Antisense-mediated S-adenosyl-L-methionine decarboxylase silencing affects heat stress responses of tobacco plants
Ifigeneia Mellidou
A B D , Katerina Karamanoli A , Helen-Isis A. Constantinidou A and Kalliopi A. Roubelakis-Angelakis C
+ Author Affiliations
- Author Affiliations
A School of Agriculture, Aristotle University, 54124 Thessaloniki, Greece.
B Institute of Plant Breeding and Genetic Resources - HAO DEMETER, 57001 Thessaloniki, Greece.
C Department of Biology, University of Crete, Voutes University campus, 70013 Heraklion, Greece.
D Corresponding author. Email: imellidou@agro.auth.gr
Functional Plant Biology 47(7) 651-658 https://doi.org/10.1071/FP19350
Submitted: 4 December 2019 Accepted: 20 February 2020 Published: 7 May 2020
Abstract
Understanding the molecular mode(s) of plant tolerance to heat stress (HS) is crucial since HS is a potential threat to sustainable agriculture and global crop production. Polyamines (PAs) seem to exert multifaceted effects in plant growth and development and responses to abiotic and biotic stresses, presumably via their homeostasis, chemical interactions and contribution to hydrogen peroxide (H2O2) cellular ‘signatures’. Downregulation of the apoplastic POLYAMINE OXIDASE (PAO) gene improved thermotolerance in tobacco (Nicotiana tabacum L.) transgenics. However, in the present work we show that transgenic tobacco plants with antisense-mediated S-ADENOSYL-L-METHIONINE DECARBOXYLASE silencing (AS-NtSAMDC) exhibited enhanced sensitivity and delayed responses to HS which was accompanied by profound injury upon HS removal (recovery), as assessed by phenological, physiological and biochemical characteristics. In particular, the AS-NtSAMDC transgenics exhibited significantly reduced rate of photosynthesis, as well as enzymatic and non-enzymatic antioxidants. These transgenics suffered irreversible damage, which significantly reduced their growth potential upon return to normal conditions. These data reinforce the contribution of increased PA homeostasis to tolerance, and can move forward our understanding on the PA-mediated mechanism(s) conferring tolerance to HS that might be targeted via traditional or biotechnological breeding for developing HS tolerant plants.
Additional keywords: heat recovery, polyamines, SAMDC transgenics, thermotolerance.
References
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
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 of Plant Science 9, 1945
| Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses.Crossref | GoogleScholarGoogle Scholar |
Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. Journal of Integrative Plant Biology 51, 489–499.
| Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress.Crossref | GoogleScholarGoogle Scholar | 19508360PubMed |
Dang F, Lin J, Xue B, Chen Y, Guan D, Wang Y, He S (2018) CaWRKY27 negatively regulates H2O2-mediated thermotolerance in pepper (Capsicum annuum). Frontiers of Plant Science 9, 1633
| CaWRKY27 negatively regulates H2O2-mediated thermotolerance in pepper (Capsicum annuum).Crossref | GoogleScholarGoogle Scholar |
Fragkostefanakis S, Röth S, Schleiff E, Scharf K-D (2015) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant, Cell & Environment 38, 1881–1895.
| Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks.Crossref | GoogleScholarGoogle Scholar |
Gémes K, Jung Kim Y, Park KY, Moschou PN, Andronis E, Valassakis C, Roussis A, Roubelakis-Angelakis KA (2016) An NADPH-oxidase/polyamine oxidase feedback loop controls oxidative burst under salinity. Plant Physiology 172, 1418–1431.
| An NADPH-oxidase/polyamine oxidase feedback loop controls oxidative burst under salinity.Crossref | GoogleScholarGoogle Scholar | 27600815PubMed |
Gémes K, Mellidou I, Karamanoli K, Beris D, Park KY, Matsi T, Haralampidis K, Constantinidou H-I, Roubelakis-Angelakis KA (2017) Deregulation of apoplastic polyamine oxidase affects development and salt response of tobacco plants. Journal of Plant Physiology 211, 1–12.
| Deregulation of apoplastic polyamine oxidase affects development and salt response of tobacco plants.Crossref | GoogleScholarGoogle Scholar | 28135604PubMed |
Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signaling & Behavior 5, 26–33.
