vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/vjgb-26-86vavilov-5292Research ArticleГЕНЕТИКА И СЕЛЕКЦИЯ РАСТЕНИЙPLANT GENETICS AND BREEDINGХолодовая акклиматизация растений томата связана с дифференциальной экспрессией генов семейства SlLHC, метаболизма каротиноидов и накопления/деградации хлорофилловCold acclimation of tomato plants is associated with differential expression of genes of the SlLHC family, carotenoid metabolism, and chlorophyll accumulation/degradationФилюшинМ. А.FilyushinM. A.

Москва

Moscow

michel7753@mail.ruЩенниковаА. В.ShchennikovaA. V.

Москва

Moscow

КочиеваЕ. З.KochievaE. Z.

Москва

Moscow

Федеральный исследовательский центр «Фундаментальные основы биотехнологии» Российской академии наукРоссияInstitute of Bioengineering, Research Center of Biotechnology of the Russian Academy of SciencesRussian Federation202613102026306843853Copyright © Филюшин М.А., Щенникова А.В., Кочиева Е.З., 20262026Филюшин М.А., Щенникова А.В., Кочиева Е.З.Filyushin M.A., Shchennikova A.V., Kochieva E.Z.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/5292

Растения томата (Solanum lycopersicum L.) чувствительны к воздействию холодового стресса, адаптационный ответ на который связан с клеточной осморегуляцией и снижением скорости фотосинтеза за счет нарушения работы антенн фотосистем I и II, включающих белки семейства Light-Harvesting Complex (LHC), связывающие хлорофиллы a/b и каротиноиды. В настоящей работе впервые проведен транскриптомный анализ дифференциальной экспрессии генов семейства SlLHC, генов биосинтеза каротиноидов и абсцизовой кислоты (АБК), а также генов ORANGE и STAY-GREEN, связанных с синтезом и деградацией хлорофиллов, в динамике двух циклов (I и II) «холодовой стресс (12 ч) – восстановление (60 ч)». Для анализа использован сорт томата Отрадный. Показано, что за 12 ч до завершения периода восстановления второго цикла (II-48) в листьях растения значительно уменьшается количество хлорофиллов a/b и каротиноидов. Выявлено, что 12 ч холодового воздействия в обоих циклах (I-12, II-12) подавляют экспрессию большинства генов семейства LHC. В тех же точках обнаружено значимое повышение уровня транскриптов генов NSY, CCD-like, LeNCED1 и NCED6, связанных с синтезом АБК. Определены гены, профиль экспрессии которых различается между первичным и повторным циклами холодового воздействия. На основании этих данных составлен список генов-кандидатов в маркеры памяти растений о холодовом стрессе: десять генов семейства SlLHC (Cab-1A, Cab-1D, CAB12, CAB5-LOC101257186, SEP2, OHP2-LOC101259223, OHP1 и LIL3-2-LOC101247899) и пять генов, ассоциированных с синтезом АБК (VDE, CCD4, CCD-like, LeNCED1 и NCED6). Полученные результаты важны для определения и осмысления участия генов, связанных с фотосинтезом, в ответе на холодовой стресс и определении холодостойкости растений томата, и могут быть использованы в селекции холодостойких сортов.

Tomato (Solanum lycopersicum L.) is sensitive to cold stress. The plant’s adaptive response to low temperatures is accompanied by cellular osmoregulation and a decrease in the rate of photosynthesis due to disruption of the antennae of photosystems I and II, including proteins of the light-harvesting complex (LHC) family that bind chlorophylls a/b and carotenoids. In this study, a transcriptome analysis of differential expression of SlLHC family genes, carotenoid and abscisic acid (ABA) biosynthesis genes, as well as ORANGE and STAY-GREEN genes associated with chlorophyll accumulation and degradation, was performed for the first time during two cycles (I and II) of “cold stress (12 h) – recovery (60 h)”. The tomato cultivar Otradnyi was used for the analysis. 12 h before the end of the recovery period of the second cycle (II-48), the content of chlorophylls a/b and carotenoids in plant leaves was shown to be significantly decreased. It was revealed that 12 h of cold exposure in both cycles (I-12, II-12) suppressed the expression of most LHC family genes. At the same time points, a significant increase in the transcript levels of the NSY, CCD-like, LeNCED1 and NCED6 genes associated with ABA synthesis was detected. Genes, expression profile of which differed between the primary and repeated cycles of cold exposure, were identified. Based on these data, a list of candidate genes for cold stress memory markers in plants was compiled: 10 SlLHC family genes (Cab-1A, Cab-1D, CAB12, CAB5LOC101257186, SEP2, OHP2-LOC101259223, OHP1 and LIL3-2-LOC101247899) and five genes associated with ABA synthesis (VDE, CCD4, CCD-like, LeNCED1 and NCED6). The obtained results are important for identifying and understanding the involvement of photosynthesis-related genes in the response to cold stress and determining cold tolerance of tomato plants, and can be used in breeding cold-resistant varieties.

