Abstract
Main conclusion
Identification of the structural changes and cell wall-related genes likely involved in cell wall extension, cellular water balance and cell wall biosynthesis on embryonic axes during germination of soybean seeds.
Abstract
Cell wall is a highly organized and dynamic structure that provides mechanical support for the cell. During seed germination, the cell wall is critical for cell growth and seedling establishment. Although seed germination has been widely studied in several species, key aspects regarding the regulation of cell wall dynamics in germinating embryonic axes remain obscure. Here, we characterize the gene expression patterns of cell wall pathways and investigate their impact on the cell wall dynamics of embryonic axes of germinating soybean seeds. We found 2143 genes involved in cell wall biosynthesis and assembly in the soybean genome. Key cell wall genes were highly expressed at specific germination stages, such as expansins, UDP-Glc epimerases, GT family, cellulose synthases, peroxidases, arabinogalactans, and xyloglucans-related genes. Further, we found that embryonic axes grow through modulation of these specific cell wall genes with no increment in biomass. Cell wall structural analysis revealed a defined pattern of cell expansion and an increase in cellulose content during germination. In addition, we found a clear correlation between these structural changes and expression patterns of cell wall genes during germination. Taken together, our results provide a better understanding of the complex transcriptional regulation of cell wall genes that drive embryonic axes growth and expansion during soybean germination.
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References
Amaya I, Botella MA, de la Calle M et al (1999) Improved germination under osmotic stress of tobacco plants overexpressing a cell wall peroxidase. FEBS Lett 457:80–84. https://doi.org/10.1016/S0014-5793(99)01011-X
Arioli T, Peng L, Betzner AS et al (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720. https://doi.org/10.1126/science.279.5351.717
Bellieny-Rabelo D, de Oliveira EAG, da Silva Ribeiro E et al (2016) Transcriptome analysis uncovers key regulatory and metabolic aspects of soybean embryonic axes during germination. Sci Rep 6:36009. https://doi.org/10.1038/srep36009
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066. https://doi.org/10.1105/tpc.9.7.1055
Bewley JD, Bradford K, Hilhorst H, Nonogaki H (2013) Seeds, 3rd edn. Springer, New York
Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–339. https://doi.org/10.1023/A:1010656104304
Buckeridge MS (2010) Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol. https://doi.org/10.1104/pp.110.158642
Burton RA, Wilson SM, Hrmova M et al (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-β-d-glucans. Science 311:1940–1942. https://doi.org/10.1126/science.1122975
Carpenter AE, Jones TR, Lamprecht MR et al (2006) Cell profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100. https://doi.org/10.1186/gb-2006-7-10-r100
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering land plants—consistency of molecular structure with the physical properties of the walls during growth. Plant J. https://doi.org/10.1111/j.1365-313x.1993.tb00007.x
Chiang GCK, Barua D, Kramer EM et al (2009) Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 106:11661–11666. https://doi.org/10.1073/pnas.0901367106
Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172. https://doi.org/10.1016/j.pbi.2015.05.014
Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot 67:463–476. https://doi.org/10.1093/jxb/erv511
Dekkers BJW, Schuurmans JAMJ, Smeekens SCM (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218:579–588. https://doi.org/10.1007/s00425-003-1154-9
Dhaubhadel S, McGarvey BD, Williams R, Gijzen M (2003) Isoflavonoid biosynthesis and accumulation in developing soybean seeds. Plant Mol Biol 53:733–743. https://doi.org/10.1023/B:PLAN.0000023666.30358.ae
Downie B, Gurusinghe S, Dahal P et al (2003) Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol 131:1347–1359. https://doi.org/10.1104/pp.016386
Farrokhi N, Burton RA, Brownfield L et al (2006) Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 4:145–167. https://doi.org/10.1111/j.1467-7652.2005.00169.x
Francoz E, Ranocha P, Nguyen-Kim H et al (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21. https://doi.org/10.1016/j.phytochem.2014.07.020
Gibeaut DM (2000) Nucleotide sugars and glycosyltransferases for synthesis of cell wall matrix polysaccharides. Plant Physiol Biochem 38:69–80. https://doi.org/10.1016/S0981-9428(00)00167-4
