[en] Salinity is a form of abiotic stress that impacts growth and development in several economically relevant crops and is a top-ranking threat to agriculture, considering the average rise in the sea level caused by global warming. Tomato is moderately sensitive to salinity and shows adaptive mechanisms to this abiotic stressor. A case study on the dwarf tomato model Micro-Tom is here presented in which the response to salt stress (NaCl 200 mM) was investigated to shed light on the changes occurring at the expression level in genes involved in cell wall-related processes, phenylpropanoid pathway, stress response, volatiles' emission and secondary metabolites' production. In particular, the response was analyzed by sampling older/younger leaflets positioned at different stem heights (top and bottom of the stem) and locations along the rachis (terminal and lateral) with the goal of identifying the most responsive one(s). Tomato plants cv. Micro-Tom responded to increasing concentrations of NaCl (0-100-200-400 mM) by reducing the leaf biomass, stem diameter and height. Microscopy revealed stronger effects on leaves sampled at the bottom and the expression analysis identified clusters of genes expressed preferentially in older or younger leaflets. Stress-related genes displayed a stronger induction in lateral leaflets sampled at the bottom. In conclusion, in tomato cv. Micro-Tom subjected to salt stress, the bottom leaflets showed stronger stress signs and response, while top leaflets were less impacted by the abiotic stressor and had an increased expression of cell wall-related genes involved in expansion.
Hoffmann, Jonas ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, rue Bommel, L-4940 Hautcharage, Luxembourg
Berni, Roberto ; Université de Liège - ULiège > TERRA Research Centre > Echanges Eau - Sol - Plantes
Sutera, Flavia Maria; SiSaf Ltd., Surrey Research Park, Guildford GU2 7RE, UK
Gutsch, Annelie; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, rue Bommel, L-4940 Hautcharage, Luxembourg
Hausman, Jean-Francois ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, rue Bommel, L-4940 Hautcharage, Luxembourg
Saffie-Siebert, Suzanne; SiSaf Ltd., Surrey Research Park, Guildford GU2 7RE, UK
Guerriero, Gea ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, rue Bommel, L-4940 Hautcharage, Luxembourg
Language :
English
Title :
The Effects of Salinity on the Anatomy and Gene Expression Patterns in Leaflets of Tomato cv. Micro-Tom.
Shahid, M.A.; Sarkhosh, A.; Khan, N.; Balal, R.M.; Ali, S.; Rossi, L.; Gómez, C.; Mattson, N.; Nasim, W.; Garcia-Sanchez, F. Insights into the Physiological and Biochemical Impacts of Salt Stress on Plant Growth and Development. Agronomy 2020, 10, 938. [CrossRef]
Mishra, A.; Tanna, B. Halophytes: Potential Resources for Salt Stress Tolerance Genes and Promoters. Front. Plant. Sci. 2017, 8. [CrossRef]
Dassanayake, M.; Larkin, J.C. Making Plants Break a Sweat: The Structure, Function, and Evolution of Plant Salt Glands. Front. Plant. Sci. 2017, 8. [CrossRef] [PubMed]
Moles, T.M.; de Brito Francisco, R.; Mariotti, L.; Pompeiano, A.; Lupini, A.; Incrocci, L.; Carmassi, G.; Scartazza, A.; Pistelli, L.; Guglielminetti, L.; et al. Salinity in Autumn-Winter Season and Fruit Quality of Tomato Landraces. Front. Plant. Sci 2019, 10. [CrossRef]
Annex 1. Crop Salt Tolerance Data. Available online: http://www.fao.org/3/y4263e/y4263e0e.htm (accessed on 24 March 2021).
