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Publikation

Cherevatskaya, M.; Cherepanov, I.; Kalganova, N.; Erofeeva, N.; Romanovskaya, E.; Frolov, A.; Bilova, T.; Moiseev, S.; Wessjohann, L. A.; Sydnone imines as a new class of promising plant growth and stress tolerance modulators—A first experimental structure–activity overview Stresses 4, 133-154, (2024) DOI: 10.3390/stresses4010008

Due to the oncoming climate changes, various environmental stresses (drought, salinity, heavy-metals, low or high temperatures, etc.) might dramatically affect crop yields and the quality of produced foods. Therefore, to meet the growing food demand of the human population, improvement of stress tolerance of the currently cultured crops is required. The knowledge of the molecular underlying mechanisms provides a versatile instrument to correct plant metabolism via chemical tools and to thereby increase their adaptive potential. This will preserve crop productivity and quality under abiotic stress conditions. Endogenously produced nitric oxide (NO) is one of the key signaling factors activating stress tolerance mechanisms in plants. Thus, the application of synthetic NO donors as stress-protective phytoeffectors might support maintaining plant growth and productivity under stressful conditions. Sydnone imines (sydnonimines) are a class of clinically established mesoionic heterocyclic NO donors which represent a promising candidate group for such phytoeffectors. Therefore, here, we provide an overview of the current progress in the application of sydnone imines as exogenous NO donors in plants, with a special emphasis on their potential as herbicides as well as herbicide antidotes, growth stimulants and stress protectors triggering plant tolerance mechanisms. We specifically address the structure–activity relationships in the context of the growth modulating activity of sydnone imines. Growth stimulating or antidote effects are typical for 4-α-hydroxybenzyl derivatives of sydnone imines containing an alkyl substituent in position N-3. The nature of the substituent of the N-6 atom has a significant influence on the activity profile and the intensity of the effect. Nevertheless, further investigations are necessary to establish reliable structure–activity relationships (SAR). Consequently, sydnone imines might be considered promising phytoeffector candidates, which are expected to exert either protective effects on plants growing under unfavorable conditions, or herbicidal ones, depending on the exact structure.
Publikation

Leonova, T.; Shumilina, J.; Kim, A.; Frolova, N.; Wessjohann, L.; Bilova, T.; Frolov, A.; Agar-based polyethylene glycol (PEG) infusion model for pea (Pisum sativum L.) — perspectives of translation to legume crop plants Biol. Commun. 67, 236-244, (2022) DOI: 10.21638/spbu03.2022.309

Due to the oncoming climate changes water deficit represents one of the most important abiotic stressors which dramatically affects crop productivity worldwide. Because of their importance as the principal source of food protein, legumes attract a special interest of plant scientists. Moreover, legumes are involved in symbiotic association with rhizobial bacteria, which is morphologically localized to root nodules. These structures are critical for fixation of atmospheric nitrogen and highly sensitive to drought. Therefore, new drought-tolerant legume cultivars need to be developed to meet the growing food demand. However, this requires a comprehensive knowledge of the molecular mechanisms behind the plant stress response. To access these mechanisms, adequate and reliable drought stress models need to be established. The agar-based polyethylene glycol (PEG) infusion model allows a physiologically relevant reduction of soil water potential (Ψw), although it is restricted to seedlings and does not give access to proteomics and metabolomics studies. Earlier, we successfully overcame this limitation and optimized this model for mature Arabidopsis plants. Here we make the next step forward and address its application to one of the major crop legumes — pea. Using a broad panel of physiological and biochemical markers, we comprehensively prove the applicability of this setup to legumes. The patterns of drought-related physiological changes are well-interpretable and generally resemble the stress response of plants grown in soil-based stop-watering models. Thus, the proposed model can be efficiently used in the study of stress-related metabolic adjustment in green parts, roots and root nodules of juvenile and flowering plants.
Publikation

Smolikova, G.; Strygina, K.; Krylova, E.; Vikhorev, A.; Bilova, T.; Frolov, A.; Khlestkina, E.; Medvedev, S.; Seed-to-seedling transition in Pisum sativum L.: A transcriptomic approach Plants 11, 1686, (2022) DOI: 10.3390/plants11131686