| Polyamines and abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Frontiers of Plant Science 7, 1343
| Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses.Crossref | GoogleScholarGoogle Scholar |
Haworth M, Marino G, Brunetti C, Killi D, De Carlo A, Centritto M (2018) The impact of heat stress and water deficit on the photosynthetic and stomatal physiology of olive (Olea europaea L.) – a case study of the 2017 heat wave. Plants 7, 76
| The impact of heat stress and water deficit on the photosynthetic and stomatal physiology of olive (Olea europaea L.) – a case study of the 2017 heat wave.Crossref | GoogleScholarGoogle Scholar |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |
Ioannidis NE Cruz JA Kotzabasis K Kramer DM 2012
Kolotilin I, Koltai H, Bar-Or C, Chen L, Nahon S, Shlomo H, Levin I, Reuveni M (2011) Expressing yeast SAMdc gene confers broad changes in gene expression and alters fatty acid composition in tomato fruit. Physiologia Plantarum 142, 211–223.
| Expressing yeast SAMdc gene confers broad changes in gene expression and alters fatty acid composition in tomato fruit.Crossref | GoogleScholarGoogle Scholar | 21338368PubMed |
Liu J-H, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Frontiers of Plant Science 6, 1–10.
| Polyamines function in stress tolerance: from synthesis to regulation.Crossref | GoogleScholarGoogle Scholar |
Luo J, Liu M, Zhang C, Zhang P, Chen J, Guo Z, Lu S (2017) Transgenic centipedegrass (Eremochloa ophiuroides [Munro] Hack.) overexpressing S-adenosylmethionine decarboxylase (SAMDC) gene for improved cold tolerance through involvement of H2O2 and NO signaling. Frontiers of Plant Science 8, 1655
| Transgenic centipedegrass (Eremochloa ophiuroides [Munro] Hack.) overexpressing S-adenosylmethionine decarboxylase (SAMDC) gene for improved cold tolerance through involvement of H2O2 and NO signaling.Crossref | GoogleScholarGoogle Scholar |
Margaritopoulou T, Kryovrysanaki N, Megkoula P, Prassinos C, Samakovli D, Milioni D, Hatzopoulos P (2016) HSP90 canonical content organizes a molecular scaffold mechanism to progress flowering. The Plant Journal 87, 174–187.
| HSP90 canonical content organizes a molecular scaffold mechanism to progress flowering.Crossref | GoogleScholarGoogle Scholar | 27121421PubMed |
Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nature Biotechnology 20, 613–618.
| Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life.Crossref | GoogleScholarGoogle Scholar | 12042867PubMed |
Mellidou I, Keulemans J, Kanellis AK, Davey MW (2012) Regulation of fruit ascorbic acid concentrations during ripening in high and low vitamin C tomato cultivars. BMC Plant Biology 12, 239
| Regulation of fruit ascorbic acid concentrations during ripening in high and low vitamin C tomato cultivars.Crossref | GoogleScholarGoogle Scholar | 23245200PubMed |
Mellidou I, Moschou PN, Ioannidis NE, Pankou C, Gėmes K, Valassakis C, Andronis EA, Beris D, Haralampidis K, Roussis A, Karamanoli A, Matsi T, Kotzabasis K, Constantinidou H-I, Roubelakis-Angelakis KA (2016) Silencing S-adenosyl-L-methionine decarboxylase (SAMDC) in Nicotiana tabacum points at a polyamine-dependent trade-off between growth and tolerance responses. Frontiers of Plant Science 7, 379
| Silencing S-adenosyl-L-methionine decarboxylase (SAMDC) in Nicotiana tabacum points at a polyamine-dependent trade-off between growth and tolerance responses.Crossref | GoogleScholarGoogle Scholar |
Mellidou I, Karamanoli K, Beris D, Haralampidis K, Constantinidou H-IA, Roubelakis-Angelakis KA (2017) Underexpression of apoplastic polyamine oxidase improves thermotolerance in Nicotiana tabacum. Journal of Plant Physiology 218, 171–174.
| Underexpression of apoplastic polyamine oxidase improves thermotolerance in Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar | 28886452PubMed |
Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Frontiers of Plant Science 5, 175
| Polyamines and abiotic stress in plants: a complex relationship.Crossref | GoogleScholarGoogle Scholar |
Moschou PN, Delis ID, Paschalidis KA, Roubelakis-Angelakis KA (2008a) Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiologia Plantarum 133, 140–156.
| Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors.Crossref | GoogleScholarGoogle Scholar | 18282192PubMed |
Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008b) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. The Plant Cell 20, 1708–1724.
| Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco.Crossref | GoogleScholarGoogle Scholar | 18577660PubMed |
Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008c) Plant polyamine catabolism: the state of the art. Plant Signaling & Behavior 3, 1061–1066.
| Plant polyamine catabolism: the state of the art.Crossref | GoogleScholarGoogle Scholar |
Nambeesan S, Datsenka T, Ferruzzi MG, Malladi A, Mattoo AK, Handa AK (2010) Overexpression of yeast spermidine synthase impacts ripening, senescence and decay symptoms in tomato. The Plant Journal 63, 836–847.
| Overexpression of yeast spermidine synthase impacts ripening, senescence and decay symptoms in tomato.Crossref | GoogleScholarGoogle Scholar | 20584149PubMed |
Paschalidis KA, Roubelakis-Angelakis KA (2005) Sites and regulation of polyamine catabolism in the tobacco plant. Correlations with cell division/expansion, cell cycle progression, and vascular development. Plant Physiology 138, 2174–2184.
| Sites and regulation of polyamine catabolism in the tobacco plant. Correlations with cell division/expansion, cell cycle progression, and vascular development.Crossref | GoogleScholarGoogle Scholar | 16040649PubMed |
Paschalidis K Tsaniklidis G Wang B-Q Delis C Trantas E Loulakakis K Makky M Sarris PF Ververidis F Liu J-H 2019
Qu A-L, Ding Y-F, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochemical and Biophysical Research Communications 432, 203–207.
| Molecular mechanisms of the plant heat stress response.Crossref | GoogleScholarGoogle Scholar | 23395681PubMed |
Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytologist 190, 556–565.
| Heat perception and signalling in plants: a tortuous path to thermotolerance.Crossref | GoogleScholarGoogle Scholar | 21138439PubMed |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Seo SY, Kim YJ, Park KY (2019) Increasing polyamine contents enhances the stress tolerance via reinforcement of antioxidative properties. Frontiers of Plant Science 10, 1331
| Increasing polyamine contents enhances the stress tolerance via reinforcement of antioxidative properties.Crossref | GoogleScholarGoogle Scholar |
Song J, Nada K, Tachibana S (2002) Suppression of S-adenosylmethionine decarboxylase activity is a major cause for high-temperature inhibition of pollen germination and tube growth in tomato (Lycopersicon esculentum Mill.). Plant & Cell Physiology 43, 619–627.
| Suppression of S-adenosylmethionine decarboxylase activity is a major cause for high-temperature inhibition of pollen germination and tube growth in tomato (Lycopersicon esculentum Mill.).Crossref | GoogleScholarGoogle Scholar |
Toumi I, Pagoulatou MG, Margaritopoulou T, Milioni D, Roubelakis-Angelakis KA (2019) Genetically modified heat shock protein 90s and polyamine oxidases in Arabidopsis reveal their interaction under heat stress affecting polyamine acetylation, oxidation and homeostasis of reactive oxygen species. Plants 8, 323
| Genetically modified heat shock protein 90s and polyamine oxidases in Arabidopsis reveal their interaction under heat stress affecting polyamine acetylation, oxidation and homeostasis of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
| Heat tolerance in plants: an overview.Crossref | GoogleScholarGoogle Scholar |
Wang W, Paschalidis K, Feng J-C, Song J, Liu J-H (2019) Polyamine catabolism in plants: a universal process with diverse functions. Frontiers of Plant Science 10, 561
| Polyamine catabolism in plants: a universal process with diverse functions.Crossref | GoogleScholarGoogle Scholar |
Wi SJ, Kim WT, Park KY (2006) Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Reports 25, 1111–1121.
| Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 16642382PubMed |
Wilkins O, Hafemeister C, Plessis A, Holloway-Phillips M-M, Pham GM, Nicotra AB, Gregorio GB, Jagadish K, Septiningsih EM, Bonneau R, Purugganan MD (2016) EGRINs (Environmental Gene Regulatory Influence Networks) in rice that function in the response to water deficit, high temperature, and agricultural environments. The Plant Cell 28, 2365–2384.
| EGRINs (Environmental Gene Regulatory Influence Networks) in rice that function in the response to water deficit, high temperature, and agricultural environments.Crossref | GoogleScholarGoogle Scholar | 27655842PubMed |
