Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-13T04:12:04.722Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  27 November 2020

Nidia H. Montechiarini ,
Luciana Delgado ,
Eligio N. Morandi ,
Néstor J. Carrillo  and
Carlos O. Gosparini Open the ORCID record for Carlos O. Gosparini [Opens in a new window]
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
Luciana Delgado
Affiliation:
Instituto de Investigaciones en Ciencias Agrarias de Rosario (IICAR-UNR/CONICET), Facultad de Ciencias Agrarias, Universidad Nacional de Rosario (UNR), 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), Zavalla, Santa Fe, Argentina
Néstor J. Carrillo
Affiliation:
Instituto de Biología Molecular y Celular de Rosario (IBR-UNR/CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), Rosario, 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), Zavalla, Santa Fe, Argentina
*
Author for Correspondence: Carlos O. Gosparini, E-mail: cgospari@unr.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

During soybean seed germination, the expansive growth potential of the embryonic axes is driven by water uptake while cell wall loosening occurs in cells from the elongation zone (EZ). Expansins are regarded as primary promoters of cell wall remodelling in all plant expansion processes, with the expression profiles of the soybean expansins supporting their cell or tissue specificity. Therefore, we used embryonic axes isolated from whole seed and focused on the EZ to study seed germination. Using a suite of degenerate primers, we amplified an abundantly expressed expansin gene at the EZ during soybean embryonic axis germination, which was identified as EXP1 by in silico analyses. Expression studies showed that EXP1 was induced under germination conditions in distilled water and down-regulated by abscisic acid (ABA), which inhibits soybean germination by physiologically restraining expansion. Moreover, we also identified a time window of ABA responsiveness within the first 6 h of incubation in water, after which ABA lost control of both EXP1 expression and embryonic axis germination, thus confirming the early role of EXP1 in the EZ during this process. By contrast, EXP1 levels in the EZ increased even when germination was impaired by osmotically limiting the water availability required to develop the embryonic axes’ growth potential. We propose that these higher EXP1 levels are involved in the fast germination of soybean embryonic axes as soon as water availability is re-established. Taken together, our results show strong EXP1 expression in the EZ and postulate EXP1 as a target candidate for soybean seed germination control.

Keywords

abscisic acidelongation zoneembryonic axesexpansingerminationpolyethylene glycolsoybean
Type
Research Paper
Information
Seed Science Research , Volume 31 , Issue 1 , March 2021 , pp. 60 - 68
Check for updates
Copyright
Copyright © The Author(s), 2020. 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

