Abstract
Pectic-oligosaccharides (POS), one of the natural biostimulants, can regulate plants growth that the bio-stimulating activities are related to their molecular size. This study assessed the promoting effects of POS derived from pomelo peel with different molecular sizes, including POS-L, POS-M, and POS-S, with a degree of polymerization (DP) > 5 approximately 91.7%, 60.5%, and 38.6%, respectively, on rice seed growth. Rice seeds were soaked in 1% (w/w) POS solution for 3 days before being sown in a petri dish for 5 days, and water was used as the control. POS treatments considerably decreased germination time by 17–19%. They also improved the seedling root and shoot length at 5 days after sowing as compared to the control. Seeds treated with POS-L exhibited the highest growth with root and shoot lengths of 68.9 and 51.6 mm, respectively, while those of seeds treated with water were 9.3 and 34.7 mm, respectively. The amylase activity of seedlings at 5 days after sowing was increased by 8.9 and 12% when treated with POS-L and POS-M, respectively. Consequently, soluble sugar levels were also increased, with glucose and sucrose appearing as major sugars. After 2 days of soaking until the fifth day of sowing, seeds and seedlings treated with POS-L and POS-M had significantly lower H2O2 accumulation than the control. According to our observations, the molecular size of POS played an important role in rice seed growth activation, i.e., larger size POS showed a more favorable impact on plant growth and metabolism.
Similar content being viewed by others
References
Albersheim P, Darvill A, Augur C, Cheong J-J, Eberhard S, Hahn MG, Marfa V, Mohnen D, O’Neill MA, Spiro MD, York WS (1992) Oligosaccharins: oligosaccharide regulatory molecules. Acc Chem Res 25:77–83. https://doi.org/10.1021/ar00014a004
Amnuaysin N, Korakotchakorn H, Chittapun S, Poolyarat N (2018) Seed germination and seedling growth of rice in response to atmospheric air dielectric-barrier discharge plasma. Songklanakarin J Sci Technol 40(4):819–823
Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiol 90(1):109–116. https://doi.org/10.1104/pp.90.1.109
Association of Official Seed Analysts (AOSA) (1990) Rules for testing seeds. Seed Sci Technol 12:1–112
Babu Y, Bayer M (2014) Plant polygalacturonases involved in cell elongation and separation-the same but different? Plants (basel) 3(4):613–623. https://doi.org/10.3390/plants3040613
Baldan B, Bertoldo A, Navazio L, Mariani P (2003) Oligogalacturonide-induced changes in the developmental pattern of Daucus carota L. somatic embryos. Plant Sci 165(22):337–348. https://doi.org/10.1016/S0168-9452(03)00193-6
Bewley JD, Black M (1994) Seed: physiology of development and germination, 2nd edn. Springer, New York
Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P (2008) Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18(6):473–482. https://doi.org/10.1093/glycob/cwn027
Cabrera JC, Wégria G, Onderwater RCA, González G, Nápoles MC, Falcón-Rodríguez AB, Costales D, Rogers HJ, Diosdado E, González S, Cabrera G, González L, Wattiez R (2013) Practical use of oligosaccharins in agriculture. Acta Hortic. https://doi.org/10.17660/ActaHortic.2013.1009.24
Camejo D, Marti MC, Jimenez A, Cabrera JC, Olmos E, Sevilla F (2011) Effect of oligogalacturonides on root length, extracellular alkalinization and O(2)(-)-accumulation in alfalfa. J Plant Physiol 168(6):566–575. https://doi.org/10.1016/j.jplph.2010.09.012
Camejo D, Martí MC, Olmos E, Torres W, Sevilla F, Jiménez A (2012) Oligogalacturonides stimulate antioxidant system in alfalfa roots. Biol Plant 56:537–544. https://doi.org/10.1007/s10535-012-0107-1
Davidsson P, Broberg M, Kariola T, Sipari N, Pirhonen M, Palva ET (2017) Short oligogalacturonides induce pathogen resistance-associated gene expression in Arabidopsis thaliana. BMC Plant Biol 17(1):19. https://doi.org/10.1186/s12870-016-0959-1
Davies P (2010) The Plant Hormones: Their Nature, Occurrence, and Functions. In: Davies P (ed) Plant hormones: biosynthesis, signal transduction, action! Springer, Dordrecht, pp 1–15
Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46(2):268–278. https://doi.org/10.1093/pcp/pci026
Du B, Luo H, He L, Zhang L, Liu Y, Mo Z, Pan S, Tian H, Duan M, Tang X (2019) Rice seed priming with sodium selenate: effects on germination, seedling growth, and biochemical attributes. Sci Rep 9(1):4311. https://doi.org/10.1038/s41598-019-40849-3
