The loss-of-function of AtNATA2 enhances AtADC2-dependent putrescine biosynthesis and priming, improving growth and salinity tolerance in Arabidopsis
Jazyk angličtina Země Dánsko Médium print
Typ dokumentu časopisecké články
Grantová podpora
JG_2024_036
Univerzita Palackého v Olomouci
PubMed
39489618
PubMed Central
PMC11659803
DOI
10.1111/ppl.14603
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis * genetika růst a vývoj fyziologie metabolismus MeSH
- fotosystém II - proteinový komplex metabolismus MeSH
- mutace ztráty funkce MeSH
- polyaminy metabolismus MeSH
- proteiny huseníčku * genetika metabolismus MeSH
- putrescin * metabolismus MeSH
- regulace genové exprese u rostlin * MeSH
- tolerance k soli * genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- fotosystém II - proteinový komplex MeSH
- polyaminy MeSH
- proteiny huseníčku * MeSH
- putrescin * MeSH
Putrescine (Put) is a promising small molecule-based biostimulant to enhance plant growth and resilience, though its mode of action remains unclear. This study investigated the Put priming effect on Arabidopsis mutant lines (Atadc1, Atadc2, Atnata1, and Atnata2) under control conditions and salinity to understand its role in regulating plant growth. The Atadc2 mutant, characterized by reduced endogenous Put levels, showed insensitivity to Put priming without growth enhancement, which was linked to significant imbalances in nitrogen metabolism, including a high Gln/Glu ratio. Contrarily, the Atnata2 mutant exhibited significant growth improvement and upregulated AtADC2 expression, particularly under Put priming, highlighting these genes' involvement in regulating plant development. Put priming enhanced plant growth by inducing the accumulation of specific polyamines (free, acetylated, conjugated, or bound form) and improving light-harvesting efficiency, particularly in the Atnata2 line. Our findings suggest that AtNATA2 may negatively regulate Put synthesis and accumulation via AtADC2 in the chloroplast, impacting light harvesting in photosystem II (PSII). Furthermore, the Atadc2 mutant line exhibited upregulated AtADC1 but reduced AcPut levels, pointing to a cross-regulation among these genes. The regulation by AtNATA2 on AtADC2 and AtADC2 on AtADC1 could be crucial for plant growth and overall stress tolerance by interacting with polyamine catabolism, which shapes the plant metabolic profile under different growth conditions. Understanding the regulatory mechanisms involving crosstalk between AtADC and AtNATA genes in polyamine metabolism and the connection with certain SMBBs like Put can lead to more effective agricultural practices, improving plant growth, nitrogen uptake, and resilience under challenging conditions.
Zobrazit více v PubMed
Angelini, R. , Cona, A. , Federico, R. , Fincato, P. , Tavladoraki, P. & Tisi, A. (2010) Plant amine oxidases “on the move”: An update. Plant Physiology and Biochemistry, 48: 560–564 PubMed
