Combined transcriptome and physiological analysis elucidates exogenous sucrose enhance the photosynthetic capacity of foxtail millet under sugar starvation

【作者】 孙梦梦； Yongchao Li； 王家刚； 原向阳；

【Author】 Mengmeng Sun;Yongchao Li;Jia-Gang Wang;Xiangyang Yuan;College of Agriculture, Shanxi Agricultural University;Hou Ji Laboratory in Shanxi Province, Shanxi Agricultural University;State Key Laboratory of Sustainable Dryland Agriculture (in Preparation), Shanxi Agricultural University;

【机构】 College of Agriculture, Shanxi Agricultural University； Hou Ji Laboratory in Shanxi Province, Shanxi Agricultural University； State Key Laboratory of Sustainable Dryland Agriculture (in Preparation), Shanxi Agricultural University；

【摘要】 【Background】Foxtail millet(Setaria italica(L.) Beauv.) is being promoted as a novel model species for drought-tolerance research and photosynthesis due to its high tolerance to stress and smaller diploid genome. Plants continuously encounter the challenge of sugar starvation during the course of development, such as foxtail millet are unable to acquire sufficient light energy to support photosynthesis under the slight light, which lead to growth inhibition and occur sugar starvation. Sucrose plays a crucial role in plant metabolism and serves as a vital component in supporting plant growth and development. Sucrose not only serves as a storage compound, and as the primary transport form of carbohydrates, it also acts as a signaling molecule, regulating various physiological processes and responses to environmental stresses. Therefore, exogenous sucrose may alleviate sugar starvation, this experiment combined transcriptome and physiological aspects to explore the mechanism of foxtail millet responding to exogenous sucrose under sugar starvation. 【Materials and methods】 Seeds of foxtail millet cultivar Jingu21 were used in this study, cultivated in a hydroponic system for 7 days, add 100 mM sucrose or 100 mM mannitol(control) after darking(complete shading) for 24 h, then sampling in 1, 3, 6, 12, 24 h separately for transcriptome sequencing. 3-week-old foxtail millet seedlings cultivated in greenhouse were studied chlorophyll fluorescence parameters from 12 h to 96 h applying identical treatment as hydroponic cultivation. 【Results】 The results showed that a total of 1385, 583, 527, 870, 806 unique genes were detected as differentially expressed genes(DEGs) by the sucrose vs. mannitol in the 1 h, 3 h, 6 h, 12 h, 24 h, respectively. Photosynthesis-light harvesting in photosystem I, photosystem I, and DNAbinding transcription factor activity, these items enriched separately in biological process(BP), cellular component(CC), and molecular function(MF) GO categories. The KEGG pathway enrichment analysis indicated that the differentially expressed genes were associated with photosynthesis-antenna proteins, carotenoid biosynthesis, and plant hormone signal transduction. A large number of DEGs were detected, such as LHCa 1-3 and LHCb 1-6, these genes were up-regulated at all five time nodes, especially have a significant increase in 12 h. Similarly, genes encoding photosynthetic reaction center proteins(Psb and Psa) of photosystem were up-regulated. Furthermore, genes related to carotenoid synthesis were significantly up-regulated at 1 h and 24 h, such as carotenoid cleavage dioxygenase(CCD), 9-cis-epoxycarotenoid dioxygenase(NCED), zerumbone synthase(ZSD1), and phytoene synthase(PSY2). Consistent with the gene transcription level, both PS I and PSII were protected, and their relative electron transport rate(ETR) and actual photochemical quantum yield(Y) showed a significant increase after 48 h. Photochemical quenching coefficient(qP) and non-photochemical quenching coefficient(NPQ) are increased simultaneously, indicating that sucrose can improve the light energy absorption of PSII for photochemical reactions, and PSII could protect itself through heat dissipation under darkness. At the same time, the net photosynthetic rate(Pn) and transpiration rate(Tr) of sucrose plants was higher than control. The steady state level of stomatal conductance(Gs), indicative of gas exchange, was higher in sucrose plants under the darkness, whereas the intercellular CO2 concentration(Ci) was decreased, indicating that sucrose treatment had a certain promotion effect on foxtail millet photosynthesis. Additionally, the carotenoid content and chlorophyll content also increased, that showed significant differences in 96 h compared to the control. 【Conclusion】 In general, our results indicated that sucrose apparently altered a large number of gene expression patterns in the photosynthesis-related metabolic pathways. Under sugar starvation with the sucrose treatment, ETR, qP, Pn, and carotenoid content of leaf all increased significantly, which can maintain the integrity of the photosynthetic system of foxtail millet and ensure that their photosynthetic capacity remains high.更多还原