Balestrini, R, Cosgrove, DJ and Bonfante, P (2005) Differential location of alpha-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220, 889–899. doi:10.1007/s00425-004-1431-2.CrossRefGoogle Scholar
Belfield, EJ, Ruperti, B, Roberts, JA and McQueen-Mason, S (2005) Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. Journal of Experimental Botany 56, 817–823. doi:10.1093/jxb/eri076.CrossRefGoogle ScholarPubMed
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, 1–12. doi:10.1038/srep36009.CrossRefGoogle ScholarPubMed
Berry, T and Bewley, JD (1992) A Role for the Surrounding Fruit Tissues in Preventing the Germination of Tomato (Lycopersicon esculentum) Seeds. Plant Physiology 100, 951–957. doi:10.1104/pp.100.2.951.CrossRefGoogle ScholarPubMed
Bewley, JD, Bradford, KJ, Hilhorst, HWM and Nonogaki, H (2013) Seeds. Physiology of development, germination and dormancy (3rd edn). New York, Springer.Google Scholar
Bradford, K and Nonogaki, H (2007) Annual plant reviews volume 27: seed development. Dormancy and Germination. doi:10.1002/9780470988848.CrossRefGoogle Scholar
Brummell, DA, Harpster, MH, Civello, PM, Palys, JM, Bennett, AB and Dunsmuir, P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11, 2203–2216. doi:10.1105/tpc.11.11.2203.CrossRefGoogle ScholarPubMed
Chen, F and Bradford, KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiology 124, 1265–1274. doi:10.1104/pp.124.3.1265.CrossRefGoogle ScholarPubMed
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. doi:10.1104/pp.010259.CrossRefGoogle ScholarPubMed
Chiu, RS, Pan, S, Zhao, R and Gazzarrini, S (2016) ABA-dependent inhibition of the ubiquitin proteasome system during germination at high temperature in Arabidopsis. Plant Journal 88, 749–761. doi:10.1111/tpj.13293.CrossRefGoogle ScholarPubMed
Corpet, F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16, 10881–10890. doi:10.1093/nar/16.22.10881.CrossRefGoogle ScholarPubMed
Cosgrove, DJ (2000) Loosening of plant cell walls by expansins. Nature 407, 321–326. doi:10.1038/35030000.CrossRefGoogle ScholarPubMed
Cosgrove, DJ (2016) Catalysts of plant cell wall loosening. F1000 Research 5, 1–13. doi:10.12688/f1000research.7180.1.CrossRefGoogle ScholarPubMed
Darley, CP, Forrester, AM and McQueen-Mason, SJ (2001) The molecular basis of plant cell wall extension. Plant Molecular Biology 47, 179–195. doi:10.1023/A:1010687600670.CrossRefGoogle ScholarPubMed
Doebley, JF, Gaut, BS and Smith, BD (2006) The molecular genetics of crop domestication. Cell 127, 1309–1321D. doi:10.1016.j.cell.2006.12.006.CrossRefGoogle ScholarPubMed
Dotto, MC, Martínez, GA and Civello, PM (2006) Expression of expansin genes in strawberry varieties with contrasting fruit firmness. Plant Physiology and Biochemistry 44, 301–307. doi:10.1016/j.plaphy.2006.06.008.CrossRefGoogle ScholarPubMed
Endo, A, Tatematsu, K, Hanada, K, Duermeyer, L, Okamoto, M, Yonekura-Sakakibara, K, Saito, K, Toyoda, T, Kawakami, N, Kamiya, Y, Seki, M and Nambara, E (2012) Tissue-specific transcriptome analysis reveals cell wall metabolism, flavonol biosynthesis and defense responses are activated in the endosperm of germinating Arabidopsis thaliana seeds. Plant and Cell Physiology 53, 16–27. doi:10.1093/pcp/pcr171.CrossRefGoogle ScholarPubMed
Gallardo, K, Job, C, Groot, SPC, Puype, M, Demol, H, Vandekerckhove, J and Job, D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiology 126, 835–848. doi:10.1104/pp.126.2.835.CrossRefGoogle ScholarPubMed
Gimeno-Gilles, C, Lelièvre, 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, 108–119. doi:10.1093/mp/ssn092.CrossRefGoogle ScholarPubMed
Giordano, W and Hirsch, AM (2004) The expression of MaEXP1, a Melilotus alba expansin gene, is upregulated during the sweetclover-Sinorhizobium meliloti interaction. Molecular Plant-Microbe Interactions 17, 613–622. doi:10.1094/MPMI.2004.17.6.613.CrossRefGoogle ScholarPubMed
Gosparini, CO, Busilacchi, HA, Vernieri, P and Morandi, EN (2007) Endogenous abscisic acid and precocious germination of developing soybean seeds. Seed Science Research 17, 165. doi:10.1017/S0960258507785872.CrossRefGoogle Scholar
Gray-Mitsumune, M, Mellerowicz, EJ, Abe, H, Schrader, J, Winzéll, A, Sterky, F, Blomqvist, K, McQueen-Mason, S, Teeri, TT and Sundberg, B (2004) Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family. Plant Physiology 135, 1552–1564. doi:10.1104/pp.104.039321.CrossRefGoogle ScholarPubMed
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, 175–183. doi:10.1007/s10725-010-9463-z.CrossRefGoogle Scholar
Jones, L and McQueen-Mason, S (2004) A role for expansins in dehydration and rehydration of the resurrection plant Craterostigma plantagineum. FEBS Letters 559, 61–65. doi:10.1016/S0014-5793(04)00023-7.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGAx: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549. doi:10.1093/molbev/msy096.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, 985–997. 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 normalization in soybean developmental and germinating seeds. Plant Cell Reports 31, 1789–1798. doi:10.1007/s00299-012-1282-4.CrossRefGoogle ScholarPubMed
