Hostname: page-component-848d4c4894-xfwgj Total loading time: 0 Render date: 2024-06-29T23:09:56.192Z Has data issue: false hasContentIssue false

Developing soybean seed germination: low ABA and high EXP1 gene expression promote embryonic axis growth whereas the seed coat delays radicle protrusion

Published online by Cambridge University Press:  23 March 2022

Nidia H. Montechiarini
Affiliation:
Cátedra de Fisiología Vegetal, Facultad de Ciencias Agrarias, Universidad Nacional de Rosario (UNR), Campo Experimental J. Villarino, CC14, S2125ZAA Zavalla, Santa Fe, Argentina
Eligio N. Morandi
Affiliation:
Instituto de Investigaciones en Ciencias Agrarias de Rosario (IICAR-UNR/CONICET), Facultad de Ciencias Agrarias, Universidad Nacional de Rosario (UNR), Campo Experimental J. Villarino, CC14, S2125ZAA Zavalla, Santa Fe, Argentina
Carlos O. Gosparini*
Affiliation:
Cátedra de Fisiología Vegetal, Facultad de Ciencias Agrarias, Universidad Nacional de Rosario (UNR), Campo Experimental J. Villarino, CC14, S2125ZAA Zavalla, Santa Fe, Argentina Instituto de Investigaciones en Ciencias Agrarias de Rosario (IICAR-UNR/CONICET), Facultad de Ciencias Agrarias, Universidad Nacional de Rosario (UNR), Campo Experimental J. Villarino, CC14, S2125ZAA Zavalla, Santa Fe, Argentina
*
Author for Correspondence: Carlos O. Gosparini, E-mail: cgospari@unr.edu.ar

Abstract

Seed germination implies an expansion process restarting the growth of the embryonic axis (Ax) and which is completed by radicle emergence through the seed covering layers. In developing soybean seeds, abscisic acid in Ax (ABAa) mainly inhibits Ax growth. Additionally, the expression of the EXP1 gene at the elongation zone (EZ) was found to be involved in the promotion of mature soybean Ax growth, which increased during water incubation and which was repressed by exogenous ABA. This work aimed to evaluate (1) the ABAa and EXP1 levels at the EZ and (2) the role of the seed coat (SC) in developing soybean seed germination. Whole seeds (Se), embryos (Em) and Ax at 25–45 d after anthesis (DAA) germinated in vitro, and germination performance increased with DAA. ABAa decreased in planta from 25 DAA until its critical non-inhibitory threshold (ABAc) at around physiological maturity (45 DAA). At earlier ages, the ABAc was reached during the in vitro incubation. Concomitantly, EXP1 transcripts accumulated with age into the pool of long-lived mRNAs and were up-regulated during incubation. Additionally, isolated Ax germinated faster, took up more water and increased its water potential more rapidly during incubation than Ax in Se. Also, a lower osmotic gradient was required to germinate at 45 DAA, when ABAa was no longer inhibitory. Simultaneously, the pressure to protrude SC through the micropylar area increased from 25 to 45 DAA. These results support the role of ABAa and EXP1 in controlling Ax growth and the SC in delaying radicle protrusion.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bellieny-Rabelo, D, De Oliveira, EAG, Da Silva Ribeiro, E, Pessoa Costa, E, Oliveira, AEA and Venancio, TM (2016) Transcriptome analysis uncovers key regulatory and metabolic aspects of soybean embryonic axes during germination. Scientific Reports 6, 112. doi:10.1038/srep36009.CrossRefGoogle ScholarPubMed
Bewley, JD (1997) Seed germination and dormancy. Plant Cell 9, 10551066. doi:10.1105/tpc.9.7.1055.CrossRefGoogle ScholarPubMed
