izvestiiatimacadИзвестия Тимирязевской сельскохозяйственной академииIZVESTIYA OF TIMIRYAZEV AGRICULTURAL ACADEMY0021-342XФГБОУ ВО РГАУ-МСХА имени К.А. Тимирязева10.26897/0021-342X-2023-4-75-94izvestiiatimacad-414Research ArticleФИЗИОЛОГИЯ РАСТЕНИЙ, МИКРОБИОЛОГИЯPLANT PHYSIOLOGY, MICROBIOLOGYФизиологические аспекты созревания и продления срока хранения сочных плодовPhysiological aspects of ripening and extending the shelf life of fleshy fruitsПанфиловаО. Ф.PanfilovaO. F.

Панфилова Ольга Федоровна, канд. с.-х. наук, доцент

127434, г. Москва, ул. Тимирязевская, 49

тел.: (910) 412–04–13

Olga F. Panfilova, CSc (Ag), Associate Professor, Associate Professor of the Department of Plant Physiology

49, Timiryazevskaya Str., Moscow, 127434

phone: (910) 412–04–13

panfilova.of@yandex.ruПильщиковаН. В.Pil’shchikovaN. V.

Пильщикова Наталия Владимировна, канд. биол. наук, доцент

127434, г. Москва, ул. Тимирязевская, 49

тел.: (915) 468–86–22

Natalia V. Pil’shchikova, CSc (Bio), Associate Professor, Associate Professor of the Department of Plant Physiology

49, Timiryazevskaya Str., Moscow, 127434

phone: (915) 468–86–22

sad200805@mail.ruРоссийский государственный аграрный университет - МСХА имени К.А.ТимирязеваРоссияRussian State Agrarian University – Moscow Timiryazev Agricultural AcademyRussian Federation202325102023147594Copyright © Панфилова О.Ф., Пильщикова Н.В., 20232023Панфилова О.Ф., Пильщикова Н.В.Panfilova O.F., Pil’shchikova N.V.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://izvestiia.timacad.ru/jour/article/view/414

В статье обсуждаются физиологические аспекты созревания сочных плодов в связи с проблемой продления срока хранения садоводческой продукции. Использованы достижения молекулярной биологии в области генетической регуляции процессов формирования качества урожая. Особое внимание обращено на гормональную регуляцию накопления питательных и биологически активных веществ в плодах. Показана роль рецепторных белков ARF/IAA и DELLA во взаимодействии сигнальных путей ауксина и ГК во время роста плодов томата, земляники и винограда. Отмечено участие белков DELLA в интеграции функционирования других фитогормонов: цитокинина, этилена, абсцизовой кислоты, брассиностероидов и жасмоновой кислоты. Приведены свидетельства взаимодействия цитокинина с ауксином и ГК в регуляции раннего развития и размера плодов. Рассмотрено сочетание факторов транскрипции и эпигенетических модификаций при формировании и старении плодов. Показано включение механизмов старения и утраты лежкости плодов в отсутствие внешних признаков. Рассмотрены особенности созревания климактерических и неклимактерических плодов. Одним из ключевых регуляторов процесса созревания как климактерических, так и неклимактерических плодов является MADS-доменный транскрипционный фактор RIPENING INHIBITOR (RIN). Регулировка созревания неклимактерических плодов представлена на примере винограда и земляники. Особое внимание уделено ростовым процессам, водному обмену, фотосинтезу, первичному и вторичному метаболизму формирующихся и созревающих плодов. Рассмотрены вопросы формирования покровов и клеточных стенок как структурной основы физических свойств продукции. Приведены перспективные способы применения регуляторов процессов жизнедеятельности в послеуборочный период для замедления старения плодов. Углубление знаний генетических, гормональных и метаболических сетей открывает широкие перспективы для улучшения и сохранения качества сочной продукции садоводства.