The seed-to-seedling transition is a crucial step in the plant life cycle. The transition occurs at the end of seed germination and corresponds to the initiation of embryonic root growth. To improve our understanding of how a seed transforms into a seedling, we germinated the Pisum sativum L. seeds for 72 h and divided them into samples before and after radicle protrusion. Before radicle protrusion, seeds survived after drying and formed normally developed seedlings upon rehydration. Radicle protrusion increased the moisture content level in seed axes, and the accumulation of ROS first generated in the embryonic root and plumule. The water and oxidative status shift correlated with the desiccation tolerance loss. Then, we compared RNA sequencing-based transcriptomics in the embryonic axes isolated from pea seeds before and after radicle protrusion. We identified 24,184 differentially expressed genes during the transition to the post-germination stage. Among them, 2101 genes showed more prominent expression. They were related to primary and secondary metabolism, photosynthesis, biosynthesis of cell wall components, redox status, and responses to biotic stress. On the other hand, 415 genes showed significantly decreased expression, including the groups related to water deprivation (eight genes) and response to the ABA stimulus (fifteen genes). We assume that the water deprivation group, especially three genes also belonging to ABA stimulus (LTI65, LTP4, and HVA22E), may be crucial for the desiccation tolerance loss during a metabolic switch from seed to seedling. The latter is also accompanied by the suppression of ABA-related transcription factors ABI3, ABI4, and ABI5. Among them, HVA22E, ABI4, and ABI5 were highly conservative in functional domains and showed homologous sequences in different drought-tolerant species. These findings elaborate on the critical biochemical pathways and genes regulating seed-to-seedling transition.
Publikation

Leonova, T.; Popova, V.; Tsarev, A.; Henning, C.; Antonova, K.; Rogovskaya, N.; Vikhnina, M.; Baldensperger, T.; Soboleva, A.; Dinastia, E.; Dorn, M.; Shiroglasova, O.; Grishina, T.; Balcke, G. U.; Ihling, C.; Smolikova, G.; Medvedev, S.; Zhukov, V. A.; Babakov, V.; Tikhonovich, I. A.; Glomb, M. A.; Bilova, T.; Frolov, A.; Does Protein Glycation Impact on the Drought-Related Changes in Metabolism and Nutritional Properties of Mature Pea (Pisum sativum L.) Seeds? Int. J. Mol. Sci. 21, 567, (2020) DOI: 10.3390/ijms21020567

Protein glycation is usually referred to as an array of non-enzymatic post-translational modifications formed by reducing sugars and carbonyl products of their degradation. The resulting advanced glycation end products (AGEs) represent a heterogeneous group of covalent adducts, known for their pro-inflammatory effects in mammals, and impacting on pathogenesis of metabolic diseases and ageing. In plants, AGEs are the markers of tissue ageing and response to environmental stressors, the most prominent of which is drought. Although water deficit enhances protein glycation in leaves, its effect on seed glycation profiles is still unknown. Moreover, the effect of drought on biological activities of seed protein in mammalian systems is still unstudied with respect to glycation. Therefore, here we address the effects of a short-term drought on the patterns of seed protein-bound AGEs and accompanying alterations in pro-inflammatory properties of seed protein in the context of seed metabolome dynamics. A short-term drought, simulated as polyethylene glycol-induced osmotic stress and applied at the stage of seed filling, resulted in the dramatic suppression of primary seed metabolism, although the secondary metabolome was minimally affected. This was accompanied with significant suppression of NF-kB activation in human SH-SY5Y neuroblastoma cells after a treatment with protein hydrolyzates, isolated from the mature seeds of drought-treated plants. This effect could not be attributed to formation of known AGEs. Most likely, the prospective anti-inflammatory effect of short-term drought is related to antioxidant effect of unknown secondary metabolite protein adducts, or down-regulation of unknown plant-specific AGEs due to suppression of energy metabolism during seed filling.
Publikation

Smolikova, G.; Gorbach, D.; Lukasheva, E.; Mavropolo-Stolyarenko, G.; Bilova, T.; Soboleva, A.; Tsarev, A.; Romanovskaya, E.; Podolskaya, E.; Zhukov, V. A.; Tikhonovich, I.; Medvedev, S.; Hoehenwarter, W.; Frolov, A.; Bringing new methods to the seed proteomics platform: Challenges and perspectives Int. J. Mol. Sci. 21, 9162, (2020) DOI: 10.3390/ijms21239162