Bewley, JD and Black, M (1994) Seeds physiology of development and germination (2nd edn). New York, Plenum Press. doi:10.1017/S0960258500002713.CrossRefGoogle Scholar
Bewley, JD, Bradford, KJ, Hilhorst, HWM and Nonogaki, H (2013) Seeds: Physiology of development, germination and dormancy (3rd edn). New York, Springer. doi:10.1007/978-1-4614-4693-4.CrossRefGoogle Scholar
Bove, J, Jullien, M and Grappin, P (2001) Functional genomics in the study of seed germination. Genome Biology 3, 1002.11002.5. doi:10.1186/gb-2001-3-1-reviews1002.CrossRefGoogle Scholar
Bradford, KJ (1994) Water stress and the water relations of seed development: a critical review. Crop Science 34, 111. doi:10.2135/cropsci1994.0011183X003400010001x.CrossRefGoogle Scholar
Chandra, S, Yadav, RR, Poonia, S, Yashpal, , Rathod, DR, Kumar, A, Lal, SK and Talukdar, A (2017) Seed coat permeability studies in wild and cultivated species of soybean. International Journal of Current Microbiology and Applied Sciences 6, 23582363. doi:10.20546/ijcmas.2017.607.279.CrossRefGoogle Scholar
Cosgrove, DJ (2000) Loosening of plant cell walls by expansins. Nature 407, 321326. doi:10.1038/35030000.CrossRefGoogle ScholarPubMed
Cosgrove, DJ (2016) Catalysts of plant cell wall loosening. F1000 Research 5, 113. doi:10.12688/f1000research.7180.1.CrossRefGoogle ScholarPubMed
Crookston, RK and Hill, DS (1978) A visual indicator of the physiological maturity of soybean seed. Crop Science 18, 867870. doi:10.2135/cropsci1978.0011183X001800050048x.CrossRefGoogle Scholar
Egli, DB and Tekrony, DM (1997) Species differences in seed water status during seed maturation and germination. Seed Science Research 7, 312. doi:10.1017/s0960258500003305.CrossRefGoogle Scholar
Finch-Savage, WE and Bassel, GW (2016) Seed vigour and crop establishment: extending performance beyond adaptation. Journal of Experimental Botany 67, 567591. doi:10.1093/jxb/erv490.CrossRefGoogle ScholarPubMed
Finch-Savage, WE and Leubner-Metzger, G (2006) Seed dormancy and the control of germination. New Phytologist 171, 501523. doi:10.1111/j.1469-8137.2006.01787.x.CrossRefGoogle ScholarPubMed
Gazara, RK, de Oliveira, EAG, Rodrigues, BC, Nunes da Fonseca, R, Oliveira, AEA and Venancio, TM (2019) Transcriptional landscape of soybean (Glycine max) embryonic axes during germination in the presence of paclobutrazol, a gibberellin biosynthesis inhibitor. Scientific Reports 9, 112. doi:10.1038/s41598-019-45898-2.CrossRefGoogle ScholarPubMed
Gimeno-Gilles, C, Leliévre, E, Viau, L, Malik-Ghulam, M, Ricoult, C, Niebel, A, Leduc, N and Limami, AM (2009) ABA-mediated inhibition of germination is related to the inhibition of genes encoding cell-wall biosynthetic and architecture: modifying enzymes and structural proteins in Medicago truncatula embryo axis. Molecular Plant 2, 108119. doi:10.1093/mp/ssn092.CrossRefGoogle Scholar
Gosparini, CO, Morandi, EN and Cairo, CA (1997) Efecto de la edad, el lavado y la temperatura sobre la germinación de las semillas inmaduras, el crecimiento radicular y el tiempo hasta la floración, de la soja. Revista de la Facultad de Agronomía, La Plata 102, 19.Google Scholar
Gosparini, CO, Busilacchi, HA, Vernieri, P and Morandi, EN (2007) Endogenous abscisic acid and precocious germination of developing soybean seeds. Seed Science Research 17, 165174. doi:10.1017/S0960258507785872.CrossRefGoogle Scholar