Arif, Y. , Singh, P. , Siddiqui, H. , Bajguz, A. & Hayat, S. (2020) Salinity induced physiological and biochemical changes in plants: An omic approach towards salt stress tolerance. Plant Physiology and Biochemistry, 156: 64–77 PubMed
Bailey‐Serres, J. , Parker, J.E. , Ainsworth, E.A. , Oldroyd, G.E.D. & Schroeder, J.I. (2019) Genetic strategies for improving crop yields. Nature, 575: 109–118 PubMed PMC
Belda‐Palazón, B. , Ruiz, L. , Martí, E. , Tárraga, S. , Tiburcio, A. F. , Culiáñez, F. , Farras, R. , Carrasco, P. & Ferrando, A. (2012). Aminopropyltransferases involved in polyamine biosynthesis localize preferentially in the nucleus of plant cells. PLoS One, 7 (10):e46907 PubMed PMC
Bělíček, J. , Ľuptáková, E. , Kopečný, D. , Frömmel, J. , Vigouroux, A. , Ćavar‐Zeljković, S. , Jagic, F. , Briozzo, P. , Kopečný, D.J. , Tarkowski, P. , Nisler, J. , De Diego, N. , Moréra, S. & Kopečná, M. (2023) Biochemical and structural basis of polyamine, lysine and ornithine acetylation catalyzed by spermine/spermidine N‐acetyltransferase in moss and maize. The Plant Journal, 114: 482–498 PubMed
Bennett, E. M. , Ekstrom, J. L. , Pegg, A. E. , & Ealick, S. E. (2002). Monomeric S‐adenosylmethionine decarboxylase from plants provides an alternative to putrescine stimulation. Biochemistry, 41: 14509–14517. PubMed
Bewley, M. C. , Graziano, V. , Jiang, J. , Matz, E. , Studier, F. W. , Pegg, A. E. , Coleman, C. S. , & Flanagan, J. M. (2006). Structures of wild‐type and mutant human spermidine/spermine N1‐acetyltransferase, a potential therapeutic drug target. Proceedings of the National Academy of Sciences, 103: 2063–2068. PubMed PMC
Bittsánszky, A. , Pilinszky, K. , Gyulai, G. , & Komives, T. (2015). Overcoming ammonium toxicity. Plant Science, 231: 184–190. PubMed
Blázquez, M.A. (2024) Polyamines: Their role in plant development and stress. Annual Review of Plant Biology, 75: 95–117. PubMed
Ćavar Zeljković, S. , De Diego, N. , Drašar, L. , Nisler, J. , Havlíček, L. , Spíchal, L. & Tarkowski, P. (2024) Comprehensive LC‐MS/MS analysis of nitrogen‐related plant metabolites. Journal of Experimental Botany, erae129, 10.1093/jxb/erae129 PubMed DOI PMC
Chen, D. , Shao, Q. , Yin, L. , Younis, A. , & Zheng, B. (2019). Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science, 9: 1945. PubMed PMC
Cona, A. , Rea, G. , Angelini, R. , Federico, R. & Tavladoraki, P. (2006a) Functions of amine oxidases in plant development and defence. Trends in Plant Science, 11: 80–88. PubMed
Cona, A. , Rea, G. , Botta, M. , Corelli, F. , Federico, R. & Angelini, R. (2006b) Flavin‐containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. Journal of Experimental Botany, 57: 2277–2289. PubMed
Cuevas, J.C. , López‐Cobollo, R. , Alcázar, R. , Zarza, X. , Koncz, C. , Altabella, T. , Salinas, J. , Tiburcio, A.F. & Ferrando, A. (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiology, 148: 1094–1105. PubMed PMC
De Diego, N. & Spíchal L. (2020) Use of plant metabolites to mitigate stress effects in crops. The Chemical Biology of Plant Biostimulants. Wiley, pp. 261–300.