For centuries, crop plants have represented the basis of the daily human diet. Among them, cereals and legumes, accumulating oils, proteins, and carbohydrates in their seeds, distinctly dominate modern agriculture, thus play an essential role in food industry and fuel production. Therefore, seeds of crop plants are intensively studied by food chemists, biologists, biochemists, and nutritional physiologists. Accordingly, seed development and germination as well as age- and stress-related alterations in seed vigor, longevity, nutritional value, and safety can be addressed by a broad panel of analytical, biochemical, and physiological methods. Currently, functional genomics is one of the most powerful tools, giving direct access to characteristic metabolic changes accompanying plant development, senescence, and response to biotic or abiotic stress. Among individual post-genomic methodological platforms, proteomics represents one of the most effective ones, giving access to cellular metabolism at the level of proteins. During the recent decades, multiple methodological advances were introduced in different branches of life science, although only some of them were established in seed proteomics so far. Therefore, here we discuss main methodological approaches already employed in seed proteomics, as well as those still waiting for implementation in this field of plant research, with a special emphasis on sample preparation, data acquisition, processing, and post-processing. Thereby, the overall goal of this review is to bring new methodologies emerging in different areas of proteomics research (clinical, food, ecological, microbial, and plant proteomics) to the broad society of seed biologists.
Publikation

Chantseva, V.; Bilova, T.; Smolikova, G.; Frolov, A.; Medvedev, S.; 3D-clinorotation induces specific alterations in metabolite profiles of germinating Brassica napus L. seeds Biol. Commun. 64, 55-74, (2019) DOI: 10.21638/spbu03.2019.107

During the whole history of their life on Earth, higher plants evolved under the constant gravity stimulus. Therefore, plants developed efficient mechanisms of gravity perception, underlying their ability to adjust the direction of growth to the gravity vector, i.e. the phenomenon of gravitropism. In this context, alterations in the magnitude and vector of the gravity field might compromise plant growth and development. This aspect was successfully addressed in gravity fields of low intensity (microgravity). On the other hand, microgravity can be simulated on the Earth by clinorotation, i.e. rotation of the experimental plant along one or several axes. This approach is routinely used for studies of gravity-related responses of crop plants, although the effect of simulated microgravity on the most sensitive ontogenetic stages — germination and seedling development — is still not sufficiently characterized. Recently, we addressed the effects of clinorotation on the proteome of germinating oilseed rape (Brassica napus) seeds. Here we extend this study to the seedling primary metabolome and address its changes in the presence of 3D-clinorotation. GC-MS analysis revealed essential alterations in patterns of sugars and sugar phosphates (specifically glucose-6-phosphate), methionine and glycerol. Thereby, abundances of individual metabolites showed high dispersion, indicating high lability and plasticity of the seedling metabolome.
Bücher und Buchkapitel

Osmolovskaya, N.; Shumilina, J.; Bureiko, K.; Chantseva, V.; Bilova, T.; Kuchaeva, L.; Laman, N.; Wessjohann, L. A.; Frolov, A.; Ion Homeostasis Response to Nutrient-Deficiency Stress in Plants (Vikas, B. & Fasullo, M., eds.). 1-23, (2019) ISBN: 978-1-78985-311-7 DOI: 10.5772/intechopen.89398

A crucial feature of plant performance is its strong dependence on the availability of essential mineral nutrients, affecting multiple vital functions. Indeed, mineral-nutrient deficiency is one of the major stress factors affecting plant growth and development. Thereby, nitrogen and potassium represent the most abundant mineral contributors, critical for plant survival. While studying plant responses to nutrient deficiency, one should keep in mind that mineral nutrients, along with their specific metabolic roles, are directly involved in maintaining cell ion homeostasis, which relies on a finely tuned equilibrium between cytosolic and vacuolar ion pools. Therefore, in this chapter we briefly summarize the role of the ion homeostasis system in cell responses to environmental deficiency of nitrate and potassium ions. Special attention is paid to the implementation of plant responses via NO3− and K+ root transport and regulation of ion distribution in cell compartments. These responses are strongly dependent on plant species, as well as severity and duration of nutrient deficiency.
Preprints

Osmolovskaya, N.; Shumilina, J.; Kim, A.; Didio, A.; Grishina, T.; Bilova, T.; Keltsieva, O. A.; Zhukov, V.; Tikhonovich, I.; Tarakhovskaya, E.; Wessjohann, L. A.; Frolov, A.; Methodology of Drought Stress Research: Experimental Setup and Physiological Characterization Preprints (2018) DOI: 10.20944/preprints201812.0145.v1