Yu, J.; Li, Y.; Han, G.; Zhou, D.; Fu, Y.; Guan, B.; Wang, G.; Ning, K.; Wu, H.; Wang, J. The Spatial Distribution Characteristics of Soil Salinity in Coastal Zone of the Yellow River Delta. Environ. Earth Sci. 2014, 72, 589–599. [CrossRef]
Gharbi, E.; Martínez, J.-P.; Benahmed, H.; Lepoint, G.; Vanpee, B.; Quinet, M.; Lutts, S. Inhibition of Ethylene Synthesis Reduces Salt-Tolerance in Tomato Wild Relative Species Solanum Chilense. J. Plant. Physiol. 2017, 210, 24–37. [CrossRef] [PubMed]
Martín-Davison, A.S.; Pérez-Díaz, R.; Soto, F.; Madrid-Espinoza, J.; González-Villanueva, E.; Pizarro, L.; Norambuena, L.; Tapia, J.; Tajima, H.; Blumwald, E.; et al. Involvement of SchRabGDI1 from Solanum Chilense in Endocytic Trafficking and Tolerance to Salt Stress. Plant. Sci. 2017, 263, 1–11. [CrossRef] [PubMed]
Kashyap, S.P.; Prasanna, H.C.; Kumari, N.; Mishra, P.; Singh, B. Understanding Salt Tolerance Mechanism Using Transcriptome Profiling and de Novo Assembly of Wild Tomato Solanum Chilense. Sci. Rep. 2020, 10, 15835. [CrossRef] [PubMed]
Žižková, E.; Dobrev, P.I.; Muhovski, Y.; Hošek, P.; Hoyerová, K.; Haisel, D.; Procházková, D.; Lutts, S.; Motyka, V.; Hichri, I. Tomato (Solanum Lycopersicum L.) SlIPT3 and SlIPT4 Isopentenyltransferases Mediate Salt Stress Response in Tomato. BMC Plant Biol. 2015, 15, 85. [CrossRef] [PubMed]
Shi, X.; Gupta, S.; Lindquist, I.E.; Cameron, C.T.; Mudge, J.; Rashotte, A.M. Transcriptome Analysis of Cytokinin Response in Tomato Leaves. PLoS ONE 2013, 8, e55090. [CrossRef]
Bacha, H.; Tekaya, M.; Drine, S.; Guasmi, F.; Touil, L.; Enneb, H.; Triki, T.; Cheour, F.; Ferchichi, A. Impact of Salt Stress on Morpho-Physiological and Biochemical Parameters of Solanum Lycopersicum Cv. Microtom Leaves. S. Afr. J. Bot. 2017, 108, 364–369. [CrossRef]
Palaniyandi, S.A.; Damodharan, K.; Yang, S.H.; Suh, J.W. Streptomyces Sp. Strain PGPA39 Alleviates Salt Stress and Promotes Growth of ‘Micro Tom’ Tomato Plants. J. Appl. Microbiol. 2014, 117, 766–773. [CrossRef] [PubMed]
Damodharan, K.; Palaniyandi, S.A.; Le, B.; Suh, J.W.; Yang, S.H. Streptomyces Sp. Strain SK68, Isolated from Peanut Rhizosphere, Promotes Growth and Alleviates Salt Stress in Tomato (Solanum Lycopersicum Cv. Micro-Tom). J. Microbiol. 2018, 56, 753–759. [CrossRef]
Al Hassan, M.; Martínez Fuertes, M.; Ramos Sánchez, F.J.; Vicente, O.; Boscaiu, M. Effects of Salt and Water Stress on Plant Growth and on Accumulation of Osmolytes and Antioxidant Compounds in Cherry Tomato. Not. Bot. Horti Agrobot. Cluj-Napoca 2015, 43. [CrossRef]
Shani, E.; Ben-Gera, H.; Shleizer-Burko, S.; Burko, Y.; Weiss, D.; Ori, N. Cytokinin Regulates Compound Leaf Development in Tomato. Plant Cell 2010, 22, 3206–3217. [CrossRef] [PubMed]
Hoffmann, J.; Berni, R.; Hausman, J.-F.; Guerriero, G. A Review on the Beneficial Role of Silicon against Salinity in Non-Accumulator Crops: Tomato as a Model. Biomolecules 2020, 10, 1284. [CrossRef]
Keshishian, E.A.; Hallmark, H.T.; Ramaraj, T.; Plačková, L.; Sundararajan, A.; Schilkey, F.; Novák, O.; Rashotte, A.M. Salt and Oxidative Stresses Uniquely Regulate Tomato Cytokinin Levels and Transcriptomic Response. Plant Direct 2018, 2, e00071. [CrossRef] [PubMed]
Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 Years of Image Analysis. Nat. Methods 2012, 9, 671–675. [CrossRef]
Untergasser, A.; Nijveen, H.; Rao, X.; Bisseling, T.; Geurts, R.; Leunissen, J.A.M. Primer3Plus, an Enhanced Web Interface to Primer3. Nucleic Acids Res. 2007, 35. [CrossRef] [PubMed]
Guerriero, G.; Mangeot-Peter, L.; Hausman, J.-F.; Legay, S. Extraction of High Quality RNA from Cannabis Sativa Bast Fibres: A Vademecum for Molecular Biologists. Fibers 2016, 4, 23. [CrossRef]
Hellemans, J.; Mortier, G.; De Paepe, A.; Speleman, F.; Vandesompele, J. Open Access Method QBase Relative Quantification Framework and Software for Management and Automated Analysis of Real-Time Quantitative PCR Data. Genome Biol. 2007, 8, 1–14. [CrossRef]
González-Aguilera, K.L.; Saad, C.F.; Chávez Montes, R.A.; Alves-Ferreira, M.; de Folter, S. Selection of Reference Genes for Quantitative Real-Time RT-PCR Studies in Tomato Fruit of the Genotype MT-Rg1. Front. Plant Sci. 2016, 7, 1386. [CrossRef] [PubMed]
Eisen, M.B.; Spellman, P.T.; Brown, P.O.; Botstein, D. Cluster Analysis and Display of Genome-Wide Expression Patterns. Proc. Natl. Acad. Sci. USA 1998, 95, 14863–14868. [CrossRef]
Chalker-Scott, L. Do anthocyanins function as osmoregulators in leaf tissues? In Advances in Botanical Research; Academic Press: Cambridge, MA, USA, 2002; Volume 37, pp. 103–127.
Cirillo, V.; D’Amelia, V.; Esposito, M.; Amitrano, C.; Carillo, P.; Carputo, D.; Maggio, A. Anthocyanins Are Key Regulators of Drought Stress Tolerance in Tobacco. Biology 2021, 10, 139. [CrossRef] [PubMed]
Eckert, C.; Sharmin, S.; Kogel, A.; Yu, D.; Kins, L.; Strijkstra, G.-J.; Polle, A. What Makes the Wood? Exploring the Molecular Mechanisms of Xylem Acclimation in Hardwoods to an Ever-Changing Environment. Forests 2019, 10, 358. [CrossRef]
Sánchez-Aguayo, I.; Rodríguez-Galán, J.M.; García, R.; Torreblanca, J.; Pardo, J.M. Salt Stress Enhances Xylem Development and Expression of S-Adenosyl-L-Methionine Synthase in Lignifying Tissues of Tomato Plants. Planta 2004, 220, 278–285. [CrossRef] [PubMed]
Rankenberg, T.; Geldhof, B.; van Veen, H.; Holsteens, K.; de Poel, B.V.; Sasidharan, R. Age-Dependent Abiotic Stress Resilience in Plants. Trends Plant Sci. 2021, 26, 692–705. [CrossRef] [PubMed]
Gao, H.-J.; Yang, H.-Y.; Bai, J.-P.; Liang, X.-Y.; Lou, Y.; Zhang, J.-L.; Wang, D.; Zhang, J.-L.; Niu, S.-Q.; Chen, Y. Ultrastructural and Physiological Responses of Potato (Solanum Tuberosum L.) Plantlets to Gradient Saline Stress. Front. Plant Sci. 2015, 5, 787. [CrossRef] [PubMed]
Navarro, A.; Bañon, S.; Olmos, E.; Sánchez-Blanco, M.J. Effects of Sodium Chloride on Water Potential Components, Hydraulic Conductivity, Gas Exchange and Leaf Ultrastructure of Arbutus Unedo Plants. Plant Sci. 2007, 172, 473–480. [CrossRef]
Guerriero, G.; Behr, M.; Hausman, J.F.; Legay, S. Textile Hemp vs. Salinity: Insights from a Targeted Gene Expression Analysis. Genes 2017, 8, 242. [CrossRef]
Shahid, S.A.; Zaman, M.; Heng, L. Introduction to Soil Salinity, Sodicity and Diagnostics Techniques. In Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques; Zaman, M., Shahid, S.A., Heng, L., Eds.; Springer International Publishing: Cham, Switzerland, 2018; pp. 1–42. ISBN 978-3-319-96190-3.