López-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. https://doi.org/10.1073/pnas.081594298.CrossRefGoogle ScholarPubMed
López-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. doi.org/10.1046/j.1365-313X.2002.01430.xCrossRefGoogle ScholarPubMed
Michel, BE (1983) Evaluation of the water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiology 72, 66–70. doi:10.1104/pp.72.1.66.CrossRefGoogle ScholarPubMed
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. http://hdl.handle.net/2133/17760.Google Scholar
Nonogaki, H, Bassel, GW and Bewley, JD (2010) Germination—still a mystery. Plant Science 179, 574–581. doi:10.1016/j.plantsci.2010.02.010.CrossRefGoogle Scholar
Paulsen, TR, Colville, L, Kranner, I, Daws, MI, Högstedt, G, Vandvik, V and Thompson, K (2013) Physical dormancy in seeds: a game of hide and seek? New Phytologist 198, 496–503. doi:10.1111/nph.12191.CrossRefGoogle ScholarPubMed
Pezzotti, M, Feron, R and Mariani, C (2002) Pollination modulates expression of the PPAL gene, a pistil-specific beta-expansin. Plant Molecular Biology 49, 187–197. doi:10.1023/A:1014962923278.CrossRefGoogle ScholarPubMed
Rajjou, L, Gallardo, K, Debeaujon, I, Vandekerckhove, J, Job, C and Job, D (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiology 134, 1598–1613. doi:10.1104/pp.103.036293.CrossRefGoogle ScholarPubMed
Rozen, S and Skaletsky, H (2000) PRIMER 3 on the WWW for general users and for biologist programmers. Methods in molecular biology 132, 365–386. doi:10.1385/1-59259-192-2:365.Google Scholar
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, 133–139. doi:10.1270/jsbbs.54.133.CrossRefGoogle Scholar
Sampedro, J and Cosgrove, DJ (2005) The expansin superfamily. Genome Biology 6, 242. doi:10.1186/gb-2005-6-12-242.CrossRefGoogle ScholarPubMed
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 on soybean embryonic axes during germination. Planta 250, 1325–1337. doi:10.1007/s00425-019-03231-1.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, 676–686. doi:10.1104/pp.77.3.676CrossRefGoogle Scholar
Schopfer, P, Bajracharya, D and Plachy, C (1979) Control of seed germination by abscisic acid: I. Time course of action in Sinapis alba L. Plant Physiology 64, 822–827. doi:10.1104/pp.64.5.822CrossRefGoogle 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, 3587–3594. doi:10.1093/jxb/erp203.CrossRefGoogle Scholar
Soeda, Y, Konings, MCJM, Vorst, OFJ, van Houwelingen, AMML, Stoopen, GM, Maliepaard, CA, Kodde, J, Bino, RJ, Groot, SPC and van der Geest, AHM (2005) Gene expression programs during Brassica oleracea seed maturation, osmopriming, and germination are indicators of progression of the germination process and the stress tolerance level. Plant Physiology 137, 354–368. doi:10.1104/pp.104.051664.CrossRefGoogle ScholarPubMed
Steinbrecher, T and Leubner-Metzger, G (2016) The biomechanics of seed germination. Journal of Experimental Botany 68, 765–783. doi:10.1093/jxb/erw428.Google Scholar
Weitbrecht, K, Müller, K and Leubner-Metzger, G (2011) First off the mark: early seed germination. Journal of Experimental Botany 62, 3289–3309. doi:10.1093/jxb/err030.CrossRefGoogle ScholarPubMed
Wolf, S, Hématy, K and Höfte, H (2012) Growth control and cell wall signaling in plants. Annual Review of Plant Biology 63, 381–407. doi:10.1146/annurev-arplant-042811-105449.CrossRefGoogle ScholarPubMed
Wrobel, RL and Yoder, JI (2001) Differential RNA expression of α-expansin gene family members in the parasitic angiosperm triphysaria versicolor (Scrophulariaceae). Gene 266, 85–93. doi:10.1016/S0378-1119(01)00376-6.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, 1–10. doi:10.1016/j.cub.2020.07.012.CrossRefGoogle ScholarPubMed
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

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material 1

Download Montechiarini et al. supplementary material(Video)
Video 31.8 MB

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material 2

Download Montechiarini et al. supplementary material(Video)
Video 32.9 MB
Supplementary material: Image

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material 3

Download Montechiarini et al. supplementary material(Image)
Image 1.8 MB
Supplementary material: Image

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material 4

Download Montechiarini et al. supplementary material(Image)
Image 2 MB
Supplementary material: Image

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material 5

Download Montechiarini et al. supplementary material(Image)
Image 9.4 MB
Supplementary material: Image

Montechiarini et al. supplementary material

Montechiarini et al. supplementary material 6

Download Montechiarini et al. supplementary material(Image)
Image 1.3 MB