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Delayed germination of Brassica parachinensis seeds by coumarin involves decreased GA4 production and a consequent reduction of ROS accumulation

Published online by Cambridge University Press:  10 August 2021

Bing-Xian Chen
Affiliation:
Guangdong Provincial Key Laboratory for Crop Germplasm Resources Preservationand Utilization, Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou, China
Yuan-Xuan Peng
Affiliation:
Guangdong Provincial Key Laboratory for Crop Germplasm Resources Preservationand Utilization, Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou, China College of Agriculture and Biology, Zhongkai University of Agriculture and Engineering, Guangzhou, China
Xue-Qin Yang
Affiliation:
College of Life Sciences, South China Agricultural University, Guangzhou, China
Jun Liu*
Affiliation:
Guangdong Provincial Key Laboratory for Crop Germplasm Resources Preservationand Utilization, Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou, China
*
*Author for Correspondence: Jun Liu, E-mail: liujun139@139.com

Abstract

The plant allelochemical coumarin effectively inhibits the germination of Brassica parachinensis (B. parachinensis) seeds. Quantification of endogenous phytohormones showed that contents of abscisic acid (ABA), ABA glucose ester, gibberellin A20 (GA20), GA3, GA15, GA24, GA9 and GA4 were higher in germinating seeds than in seedlings. Moreover, the presence of coumarin significantly reduced the content of bioactive GA4 which is thought to positively regulate seed germination. Histochemical staining and spectrophotometry of reactive oxygen species (ROS) revealed that exogenous GA3 and GA4+7 could effectively promote the production of endogenous ROS during germination and that the GA synthesis inhibitor paclobutrazol could effectively inhibit production of ROS. Coumarin significantly inhibited the accumulation of ROS, especially superoxide anion radical (${\rm O}_2^{{\cdot}{-}} $). This inhibitory effect could be restored by the addition of exogenous GA3 and GA4+7. Coumarin also inhibited the activity of the ROS-degrading enzymes such as superoxide dismutase, catalase and peroxidase as well as β-amylase in seeds and seedlings. Taken together, we propose a model for the regulation of seed germination in B. parachinensis by coumarin, Gas and ROS, in which coumarin may delay seed germination by reducing endogenous GA4, thus decreasing the accumulation of ROS.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

These authors contributed equally to this study.

