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Filyushin M.A., Anisimova O.K., Dzos E.A., Shchennikova A.V., Kochiev E.Z. Relationship between the response of tomato plants to salt stress and the features of regulation of phenolic compounds biosynthesis. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 1, p. 21-32.
(how to cite this article)

doi: 10.15389/agrobiology.2025.1.21eng

UDC: 635.64:58.04:577.2

Acknowledgements:
Supported by the Russian Science Foundation (grant No. 24-16-00043, analysis of the content of phenolic compounds and gene expression) and the Ministry of Science and Higher Education of the Russian Federation (growing plants, exposure to salt stress, assessment of stress resistance and collection of material for analysis)

 

RELATIONSHIP BETWEEN THE RESPONSE OF TOMATO PLANTS TO SALT STRESS AND THE FEATURES OF REGULATION OF PHENOLIC COMPOUNDS BIOSYNTHESIS

M.A. Filyushin^{1 ✉}, O.K. Anisimova¹, E.A. Dzos^{1, 2},
A.V. Shchennikova¹, E.Z. Kochieva¹

¹Institute of Bioengineering, Federal Research Center Fundamentals of Biotechnology RAS, 33/2, Leninskii prospect, Moscow, 119071 Russia, e-mail michel7753@mail.ru (✉ corresponding author), lelikanis@yandex.ru, elenadzhos@mail.ru, shchennikova@yandex.ru, ekochieva@yandex.ru;

²Federal Research Center for Vegetable Growing, 14, ul. Selektsionnaya, pos. VNIISSOK, Odintsovskii Region, Moscow Province, 143080 Russia

ORCID:
Filyushin M.A. orcid.org/0000-0003-3668-7601
Shchennikova A.V. orcid.org/0000-0003-4692-3727
Anisimova O.K. orcid.org/0000-0001-7693-8714
Kochieva E.Z. orcid.org/0000-0002-6091-0765
Dzos E.A. orcid.org/0000-0002-2216-0094

Final revision received September 05, 2024
Accepted October 06, 2024

Salt stress has a negative impact on the yield of tomato crop (Solanum lycopersicum L.). Excessive salt content in the soil results in an osmotic and ionic imbalance in plant cells, which leads to oxidative stress, metabolic changes and, thus, impaired seed germination and plant viability. One of the modern approaches to increasing the salt tolerance of tomato varieties can be priming of seeds (pre-sowing) or seedlings with NaCl solutions (cis-priming) or other chemical agents capable of stimulating salt tolerance (trans-priming). It is known that priming can lead to epigenetic modifications in the plant genome, which are necessary to increase the effectiveness of the response to repeated salinity events. Such modifications can be preserved throughout the life of the plant or inherited in subsequent generations which is called the stress memory of the plant. The mechanism underlying tomato salt tolerance is poorly understood; however, given data on other plant species, it may be related to the content of phenolic compounds and the activity of L-phenylalanine ammonia lyases (PAL), enzymes that catalyze the first stage of the phenylpropanoid pathway. In this work, for the first time, using tomato varieties of domestic selection with different salt tolerance, the dynamics of the content of phenolic compounds and the expression of key genes of the phenylpropanoid (PAL5 gene group) and flavonoid (CHS2) pathways during the process of exposure of plants to salt stress were determined. It was found that the concentration of phenolic compounds after 1 h of exposure to NaCl and a decrease in the expression of PAL5 group genes after 24 h of exposure could be used as biomarkers of the presence of stress memory in tomato plants. The aim of our study was to assess possible links between tomato salt tolerance and the regulation of phenolic compound biosynthesis. Accessions of four tomato S. lycopersicum varieties were used: Otradny (variety code 8006741), Gnom (9401318), Fonarik (9608117) and VS-342-18 (variety under development/registration) bred at the Federal Scientific Vegetable Center (FSVC, Moscow Province). According to preliminary data from the FSVC, the Otradny and Gnom varieties could have increased resistance to excess salt in the soil, while the Fonarik and VS-342-18 varieties are sensitive to salinity. Plants from seeds of the 2023 harvest were grown in an experimental climate control facility (Federal Research Center of Biotechnology RAS) under the following regime: 16 h/8 h (day/night), 23 °C/21 °C. Adult plants at the stage of formed 8-10 leaves were exposed to salt stress. For this purpose, experimental and control plants were removed from the soil and transferred to water. After 1 h, experimental plants were placed in an aqueous solution containing 100 mM NaCl to simulate salt stress; control plants continued to be kept in water. Probes (all leaves from one plant) collected 1, 6, and 24 h after the beginning of stress exposure were used to analyze the content of phenolic compounds and the expression of key genes of the phenylpropanoid and flavonoid pathways. The target genes of the phenylpropanoid and flavonoid pathways (PAL group genes and the CHS2 gene) were selected based on the position of the genes in the metabolic pathways and transcriptome data from the TomExpress database. Gene expression was determined by quantitative real-time PCR (qRT-PCR). Primer sequences were selected based on the comparative structural analysis of the target genes and their mRNA using MEGA 7.0 and NCBI-Blast. It was observed that all four varieties showed a significant increase in the content of phenolic compounds by the 24th h of NaCl exposure (depending on the variety, ~ 1.4-4.7 times compared to the control), whereas 1 h after the beginning of stress exposure, only the most salt-tolerant Otradny variety was characterized by active accumulation of phenolic compounds (~ 2 times compared to the control). The salt-sensitive varieties Fonarik and VS-342-18 turned out to be similar in the profile of phenols concentration changes under stress. The resistant varieties Otradny and Gnome showed similar dynamics only in the period from the 6th h to the 24th h, and at the point of 1 h the opposite dynamics, where the most resistant variety Otradny was characterized by active accumulation of phenolic compounds (by ~ 2 times in comparison with the control), the variety Fonarik by a decrease in their amount (by ~ 2 times in comparison with the control). Using in silico analysis of tomato transcriptomes, the target genes of the phenylpropanoid and flavonoid pathways that are most highly expressed in tomato leaves were identified among the genes encoding L-phenylalanine ammonia lyases and chalcone synthases. The group of selected genes included four (out of 16 known) PAL genes (Solyc09g007890, Solyc09g007900, Solyc09g007910 — PAL5, Solyc09g007920 — PAL3) and a gene (one of two known) encoding chalcone synthase CHS2 (Solyc05g053550). It was shown that each of the four tomato varieties was characterized by individual dynamics of target gene expression under stress. The most salt-tolerant variety Otradny differed from the other analyzed varieties in the decrease in the content of PAL5 group gene transcripts 24 h after the onset of stress. In the case of the CHS2 gene, the salt-sensitive varieties Fonarik and VS-342-18 showed directly opposite dynamics of gene expression, while the resistant varieties Otradny and Gnom had a similar response. At the same time, no specific features of CHS2 expression were observed in the Otradny variety in comparison with other varieties. Based on the data obtained, we assumed about the possible use of the concentration of phenolic compounds after 1 h of exposure to salt stress and a decrease in the expression activity of the PAL5 group genes after 24 h of exposure as biomarkers of the presence of stress memory in tomato plants. The obtained data can be used in the breeding of salt-tolerant tomato varieties.

Keywords: tomato, salt tolerance, stress memory, phenylpropanoid pathway genes, phenolic metabolism, phenolic compound content, tomato breeding for resistance.

 

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