Abstract
Key message
Ethylene formation via methionine reacting with trichloroisocyanuric acid under FeSO4 condition in a non-enzymatical manner provides one economically and efficiently novel ethylene-forming approach in planta.
Abstract
Rice seed germination can be stimulated by trichloroisocyanuric acid (TCICA). However, the molecular basis of TCICA in stimulating rice seed germination remains unclear. In this study, the molecular mechanism on how TCICA stimulated rice seed germination was examined via comparative transcriptome. Results showed that clustering of transcripts of TCICA-treated seeds, water-treated seeds, and dry seeds was clearly separated. Twenty-two and three hundred differentially expressed genes were identified as TCICA treatment responsive genes and TCICA treatment potentially responsive genes, respectively. Two and one TCICA treatment responsive genes were involved in ethylene signal transduction and iron homeostasis, respectively. Seventeen of the three hundred TCICA treatment potentially responsive genes were significantly annotated to iron ion binding. Meanwhile, level of methionine (ethylene precursor) showed a 73.9% decrease in response to TCICA treatment. Ethylene was then proved to produce via methionine reacting with TCICA under FeSO4 condition in vitro. Revealing ethylene formation by TCICA not only may bring novel insights into crosstalk between ethylene and other phytohormones during rice seed germination, but also may provide one economically and efficiently novel approach to producing ethylene in planta independently of the ethylene biosynthesis in plants and thereby may broaden its applications in investigational and applied purposes.
Similar content being viewed by others
Data availability
The data underlying this article are available in Supplementary Information.
References
Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489
Ahammed GJ, Gantait S, Mitra M, Yang Y, Li X (2020) Role of ethylene crosstalk in seed germination and early seedling development: a review. Plant Physiol Biochem 151:124–131
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Atassi H (1973) Reaction of amino acids and proteins with trichloroisocyanlic acid. Tetrahedron Lett 49:4893–4896
Chhabra G, Ahmad N (2023) Trichloroisocyanuric acid, a swimming pool disinfectant: new developments and role in UV-induced skin inflammation(dagger). Photochem Photobiol 99:869–871
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190
Han C, Yang P (2015) Studies on the molecular mechanisms of seed germination. Proteomics 15:1671–1679
Joung JG, Corbett AM, Fellman SM, Tieman DM, Klee HJ, Giovannoni JJ, Fei Z (2009) Plant MetGenMAP: an integrative analysis system for plant systems biology. Plant Physiol 151:1758–1768
Jurdak R, de Almeida GRG, Chaumont N, Schivre G, Bourbousse C, Barneche F, Bou DKM, Bailly C (2022) Intracellular reactive oxygen species trafficking participates in seed dormancy alleviation in Arabidopsis seeds. New Phytol 234:850–866
Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280
Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4
Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Biol 4:283–307
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Lieberman M, Kunishi AT (1965) Ethylene production from methionine. Biochem J 97:449–459
Lieberman M, Mapson L (1964) Genesis and biogenesis of ethylene. Nautre 204:343–345
Liu D, Chen X, Liu J, Ye J, Guo Z (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63:3899–3911
Manivannan S, Kaveri K (2014) Kinetics of oxidation of amino acid by trichloroisocyanuric acid in aqueous acetic acid medium. Int J Adv Chem Sci Appl 2:49–52
Matilla AJ, Matilla-Vázquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175:87–97
Mei S, Zhang M, Ye J, Du J, Jiang Y, Hu Y (2023) Auxin contributes to jasmonate-mediated regulation of abscisic acid signaling during seed germination in Arabidopsis. Plant Cell 35:1110–1133
Miao C, Wang Z, Zhang L, Yao J, Hua K, Liu X, Shi H, Zhu J (2019) The grain yield modulator miR156 regulates seed dormancy through the gibberellin pathway in rice. Nature Commun 10:3822