References

Ahammed, GJ, Gantait, S, Mitra, M, Yang, Y and Li, X (2020) Role of ethylene crosstalk in seed germination and early seedling development: a review. Plant Physiology and Biochemistry. doi:10.1016/j.plaphy.2020.03.016.CrossRefGoogle ScholarPubMed
Arc, E, Sechet, J, Corbineau, F, Rajjou, L and Marion-Poll, A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Frontiers in Plant Science 4, 63.Google ScholarPubMed
Bailly, C (2019) The signalling role of ROS in the regulation of seed germination and dormancy. Biochemical Journal 476, 30193032.CrossRefGoogle ScholarPubMed
Bailly, C, El-Maarouf-Bouteau, H and Corbineau, F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. Comptes Rendus Biologies 331, 806814.CrossRefGoogle ScholarPubMed
Barba-Espin, G, Nicolas, E, Almansa, MS, Cantero-Navarro, E, Albacete, A, Hernández, JA and Díaz-Vivancos, P (2012) Role of thioproline on seed germination: interaction ROS-ABA and effects on antioxidative metabolism. Plant Physiology and Biochemistry 59, 3036.CrossRefGoogle ScholarPubMed
Berrie, AMM, Parker, W, Knights, BA and Hendrie, MR (1968) Studies on lettuce seed germination-I. Coumarin induced dormancy. Phytochemistry 7, 567573.CrossRefGoogle Scholar
Bewley, JD and Black, M (1982) Physiology and biochemistry of seeds in relation to germination: volume 2: viability, dormancy, and environmental control. Heidelberg, Springer Verlag.CrossRefGoogle Scholar
Bewley, JD, Bradford, K, Hilhorst, H and Nonogaki, H (2013) Seeds: physiology of development, germination and dormancy (3rd edn). New York, Springer-Verlag.CrossRefGoogle Scholar
Brewer, PB, Koltai, H and Beveridge, CA (2013) Diverse roles of strigolactones in plant development. Molecular Plant 6, 1828.CrossRefGoogle ScholarPubMed
Chen, B, Ma, J, Xu, Z and Wang, X (2016a) Abscisic acid and ethephon regulation of cellulase in the endosperm cap and radicle during lettuce seed germination. Journal of Integrative Plant Biology 58, 859869.CrossRefGoogle Scholar
Chen, B-X, Li, W-Y, Gao, Y-T, Chen, Z-J, Zhang, W-N, Liu, Q-J and Chen, Z (2016b) Involvement of polyamine oxidase-produced hydrogen peroxide during coleorhiza-limited germination of rice seeds. Frontiers in Plant Science 7, 1219.CrossRefGoogle Scholar
Chen, B-X, Peng, Y-X, Gao, J-D, Zhang, Q, Liu, Q-J, Fu, H and Liu, J (2019) Coumarin-induced delay of rice seed germination is mediated by suppression of abscisic acid catabolism and reactive oxygen species production. Frontiers in Plant Science 10, 828.CrossRefGoogle ScholarPubMed
Cosgrove, DJ (2016) Catalysts of plant cell wall loosening. F1000Research 5, 119.CrossRefGoogle ScholarPubMed
Díaz-Vivancos, P, Barba-Espín, G and Hernández, JA (2013) Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Reports 32, 14911502.CrossRefGoogle Scholar
Duan, Y, Zhang, W, Li, B, Wang, Y, Li, K, Han, C, Zhang, Y and Li, X (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytologist 186, 681695.CrossRefGoogle ScholarPubMed
Gill, SS and Tuteja, N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909930.CrossRefGoogle ScholarPubMed
Gomes, MP, Smedbol, É, Carneiro, MMLC, Garcia, QS and Juneau, P (2014) Reactive oxygen species and plant hormones, pp. 6588 in Ahmad, P (Ed.), Oxidative damage to plants, San Diego, Elsevier Academic Press.CrossRefGoogle Scholar
He, X (2019) The mechanism of coumarin inhibiting the germination and growth of Lolium perenne L. Master Dissertation. Southwest University, Chongqing, China.Google Scholar
Iglesias-Fernández, R and Matilla, A (2009) After-ripening alters the gene expression pattern of oxidases involved in the ethylene and gibberellin pathways during early imbibition of Sisymbrium officinale L. seeds. Journal of Experimental Botany 60, 16451661.CrossRefGoogle ScholarPubMed
Jeevan Kumar, SP, Rajendra Prasad, S, Banerjee, R and Thammineni, C (2015) Seed birth to death: dual functions of reactive oxygen species in seed physiology. Annals of Botany 116, 663668.CrossRefGoogle ScholarPubMed
Khan, AA and Tolbert, NE (1966) Light-controlled cycocel reversal of coumarin inhibition of lettuce seed germination and root growth. Physiologia Plantarum 19, 7680.CrossRefGoogle Scholar
Koźmińska, A, Al Hassan, M, Wiszniewska, A, Hanus-Fajerska, E, Boscaiu, M and Vicente, O (2019) Responses of succulents to drought: comparative analysis of four Sedum (Crassulaceae) species. Scientia Horticulturae 243, 235242.CrossRefGoogle Scholar
Lambeth, JD and Neish, AS (2014) Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annual Review of Pathology: Mechanisms of Disease 9, 119145.CrossRefGoogle ScholarPubMed
Li, W-Y, Chen, B-X, Chen, Z-J, Gao, Y-T, Chen, Z and Liu, J (2017) Reactive oxygen species generated by NADPH oxidases promote radicle protrusion and root elongation during rice seed germination. International Journal of Molecular Sciences 18, 110.CrossRefGoogle ScholarPubMed
Liszkay, A, van der Zalm, E and Schopfer, P (2004) Production of reactive oxygen intermediates (${\rm O}_2^{{\cdot}{-}} $, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiology 136, 31143123.CrossRefGoogle Scholar
Liu, Y, Ye, N, Liu, R, Chen, M and Zhang, J (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany 61, 29792990.CrossRefGoogle ScholarPubMed
Llanes, A, Andrade, A, Masciarelli, O, Alemano, S and Luna, V (2016) Drought and salinity alter endogenous hormonal profiles at the seed germination phase. Seed Science Research 26, 113.CrossRefGoogle Scholar
Majda, M and Robert, S (2018) The role of auxin in cell wall expansion. International Journal of Molecular Sciences 19, 951.CrossRefGoogle ScholarPubMed