Gidrol X, Lin WS, Dégousée N et al (1994) Accumulation of reactive oxygen species and oxidation of cytokinin in germinating soybean seeds. Eur J Biochem 224:21–28. https://doi.org/10.1111/j.1432-1033.1994.tb19990.x
Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266:605–614. https://doi.org/10.1126/science.266.5185.605
Hall Q, Cannon MC (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14:1161–1172. https://doi.org/10.1105/tpc.010477
Hou SY, Shen J, Sun ZX, Li HY (2018) Identification of genes related to cell wall metabolism and fruit ripening in Ziziphus jujube using RNA-seq and expression analysis. Russ J Plant Physiol 65:604–610. https://doi.org/10.1134/S102144371804012X
Houston K, Tucker MR, Chowdhury J et al (2016) The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci 7:984. https://doi.org/10.3389/fpls.2016.00984
Hu Y, Yu D (2014) BRASSINOSTEROID INSENSITIVE2 Interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant Cell 26:4394–4408. https://doi.org/10.1105/tpc.114.130849
Karnovsky M (1964) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A–138A
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36. https://doi.org/10.1016/S1369-5266(01)00219-9
Kumar M, Campbell L, Turner S (2016) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531. https://doi.org/10.1093/jxb/erv533
Liepman AH, Wightman R, Geshi N et al (2010) Arabidopsis—a powerful model system for plant cell wall research. Plant J 61:1107–1121. https://doi.org/10.1111/j.1365-313X.2010.04161.x
McCann MC, Roberts K (1994) Changes in cell wall architecture during cell elongation. J Exp Bot 45:1683–1691
Müller K, Linkies A, Vreeburg RAM et al (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150:1855–1865. https://doi.org/10.1104/pp.109.139204
Müller K, Levesque-Tremblay G, Bartels S et al (2013) Demethylesterification of cell wall pectins in arabidopsis plays a role in seed germination. Plant Physiol 161:305–316. https://doi.org/10.1104/pp.112.205724
Reiter WD (2008) Biochemical genetics of nucleotide sugar interconversion reactions. Curr Opin Plant Biol 11:236–243. https://doi.org/10.1016/j.pbi.2008.03.009
Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. https://doi.org/10.1038/nature08670
Sechet J, Frey A, Cuzzi D et al (2016) Xyloglucan metabolism differentially impacts the cell wall characteristics of the endosperm and embryo during Arabidopsis seed germination. Plant Physiol 170:1367–1380. https://doi.org/10.1104/pp.15.01312
Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7:277–284. https://doi.org/10.1016/j.pbi.2004.03.004
Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell Online 5:9–23. https://doi.org/10.1105/tpc.5.1.9
Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588. https://doi.org/10.1146/annurev.arplant.043008.092039
Steinbrecher T, Leubner-Metzger G (2016) The biomechanics of seed germination. J Exp Bot 68:765–783. https://doi.org/10.1093/jxb/erw428
Sticklen MB (2008) Plant genetic engineering for biofuel production: towards affordable cellulosic ethanol. Nat Rev Genet 9:433–443. https://doi.org/10.1038/nrg2336
Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657. https://doi.org/10.1146/annurev.pp.35.060184.003101
Verbančič J, Lunn JE, Stitt M, Persson S (2018) Carbon supply and the regulation of cell wall synthesis. Mol Plant 11:75–94. https://doi.org/10.1016/j.molp.2017.10.004
Ververis C, Georghiou K, Christodoulakis N et al (2004) Fiber dimensions, lignin and cellulose content of various plant materials and their suitability for paper production. Ind Crops Prod 19:245–254. https://doi.org/10.1016/j.indcrop.2003.10.006
Weisshaar B, Jenkinst GI (1998) Phenylpropanoid biosynthesis and its regulation. Curr Opin Plant Biol 1:251–257. https://doi.org/10.1016/S1369-5266(98)80113-1
Yong W, Link B, O’Malley R et al (2005) Genomics of plant cell wall biogenesis. Planta 221:747–751. https://doi.org/10.1007/s00425-005-1563-z
Acknowledgements
We are grateful to Professor Kátia Valevski Sales Fernandes for language revision of the manuscript.
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This work was supported by Fundação de Apoio à Pesquisa no Estado do Rio de Janeiro (FAPERJ) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
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Sangi, S., Santos, M.L.C., Alexandrino, C.R. et al. Cell wall dynamics and gene expression on soybean embryonic axes during germination. Planta 250, 1325–1337 (2019). https://doi.org/10.1007/s00425-019-03231-1
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DOI: https://doi.org/10.1007/s00425-019-03231-1