Le Gall, H.; Philippe, F.; Domon, J.-M.; Gillet, F.; Pelloux, J.; Rayon, C. Cell Wall Metabolism in Response to Abiotic Stress. Plants 2015, 4, 112–166. [CrossRef]
Cuong, D.M.; Kwon, S.-J.; Nguyen, B.V.; Chun, S.W.; Kim, J.K.; Park, S.U. Effect of Salinity Stress on Phenylpropanoid Genes Expression and Related Gene Expression in Wheat Sprout. Agronomy 2020, 10, 390. [CrossRef]
Bouwmeester, H.; Schuurink, R.C.; Bleeker, P.M.; Schiestl, F. The Role of Volatiles in Plant Communication. Plant J. 2019, 100, 892–907. [CrossRef] [PubMed]
Sharma, A.; Shahzad, B.; Rehman, A.; Bhardwaj, R.; Landi, M.; Zheng, B. Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants under Abiotic Stress. Molecules 2019, 24, 2452. [CrossRef]
Gayoso, C.; Pomar, F.; Novo-Uzal, E.; Merino, F.; Martínez de Ilárduya, Ó. The Ve-Mediated Resistance Response of the Tomato to Verticillium Dahliae Involves H2O2, Peroxidase and Lignins and Drives PAL Gene Expression. BMC Plant Biol. 2010, 10, 232. [CrossRef] [PubMed]
Wada, K.C.; Mizuuchi, K.; Koshio, A.; Kaneko, K.; Mitsui, T.; Takeno, K. Stress Enhances the Gene Expression and Enzyme Activity of Phenylalanine Ammonia-Lyase and the Endogenous Content of Salicylic Acid to Induce Flowering in Pharbitis. J. Plant Physiol. 2014, 171, 895–902. [CrossRef]
Zhang, J.; Zeng, L.; Chen, S.; Sun, H.; Ma, S. Transcription Profile Analysis of Lycopersicum Esculentum Leaves, Unravels Volatile Emissions and Gene Expression under Salinity Stress. Plant Physiol. Biochem. 2018, 126, 11–21. [CrossRef]
Huang, J.; Gu, M.; Lai, Z.; Fan, B.; Shi, K.; Zhou, Y.-H.; Yu, J.-Q.; Chen, Z. Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress. Plant Physiol. 2010, 153, 1526–1538. [CrossRef] [PubMed]
Chang, A.; Lim, M.-H.; Lee, S.-W.; Robb, E.J.; Nazar, R.N. Tomato Phenylalanine Ammonia-Lyase Gene Family, Highly Redundant but Strongly Underutilized. J. Biol. Chem. 2008, 283, 33591–33601. [CrossRef]
Rigano, M.M.; Raiola, A.; Docimo, T.; Ruggieri, V.; Calafiore, R.; Vitaglione, P.; Ferracane, R.; Frusciante, L.; Barone, A. Metabolic and Molecular Changes of the Phenylpropanoid Pathway in Tomato (Solanum Lycopersicum) Lines Carrying Different Solanum Pennellii Wild Chromosomal Regions. Front. Plant Sci. 2016, 7, 1484. [CrossRef]
Li, Y.; Kim, J.I.; Pysh, L.; Chapple, C. Four Isoforms of Arabidopsis 4-Coumarate:CoA Ligase Have Overlapping yet Distinct Roles in Phenylpropanoid Metabolism. Plant Physiol. 2015, 169, 2409–2421. [CrossRef] [PubMed]