De Diego, N. , Fürst, T. , Humplík, J.F. , Ugena, L. , Podlešáková, K. & Spíchal, L. (2017) An automated method for high‐throughput screening of Arabidopsis rosette growth in multi‐well plates and its validation in stress conditions. Frontiers in Plant Science, 8: 1702. PubMed PMC
Doneva, D. , Pál, M. , Brankova, L. , Szalai, G. , Tajti, J. , Khalil, R. , Ivanovska, B. , Velikova, V. , Misheva, S. , Janda, T. & Peeva, V. (2021) The effects of putrescine pre‐treatment on osmotic stress responses in drought‐tolerant and drought‐sensitive wheat seedlings. Physiologia Plantarum, 171: 200–216. PubMed
Ferrante, A. , Hasanuzzaman, M. , Jiménez‐Arias, D. , Boto, A. , García‐García, A.L. , García‐Machado, F.J. , Borges, A.A. & Morales‐Sierra, S. (2020) Pure organic active compounds against abiotic stress: A biostimulant overview. Frontiers in Plant Science, 11: 575829. PubMed PMC
Fincato, P. , Moschou, P.N. , Spedaletti, V. , Tavazza, R. , Angelini, R. , Federico, R. , Roubelakis‐Angelakis, K.A. & Tavladoraki, P. (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. Journal of Experimental Botany, 62: 1155–1168. PubMed
Fuell, C. , Elliott, K. A. , Hanfrey, C. C. , Franceschetti, M. , & Michael, A. J. (2010). Polyamine biosynthetic diversity in plants and algae. Plant Physiology and Biochemistry, 48: 513–520. PubMed
Gent, L. , & Forde, B. G. (2017). How do plants sense their nitrogen status? Journal of Experimental Botany, 68(10): 2531–2539. PubMed
Ghahremani, Z. , Alizadeh, B. , Barzegar, T. , Nikbakht, J. , Ranjbar, ME. & Nezamdoost, D. (2023) The mechanism of enhancing drought tolerance threshold of pepper plant treated with putrescine and salicylic acid. Plant Stress, 9: 100199.
Hachiya, T. , Inaba, J. , Wakazaki, M. , Sato, M. , Toyooka, K. , Miyagi, A. , Kawai‐Yamada, M. , Sugiura, D. , Nakagawa, T. , Kiba, T. , Gojon, A. & Sakakibara, H. (2021) Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana . Nature Communicatios, 12: 4944. PubMed PMC
Hanfrey, C. , Sommer, S. , Mayer, M.J. , Burtin, D. & Michael, A.J. (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. The Plant Journal, 27: 551–560. PubMed
Hegde, S. S. , Chandler, J. , Vetting, M. W. , Yu, M. , & Blanchard, J. S. (2007). Mechanistic and structural analysis of human spermidine/spermine N1‐acetyltransferase. Biochemistry, 46: 7187–7195. PubMed PMC
Hernándiz, A.E. , Aucique‐Perez, C.E. , Ćavar Zeljković, S. , Štefelová, N. , Salcedo Sarmiento, S. , Spíchal, L. & De Diego, N. (2022a) Priming with small molecule‐based biostimulants to improve abiotic stress tolerance in Arabidopsis thaliana . Plants, 11(10): 1287. PubMed PMC
Hernandiz, A.E. , Jiménez‐Arias, D. , Morales‐Sierra, S. , Borges, A.A. & De Diego, N. (2022b) Addressing the contribution of small molecule‐based biostimulants to the biofortification of maize in a water restriction scenario. Frontiers in Plant Science, 13: 944066. PubMed PMC
Hummel, I. , Bourdais, G. , Gouesbet, G. , Couée, I. , Malmberg, R.L. & Amrani, A. E. (2004) Differential gene expression of ARGININE DECARBOXYLASE ADC1 and ADC2 in Arabidopsis thaliana: characterization of transcriptional regulation during seed germination and seedling development. New Phytologist, 163: 519–531. PubMed
Jalili, I. , Ebadi, A. , Askari, MA. , Kalatehjari, S. & Aazami, M.A. (2023) Foliar application of putrescine, salicylic acid, and ascorbic acid mitigates frost stress damage in Vitis vinifera cv. ‘Giziluzum’. BMC Plant Biology, 23(1:135. PubMed PMC
Jammes, F. , Leonhardt, N. , Tran, D. , Bousserouel, H. , Véry, A. , Renou, J. , Vavasseur, A. , Kwak, J. M. , Sentenac, H. & Bouteau, F. (2014). Acetylated 1,3‐diaminopropane antagonizes abscisic acid‐mediated stomatal closing in Arabidopsis. The Plant Journal, 79: 322–333. PubMed
Khosroshahi, M. R. Z. , Esna‐Ashari, M. , & Ershadi, A. (2007). Effect of exogenous putrescine on post‐harvest life of strawberry (Fragaria ananassa Duch.) fruit, cultivar Selva. Scientia Horticulturae, 114(1): 27–32.
