ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress
With global climate change, the frequency and intensity of waterlogging events are increasing due to frequent and heavy precipitation. Little is known however about the response of plants to repeated waterlogging stress events. The aim is to clarify physiological regulation mechanisms of tomato plan...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-08-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1238108/full |
| _version_ | 1797736041774317568 |
|---|---|
| author | Lifei Niu Fangling Jiang Jian Yin Yinlei Wang Yankai Li Xiaqing Yu Xiaoming Song Carl-Otto Ottosen Eva Rosenqvist Ron Mittler Zhen Wu Rong Zhou Rong Zhou |
| author_facet | Lifei Niu Fangling Jiang Jian Yin Yinlei Wang Yankai Li Xiaqing Yu Xiaoming Song Carl-Otto Ottosen Eva Rosenqvist Ron Mittler Zhen Wu Rong Zhou Rong Zhou |
| author_sort | Lifei Niu |
| collection | DOAJ |
| description | With global climate change, the frequency and intensity of waterlogging events are increasing due to frequent and heavy precipitation. Little is known however about the response of plants to repeated waterlogging stress events. The aim is to clarify physiological regulation mechanisms of tomato plants under repeated waterlogging stress, and whether Trichoderma harzianum can alleviate waterlogging injury. We identified two genotypes of tomato, ‘MIX-002’ and ‘LA4440’, as waterlogging tolerant and sensitive genotypes, respectively, based on plant biomass accumulation. The two tomato genotypes were subjected to a waterlogging priming treatment for 2 days (excess water for 1 cm above substrate surface) followed by a recovery stage for 2 days, and then a second waterlogging stress for 5 days (excess water for 1 cm above substrate surface) followed by a second recovery stage for 3 days. Leaf physiological, plant growth parameters, and the expression of five key genes were investigated. We found that the two genotypes responded differently to waterlogging priming and stress in terms of photosynthesis, reactive oxygen species (ROS), and osmotic regulatory mechanisms. Waterlogging stress significantly increased H2O2 content of ‘MIX-002’, while that of ‘LA4440’ had no significant change. Under waterlogging stress, photosynthesis of the two genotypes treated with waterlogging priming returned to the control level. However, Trichoderma harzianum treatment during the second recovery stage did not show positive mitigative effects. The plants of ‘LA4440’ with priming showed lower peroxidase (POD) activity and proline content but higher H2O2 content than that without priming under waterlogging stress. Under waterlogging stress with priming as compared to without priming, SODCC2 was downregulated in two tomatoes, and AGR2 and X92888 were upregulated in ‘MIX-002’ but downregulated in ‘LA4440’. Overall, the two tomato genotypes exhibited distinct photosynthetic, ROS and osmotic regulatory mechanisms responding to the waterlogging stress. Waterlogging priming can induce stress memory by adjusting stomatal conductance, sustaining ROS homeostasis, regulating osmotic regulatory substances and key gene expressions mediated by H2O2, and thus alleviate the damage on tomato photosynthesis when waterlogging reoccurred. |
| first_indexed | 2024-03-12T13:07:51Z |
| format | Article |
| id | doaj.art-efca72ed806b444c8a8cad3dc8cdd156 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-12T13:07:51Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-efca72ed806b444c8a8cad3dc8cdd1562023-08-28T12:58:25ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.12381081238108ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stressLifei Niu0Fangling Jiang1Jian Yin2Yinlei Wang3Yankai Li4Xiaqing Yu5Xiaoming Song6Carl-Otto Ottosen7Eva Rosenqvist8Ron Mittler9Zhen Wu10Rong Zhou11Rong Zhou12College of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaCollege of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaCollege of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaVegetable Institute, Jiangsu Academy of Agriculture Science, Nanjing, Jiangsu, ChinaCollege of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaCollege of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaCollege of Life Sciences, North China University of Science and Technology, Tangshan, Hebei, ChinaDepartment of Food Science, Aarhus University, Aarhus, DenmarkDepartment of Plant and Environmental Sciences, University of Copenhagen, Taastrup, DenmarkDivision of Plant Science and Technology, College of Agriculture, Food and Natural Resources, University of Missouri, Bond Life Sciences Center, Columbia, MO, United StatesCollege