Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways
Sucrose (Suc) accumulation is one of the key indicators of leaf senescence onset, but little is known about its regulatory role. Here, we found that application of high (120–150 mM) and low levels (60 mM) of Suc to young leaf (YL) and fully expanded leaf (FEL) discs, respectively, decreased chloroph...
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| Format: | Article |
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2022-06-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/12/6498 |
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| author | Muhammad Asim Quaid Hussain Xiaolin Wang Yanguo Sun Haiwei Liu Rayyan Khan Shasha Du Yi Shi Yan Zhang |
| author_facet | Muhammad Asim Quaid Hussain Xiaolin Wang Yanguo Sun Haiwei Liu Rayyan Khan Shasha Du Yi Shi Yan Zhang |
| author_sort | Muhammad Asim |
| collection | DOAJ |
| description | Sucrose (Suc) accumulation is one of the key indicators of leaf senescence onset, but little is known about its regulatory role. Here, we found that application of high (120–150 mM) and low levels (60 mM) of Suc to young leaf (YL) and fully expanded leaf (FEL) discs, respectively, decreased chlorophyll content and maximum photosynthetic efficiency. Electrolyte leakage and malondialdehyde levels increased at high Suc concentrations (90–120 mM in YL and 60 and 150 mM in FEL discs). In FEL discs, the senescence-associated gene <i>NtSAG12</i> showed a gradual increase in expression with increased Suc application; in contrast, in YL discs, <i>NtSAG12</i> was upregulated with low Suc treatment (60 mM) but downregulated at higher levels of Suc. In YL discs, trehalose-6-phosphate (T6P) accumulated at a low half-maximal effective concentration (EC50) of Suc (1.765 mM). However, T6P levels declined as trehalose 6 phosphate synthase (TPS) content decreased, resulting in the maximum velocity of sucrose non-fermenting-1-related protein kinase (SnRK) and hexokinase (HXK) occurring at higher level of Suc. We therefore speculated that senescence was induced by hexose accumulation. In FEL discs, the EC50 of T6P occurred at a low concentration of Suc (0.9488 mM); T6P levels progressively increased with higher TPS content, which inhibited SnRK activity with a dissociation constant (<i>K<sub>d</sub></i>) of 0.001475 U/g. This confirmed that the T6P–SnRK complex induced senescence in detached FEL discs. |
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| last_indexed | 2024-03-09T23:35:09Z |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-7706e41a6ec7471eb27bfb8d1c42c07a2023-11-23T17:01:45ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-06-012312649810.3390/ijms23126498Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling PathwaysMuhammad Asim0Quaid Hussain1Xiaolin Wang2Yanguo Sun3Haiwei Liu4Rayyan Khan5Shasha Du6Yi Shi7Yan Zhang8Key Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaState Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, 666 Wusu Street, Hangzhou 311300, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaKey Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaSucrose (Suc) accumulation is one of the key indicators of leaf senescence onset, but little is known about its regulatory role. Here, we found that application of high (120–150 mM) and low levels (60 mM) of Suc to young leaf (YL) and fully expanded leaf (FEL) discs, respectively, decreased chlorophyll content and maximum photosynthetic efficiency. Electrolyte leakage and malondialdehyde levels increased at high Suc concentrations (90–120 mM in YL and 60 and 150 mM in FEL discs). In FEL discs, the senescence-associated gene <i>NtSAG12</i> showed a gradual increase in expression with increased Suc application; in contrast, in YL discs, <i>NtSAG12</i> was upregulated with low Suc treatment (60 mM) but downregulated at higher levels of Suc. In YL discs, trehalose-6-phosphate (T6P) accumulated at a low half-maximal effective concentration (EC50) of Suc (1.765 mM). However, T6P levels declined as trehalose 6 phosphate synthase (TPS) content decreased, resulting in the maximum velocity of sucrose non-fermenting-1-related protein kinase (SnRK) and hexokinase (HXK) occurring at higher level of Suc. We therefore speculated that senescence was induced by hexose accumulation. In FEL discs, the EC50 of T6P occurred at a low concentration of Suc (0.9488 mM); T6P levels progressively increased with higher TPS content, which inhibited SnRK activity with a dissociation constant (<i>K<sub>d</sub></i>) of 0.001475 U/g. This confirmed that the T6P–SnRK complex induced senescence in detached FEL discs.https://www.mdpi.com/1422-0067/23/12/6498sucrose concentrationsugar signaling dynamicsglucosetrehalose-6-phosphate<i>SnRK1</i>senescence |
| spellingShingle | Muhammad Asim Quaid Hussain Xiaolin Wang Yanguo Sun Haiwei Liu Rayyan Khan Shasha Du Yi Shi Yan Zhang Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways International Journal of Molecular Sciences sucrose concentration sugar signaling dynamics glucose trehalose-6-phosphate <i>SnRK1</i> senescence |
| title | Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways |
| title_full | Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways |
| title_fullStr | Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways |
| title_full_unstemmed | Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways |
| title_short | Mathematical Modeling Reveals That Sucrose Regulates Leaf Senescence via Dynamic Sugar Signaling Pathways |
| title_sort | mathematical modeling reveals that sucrose regulates leaf senescence via dynamic sugar signaling pathways |
| topic | sucrose concentration sugar signaling dynamics glucose trehalose-6-phosphate <i>SnRK1</i> senescence |
| url | https://www.mdpi.com/1422-0067/23/12/6498 |
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