Naing AH, Xu J, Kim CK (2022) Editing of 1-aminocyclopropane-1-carboxylate oxidase genes negatively affects petunia seed germination. Plant Cell Rep 41:209–220
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454
Subbiah V, Reddy KJ (2010) Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J Biosci 35:451–458
Sultana MS, Mazarei M, Millwood RJ, Liu W, Hewezi T, Stewart CJ (2022) Functional analysis of soybean cyst nematode-inducible synthetic promoters and their regulation by biotic and abiotic stimuli in transgenic soybean (Glycine max). Front Plant Sci 13:988048
Sun M, Tuan PA, Izydorczyk MS, Ayele BT (2020) Ethylene regulates post-germination seedling growth in wheat through spatial and temporal modulation of ABA/GA balance. J Exp Bot 71:1985–2004
Sybilska E, Daszkowska-Golec A (2023) A complex signaling trio in seed germination: auxin-JA-ABA. Trends Plant Sci 28:873–875
Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129
Wang Y, Diao P, Kong L, Yu R, Zhang M, Zuo T, Fan Y, Niu Y, Yan F, Wuriyanghan H (2020) Ethylene enhances seed germination and seedling growth under salinity by reducing oxidative stress and promoting chlorophyll content via ETR2 pathway. Front Plant Sci 11:1066
Wioletta EP, Piotr P, Katarzyna G, Sylwia BO, Andrzej J, Hiroyuki N, Ryszard JG (2018) Jasmonic acid and ethylene are involved in the accumulation of osmotin in germinating tomato seeds. J Plant Physiol 232:74–81
Xiong M, Yu J, Wang J, Gao Q, Huang L, Chen C, Zhang C, Fan X, Zhao D, Liu QQ, Li QF (2022) Brassinosteroids regulate rice seed germination through the BZR1-RAmy3D transcriptional module. Plant Physiol 189:402–418
Xu J, Zhang S (2015) Ethylene biosynthesis and regulation in plants. In: Wen C (ed) Ethylene in plants. Springer, New York, pp 1–4
Yang S, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol 35:155–189
Zhang W, Yan C, Li M, Yang L, Ma B, Meng H, Xie L, Chen J (2017) Transcriptome analysis reveals the response of iron homeostasis to early feeding by small brown planthopper in rice. J Agric Food Chem 65:1093–1101
Zhao X, Dou L, Gong Z, Wang X, Mao T (2019) BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis. New Phytol 221:908–918
Zhao H, Yin CC, Ma B, Chen SY, Zhang JS (2021) Ethylene signaling in rice and Arabidopsis: New regulators and mechanisms. J Integr Plant Biol 63:102–125
Acknowledgements
We sincerely thank Mr Changqing Zheng (Institute of Fruit Science of Zhejiang University) for kindly detecting the ethylene formation.
Funding
This work was supported by Zhejiang Provincial Natural Science Foundation of China under Grant No. LY20C130002 and the National Natural Science Foundation of China (Grant No. 31301289).
Author information
Authors and Affiliations
Contributions
ZWL and LM contributed to the study design and drafted the article. YL, LM, QY, ZJ and LJ analyzed the experiment results, prepared figures and tables. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have not disclosed any conflict interests.
Additional information
Communicated by Chun-Hai Dong.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
299_2023_3058_MOESM1_ESM.doc
Supplementary file1 Figure S1 Principal component analysis of the transcriptomic alterations among experimental groups. TR, W and CK represent the transcriptomic alterations of TCICA-treated seeds, water-treated seeds and dry seeds (DOC 52 KB)
299_2023_3058_MOESM2_ESM.pdf
Supplementary file2 The KEGG pathway analysis for the TCICA treatment (potentially) responsive genes involving phytohormones biosynthesis and signal transduction. The red arrow indicates the up-regulated phytohormones biosynthesis. The down-regulated genes were indicated with black frame and green background; and the up- or down-regulated genes were indicated with blue frame and green background (PDF 126 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ling, Y., Jinshi, Z., Yilu, Q. et al. Transcriptome profiling reveals ethylene formation in rice seeds by trichloroisocyanuric acid. Plant Cell Rep 42, 1721–1732 (2023). https://doi.org/10.1007/s00299-023-03058-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-023-03058-x