kulaveerasingam, H, Chew, FT and Yu, H (2015) TRANSPARENT TESTA GLABRA1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiology 169, 391–402.Google Scholar
Corbineau, F and Côme, D (1993) The concept of dormancy in cereal seeds. Proceedings of the 4th International Workshop on Seeds. Basic and Applied Aspects of Seed Biology, July 1993, Angers, France.Google Scholar
Cosgrove, DJ (2005) Growth of the plant cell wall. Nature Reviews Molecular Cell Biology, 11, 850–861.Google Scholar
Debeaujon, I, Léon-Kloosterziel, KM and Koornneef, M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122, 403–414.Google Scholar
Debeaujon, I, Nesi, N, Perez, P, Devic, M, Grandjean, O, Caboche, M and Lepiniec, L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15, 2514–2531.Google Scholar
De Giorgi, J, Piskurewicz, U, Loubery, S, Utz-Pugin, A, Bailly, C, Mène-Saffrané, L and Lopez-Molina, L (2015) An endosperm-associated cuticle is required for Arabidopsis seed viability, dormancy and early control of germination. PLoS Genetics 12, e1005708.Google Scholar
Delmas, F, Sankaranarayanan, S, Deb, S, Widdup, E, Bournonville, C, Bollier, N, Northey, JG, McCourt, P and Samuel, MA (2013) ABI3 controls embryo degreening through Mendel's I locus. Proceedings of the National Academy of Sciences of the USA 40, E3888–E3894.Google Scholar
Edwards, MM (1968) Dormancy in seeds of Charlock: III. Occurrence and mode of action of an inhibitor associated with dormancy. Journal of Experimental Botany 19, 601–610.Google Scholar
Finkelstein, RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant Journal 5, 765–771.Google Scholar
Finkelstein, RR, Gampalab, SSL and Rock, CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14, S15–S45.Google Scholar
Footitt, S, Douterelo-Soler, I, Clay, H and Finch-Savage, WE (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences of the USA 50, 20236–20241.Google Scholar
Giraudat, J, Hauge, BM, Valon, C, Smalle, J, Parcy, F and Goodman, HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 10, 1251–1261.Google Scholar
Hutchison, KW, Singer, PB, McInnis, S, Diaz-Sala, C and Greenwood, MS (1999) Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin. Plant Physiology 120, 827–832.Google Scholar
Kang, J, Yim, S, Choi, H, Kim, A, Lee, KP, Lopez-Molina, L, Martinoia, E and Lee, Y (2015) Abscisic acid transporters cooperate to control seed germination. Nature Communications 6, 1–10.Google Scholar
Karssen, CM and Laçka, E (1985) A revision of the hormone balance theory of seed dormancy: studies on gibberellin and/or abscisic acid-deficient mutants of Arabidopsis thaliana. in Bopp, M (ed), Plant Growth Substances. Heidelberg, Berlin: Springer, pp. 315–323Google Scholar
Lee, S, Cheng, H, King, KE, Wang, W, He, Y, Hussain, A, Lo, J, Harberd, NP and Peng, J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes & Development 16, 646–658.Google Scholar
Lee, KP, Piskurewicz, U, Turecková, V, Strnad, M and Lopez-Molina, L (2010) A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proceedings of the National Academy of Sciences of the USA 44, 19108–19113.Google Scholar
Lee, KP, 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 & Development 17, 1984–1996.Google Scholar
Linkies, A, Müller, K, Morris, K, Turecková, V, Wenk, M, Cadman, CS, Corbineau, F, Strnad, M, Lynn, JR, Finch-Savage, WE and Leubner-Metzger, G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21, 3803–3822.Google Scholar
Liu, PP, Koizuka, N, Homrichhausen, TM, Hewitt, JR, Martin, RC and Nonogaki, H (2005) Large-scale screening of Arabidopsis enhancer-trap lines for seed germination-associated genes. Plant Journal 41, 936–944.Google Scholar
Lopez-Molina, L, Mongrand, S and Chua, NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 98, 4782–4787.Google Scholar
Lopez-Molina, L, Mongrand, S, McLachlin, DT, Chait, BT and Chua, NH (2002) ABI5 acts downstream of ABI3 to execute an ABA dependent growth arrest during germination. Plant Journal 32, 317–328.Google Scholar
Luckwill, LC (1952) Growth-inhibiting and growth-promoting substances in relation to the dormancy and after-ripening of apple seeds. Journal of Horticultural Science 1, 53–67.Google Scholar
MacGregor, DR, Kendall, SL, Florance, H, Fedi, F, Moore, K, Paszkiewicz, K, Smirnoff, N and Penfield, S (2015) Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism. New Phytologist 205, 642–652.Google Scholar
Marowa, P, Ding, A and Kong, Y (2016) Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Reports 35, 949–965.Google Scholar