Eberhard S, Doubrava N, Marfa V, Mohnen D, Southwick A, Darvill A, Albersheim P (1989) Pectic cell wall fragments regulate tobacco thin-cell-layer explant morphogenesis. Plant Cell 1(8):747–755. https://doi.org/10.1105/tpc.1.8.747
Ellis RA, Roberts EH (1981) The quantifcation of aging and survival in orthodox seeds. Seed Sci Technol 9:373–409
Falasca G, Capitani F, Rovere FD, Zaghi D, Franchin C, Biondi S, Altamura MM (2008) Oligogalacturonides enhance cytokinin-induced vegetative shoot formation in tobacco explants, inhibit polyamine biosynthetic gene expression, and promote long-term remobilisation of cell calcium. Planta 227:835–852. https://doi.org/10.1007/s00425-007-0660-6
Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, Lorenzo GD (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00049
Gamir J, Minchev Z, Berrio E, García JM, De Lorenzo G, Pozo MJ (2021) Roots drive oligogalacturonide-induced systemic immunity in tomato. Plant Cell Environ 44(1):275–289. https://doi.org/10.1111/pce.13917
Guarnizo N, Oliveros D, Murillo-Arango W, Bermúdez-Cardona MB (2020) Oligosaccharides: defense inducers, their recognition in plants. Commercial Uses Perspect Mol 25(24):5972. https://doi.org/10.3390/molecules25245972
Hernández-Mata G, Mellado-Rojas ME, Richards-Lewis A, López-Bucio J, Beltrán-Pena E, Soriano-Bello EL (2010) Plant immunity induced by oligogalacturonides alters root growth in a process involving flavonoid accumulation in Arabidopsis thaliana. J Plant Growth Regul 29:441–454. https://doi.org/10.1007/s00344-010-9156-x
Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LS (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420. https://doi.org/10.3389/fpls.2015.00420
Khan TA, Yusuf M, Fariduddin Q (2018) Hydrogen peroxide in regulation of plant metabolism: signalling and its effect under abiotic stress. Photosynthetica 56:1237–1248. https://doi.org/10.1007/s11099-018-0830-8
Kim J, Shiu SH, Thoma S, Li WH, Patterson SE (2006) Patterns of expansion and expression divergence in the plant polygalacturonase gene family. Genome Biol 7(9):R87. https://doi.org/10.1186/gb-2006-7-9-r87
Laware SL, Raskar S (2014) Effect of titanium dioxide nanoparticles on hydrolytic and antioxidant enzymes during seed germination in onion. Int J Curr Microbiol Appl Sci 3(7):749–760
Liners F, Thibault JF, Van Cutsem P (1992) Influence of the degree of polymerization of oligogalacturonates and of esterification pattern of pectin on their recognition by monoclonal antibodies. Plant Physiol 99(3):1099–1104. https://doi.org/10.1104/pp.99.3.1099
Malinovsky FG, Fangel JU, Willats WG (2014) The role of the cell wall in plant immunity. Front Plant Sci 5:178. https://doi.org/10.3389/fpls.2014.00178
Martins D, English AM (2014) Catalase activity is stimulated by H2O2 in rich culture medium and is required for H2O2 resistance and adaptation in yeast. Redox Biol 2:308–313. https://doi.org/10.1016/j.redox.2013.12.019
Mata GH, Sepúlveda B, Richards A, Soriano E (2006) The architecture of Phaseolus vulgaris root is altered when a defense response is elicited by an oligogalacturonide. Braz J Plant Physiol 18(2):351–355. https://doi.org/10.1590/S1677-04202006000200012
Matsukura C, Saitoh T, Hirose T, Ohsugi R, Perata P, Yamaguchi J (2000) Sugar uptake and transport in rice embryo. Expression of companion cell-specific sucrose transporter (OsSUT1) induced by sugar and light. Plant Physiol 124(1):85–93. https://doi.org/10.1104/pp.124.1.85
Minzanova ST, Mironov VF, Arkhipova DM, Khabibullina AV, Mironova LG, Zakirova YM, Milyukov VA (2018) Biological activity and pharmacological application of pectic polysaccharides: a review. Polymers 10(12):1407. https://doi.org/10.3390/polym10121407
Miranda JH, Williams RW, Kerven G (2007) Galacturonic acid-induced changes in strawberry plant development in vitro. In Vitro Cell Dev Biol 43(6):639–643. https://doi.org/10.1007/s11627-007-9052-7
Osuna D, Prieto P, Aguilar M (2015) Control of seed germination and plant development by carbon and nitrogen availability. Front Plant Sci 6:1023. https://doi.org/10.3389/fpls.2015.01023
Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012. https://doi.org/10.1093/aobpla/pls014
Posmyk MM, Szafranska K (2016) Biostimulators: a new trend towards solving an old problem. Front Plant Sci 7:748. https://doi.org/10.3389/fpls.2016.00748