This review discusses the physiological aspects of the ripening of juicy fruits in relation to the problem of extending the shelf life of horticultural products. The achievements of molecular biology in the field of genetic regulation of plant quality formation processes are used. Particular attention is paid to the hormonal regulation of the accumulation of nutrients and biologically active substances in fruits. The role of ARF/IAA and DELLA receptor proteins in the interaction of auxin and GA signalling pathways during the growth of tomato, strawberry, and grape fruits is demonstrated. The involvement of DELLA proteins in integrating the function of other phytohormones – cytokinin, ethylene, abscisic acid, brassinosteroids and jasmonic acid – is noted. Evidence is presented for the interaction of cytokinin with auxin and GA in the regulation of early development and fruit size. The combination of transcription factors and epigenetic modifications during fruit development and senescence is considered. The involvement of mechanisms of senescence and loss of fruit shelf life in the absence of external signs is shown. The ripening characteristics of climacteric and nonclimacteric fruits are considered. One of the key regulators of the ripening process in both climacteric and non-climacteric fruits is the MADS domain transcription factor RIPENING INHIBITOR (RIN). The regulation of non-climacteric fruit ripening is reviewed using grape and strawberry as examples. Special attention is paid to growth processes, water exchange, photosynthesis, primary and secondary metabolism of developing and ripening fruits. The formation of integuments and cell walls as a structural basis for the physical properties of products is considered. Promising methods of using regulators of vital processes in the post-harvest period to slow down the fruit senescence are given. Increased knowledge of genetic, hormonal and metabolic networks opens up broad prospects for improving and maintaining the quality of fleshy horticultural products.