Kotakis, C. , Theodoropoulou, E. , Tassis, K. , Oustamanolakis, C. , Ioannidis, N.E. & Kotzabasis, K. (2014) Putrescine, a fast‐acting switch for tolerance against osmotic stress. Journal of Plant Physiology, 171: 48–51. PubMed
Livak, K. J. , & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real‐time quantitative PCR and the 2− ΔΔCT method. methods, 25(4): 402–408. PubMed
Lou, Y.R. , Ahmed, S. , Yan, J. , Adio, A.M. , Powell, H.M. , Morris, P.F. & Jander, G. (2020) Arabidopsis ADC1 functions as an Nδ‐acetylornithine decarboxylase. Journal of Integrative Plant Biology, 62: 601–613. PubMed
Lou, Y.R. , Bor, M. , Yan, J. , Preuss, A.S. & Jander, G. (2016) Arabidopsis NATA1 acetylates putrescine and decreases defense‐related hydrogen peroxide accumulation. Plant Physiology, 171: 1443–1455. PubMed PMC
Maruri‐López, I. & Jiménez‐Bremont, J.F. (2017) Hetero‐ and homodimerization of Arabidopsis thaliana arginine decarboxylase AtADC1 and AtADC2. Biochemical and Biophysical Research Communications, 484: 508–513. PubMed
Mattioli, R. , Pascarella, G. , D'Incà, R. , Cona, A. , Angelini, R. , Morea, V. & Tavladoraki, P. (2022) Arabidopsis N‐acetyltransferase activity 2 preferentially acetylates 1,3‐diaminopropane and thialysine. Plant Physiology and Biochemistry, 170: 123–132. PubMed
Maxwell, K. & Johnson, G.N. (2000) Chlorophyll fluorescence—a practical guide. Journal of Experimental Botany, 51: 659–668. PubMed
Montemayor, E. J. , & Hoffman, D. W. (2008). The crystal structure of spermidine/spermine N 1‐acetyltransferase in complex with spermine provides insights into substrate binding and catalysis. Biochemistry, 47: 9145–9153. PubMed
Muñiz, L. , Minguet, E. G. , Singh, S. K. , Pesquet, E. , Vera‐Sirera, F. , Moreau‐Courtois, C. L. , Carbonell, J. , Blázquez, M.A. & Tuominen, H. (2008). ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development, 135: 2573–2582. PubMed
Murashige, T. & Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15: 473–497.
Murch, S.J. & Erland, L.A.E. (2021) A systematic review of melatonin in plants: An example of evolution of literature. Frontiers in Plant Science, 12: 683047. PubMed PMC
Niu, C. , Wang, G. , Sui, J. , Liu, G. , Ma, F. & Bao, Z. (2022) Biostimulants alleviate temperature stress in tomato seedlings. Scientia Horticulturae, 293: 110712.
Planas‐Portell, J. , Gallart, M. , Tiburcio, A. F. , & Altabella, T. (2013). Copper‐containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana . BMC Plant Biology, 13: 109. PubMed PMC
Pouvreau, J.B. , Gaudin, Z. , Auger, B. , Lechat, M.M. , Gauthier, M. , Delavault, P. & Simier, P. (2013) A high‐throughput seed germination assay for root parasitic plants. Plant Methods, 9: 32. PubMed PMC
Rahman, A. , Nagy, K. , Hamow, K. Á. , Pál, M. , Janda, T. , Dernovics, M. , Szőke, C. , & Szalai, G. (2024). Cadmium stress responses under white or blue light are influenced by putrescine pre‐treatment in wheat. Environmental and Experimental Botany, 222: 105746.