Hernández-Nistal, J, Martín, I, Esteban, R, Dopico, B and Labrador, E (2010) Abscisic acid delays chickpea germination by inhibiting water uptake and down-regulating genes encoding cell wall remodelling proteins. Plant Growth Regulation 61, 175183. doi:10.1007/s10725-010-9463-z.CrossRefGoogle Scholar
Hilhorst, HWM (1995) A critical update on seed dormancy. I. Primary dormancy. Seed Science Research 5, 6173. doi:10.1017/S0960258500002634.CrossRefGoogle Scholar
Iglesias, RG and Babiano, MJ (1997) Endogenous abscisic acid during the germination of chick-pea seeds. Physiologia Plantarum 100, 500504. doi:10.1111/j.1399-3054.1997.tb03054.x.CrossRefGoogle Scholar
ISTA (2016) International Rules for Seed Testing, Vol. 2016, Full issue i-19-8 (284). Bassersdorf, Switzerland, The International Seed Testing Association (ISTA). https://vri.umayor.cl/images/ISTA_Rules_2016_Spanish.pdfGoogle Scholar
Itoyama, H, Nakagawa, ACS, Ariyoshi, Y, Ario, N, Yuasa, T, Iwaya-Inoue, M and Ishibashi, Y (2020) Lignin deposits in pedicel xylem vessels regulate water transport during seed maturation in soybean. Crop Science 60, 954960. doi:10.1002/csc2.20121.CrossRefGoogle Scholar
Kebede, H, Smith, JR and Ray, JD (2014) Identification of a single gene for seed coat impermeability in soybean PI 594619. Theoretical and Applied Genetics 127, 19912003. doi:10.1007/s00122-014-2355-2.CrossRefGoogle ScholarPubMed
Kermode, AR (2005) Role of abscisic acid in seed dormancy. Journal of Plant Growth Regulation 24, 319344. doi:10.1007/s00344-005-0110-2.CrossRefGoogle Scholar
Koizumi, M, Kikuchi, K, Isobe, S, Ishida, N, Naito, S and Kano, H (2008) Role of seed coat in imbibing soybean seeds observed by micro-magnetic resonance imaging. Annals of Botany 102, 343352. doi:10.1093/aob/mcn095.CrossRefGoogle ScholarPubMed
Kucera, B, Cohn, MA and Leubner-Metzger, G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281307. doi:10.1079/SSR2005218.CrossRefGoogle Scholar
Lee, D-K, Ahn, JH, Song, S-K, Choi, YD and Lee, JS (2003) Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiology 131, 985997. doi:10.1104/pp.009902.CrossRefGoogle Scholar
Li, Q, Fan, C-M, Zhang, X-M and Fu, Y-F (2012) Validation of reference genes for real-time quantitative PCR normalisation in soybean developmental and germinating seeds. Plant Cell Reports 31, 17891798. doi:10.1007/s00299-012-1282-4.CrossRefGoogle Scholar
Liu, X and Hou, X (2018) Antagonistic regulation of ABA and GA in metabolism and signaling pathways. Frontiers in Plant Science. doi:10.3389/fpls.2018.00251.Google Scholar
, P, Kang, M, Jiang, X, Dai, F, Gao, J and Zhang, C (2013) RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis. Planta 237, 15471559. doi:10.1007/s00425-013-1867-3.CrossRefGoogle ScholarPubMed
Maidl Souza, N, Topham, AT and Bassel, GW (2017) Quantitative analysis of the 3D cell shape changes driving soybean germination. Journal of Experimental Botany 68, 15311537. doi:10.1093/jxb/erx048.CrossRefGoogle Scholar
Matilla, AJ (2020) Seed dormancy: molecular control of its induction and alleviation. Plants 9, 1402. doi:10.3390/plants9101402.CrossRefGoogle ScholarPubMed
Mc Donald, MB Jr., Vertucci, CW and Roos, EE (1988) Seed coat regulation of soybean seed imbibition. Crop Science 28, 987992. doi:10.2135/cropsci1988.0011183X002800060025x.CrossRefGoogle Scholar
Michel, BE (1983) Evaluation of the potential of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiology 72, 6670. doi:10.1104/pp.72.1.66.CrossRefGoogle Scholar
Miller, SS, Bowman, LA, Gijzen, M and Miki, BLA (1999) Early development of the seed coat of soybean (Glycine max). Annals of Botany 84, 297304. doi:10.1006/anbo.1999.0915.CrossRefGoogle Scholar