генетическая регуляциягормональная регуляцияпервичный метаболизмвторичный метаболизмформирование сочных плодовсозреваниестарениеgenetic regulationhormonal regulationprimary metabolismsecondary metabolismformation of fleshy fruitsripeningsenescenceReferencesВоронков А.С., Иванова Т.В., Кузнецова Э.И., Кумахова Т.Х. Адаптивные возможности плода Malus domestica Borkh. (Rosaceae) в условиях высотной поясности // Физиология растений. – 2019. – Том 66. – № 6. – С. 441-451.Voronkov A.S., Ivanova T.V., Kuznecova E.I., Kumahova T.H. Adaptivnye vozmozhnosti ploda Malus domestica Borkh. (Rosaceae) v usloviyah vysotnoj poyasnosti // Fiziologiya rastenij. – 2019. – Tom 66. – № 6. – S. 441-451.Ефремов Г.И., Джос Е.А., Ашихмин А.А., Кочиева Е.З., Щенникова А.В. Влияние содержания каротиноидов и активности гена каротиноид-цис-транс-изомераза CRTISO на окраску плода томата // Физиология растений. – 2022. – Том 69. – № 4. – С. 352-362.Efremov G.I., Dzhos E.A., Ashihmin A.A., Kochieva E.Z., SHCHennikova A.V. Vliyanie soderzhaniya karotinoidov i aktivnosti gena karotinoid-cis-trans-izomeraza CRTISO na okrasku ploda tomata // Fiziologiya rastenij. – 2022. – Tom 69. – № 4. – S. 352-362.Слугина М.А. Транскрипционный фактор RIPENING INHIBITOR и его гомологи в регуляции созревания сочного плода различных видов растений // Физиология растений. – 2021. – Том 68. – № 5. – С. 451-468.Slugina M.A. Transkripcionnyj faktor RIPENING INHIBITOR i ego gomologi v regulyacii sozrevaniya sochnogo ploda razlichnyh vidov rastenij // Fiziologiya rastenij. – 2021. – Tom 68. – № 5. – S. 451-468.Слугина М.А., Джос Е.А., Щенникова А.В., Кочиева Е.З. Содержание сахаров в зрелом томате коррелирует с уровнем репрессии изоформы RIN2i гена Ripening inhibitor //Физиология растений. – 2021. – Том 68. - № 6. – С. 589-599.Slugina M.A., Dzhos E.A., Shchennikova A.V., Kochieva E.Z. Soderzhanie saharov v zrelom tomate korreliruet s urovnem repressii izoformy RIN2i gena Ripening inhibitor //Fiziologiya rastenij. – 2021. – Tom 68. - № 6. – S. 589-599.Кошкин Е.И., Панфилова О.Ф. Физиологические основы селекции растений. М: РГАУ-МСХА. – 2014. – 228 с.Koshkin E.I., Panfilova O.F. Fiziologicheskie osnovy selekcii rastenij. M: RGAU-MSKHA, 2014.Панфилова О.Ф., Пильщикова Н.В. Старение органов растения как реализация генетической программы развития //Субтропическое и декоративное садоводство. – 2017. – № 61. – С. 174-180.Panfilova O.F., Pil'shchikova N.V. Starenie organov rasteniya kak realizaciya geneticheskoj programmy razvitiya //Subtropicheskoe i dekorativnoe sadovodstvo. – 2017. – № 61. – S. 174-180.Панфилова О.Ф., Пильщикова Н.В. Развитие цветка и сохранение декоративных качеств цветов лилии (Lilium L.) азиатских гибридов //Субтропическое и декоративное садоводство. – 2018. – № 65. – С. 74-78.Panfilova O.F., Pil'shchikova N.V. Razvitie cvetka i sohranenie dekorativnyh kachestv cvetov lilii (Lilium L.) aziatskih gibridov //Subtropicheskoe i dekorativnoe sadovodstvo. – 2018. – № 65. – S. 74-78.Филюшин М.А., Джос Е.А., Щенникова А.В., Кочиева Е.З. Зависимость окраски плодов перца от соотношения основных пигментов и профиля экспрессии генов биосинтеза каротиноидов и антоцианов // Физиология растений. – 2020. – Том 67. –№ 6. – С. 644-653.Filyushin M.A., Dzhos E.A., Shchennikova A.V., Kochieva E.Z. Zavisimost' okraski plodov perca ot sootnosheniya osnovnyh pigmentov i profilya ekspressii genov biosinteza karotinoidov i antocianov // Fiziologiya rastenij. – 2020. – Tom 67. –№ 6. – S. 644-653.Alexander L.,Grierson D. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening // J. Exp. Bot. – 2002. V. 53. P. 2039.Alexander L., Grierson D. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening // J. Exp. Bot. – 2002. V. 53. P. 2039.Baldwin E.A., Scott J.W., Shewmaker C.K., Schuch W. Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components // Hort Science. – 2000. – V. 35. – Pp. 1013-1022.Baldwin E.A., Scott J.W., Shewmaker C.K., Schuch W. Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components // Hort Science. – 2000. – V. 35. – Pp. 1013-1022.Chang B-M., Keller M. Cuticle and skin cell walls have common and unique roles in grape berry splitting // Horticulture Research. – 2021. – V. 8. – Volume 8. – Article number: 168.Chang B-M., Keller M. Cuticle and skin cell walls have common and unique roles in grape berry splitting // Horticulture Research. – 2021. – V. 8. – Volume 8. – Article number: 168.Gambhir P., Singh V., Parida A., Raghuvanshi U., Kumar R., Sharma A.K. Ethylene response factor ERF.D7 activates auxin response factor 2 paralogs to regulate tomato fruit ripening //Plant Physiology. – 2022. – V. 190. – Issue 4. – Pp. 2775-2796.Gambhir P., Singh V., Parida A., Raghuvanshi U., Kumar R., Sharma A.K. Ethylene response factor ERF.D7 activates auxin response factor 2 paralogs to regulate tomato fruit ripening //Plant Physiology. – 2022. – V. 190. – Issue 4. – Pp. 2775-2796.Gan L, Song M., Wang X., Yang N., Li H., Liu X., Li Y. Cytokinins are involved in regulation of tomato pericarp thickness and fruit size //Horticulture Research. – 2022. – V. 9. – uhab 041.Gan L, Song M., Wang X., Yang N., Li H., Liu X., Li Y. Cytokinins are involved in regulation of tomato pericarp thickness and fruit size //Horticulture Research. – 2022. – V. 9. – uhab 041.Godoy F., Kühn N., Muñoz M., Marchandon G., Gouthu S., Deluc L., Delrot S., Lauvergeat V., Arce-Johnson P. The role of auxin during early berry development in grapevine as revealed by transcript profiling from pollination to fruit set // Horticulture Research. – 2021. – V. 8. – P. 140.Godoy F., Kühn N., Muñoz M., Marchandon G., Gouthu S., Deluc L., Delrot S., Lauvergeat V., Arce-Johnson P. The role of auxin during early berry development in grapevine as revealed by transcript profiling from pollination to fruit set // Horticulture Research. – 2021. – V. 8. – P. 140.He H., Yamamuro Ch. Interplays between auxin and GA signaling coordinate early fruit development // Horticulture Research. – 2022. – V. 9. – uhab 078.He H., Yamamuro Ch. Interplays between auxin and GA signaling coordinate early fruit development // Horticulture Research. – 2022. – V. 9. – uhab 078.Huang X.-Yu, Wang Ch.-K., Zhao Yu-W., Sun C.-H., Hu D.-G. Mechanisms and regulation of organic acid accumulation in plant vacuoles // Horticulture Research. – 2021. – V. 8. – P. 227.Huang X.-Yu, Wang Ch.-K., Zhao Yu-W., Sun C.-H., Hu D.-G. Mechanisms and regulation of organic acid accumulation in plant vacuoles // Horticulture Research. – 2021. – V. 8. – P. 227.Jiang F., Lopez A., Jeon Sh., Tonetto de Freitas S., Yu Q., Wu Z., Labavitch J.M., Tian Sh., Powell A.L.T. Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking //Horticulture Research. – 2019. – V. 6. – Article number: 17.Jiang F., Lopez A., Jeon Sh., Tonetto de Freitas S., Yu Q., Wu Z., Labavitch J.M., Tian Sh., Powell A.L.T. Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking //Horticulture Research. – 2019. – V. 6. – Article number: 17.Kokalj D., Zlatić E., Kobav B.,Vidrih R. Postharvest flavonol and anthocyanin accumulation in three apple cultivars in response to blue-light-emitting diode light // Scientia Horticulturae. – 2019. – V. 257. – 108711.Kokalj D., Zlatić E., Kobav B.,Vidrih R. Postharvest flavonol and anthocyanin accumulation in three apple cultivars in response to blue-light-emitting diode light // Scientia Horticulturae. – 2019. – V. 257. – 108711.Leszczuk A., Kalaitzis P., Blazakis K.N., Zdunek A. The role of arabinogalactan proteins (AGPs) in fruit ripening – a review //Horticulture Research. – 2020. – V. 7. – Article number: 176.Leszczuk A., Kalaitzis P., Blazakis K.N., Zdunek A. The role of arabinogalactan proteins (AGPs) in fruit ripening – a review //Horticulture Research. – 2020. – V. 7. – Article number: 176.Li B.-J., Grierson D., Shi Y., Chen K.-S. Roles of abscisic acid in regulating ripening and quality of strawberry, a model non-climacteric fruit // Horticulture Research. – 2022. – V. 9.