Cosgrove, D.J. Plant Expansins: Diversity and Interactions with Plant Cell Walls. Curr. Opin. Plant Biol 2015, 25, 162–172. [CrossRef] [PubMed]
Lü, P.; Kang, M.; Jiang, X.; Dai, F.; Gao, J.; Zhang, C. RhEXPA4, a Rose Expansin Gene, Modulates Leaf Growth and Confers Drought and Salt Tolerance to Arabidopsis. Planta 2013, 237, 1547–1559. [CrossRef]
Abuqamar, S.; Ajeb, S.; Sham, A.; Enan, M.R.; Iratni, R. A Mutation in the Expansin-like A2 Gene Enhances Resistance to Necrotrophic Fungi and Hypersensitivity to Abiotic Stress in Arabidopsis Thaliana. Mol. Plant Pathol. 2013, 14, 813–827. [CrossRef]
Baumann, M.J.; Eklöf, J.M.; Michel, G.; Kallas, Å.M.; Teeri, T.T.; Czjzek, M.; Brumer, H. Structural Evidence for the Evolution of Xyloglucanase Activity from Xyloglucan Endo-Transglycosylases: Biological Implications for Cell Wall Metabolism. Plant Cell 2007, 19, 1947–1963. [CrossRef]
Cosgrove, D.J. Re-Constructing Our Models of Cellulose and Primary Cell Wall Assembly. Curr. Opin. Plant Biol. 2014, 22, 122–131. [CrossRef]
Nishitani, K.; Tominaga, R. Endo-Xyloglucan Transferase, a Novel Class of Glycosyltransferase That Catalyzes Transfer of a Segment of Xyloglucan Molecule to Another Xyloglucan Molecule. J. Biol. Chem. 1992, 267, 21058–21064. [CrossRef]
Fry, S.C.; Smith, R.C.; Renwick, K.F.; Martin, D.J.; Hodge, S.K.; Matthews, K.J. Xyloglucan Endotransglycosylase, a New Wall-Loosening Enzyme Activity from Plants. Biochem. J. 1992, 282, 821–828. [CrossRef]
Thompson, J.E.; Fry, S.C. Restructuring of Wall-Bound Xyloglucan by Transglycosylation in Living Plant Cells. Plant J. 2001, 26, 23–34. [CrossRef]
Zheng, S.J.; Zhu, X.F.; Shi, Y.Z.; Lei, G.J.; Fry, S.C.; Zhang, B.C.; Zhou, Y.H.; Braam, J.; Jiang, T.; Xu, X.Y.; et al. XTH31, Encoding an in Vitro XEH/XET-Active Enzyme, Regulates Aluminum Sensitivity by Modulating in Vivo XET Action, Cell Wall Xyloglucan Content, and Aluminum Binding Capacity in Arabidopsis. Plant Cell 2012, 24, 4731–4747. [CrossRef]
Choi, J.Y.; Seo, Y.S.; Kim, S.J.; Kim, W.T.; Shin, J.S. Constitutive Expression of CaXTH3, a Hot Pepper Xyloglucan Endotransglu-cosylase/Hydrolase, Enhanced Tolerance to Salt and Drought Stresses without Phenotypic Defects in Tomato Plants (Solanum Lycopersicum Cv. Dotaerang). Plant Cell Rep. 2011, 30, 867–877. [CrossRef]
Selmar, D.; Kleinwächter, M. Stress Enhances the Synthesis of Secondary Plant Products: The Impact of Stress-Related over-Reduction on the Accumulation of Natural Products. Plant Cell Physiol. 2013, 54, 817–826. [CrossRef] [PubMed]