McGinnis, KM, Thomas, SG, Soule, JD, Strader, LC, Zale, JM, Sun, TP and Steber, CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15, 1120–1130.Google Scholar
Müller, K, Tintelnot, S and Leubner-Metzger, G (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant and Cell Physiology 47, 864–877.Google Scholar
Nambara, E, Hayama, R, Tsuchiya, Y, Nishimura, M, Kawaide, H, Kamiya, Y and Naito, S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Developmental Biology 220, 412–423.Google Scholar
Nambara, E, Suzuki, M, Abrams, S, McCarty, DR, Kamiya, Y and McCourt, P (2002) A screen for genes that function in abscisic acid signaling in Arabidopsis thaliana. Genetics 161, 1247–1255.Google Scholar
Ooms, JJJ, Léon-Kloosterziel, KM, Bartels, D, Koornneef, M and Karssen, CM (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana: a comparative study using abscisic acid-insensitive abi3 mutants. Plant Physiology 102, 1185–1191Google Scholar
Parcy, F, Valon, C, Kohara, A, Misera, S and Giraudat, J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9, 1265–1277.Google Scholar
Penfield, S, Rylott, ER, Gilday, AD, Graham, S, Larson, TR and Graham, IA (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. Plant Cell 16, 2705–2718.Google Scholar
Penfield, S, Gilday, AD, Halliday, KJ and Graham, IA (2006a) DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy. Current Biology 16, 2366–2370.Google Scholar
Penfield, S, Li, Y, Gilday, AD, Graham, S and Graham, IA (2006b) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18, 1887–1899.Google Scholar
Piskurewicz, U, Jikumaru, Y, Kinoshita, N, Nambara, E, Kamiya, Y and Lopez-Molina, L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20, 2729–2745.Google Scholar
Piskurewicz, U, Turecková, V, Lacombe, E and Lopez-Molina, L (2009) Far-red light inhibits germination through DELLA-dependent stimulation of ABA synthesis and ABI3 activity. EMBO Journal 28, 2259–2271.Google Scholar
Rajjou, L, Duval, M, Gallardo, K, Catusse, J, Bally, J, Job, C and Job, D (2012) Seed germination and vigor. Annual Reviews of Plant Biology 63, 507–533.Google Scholar
Sagasser, M, Lu, GH, Hahlbrock, K and Weisshaar, B (2002) A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes & Development 16, 138–149.Google Scholar
Shcherban, TY, Shi, J, Durachko, DM, Guiltinan, MJ, McQueen-Mason, SJ, Shieh, M and Cosgrove, DJ (1995) Molecular cloning and sequence analysis of expansins – a highly conserved, multigene family of proteins that mediate cell wall extension in plants. Proceedings of the National Academy of Sciences of the USA 92, 9245–9249.Google Scholar
Shirley, BW, Kubasek, WL, Storz, G, Bruggemann, E, Koornneef, M, Ausubel, FM and Goodman, HM (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant Journal 8, 659–671.Google Scholar
Topham, AT, Taylor, RE, Yan, D, Nambara, E, Johnston, IG and Bassel, GW (2017) Temperature variability is integrated by a spatially embedded decision-making center to break dormancy in Arabidopsis seeds. Proceedings of the National Academy of Sciences of the USA 114, 6629–6634.Google Scholar
Tsuchiya, Y, Nambara, E, Naito, S and McCourt, P (2004) The FUS3 transcription factor functions through the epidermal regulator TTG1 during embryogenesis in Arabidopsis. Plant Journal 37, 73–81.Google Scholar
Tyler, L, Thomas, SG, Hu, J, Dill, A, Alonso, JM, Ecker, JR and Sun, TP (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiology 135, 1008–1019.Google Scholar
Vaistij, FE, Gan, Y, Penfield, S, Gilday, AD, Dave, A, He, Z, Josse, EM, Choi, G, Halliday, KJ and Graham, IA (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proceedings of the National Academy of Sciences of the USA 110, 10866–10871.Google Scholar
Vishwanath, SJ, Kosma, DK, Pulsifer, IP, Scandola, S, Pascal, S, Joubès, J, Dittrich-Domergue, F, Lessire, R, Rowland, O and Domergue, F (2013) Suberin-associated fatty alcohols in Arabidopsis: distributions in roots and contributions to seed coat barrier properties. Plant Physiology 163, 1118–1132.Google Scholar
Wyatt, JE (1977) Seed coat and water absorption properties of seed of near-isogenic snap bean lines differing in seed coat color. Journal of the American Society for Horticultural Science 102, 478–480.Google Scholar
Yamaguchi, S, Kamiya, Y and Sun, T (2001) Distinct cell-specific expression patterns of early and late gibberellin biosynthetic genes during Arabidopsis seed germination. Plant Journal 28, 443–453.Google Scholar
Yan, A, Wu, M, Yan, L, Hu, R, Ali, I and Gan, Y (2014) AtEXP2 is involved in seed germination and abiotic stress response in Arabidopsis. PLoS One 9, e85208.Google Scholar
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