– uhaс 089.Li B.-J., Grierson D., Shi Y., Chen K.-S. Roles of abscisic acid in regulating ripening and quality of strawberry, a model non-climacteric fruit // Horticulture Research. – 2022. – V. 9.– uhaс 089.Li M., Galimba K.D., Xiao Y., Dardick Ch., Mount S.M., Callahan A., Lui Z. Comparative transcriptomic analysis of apple and peach fruits: insights into fruit type specification //The Plant Journal. – 2021.– V. 109. – Issue 6. – Pp. 1614-1629.Li M., Galimba K.D., Xiao Y., Dardick Ch., Mount S.M., Callahan A., Lui Z. Comparative transcriptomic analysis of apple and peach fruits: insights into fruit type specification //The Plant Journal. – 2021.– V. 109. – Issue 6. – Pp. 1614-1629.Li T., Dai Z., Zeng B., Li J., Ouyang J., Kang L., Wang W., Jia W. Autocatalytic biosynthesis of abscisic acid and its synergistic action with auxin to regulate strawberry fruit ripening // Horticulture Research. – 2022. – V. 9. – uhab 076.Li T., Dai Z., Zeng B., Li J., Ouyang J., Kang L., Wang W., Jia W. Autocatalytic biosynthesis of abscisic acid and its synergistic action with auxin to regulate strawberry fruit ripening // Horticulture Research. – 2022. – V. 9. – uhab 076.Li X., Wang X., Zhang Y., Zhang A., You Ch.-X. Regulation of fleshy fruit ripening: from transcription factors to epigenetic modifications // Horticulture Research. – 2022. – V. 9. – uhaс 013.Li X., Wang X., Zhang Y., Zhang A., You Ch.-X. Regulation of fleshy fruit ripening: from transcription factors to epigenetic modifications // Horticulture Research. – 2022. – V. 9. – uhaс 013.Menzel Ch. M. A review of fruit development in strawberry: high temperatures accelerate flower development and decrease the size of the flowers and fruit // The Journal of Horticultural Science and Biotechnology. – 2023. – Published online: 05 Feb 2023.Menzel Ch. M. A review of fruit development in strawberry: high temperatures accelerate flower development and decrease the size of the flowers and fruit // The Journal of Horticultural Science and Biotechnology. – 2023. – Published online: 05 Feb 2023.Ntagkas N., Woltering E., Nicole C., Labrie C., Marcelis L.F.M. Light regulation of vitamin C in tomato fruit is mediated through photosynthesis // Environ. Exp. Bot. – 158. – PP. 180 – 188.Ntagkas N., Woltering E., Nicole C., Labrie C., Marcelis L.F.M. Light regulation of vitamin C in tomato fruit is mediated through photosynthesis // Environ. Exp. Bot. – 158. – PP. 180 – 188.Pesaresi P., Mizzotti C., Colombo M., Masiero S. Genetic regulation and structural changes during tomato fruit development and ripening // Front. Plant Sci. – 2014. - № 5. – P. 124.Pesaresi P., Mizzotti C., Colombo M., Masiero S. Genetic regulation and structural changes during tomato fruit development and ripening // Front. Plant Sci. – 2014. - № 5. – P. 124.Quinet M., Angosto T., Yuste-Lisbona F. J., Blanchard- Gros R., Bigot S., Martinez J. P., Lutts S. Tomato Fruit Development and Metabolism // Front. Plant Sci. – 2019. – V. 10. – P. 1554.Quinet M., Angosto T., Yuste-Lisbona F. J., Blanchard- Gros R., Bigot S., Martinez J. P., Lutts S. Tomato Fruit Development and Metabolism // Front. Plant Sci. – 2019. – V. 10. – P. 1554.Rambla J.L., Tikunov Y.M., Monforte A.J., Bovy A.G., Granell A. The expanded tomato fruit volatile landscape // J. Exp. Bot. – 2014. – V. 65. – Pp. 4613-4623.Rambla J.L., Tikunov Y.M., Monforte A.J., Bovy A.G., Granell A. The expanded tomato fruit volatile landscape // J. Exp. Bot. – 2014. – V. 65. – Pp. 4613-4623.Rossi F., Manfrini L., Venturi M., Grappadelli L.C., Morandi B. Fruit transpiration drives interspecific variability in fruit growth strategies // Horticulture Research. – V. 9. – 2022. – uhac 036.Rossi F., Manfrini L., Venturi M., Grappadelli L.C., Morandi B. Fruit transpiration drives interspecific variability in fruit growth strategies // Horticulture Research. – V. 9. – 2022. – uhac 036.Shipman