Ruan, J. , Haerdter, R. , & Gerendás, J. (2010). Impact of nitrogen supply on carbon/nitrogen allocation: a case study on amino acids and catechins in green tea [Camellia sinensis (L.) O. Kuntze] plants. Plant Biology, 12(5): 724–734. PubMed
Sequera‐Mutiozabal, M. , Antoniou, C. , Tiburcio, A.F. , Alcázar, R. & Fotopoulos, V. (2017) Polyamines: Emerging hubs promoting drought and salt stress tolerance in plants. Current Molecular Biology Reports, 3: 28–36.
Shahzad, B. , Rehman, A. , Tanveer, M. , Wang, L. , Park, S.K. & Ali, A. (2022) Salt stress in brassica: effects, tolerance mechanisms, and management. Journal of Plant Growth Regulation, 41: 781–795.
Shu. S. , Yuan, Y. , Chen, J. , Sun, J. , Zhang, W. , Tang, Y. , Zhong, M. & Guo, S. (2015) The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress. Scientific Reports, 5: 14390. PubMed PMC
Siddappa, S. & Marathe, G.K. (2020) What we know about plant arginases? Plant Physiology and Biochemistry, 156: 600–610. PubMed
Solé‐Gil, A. , Hernández‐García, J. , López‐Gresa, M. P. , Blázquez, M. A. , & Agustí, J. (2019). Conservation of thermospermine synthase activity in vascular and non‐vascular plants. Frontiers in Plant Science, 10: 663. PubMed PMC
Sorrentino, M. , De Diego, N. , Ugena, L. , Spíchal, L. , Lucini, L. , Miras‐Moreno, B. , Zhang, L. , Rouphael, Y. , Colla, G. & Panzarová, K. (2021) Seed priming with protein hydrolysates improves arabidopsis growth and stress tolerance to abiotic stresses. Frontiers in Plant Science, 12: 626301. PubMed PMC
Tavladoraki, P. , Cona, A. , & Angelini, R. (2016). Copper‐containing amine oxidases and FAD‐dependent polyamine oxidases are key players in plant tissue differentiation and organ development. Frontiers in Plant Science, 7: 824. PubMed PMC
Ugena, L. , Hýlová, A. , Podlešáková, K. , Humplík, J.F. , Doležal, K. , De Diego, N. & Spíchal, L. (2018) Characterization of biostimulant mode of action using novel Multi‐Trait High‐Throughput screening of Arabidopsis germination and rosette growth. Frontiers in Plant Science, 9: 1327. PubMed PMC
Urano, K. , Hobo, T. & Shinozaki, K. (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Letters, 579: 1557–1564. PubMed
Urano, K. , Yoshiba, Y. , Nanjo, T. , Ito, T. , Yamaguchi‐Shinozaki, K. & Shinozaki, K. (2004) Arabidopsis stress‐inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochemical and Biophysical Research Communications, 313: 369–375. PubMed
Urra, M. , Buezo, J. , Royo, B. , Cornejo, A. , López‐Gómez, P. , Cerdán, D. , Esteban, R. , Martínez‐Merino, V. , Gogorcena, Y. , Tavladoraki P. & Moran, J.F. (2022) The importance of the urea cycle and its relationships to polyamine metabolism during ammonium stress in Medicago truncatula . Journal of Experimental Botany, 73: 5581–5595. PubMed PMC
Zhao, X. , Zhang, Y. , Zhang, X. & Shan C. (2023) Putrescine improves salt tolerance of wheat seedlings by regulating ascorbate and glutathione metabolism, photosynthetic performance, and ion homeostasis. Plant Soil and Enviroment, 69: 512–521.
Zhou, W. , Sun, Q. J. , Zhang, C. F. , Yuan, Y. Z. , Zhang, J. , & Lu, B. B. (2004). Effect of salt stress on ammonium assimilation enzymes of the roots of rice (Oryza sativa) cultivars differing in salinity resistance. Acta Botanica Sinica‐English Edition‐, 46(8): 921–927.