Drought is one of the major stress factors affecting growth and development of plants. In this context, drought-related losses of crop plant productivity impede sustainable agriculture all over the world. In general, plants responses to water deficit by multiple physiological and metabolic adaptations at the molecular, cellular and organism levels. To understand the underlying mechanisms of drought tolerance, adequate stress models and arrays of reliable stress markers are required. Therefore, in this review we comprehensively address currently available models of drought stress, based on culturing plants in soil, hydroponic or agar culture. These experimental setups give access to different aspects of plant response to drought, like decrease of tissue water potential, reduction of stomata conductance and photosynthesis efficiency, accumulation of low-molecular weight solutes (metabolic adjustment) and drought protective proteins. Till now, this pattern of markers was successfully extended to the methods of enzyme chemistry, molecular biology and omics techniques. Thus, conventional tests can be efficiently complemented by determination of phytohormone and reactive oxygen species (ROS) contents, activities of antioxidant enzymes, as well as comprehensive profiling of transcriptome, proteome and metabolome.
Preprints

Mamontova, T.; Lukasheva, E.; Mavropolo-Stolyarenko, G.; Proksch, C.; Bilova, T.; Kim, A.; Babakov, V.; Grishina, T.; Hoehenwarter, W.; Medvedev, S.; Smolikova, G.; Frolov, A.; Proteome Map of Pea (Pisum Sativum L.) Embryos Containing Different Amounts of Residual Chlorophylls Preprints (2018) DOI: 10.20944/preprints201812.0069.v1

Due to low culturing costs and high seed protein contents, legumes represent the main global source of food protein. Pea (Pisum sativum L.) is one of the major economically important legume crops, impacting both animal feed and human nutrition. Therefore, the quality of pea seeds needs to be ensured in the context of sustainable crop production and nutritional efficiency. Obviously, changes in seed protein patterns might directly affect both of these aspects. Thus, here we address the pea seed proteome in more detail and provide, to the best of our knowledge, the most comprehensive annotation of the functions and intracellular localization of pea seed proteins. Accordingly, 1938 and 1989 non-redundant proteins were identified in yellow and green pea seeds, in total. Only 35 and 44 proteins, respectively, could be additionally identified after protamine sulfate precipitation (PSP) potentially indicating the high efficiency of our experimental workflow. In total 981 protein groups could be assigned to 34 functional classes, which were to a large extent differentially represented in yellow and green seeds. Closer analysis of these differences by processing of the data in KEGG and String databases revealed their possible relation to a higher metabolic status and reduced longevity of green seeds.
Publikation

Mamontova, T.; Lukasheva, E.; Mavropolo-Stolyarenko, G.; Proksch, C.; Bilova, T.; Kim, A.; Babakov, V.; Grishina, T.; Hoehenwarter, W.; Medvedev, S.; Smolikova, G.; Frolov, A.; Proteome Map of Pea (Pisum sativum L.) Embryos Containing Different Amounts of Residual Chlorophylls Int. J. Mol. Sci. 19, 4066, (2018) DOI: 10.3390/ijms19124066

Due to low culturing costs and high seed protein contents, legumes represent the main global source of food protein. Pea (Pisum sativum L.) is one of the major legume crops, impacting both animal feed and human nutrition. Therefore, the quality of pea seeds needs to be ensured in the context of sustainable crop production and nutritional efficiency. Apparently, changes in seed protein patterns might directly affect both of these aspects. Thus, here, we address the pea seed proteome in detail and provide, to the best of our knowledge, the most comprehensive annotation of the functions and intracellular localization of pea seed proteins. To address possible intercultivar differences, we compared seed proteomes of yellow- and green-seeded pea cultivars in a comprehensive case study. The analysis revealed totally 1938 and 1989 nonredundant proteins, respectively. Only 35 and 44 proteins, respectively, could be additionally identified after protamine sulfate precipitation (PSP), potentially indicating the high efficiency of our experimental workflow. Totally 981 protein groups were assigned to 34 functional classes, which were to a large extent differentially represented in yellow and green seeds. Closer analysis of these differences by processing of the data in KEGG and String databases revealed their possible relation to a higher metabolic status and reduced longevity of green seeds.
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