E.N., Yu J., Zhou J., Albornoz K., Beckles D.M. Can gene editing reduce postharvest waste and loss of fruit, vegetables, and ornamentals? // Horticulture Research. – 2019. – V.8. – P.1.Shipman E.N., Yu J., Zhou J., Albornoz K., Beckles D.M. Can gene editing reduce postharvest waste and loss of fruit, vegetables, and ornamentals? // Horticulture Research. – 2019. – V.8. – P.1.Tian Z. Anatomical and Transcriptomic Comparison Between Small and Large Fruit Size During Fruit Development in Apple // The 9th International Horticulture Research Conference. – 2022. – Wuhan, China. – doi:10.48130/IHRC2022-pst-0405.Tian Z. Anatomical and Transcriptomic Comparison Between Small and Large Fruit Size During Fruit Development in Apple // The 9th International Horticulture Research Conference. – 2022. – Wuhan, China. – doi:10.48130/IHRC2022-pst-0405.Vrebalov J., Ruezinsky D., Padmanabhan V., White R., Medrano D., Drake R. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. //Science. – 2002.- V. 296. – Pp. 343-346.Vrebalov J., Ruezinsky D., Padmanabhan V., White R., Medrano D., Drake R. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. //Science. – 2002.- V. 296. – Pp. 343-346.Wada H., Nakata K., Nonami H., Erra-Balsells R., Tatsuki M., Hatakeyama Y., Tanaka F. Direct evidence for dynamics of cell heterogeneity in watercored apples: turgor-associated metabolic modifications and within-fruit water potential gradient unveiled by single-cell analyses // Horticulture Research. – 2021. – V. 8. – P. 187.Wada H., Nakata K., Nonami H., Erra-Balsells R., Tatsuki M., Hatakeyama Y., Tanaka F. Direct evidence for dynamics of cell heterogeneity in watercored apples: turgor-associated metabolic modifications and within-fruit water potential gradient unveiled by single-cell analyses // Horticulture Research. – 2021. – V. 8. – P. 187.Wang Sh., Li L.-X., Zhang Z., Fang Y., Li D.,Chen X.-S., Feng Sh.-Q. Ethylene precisely regulates anthocyanin synthesis in apple via a module comprising MdEIL1, MdMYB1 and MdMYB17 // Horticulture Research. – 2022. – V. 9. – uhac 34.Wang Sh., Li L.-X., Zhang Z., Fang Y., Li D.,Chen X.-S., Feng Sh.-Q. Ethylene precisely regulates anthocyanin synthesis in apple via a module comprising MdEIL1, MdMYB1 and MdMYB17 // Horticulture Research. – 2022. – V. 9. – uhac 34.Wang Y., Hao Y., Zhou, D., Pan L., Tu K. Differences in commercial quality and carotenoids profile of yellow-and white-fleshed nectarine fruit during low temperature storage and the regulation of carotenoids by sugar. //Postharvest Biology and Technology. – 2023. – V. 197. – 112206.Wang Y., Hao Y., Zhou, D., Pan L., Tu K. Differences in commercial quality and carotenoids profile of yellow-and white-fleshed nectarine fruit during low temperature storage and the regulation of carotenoids by sugar. //Postharvest Biology and Technology. – 2023. – V. 197. – 112206.Xia H.,Wang X., Su W., Jiang L.,Lin L.,Deng Q., Wang J.,Deng H., Hu R., Liao M., Liang D. Changes in the carotenoids profile of two yellow-fleshed kiwifruit cultivars during storage // Postharvest Biology and Technology. – 2020. – V.164. – 111162.Xia H.,Wang X., Su W., Jiang L.,Lin L.,Deng Q., Wang J.,Deng H., Hu R., Liao M., Liang D. Changes in the carotenoids profile of two yellow-fleshed kiwifruit cultivars during storage // Postharvest Biology and Technology. – 2020. – V.164. – 111162.Zhong H., Liu Z., Zhang F., Zhou X., Sun X., Li Y., Liu W., Xiao, H. Wang N., Lu H. Metabolomic and transcriptomic analyses reveal the effects of self- and hetero-grafting on anthocyanin biosynthesis in grapevine. // Horticulture Research. – 2022. – V. 9. – uhac103.Zhong H., Liu Z., Zhang F., Zhou X., Sun X., Li Y., Liu W., Xiao, H. Wang N., Lu H. Metabolomic and transcriptomic analyses reveal the effects of self- and hetero-grafting on anthocyanin biosynthesis in grapevine. // Horticulture Research. – 2022. – V. 9. – uhac103.

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