Solanum lycopersicum L.холодовой стресссемейство белков LHCхлорофилл a/b-связывающие белкибиосинтез каротиноидовАБКэкспрессия геновSolanum lycopersicum L.cold stressLHC protein familychlorophyll a/b-binding proteinscarotenoid biosynthesisABAgene expressionThe work was supported by the Russian Science Foundation (grant No. 24-16-00043, transcriptome analysis) and the Ministry of Science and Higher Education of the Russian Federation (obtaining and preparing plants, biochemical analysis)ReferencesAgurla S., Gahir S., Munemasa S., Murata Y., Raghavendra A.S. Mechanism of stomatal closure in plants exposed to drought and cold stress. In: Iwaya-Inoue M., Sakurai M., Uemura M. (Eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology. Vol. 1081. Springer, 2018;215-232. doi 10.1007/978-981-13-1244-1_12Agurla S., Gahir S., Munemasa S., Murata Y., Raghavendra A.S. Mechanism of stomatal closure in plants exposed to drought and cold stress. In: Iwaya-Inoue M., Sakurai M., Uemura M. (Eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology. Vol. 1081. Springer, 2018;215-232. doi 10.1007/978-981-13-1244-1_12Aina O., Bakare O.O., Fadaka A.O., Keyster M., Klein A. Plant biomarkers as early detection tools in stress management in food crops: a review. Planta. 2024;259(3):60. doi 10.1007/s00425-024-04333-1Aina O., Bakare O.O., Fadaka A.O., Keyster M., Klein A. Plant biomarkers as early detection tools in stress management in food crops: a review. Planta. 2024;259(3):60. doi 10.1007/s00425-024-04333-1Ashraf M., Harris P.J.C. Photosynthesis under stressful environments: an overview. Photosynthetica. 2013;51:163-190. doi 10.1007/s11099-013-0021-6Ashraf M., Harris P.J.C. Photosynthesis under stressful environments: an overview. Photosynthetica. 2013;51:163-190. doi 10.1007/s11099-013-0021-6Bäurle I., Trindade I. Chromatin regulation of somatic abiotic stress memory. J Exp Bot. 2020;71(17):5269-5279. doi 10.1093/jxb/eraa098Bäurle I., Trindade I. Chromatin regulation of somatic abiotic stress memory. J Exp Bot. 2020;71(17):5269-5279. doi 10.1093/jxb/eraa098Browse J., Xin Z. Temperature sensing and cold acclimation. Curr Opin Plant Biol. 2001;4:241-246. doi 10.1016/s1369-5266(00)00167-9Browse J., Xin Z. Temperature sensing and cold acclimation. Curr Opin Plant Biol. 2001;4:241-246. doi 10.1016/s1369-5266(00)00167-9Chen K., Li G.J., Bressan R.A., Song C.P., Zhu J.K., Zhao Y. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 2020;62(1):25-54. doi 10.1111/jipb.12899Chen K., Li G.J., Bressan R.A., Song C.P., Zhu J.K., Zhao Y. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 2020;62(1):25-54. doi 10.1111/jipb.12899Ding Y., Shi Y., Yang S. Regulatory networks underlying plant responses and adaptation to cold stress. Annu Rev Genet. 2024;58(1):43-65. doi 10.1146/annurev-genet-111523-102226Ding Y., Shi Y., Yang S. Regulatory networks underlying plant responses and adaptation to cold stress. Annu Rev Genet. 2024;58(1):43-65. doi 10.1146/annurev-genet-111523-102226Efremov G.I., Slugina M.A., Shchennikova A.V., Kochieva E.Z. Differential regulation of phytoene synthase PSY1 during fruit carotenogenesis in cultivated and wild tomato species (Solanum section Lycopersicon). Plants. 2020;9(9):1169. doi 10.3390/plants9091169Efremov G.I., Slugina M.A., Shchennikova A.V., Kochieva E.Z. Differential regulation of phytoene synthase PSY1 during fruit carotenogenesis in cultivated and wild tomato species (Solanum section Lycopersicon). Plants. 2020;9(9):1169. doi 10.3390/plants9091169ElShamey E., Zeng Y., Ding Y., Yang J. Functional phytochemicals in tomatoes: biosynthesis, gene regulation, and human health implications. Front Plant Sci. 2025;16:1662388. doi 10.3389/fpls.2025.1662388ElShamey E., Zeng Y., Ding Y., Yang J. Functional phytochemicals in tomatoes: biosynthesis, gene regulation, and human health implications. Front Plant Sci. 2025;16:1662388. doi 10.3389/fpls.2025.1662388Filyushin M.A., Shchennikova A.V., Kochieva E.Z. Differential expression profile of DREB2 subfamily transcription factor genes in the dynamics of salt stress and post-stress recovery in tomato plants. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov J Genet Breed. 2025;29(8):1213-1220. doi 10.18699/vjgb-25-128Filyushin M.A., Shchennikova A.V., Kochieva E.Z. Differential expression profile of DREB2 subfamily transcription factor genes in the dynamics of salt stress and post-stress recovery in tomato plants. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov J Genet Breed. 2025;29(8):1213-1220. doi 10.18699/vjgb-25-128Friedrich T., Faivre L., Bäurle I., Schubert D. Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ. 2019; 42(3):762-770. doi 10.1111/pce.13373Friedrich T., Faivre L., Bäurle I., Schubert D. Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ. 2019; 42(3):762-770. doi 10.1111/pce.13373Gao Y., Zhou X., Huang H., Wang C., Xiao X., Wen J., Wu J., Zhou S., de Dios V.R., Rodríguez L.G., Yao Y., Liu J., Deng H. ORANGE proteins mediate adaptation to high light and resistance to Pseudomonas syringae in tomato by regulating chlorophylls and carotenoids accumulation. Int J Biol Macromol. 2025;306(Pt.4):141739. doi 10.1016/j.ijbiomac.2025.141739Gao Y., Zhou X., Huang H., Wang C., Xiao X., Wen J., Wu J., Zhou S., de Dios V.R., Rodríguez L.G., Yao Y., Liu J., Deng H. ORANGE proteins mediate adaptation to high light and resistance to Pseudomonas syringae in tomato by regulating chlorophylls and carotenoids accumulation. Int J Biol Macromol. 2025;306(Pt.4):141739. doi 10.1016/j.ijbiomac.2025.141739Ikuyinminu E., Goñi O., Łangowski Ł., O’Connell S. Transcriptome, biochemical and phenotypic analysis of the effects of a precision engineered biostimulant for inducing salinity stress tolerance in tomato. Int J Mol Sci. 2023;24(8):6988. doi 10.3390/ijms24086988Ikuyinminu E., Goñi O., Łangowski Ł., O’Connell S. Transcriptome, biochemical and phenotypic analysis of the effects of a precision engineered biostimulant for inducing salinity stress tolerance in tomato. Int J Mol Sci. 2023;24(8):6988. doi 10.3390/ijms24086988Jacques C., Salon C., Barnard R.L., Vernoud V., Prudent M. Drought stress memory at the plant cycle level: a review. Plants (Basel). 2021;10(9):1873. doi 10.3390/plants10091873Jacques C., Salon C., Barnard R.L., Vernoud V., Prudent M. Drought stress memory at the plant cycle level: a review. Plants (Basel). 2021;10(9):1873. doi 10.3390/plants10091873Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 1999;4(6):236-240. doi 10.1016/s1360-1385(99)01419-3Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 1999;4(6):236-240. doi 10.1016/s1360-1385(99)01419-3Kidokoro S., Shinozaki K., Yamaguchi-Shinozaki K. Transcriptional regulatory network of plant cold-stress responses. Trends Plant Sci. 2022;27(9):922-935. doi 10.1016/j.tplants.2022.01.008Kidokoro S., Shinozaki K., Yamaguchi-Shinozaki K. Transcriptional regulatory network of plant cold-stress responses. Trends Plant Sci. 2022;27(9):922-935. doi 10.1016/j.tplants.2022.01.008Klimmek F., Sjödin A., Noutsos C., Leister D., Jansson S. Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol. 2006;140(3):793-804. doi 10.1104/pp.105.073304Klimmek F., Sjödin A., Noutsos C., Leister D., Jansson S. Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol. 2006;140(3):793-804. doi 10.1104/pp.105.073304Lan Y., Song Y., Zhao F., Cao Y., Luo D., Qiao D., Cao Y., Xu H. Phylogenetic, structural and functional evolution of the LHC gene family in plant species. Int J Mol Sci. 2022;24(1):488. doi 10.3390/ijms24010488Lan Y., Song Y., Zhao F., Cao Y., Luo D., Qiao D., Cao Y., Xu H. Phylogenetic, structural and functional evolution of the LHC gene family in plant species. Int J Mol Sci. 2022;24(1):488. doi 10.3390/ijms24010488Li Y., Cao T., Guo Y., Grimm B., Li X., Duanmu D., Lin R. Regulatory and retrograde signaling networks in the chlorophyll biosynthetic pathway. J Integr Plant Biol. 2025;67(4):887-911. doi 10.1111/jipb.13837Li Y., Cao T., Guo Y., Grimm B., Li X., Duanmu D., Lin R. Regulatory and retrograde signaling networks in the chlorophyll biosynthetic pathway. J Integr Plant Biol. 2025;67(4):887-911. doi 10.1111/jipb.13837Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. doi 10.1186/s13059-014-0550-8Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. doi 10.1186/s13059-014-0550-8Meng F., Ma M., Li S., Liang P., Liang Y., Shi H., Huang S., Su H., Deng Y., Akram M.A., Shen X., Feng R., Zhan X., Ma F. Genomewide identification of light-harvesting chlorophyll a/b-binding (LHC) gene family in tomato and functional analysis of SlLhcb1.11 and SlELIP1 under cold stress. Genomics. 2025;117(2):111022. doi 10.1016/j.ygeno.2025.111022Meng F., Ma M., Li S., Liang P., Liang Y., Shi H., Huang S., Su H., Deng Y., Akram M.A., Shen X., Feng R., Zhan X., Ma F. Genomewide identification of light-harvesting chlorophyll a/b-binding (LHC) gene family in tomato and functional analysis of SlLhcb1.11 and SlELIP1 under cold stress. Genomics. 2025;117(2):111022. doi 10.1016/j.ygeno.2025.111022Mesa T., Polo J., Arabia A., Caselles V., Munné-Bosch S. Differential physiological response to heat and cold stress of tomato plants and its implication on fruit quality. J Plant Physiol. 2022;268:153581. doi 10.1016/j.jplph.2021.153581Mesa T., Polo J., Arabia A., Caselles V., Munné-Bosch S. Differential physiological response to heat and cold stress of tomato plants and its implication on fruit quality. J Plant Physiol. 2022;268:153581. doi 10.1016/j.jplph.2021.153581Nakashima K., Yamaguchi-Shinozaki K. ABA signaling in stress-response and seed development. Plant Cell Rep. 2013;32(7):959-970. doi 10.1007/s00299-013-1418-1Nakashima K., Yamaguchi-Shinozaki K. ABA signaling in stress-response and seed development. Plant Cell Rep. 2013;32(7):959-970. doi 10.1007/s00299-013-1418-1Neilson K.A., Mariani M., Haynes P.A. Quantitative proteomic analysis of cold-responsive proteins in rice. Proteomics. 2011;11(9):1696- 1706. doi 10.1002/pmic.201000727Neilson K.A., Mariani M., Haynes P.A. Quantitative proteomic analysis of cold-responsive proteins in rice. Proteomics. 2011;11(9):1696- 1706. doi 10.1002/pmic.201000727Piechulla B., Merforth N., Rudolph B. Identification of tomato Lhc promoter regions necessary for circadian expression. Plant Mol Biol. 1998;38(4):655-662. doi 10.1023/a:1006094015513Piechulla B., Merforth N., Rudolph B. Identification of tomato Lhc promoter regions necessary for circadian expression. Plant Mol Biol. 1998;38(4):655-662. doi 10.1023/a:1006094015513Pietrzykowska M., Suorsa M., Semchonok D.A., Tikkanen M., Boekema E.J., Aro E.-M., Jansson S. The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. Plant Cell. 2014;26(9):3646-3660. doi 10.1105/tpc.114.127373Pietrzykowska M., Suorsa M., Semchonok D.A., Tikkanen M., Boekema E.J., Aro E.-M., Jansson S. The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. Plant Cell. 2014;26(9):3646-3660. doi 10.1105/tpc.114.127373Soualiou S., Duan F., Li X., Zhou W. Nitrogen supply alleviates cold stress by increasing photosynthesis and nitrogen assimilation in maize seedlings. J Exp Bot. 2023;74(10):3142-3162. doi 10.1093/jxb/erad073Soualiou S., Duan F., Li X., Zhou W. Nitrogen supply alleviates cold stress by increasing photosynthesis and nitrogen assimilation in maize seedlings. J Exp Bot. 2023;74(10):3142-3162. doi 10.1093/jxb/erad073Sreenivasulu N., Harshavardhan V.T., Govind G., Seiler C., Kohli A. Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene. 2012; 506(2):265-273. doi 10.1016/j.gene.2012.06.076Sreenivasulu N., Harshavardhan V.T., Govind G., Seiler C., Kohli A. Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene. 2012; 506(2):265-273. doi 10.1016/j.gene.2012.06.076Tee E.E. Orange is the new green: Arabidopsis ORANGE represses chloroplast biogenesis. Plant Cell. 2019;31(12):2824-2825. doi 10.1105/tpc.19.00670Tee E.E. Orange is the new green: Arabidopsis ORANGE represses chloroplast biogenesis. Plant Cell. 2019;31(12):2824-2825. doi 10.1105/tpc.19.00670Villagómez-Aranda A.L., Feregrino-Pérez A.A., García-Ortega L.F., González-Chavira M.M., Torres-Pacheco I., Guevara-González R.G. Activating stress memory: eustressors as potential tools for plant breeding. Plant Cell Rep. 2022;41(7):1481-1498. doi 10.1007/s00299-022-02858-xVillagómez-Aranda A.L., Feregrino-Pérez A.A., García-Ortega L.F., González-Chavira M.M., Torres-Pacheco I., Guevara-González R.G. Activating stress memory: eustressors as potential tools for plant breeding. Plant Cell Rep. 2022;41(7):1481-1498. doi 10.1007/s00299-022-02858-xXu C., Wang Y., Yang H., Tang Y., Liu B., Hu X., Hu Z. Cold acclimation alleviates photosynthetic inhibition and oxidative damage induced by cold stress in citrus seedlings. Plant Signal Behav. 2023; 18(1):2285169. doi 10.1080/15592324.2023.2285169Xu C., Wang Y., Yang H., Tang Y., Liu B., Hu X., Hu Z. Cold acclimation alleviates photosynthetic inhibition and oxidative damage induced by cold stress in citrus seedlings. Plant Signal Behav. 2023; 18(1):2285169. doi 10.1080/15592324.2023.2285169Yamori W., Hikosaka K., Way D.A. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res. 2014;119(1-2):101-117. doi 10.1007/s11120-013-9874-6Yamori W., Hikosaka K., Way D.A. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res. 2014;119(1-2):101-117. doi 10.1007/s11120-013-9874-6Yan J., Liu J., Yang S., Jiang C., Liu Y., Zhang N., Sun X., … Liu Y., Sun Z., Qi M., Wang F., Li T. Light quality regulates plant biomass and fruit quality through a photoreceptor-dependent HY5-LHC/ CYCB module in tomato. Hortic Res. 2023;10(12):uhad219. doi 10.1093/hr/uhad219Yan J., Liu J., Yang S., Jiang C., Liu Y., Zhang N., Sun X., … Liu Y., Sun Z., Qi M., Wang F., Li T. Light quality regulates plant biomass and fruit quality through a photoreceptor-dependent HY5-LHC/ CYCB module in tomato. Hortic Res. 2023;10(12):uhad219. doi 10.1093/hr/uhad219Zhang Q., Ma C., Wang X., Ma Q., Fan S., Zhang C. Genome-wide identification of the light-harvesting chlorophyll a/b binding (Lhc) family in Gossypium hirsutum reveals the influence of GhLhcb2.3 on chlorophyll a synthesis. Plant Biol (Stuttg). 2021;23(5):831-842. doi 10.1111/plb.13294Zhang Q., Ma C., Wang X., Ma Q., Fan S., Zhang C. Genome-wide identification of the light-harvesting chlorophyll a/b binding (Lhc) family in Gossypium hirsutum reveals the influence of GhLhcb2.3 on chlorophyll a synthesis. Plant Biol (Stuttg). 2021;23(5):831-842. doi 10.1111/plb.13294Zhao S., Gao H., Luo J., Wang H., Dong Q., Wang Y., Yang K., Mao K., Ma F. Genome-wide analysis of the light-harvesting chlorophyll a/b-binding gene family in apple (Malus domestica) and functional characterization of MdLhcb4.3, which confers tolerance to drought and osmotic stress. Plant Physiol Biochem. 2020;154:517-529. doi 10.1016/j.plaphy.2020.06.022Zhao S., Gao H., Luo J., Wang H., Dong Q., Wang Y., Yang K., Mao K., Ma F. Genome-wide analysis of the light-harvesting chlorophyll a/b-binding gene family in apple (Malus domestica) and functional characterization of MdLhcb4.3, which confers tolerance to drought and osmotic stress. Plant Physiol Biochem. 2020;154:517-529. doi 10.1016/j.plaphy.2020.06.022

The authors declare that there are no conflicts of interest present.