Satapathy S, Rout JR, Kerry RG, Thatoi H, Sahoo SL (2020) Biochemical prospects of various microbial pectinase and pectin: an approachable concept in pharmaceutical bioprocessing. Front Nutr 7:117. https://doi.org/10.3389/fnut.2020.00117
Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125(4):1591–1602. https://doi.org/10.1104/pp.125.4.1591
Scofield GN, Aoki N, Hirose T, Takano M, Jenkins CL, Furbank RT (2007) The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants. J Exp Bot 58(3):483–495. https://doi.org/10.1093/jxb/erl217
Shibuya N, Minami E (2001) Oligosaccharide signalling for defence responses in plant. Physiol Mol Plant Pathol 59(5):223–233. https://doi.org/10.1006/pmpp.2001.0364
Sitrit Y, Hadfield KA, Bennett AB, Bradford KJ, Downie AB (1999) Expression of a polygalacturonase associated with tomato seed germination. Plant Physiol 121(2):419–428. https://doi.org/10.1104/pp.121.2.419
Smirnoff N, Arnaud D (2019) Hydrogen peroxide metabolism and functions in plants. New Phytol 221(3):1197–1214. https://doi.org/10.1111/nph.15488
Stein O, Granot D (2018) Plant fructokinases: evolutionary, developmental, and metabolic aspects in sink tissues. Front Plant Sci 9:339. https://doi.org/10.3389/fpls.2018.00339
Thakur M, Sohal BS (2013) Role of elicitors in inducing resistance in plants against pathogen infection: a review. ISRN Biochem 2013:762412. https://doi.org/10.1155/2013/762412
Vallarino JG, Osorio S (2012) Signaling role of oligogalacturonides derived during cell wall degradation. Plant Signal Behav 7(11):1447–1449. https://doi.org/10.4161/psb.21779
Voxeur A, Hofte H (2020) Pectin-derived immune elicitors in response to lignin modification in plants. Proc Natl Acad Sci USA 117(9):4442–4444. https://doi.org/10.1073/pnas.2000509117
Wandee Y, Uttapap D, Mischnick P (2019) Yield and structural composition of pomelo peel pectins extracted under acidic and alkaline conditions. Food Hydrocoll 87:237–244. https://doi.org/10.1016/j.foodhyd.2018.08.017
Wandee Y, Uttapap D, Mischnick P, Rungsardthong V (2021) Production of pectic-oligosaccharides from pomelo peel pectin by oxidative degradation with hydrogen peroxide. Food Chem 348:129078. https://doi.org/10.1016/j.foodchem.2021.129078
Wang F, Sun X, Shi X, Zhai H, Tian C, Kong F, Liu B, Yuan X (2016) A global analysis of the polygalacturonase gene family in soybean (Glycine max). PLoS ONE 11(9):e0163012. https://doi.org/10.1371/journal.pone.0163012
Wojtyla L, Garnczarska M, Zalewski T, Bednarski W, Ratajczak L, Jurga S (2006) A comparative study of water distribution, free radical production and activation of antioxidative metabolism in germinating pea seeds. J Plant Physiol 163(12):1207–1220. https://doi.org/10.1016/j.jplph.2006.06.014
Wojtyla L, Lechowska K, Kubala S, Garnczarska M (2016) Different modes of hydrogen peroxide action during seed germination. Front Plant Sci 7:66. https://doi.org/10.3389/fpls.2016.00066
Zhang S, Tang W, Jiang L, Hou Y, Yang F, Chen W, Li X (2015) Elicitor activity of algino-oligosaccharide and its potential application in protection of rice plant (Oryza saliva L.) against Magnaporthe grisea. Biotechnol Biotechnol Equip 29(4):646–652. https://doi.org/10.1080/13102818.2015.1039943
Acknowledgements
This research was funded by King Mongkut’s University of Technology Thonburi, Thailand, through the Post-doctoral Fellowship and the National Research Council of Thailand of the NRCT Senior Research Scholar Program (Contract No.814-2020).
Funding
This work received support from King Mongkut’s University of Technology Thonburi, Post-doctoral Fellowship, National Research Council of Thailand, The NRCT Senior Research Scholar Program (Contract No. 814-2020).
Author information
Authors and Affiliations
Contributions
DU: conceptualization; WU and YW: methodology; WU: validation; WU and DK: formal analysis; WU and YW: investigation; DU: resources; WU: data curation; WU: writing—original draft preparation; YW and DU: writing—review and editing; WU and DK: visualization; DU: supervision; DU and VR: project administration; VR: funding acquisition. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Handling Editor: Mikihisa Umehara.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Udchumpisai, W., Uttapap, D., Wandee, Y. et al. Promoting Effect of Pectic-Oligosaccharides Produced from Pomelo Peel on Rice Seed Germination and Early Seedling Growth. J Plant Growth Regul 42, 2176–2188 (2023). https://doi.org/10.1007/s00344-022-10690-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-022-10690-6