Miles, DFN, TeKrony, DM and Egli, DB (1988) Changes in viability, germination, and respiration of freshly harvested soybean seed during development. Crop Science 28, 700704. doi:10.2135/cropsci1988.0011183X002800040030x.CrossRefGoogle Scholar
Montechiarini, NH (2018) Regulación de la expresión del programa de germinación en semillas de soja. Doctoral thesis, Facultad de Cs, Agrarias, Universidad Nacional de Rosario, Argentina. Available at: http://hdl.handle.net/2133/17760.Google Scholar
Montechiarini, NH, Delgado, L, Morandi, EN, Carrillo, NJ and Gosparini, CO (2020) The expansin EXP1 gene in the elongation zone is induced during soybean embryonic axis germination and differentially expressed in response to ABA and PEG treatments. Seed Science Research 31, 6068. doi:10.1017/S0960258520000379CrossRefGoogle Scholar
Morandi, EN, Schussler, JR and Brenner, ML (1990) Photoperiodically induced changes in seed growth rate of soybean as related to endogenous concentrations of ABA and sucrose in seed tissues. Annals of Botany 66, 605611. doi:10.1093/oxfordjournals.aob.a088070.CrossRefGoogle Scholar
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 Journal 41, 697709. doi:10.1111/j.1365-313X.2005.02337.xCrossRefGoogle Scholar
Nambara, E and Nonogaki, H (2012) Seed biology in the 21st century: perspectives and new directions. Plant & Cell Physiology 53, 14. doi:10.1093/pcp/pcr184.CrossRefGoogle ScholarPubMed
Nonogaki, H (2014) Seed dormancy and germination-emerging mechanisms and new hypotheses. Frontiers in Plant Science 5, 114. doi:10.3389/fpls.2014.00233.CrossRefGoogle ScholarPubMed
Penfield, S (2017) Seed dormancy and germination. Current Biology 27, 874878. doi:10.1016/j.cub.2017.05.050.CrossRefGoogle ScholarPubMed
Pfaffl, MW, Horgan, GW and Dempfle, L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30. doi:10.1093/nar/30.9.e36.CrossRefGoogle Scholar
Qutob, D, Ma, F, Peterson, CA, Bernards, MA and Gijzen, M (2008) Structural and permeability properties of the soybean seed coat. Botany 86, 219227. doi:10.1139/B08-002.CrossRefGoogle Scholar
Rajjou, L, Duval, M, Gallardo, K, Catusse, J, Bally, J, Job, C and Job, D (2012) Seed germination and vigor. Annual Review of Plant Biology 63, 507533. doi:10.1146/annurev-arplant-042811-105550.CrossRefGoogle ScholarPubMed
Rubio de Casas, R, Willis, CG, Pearse, WD, Baskin, CC, Baskin, JM and Cavender-Bares, J (2017) Global biogeography of seed dormancy is determined by seasonality and seed size: a case study in the legumes. New Phytologist 214, 15271536. doi:10.1111/nph.14498.CrossRefGoogle ScholarPubMed
Sakamoto, SI, Abe, J, Kanazawa, A and Shimamoto, Y (2004) Marker-assisted analysis for soybean hard seededness with isozyme and simple sequence repeat loci. Breeding Science 54, 133139. doi:10.1270/jsbbs.54.133.CrossRefGoogle Scholar
Sangi, S, Santos, MLC, Alexandrino, CR, Da Cunha, M, Coelho, FS, Ribeiro, GP, Lenz, D, Ballesteros, H, Hemerly, AS, Venâncio, TM, Oliveira, AEA and Grativol, C (2019) Cell wall dynamics and gene expression in soybean embryonic axes during germination. Planta 250, 13251337. doi:10.1007/s00425-019-03231-1.CrossRefGoogle ScholarPubMed
Sano, N, Ono, H, Murata, K, Yamada, T, Hirasawa, T and Kanekatsu, M (2015) Accumulation of long-lived mRNAs associated with germination in embryos during seed development of rice. Journal of Experimental Botany 66, 40354046. doi:10.1093/jxb/erv209.CrossRefGoogle ScholarPubMed