Mhamdi, A and Van Breusegem, F (2018) Reactive oxygen species in plant development. Development 145, dev164376.CrossRefGoogle ScholarPubMed
Morohashi, Y (2002) Peroxidase activity develops in the micropylar endosperm of tomato seeds prior to radicle protrusion. Journal of Experimental Botany 53, 16431650.CrossRefGoogle ScholarPubMed
Müller, K, Hess, B and Leubner-Metzger, G (2007) A role for reactive oxygen species in endosperm weakening, pp. 287295 in Adkins, S; Ashmore, S and Navie, S (Eds) Seeds: biology, development and ecology. Wallingford, CAB International.Google Scholar
Müller, K, Linkies, A, Vreeburg, RA, Fry, SC, Krieger-Liszkay, A and Leubner-Metzger, G (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiology 150, 18551865.CrossRefGoogle ScholarPubMed
Nandi, S, Das, G and Sen-Mandi, S (1995) β-amylase activity as an index for germination potential in rice. Annals of Botany 75, 463467.CrossRefGoogle Scholar
Nonogaki, H, Gee, OH and Bradford, KJ (2000) A germination-specific endo-β-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiology 123, 12351246.CrossRefGoogle ScholarPubMed
Paulsen, GM and Auld, AS (2004) Preharvest sprouting of cereals, pp. 199219 in Benech-Arnold, RL and Sánchez, RA (Eds) Handbook of seed physiology: applications to agriculture. Binghamton, New York, The Haworth Press.Google Scholar
Penfield, S (2017) Seed dormancy and germination. Current Biology 27, R874R878.CrossRefGoogle ScholarPubMed
Plackett, AR and Wilson, ZA (2018) Gibberellins and plant reproduction. Annual Plant Reviews online 15, 323358.Google Scholar
Rodríguez-Gacio, MC, Iglesias-Fernández, R, Carbonero, P and Matilla, ÁJ (2012) Softening-up mannan-rich cell walls. Journal of Experimental Botany 63, 39753988.CrossRefGoogle Scholar
Rose, JK, Catalá, C, Gonzalez-Carranza, ZH and Roberts, JA (2003) Cell wall disassembly. Annual Plant Reviews 8, 264324.Google Scholar
Sampedro, J, Valdivia, ER, Fraga, P, Iglesias, N, Revilla, G and Zarra, I (2017) Soluble and membrane-bound β-glucosidases are involved in trimming the xyloglucan backbone. Plant Physiology 173, 10171030.CrossRefGoogle ScholarPubMed
Schopfer, P, Plachy, C and 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 Physiology 125, 15911602.CrossRefGoogle ScholarPubMed
Shu, K, Liu, X, Xie, Q and He, Z (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Molecular Plant 9, 3445.CrossRefGoogle ScholarPubMed
Shuai, H, Meng, Y, Luo, X, Chen, F, Zhou, W, Dai, Y, Qi, Y, Du, J, Yang, F, Liu, J, Yang, W and Shu, K (2017) Exogenous auxin represses soybean seed germination through decreasing the gibberellin/abscisic acid (GA/ABA) ratio. Scientific Reports 7, 111.CrossRefGoogle ScholarPubMed
Steinbrecher, T and Leubner-Metzger, G (2017) The biomechanics of seed germination. Journal of Experimental Botany 68, 765783.Google ScholarPubMed
Thomas, SG and Hedden, P (2018) Gibberellin metabolism and signal transduction. Annual Plant Reviews 15, 147184.CrossRefGoogle Scholar
Tuan, PA, Kumar, R, Rehal, PK, Toora, PK and Ayele, BT (2018) Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals. Frontiers in Plant Science 9, 668.CrossRefGoogle ScholarPubMed
Wang, J, Yao, D, Xu, J, Wu, C, Zhao, G and Hua, C (2017) Effect of coumarin on Sorghum sudanense seed germination and seedling growth. Pratacultural Science 34, 22792288.Google Scholar
Waszczak, C, Carmody, M and Kangasjärvi, J (2018) Reactive oxygen species in plant signaling. Annual Review of Plant Biology 69, 209236.CrossRefGoogle ScholarPubMed
Williams, RD, Peal, LK, Bartholomew, PW and Williams, SJ (2005) Seed hydration-dehydration in an allelochemical (coumarin) alters germination and seedling growth. Allelopathy Journal 15, 183196.Google Scholar
Xiao, C, Wang, L, Hu, D, Zhou, Q and Huang, X (2019) Effects of exogenous bisphenol A on the function of mitochondria in root cells of soybean (Glycine max L.) seedlings. Chemosphere 222, 619627.CrossRefGoogle ScholarPubMed
Yamaguchi, S, Kamiya, Y and Nambara, E (2007) Regulation of ABA and GA levels during seed development and germination in Arabidopsis, pp. 224247 in Bradford, KJ and Nonogaki, H (Eds) Annual plant reviews volume 27: seed development, dormancy and germination. Oxford, Blackwell Publishing.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Ye, N, Zhu, G, Liu, Y, Zhang, A, Li, Y, Liu, R, Shi, L, Jia, L and Zhang, J (2012) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. Journal of Experimental Botany 63, 18091822.CrossRefGoogle ScholarPubMed
Ye, N, Li, H and Zhu, G (2014) Copper suppresses abscisic acid catabolism and catalase activity, and inhibits seed germination of rice. Plant & Cell Physiology 55, 20082016.CrossRefGoogle ScholarPubMed
Zhang, Y (2009) Plant physiology experiment course. Beijing, Higher Education Press.Google Scholar
Zhang, FQ, Wang, YS, Lou, ZP and Dong, JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67, 4450.CrossRefGoogle Scholar
Zhang, H-J, Zhang, N, Yang, R-C, Wang, L, Sun, Q-Q, Li, D-B, Cao, Y-Y, Weeda, S, Zhao, B, Ren, S and Guo, Y-D (2014a) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). Journal of Pineal Research 57, 269279.CrossRefGoogle Scholar
Zhang, Y, Chen, B, Xu, Z, Shi, Z, Chen, S, Huang, X, Chen, J and Wang, X (2014b) Involvement of reactive oxygen species in endosperm cap weakening and embryo elongation growth during lettuce seed germination. Journal of Experimental Botany 65, 31893200.CrossRefGoogle Scholar
Zhu, G, Ye, N and Zhang, J (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant & Cell Physiology 50, 644651.CrossRefGoogle Scholar
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