【Abstract】 【Background】Foxtail millet(Setaria italica(L.) Beauv.) is being promoted as a novel model species for drought-tolerance research and photosynthesis due to its high tolerance to stress and smaller diploid genome. Plants continuously encounter the challenge of sugar starvation during the course of development, such as foxtail millet are unable to acquire sufficient light energy to support photosynthesis under the slight light, which lead to growth inhibition and occur sugar starvation. Sucrose plays a crucial role in plant metabolism and serves as a vital component in supporting plant growth and development. Sucrose not only serves as a storage compound, and as the primary transport form of carbohydrates, it also acts as a signaling molecule, regulating various physiological processes and responses to environmental stresses. Therefore, exogenous sucrose may alleviate sugar starvation, this experiment combined transcriptome and physiological aspects to explore the mechanism of foxtail millet responding to exogenous sucrose under sugar starvation. 【Materials and methods】 Seeds of foxtail millet cultivar Jingu21 were used in this study, cultivated in a hydroponic system for 7 days, add 100 mM sucrose or 100 mM mannitol(control) after darking(complete shading) for 24 h, then sampling in 1, 3, 6, 12, 24 h separately for transcriptome sequencing. 3-week-old foxtail millet seedlings cultivated in greenhouse were studied chlorophyll fluorescence parameters from 12 h to 96 h applying identical treatment as hydroponic cultivation. 【Results】 The results showed that a total of 1385, 583, 527, 870, 806 unique genes were detected as differentially expressed genes(DEGs) by the sucrose vs. mannitol in the 1 h, 3 h, 6 h, 12 h, 24 h, respectively. Photosynthesis-light harvesting in photosystem I, photosystem I, and DNAbinding transcription factor activity, these items enriched separately in biological process(BP), cellular component(CC), and molecular function(MF) GO categories. The KEGG pathway enrichment analysis indicated that the differentially expressed genes were associated with photosynthesis-antenna proteins, carotenoid biosynthesis, and plant hormone signal transduction. A large number of DEGs were detected, such as LHCa 1-3 and LHCb 1-6, these genes were up-regulated at all five time nodes, especially have a significant increase in 12 h. Similarly, genes encoding photosynthetic reaction center proteins(Psb and Psa) of photosystem were up-regulated. Furthermore, genes related to carotenoid synthesis were significantly up-regulated at 1 h and 24 h, such as carotenoid cleavage dioxygenase(CCD), 9-cis-epoxycarotenoid dioxygenase(NCED), zerumbone synthase(ZSD1), and phytoene synthase(PSY2). Consistent with the gene transcription level, both PS I and PSII were protected, and their relative electron transport rate(ETR) and actual photochemical quantum yield(Y) showed a significant increase after 48 h. Photochemical quenching coefficient(qP) and non-photochemical quenching coefficient(NPQ) are increased simultaneously, indicating that sucrose can improve the light energy absorption of PSII for photochemical reactions, and PSII could protect itself through heat dissipation under darkness. At the same time, the net photosynthetic rate(Pn) and transpiration rate(Tr) of sucrose plants was higher than control. The steady state level of stomatal conductance(Gs), indicative of gas exchange, was higher in sucrose plants under the darkness, whereas the intercellular CO2 concentration(Ci) was decreased, indicating that sucrose treatment had a certain promotion effect on foxtail millet photosynthesis. Additionally, the carotenoid content and chlorophyll content also increased, that showed significant differences in 96 h compared to the control. 【Conclusion】 In general, our results indicated that sucrose apparently altered a large number of gene expression patterns in the photosynthesis-related metabolic pathways. Under sugar starvation with the sucrose treatment, ETR, qP, Pn, and carotenoid content of leaf all increased significantly, which can maintain the integrity of the photosynthetic system of foxtail millet and ensure that their photosynthetic capacity remains high.更多还原