Savvas, D.; Ntatsi, G. Biostimulant Activity of Silicon in Horticulture. Sci. Hortic. 2015, 196, 66–81. [CrossRef]
Rubio, M.C.; Bustos-Sanmamed, P.; Clemente, M.R.; Becana, M. Effects of Salt Stress on the Expression of Antioxidant Genes and Proteins in the Model Legume Lotus Japonicus. New Phytol. 2009, 181, 851–859. [CrossRef] [PubMed]
Shavrukov, Y. Salt Stress or Salt Shock: Which Genes Are We Studying? J. Exp. Bot. 2013, 64, 119–127. [CrossRef] [PubMed]
Muñoz-Mayor, A.; Pineda, B.; Garcia-Abellán, J.O.; Antón, T.; Garcia-Sogo, B.; Sanchez-Bel, P.; Flores, F.B.; Atarés, A.; Angosto, T.; Pintor-Toro, J.A.; et al. Overexpression of Dehydrin Tas14 Gene Improves the Osmotic Stress Imposed by Drought and Salinity in Tomato. J. Plant Physiol. 2012, 169, 459–468. [CrossRef]
Cao, J.; Li, X. Identification and Phylogenetic Analysis of Late Embryogenesis Abundant Proteins Family in Tomato (Solanum Lycopersicum). Planta 2014, 241, 757–772. [CrossRef]
Tolleter, D.; Hincha, D.K.; Macherel, D. A Mitochondrial Late Embryogenesis Abundant Protein Stabilizes Model Membranes in the Dry State. Biochim. Biophys. Acta Biomembr. 2010, 1798, 1926–1933. [CrossRef]
Liu, Y.; Song, Q.; Li, D.; Yang, X.; Li, D. Multifunctional Roles of Plant Dehydrins in Response to Environmental Stresses. Front. Plant Sci. 2017, 8, 1018. [CrossRef]
Liu, Y.; Wang, L.; Xing, X.; Sun, L.; Pan, J.; Kong, X.; Zhang, M.; Li, D. ZmLEA3, a Multifunctional Group 3 LEA Protein from Maize (Zea Mays L.), Is Involved in Biotic and Abiotic Stresses. Plant Cell Physiol. 2013, 54, 944–959. [CrossRef]
Belver, A.; Olías, R.; Huertas, R.; Rodríguez-Rosales, M.P. Involvement of SlSOS2 in Tomato Salt Tolerance. Bioengineered 2012, 3. [CrossRef]
Mosblech, A.; Feussner, I.; Heilmann, I. Oxylipins: Structurally Diverse Metabolites from Fatty Acid Oxidation. Plant Physiol. Biochem. 2009, 47, 511–517. [CrossRef]
Andreou, A.; Feussner, I. Lipoxygenases–Structure and Reaction Mechanism. Phytochemistry 2009, 70, 1504–1510. [CrossRef] [PubMed]
Almutairi, Z.M. Effect of Nano-Silicon Application on the Expression of Salt Tolerance Genes in Germinating Tomato (Solanum Lycopersicum L.) Seedlings under Salt Stress. POJ 2016, 9, 106–114.
Yang, X.; Zhu, W.; Zhang, H.; Liu, N.; Tian, S. Heat Shock Factors in Tomatoes: Genome-Wide Identification, Phylogenetic Analysis and Expression Profiling under Development and Heat Stress. PeerJ 2016, 2016, e1961. [CrossRef] [PubMed]