of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaCollege of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaDepartment of Food Science, Aarhus University, Aarhus, DenmarkWith global climate change, the frequency and intensity of waterlogging events are increasing due to frequent and heavy precipitation. Little is known however about the response of plants to repeated waterlogging stress events. The aim is to clarify physiological regulation mechanisms of tomato plants under repeated waterlogging stress, and whether Trichoderma harzianum can alleviate waterlogging injury. We identified two genotypes of tomato, ‘MIX-002’ and ‘LA4440’, as waterlogging tolerant and sensitive genotypes, respectively, based on plant biomass accumulation. The two tomato genotypes were subjected to a waterlogging priming treatment for 2 days (excess water for 1 cm above substrate surface) followed by a recovery stage for 2 days, and then a second waterlogging stress for 5 days (excess water for 1 cm above substrate surface) followed by a second recovery stage for 3 days. Leaf physiological, plant growth parameters, and the expression of five key genes were investigated. We found that the two genotypes responded differently to waterlogging priming and stress in terms of photosynthesis, reactive oxygen species (ROS), and osmotic regulatory mechanisms. Waterlogging stress significantly increased H2O2 content of ‘MIX-002’, while that of ‘LA4440’ had no significant change. Under waterlogging stress, photosynthesis of the two genotypes treated with waterlogging priming returned to the control level. However, Trichoderma harzianum treatment during the second recovery stage did not show positive mitigative effects. The plants of ‘LA4440’ with priming showed lower peroxidase (POD) activity and proline content but higher H2O2 content than that without priming under waterlogging stress. Under waterlogging stress with priming as compared to without priming, SODCC2 was downregulated in two tomatoes, and AGR2 and X92888 were upregulated in ‘MIX-002’ but downregulated in ‘LA4440’. Overall, the two tomato genotypes exhibited distinct photosynthetic, ROS and osmotic regulatory mechanisms responding to the waterlogging stress. Waterlogging priming can induce stress memory by adjusting stomatal conductance, sustaining ROS homeostasis, regulating osmotic regulatory substances and key gene expressions mediated by H2O2, and thus alleviate the damage on tomato photosynthesis when waterlogging reoccurred.https://www.frontiersin.org/articles/10.3389/fpls.2023.1238108/fulltomatorepeated waterloggingprimingstress memoryH2O2Trichoderma harzianum |
| spellingShingle | Lifei Niu Fangling Jiang Jian Yin Yinlei Wang Yankai Li Xiaqing Yu Xiaoming Song Carl-Otto Ottosen Eva Rosenqvist Ron Mittler Zhen Wu Rong Zhou Rong Zhou ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress Frontiers in Plant Science tomato repeated waterlogging priming stress memory H2O2 Trichoderma harzianum |
| title | ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress |
| title_full | ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress |
| title_fullStr | ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress |
| title_full_unstemmed | ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress |
| title_short | ROS-mediated waterlogging memory, induced by priming, mitigates photosynthesis inhibition in tomato under waterlogging stress |
| title_sort | ros mediated waterlogging memory induced by priming mitigates photosynthesis inhibition in tomato under waterlogging stress |
| topic | tomato repeated waterlogging priming stress memory H2O2 Trichoderma harzianum |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1238108/full |
| work_keys_str_mv | AT lifeiniu rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT fanglingjiang rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT jianyin rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT yinleiwang rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT yankaili rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT xiaqingyu rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT xiaomingsong rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT carlottoottosen rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT evarosenqvist rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT ronmittler rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT zhenwu rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT rongzhou rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress AT rongzhou rosmediatedwaterloggingmemoryinducedbyprimingmitigatesphotosynthesisinhibitionintomatounderwaterloggingstress |