Sano, N, Rajjou, L and North, HM (2020) Lost in translation: physiological roles of stored mRNAs in seed germination. Plants 9, 347. doi:10.3390/plants9030347.CrossRefGoogle ScholarPubMed
Schopfer, P and Plachy, C (1985) Control of seed germination by abscisic acid. III Effect on embryo growth potential (minimum turgor pressure) and growth coefficient (cell wall extensibility) in Brassica napus L. Plant Physiology 77, 676686. doi:10.1104/pp.77.3.676.CrossRefGoogle Scholar
Shu, K, Zhou, W, Chen, F, Luo, X and Yang, W (2018) Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Frontiers in Plant Science 9, 18. doi:10.3389/fpls.2018.00416.CrossRefGoogle ScholarPubMed
Sliwinska, E, Bassel, GW and Bewley, JD (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. Journal of Experimental Botany 60, 35873594. doi:10.1093/jxb/erp203.CrossRefGoogle Scholar
Smýkal, P, Vernoud, V, Blair, MW, Soukup, A and Thompson, RD (2014) The role of the testa during development and in establishment of dormancy of the legume seed. Frontiers in Plant Science 5, 119. doi:10.3389/fpls.2014.00351.Google ScholarPubMed
Steinbrecher, T and Leubner-Metzger, G (2017) The biomechanics of seed germination. Journal of Experimental Botany 68, 765783. doi:10.1093/jxb/erw428.Google ScholarPubMed
Steinbrecher, T and Leubner-Metzger, G (2018) Tissue and cellular mechanics of seeds. Current Opinion in Genetics & Development 51, 110. doi:10.1016/j.gde.2018.03.001.CrossRefGoogle ScholarPubMed
Valio, IFM (1986) The role of seed coat in early stages of soybean germination. Biologia Plantarum 28, 258264. doi:10.1007/BF02902289.CrossRefGoogle Scholar
Vernieri, P, Perata, P, Armellini, D, Bugnoli, M, Presentini, R, Lorenzi, R, Ceccarelli, N, Alpi, A and Tognoni, F (1989a) Solid phase radioimmunoassay for the quantitation of abscisic acid in plant crude extracts using a new monoclonal antibody. Journal of Plant Physiology 134, 441446. doi:10.1016/S0176-1617(89)80007-0.CrossRefGoogle Scholar
Xu, N, Coulter, KM and Bewley, JD (1990) Absisic acid and osmoticum prevent germination of developing alfalfa embryos, but only osmoticum manteins the synthesis of developmental proteins. Planta 182, 182190. doi.org/10.1007/BF02411389.CrossRefGoogle Scholar
Xu, H, Lantzouni, O, Bruggink, T, Benjamins, R, Lanfermeijer, F, Denby, K, Schwechheimer, C and Bassel, GW (2020) A molecular signal integration network underpinning Arabidopsis seed germination. Current Biology 30, 110. doi:10.1016/j.cub.2020.07.012.CrossRefGoogle ScholarPubMed
Yan, D, Duermeyer, L, Leoveanu, C and Nambara, E (2014) The functions of the endosperm during seed germination. Plant & Cell Physiology 55, 15211533. doi:10.1093/pcp/pcu089.CrossRefGoogle ScholarPubMed
Zanakis, G, Ellis, R and Summerfield, R (1994) Seed quality in relation to seed development and maturation in three genotypes of soyabean (Glycine max). Experimental Agriculture 30, 139156. doi:10.1017/S0014479700024091.CrossRefGoogle Scholar
Zhu, Y, Wu, N, Song, W, Yin, G, Qin, Y, Yan, Y and Hu, Y (2014) Soybean (Glycine max) expansin gene superfamily origins: segmental and tandem duplication events followed by divergent selection among subfamilies. BMC Plant Biology 14, 93. doi:10.1186/1471-2229-14-93.CrossRefGoogle ScholarPubMed
Supplementary material: File

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material

Download Montechiarini et al. supplementary material(File)
File 2.5 MB