外源硫化氢对盐碱胁迫下裸燕麦光合碳代谢的调控

doi:10.17521/cjpe.2022.0032

摘要/Abstract

摘要：

为探讨外源H₂S对盐碱胁迫下植物光合碳代谢的调控效应, 采用盆栽土培实验, 以裸燕麦(Avena nuda)为材料, 研究喷施50 µmol·L⁻¹H₂S供体硫氢化钠(NaHS)溶液对3.00 g·kg^-1盐碱胁迫下叶片光合和荧光参数, 单糖、寡糖和淀粉含量, 卡尔文循环和糖代谢关键酶活性及产量构成因素的影响。结果表明: (1)盐碱胁迫下喷施NaHS显著降低裸燕麦叶片叶绿素含量、胞间CO₂浓度、光系统II (PSII)初始荧光、最大荧光、调节性能量耗散量子产量、光化学荧光淬灭和非光化学淬灭, 显著提高Hill反应活力、净光合速率、蒸腾速率、气孔导度、表观CO₂利用效率、PSII最大光化学效率和核酮糖1,5-二磷酸羧化酶(Rubisco)、Rubisco活化酶、3-磷酸甘油醛脱氢酶和转酮醇酶活性。说明外源H₂S通过减少光能吸收和降低PSII天线色素吸收光能用于光化学电子传递份额、提高原初光能转化效率和促进水的光解、调控卡尔文循环关键酶活性和增强CO₂利用效率缓解盐碱胁迫诱导的光抑制和光合速率下降。(2)盐碱胁迫下喷施NaHS后第7天, 裸燕麦叶片α-淀粉酶和蔗糖磷酸合成酶活性显著提高, 淀粉、还原糖含量和中性转化酶活性显著降低; 第14天, 可溶性总糖、还原糖含量和蔗糖合成酶、蔗糖磷酸合成酶活性显著下降, 中性转化酶活性显著提高; 第7天和第14天葡萄糖、果糖、半乳糖含量不同程度提高, 棉子糖含量显著下降, 而总淀粉酶、β-淀粉酶、淀粉磷酸化酶、腺苷二磷酸葡萄糖焦磷酸化酶、酸性转化酶活性和岩藻糖、海藻糖、蔗糖含量无显著变化。这表明外源H₂S参与盐碱胁迫下裸燕麦淀粉和蔗糖代谢及多糖和低聚糖之间转化的调控。(3)喷施NaHS对盐碱胁迫下裸燕麦的株高、穗数、穗铃数、千粒质量和生物学产量无显著影响, 而穗粒数和籽粒产量显著提高。综上所述, 外源H₂S参与盐碱胁迫下裸燕麦光合碳代谢调控, 它能够增强裸燕麦对盐碱胁迫的耐性。

关键词: 硫化氢, 裸燕麦, 盐碱胁迫, 光合参数, 荧光参数, 碳代谢, 产量构成

Abstract:

Aims The purpose of this study was to investigate the regulatory effect of exogenous H₂S on the photosynthetic carbon metabolism of plants under saline-alkali stress.

Methods The Avena nude was selected and a potted soil culture experiment was conducted to study the effects of spraying 50 µmol·L⁻¹ H₂S donor sodium hydrosulfide (NaHS) solution on photosynthetic and fluorescence parameters, the contents of monosaccharides, oligosaccharides and starch, the activities of key enzymes in Calvin cycle and sugar metabolism in leaves, and yield components under 3.00 g·kg^-1 saline-alkali stress.

Important findings (1) Spraying NaHS significantly decreased chlorophyll content, intercellular CO₂ concentration, photosystem II (PSII) initial fluorescence, maximum fluorescence, regulatory energy dissipation, photochemical quenching, non-photochemical quenching, and significantly increased Hill reaction activity, net photosynthetic rate, transpiration rate, stomatal conductance, apparent CO₂ utility efficiency, PSII maximum photochemical efficiency, and the activities of ribulose-1,5-bisphophate carboxylase (Rubisco), Rubisco activase, glyceraldehyde-3-phosphate dehydrogenase and transketolase in A. nude leaves under salt-alkali stress. These indicated that exogenous H₂S could alleviate saline-alkali stress-induced photoinhibition and photosynthetic rate decrease by reducing light energy absorption and the portion of light energy absorbed by the PSII antenna pigment which was used for photochemical electron transfer, improving primary photochemical efficiency and promoting water photolysis of PSII, regulating key enzyme activities in the Calvin cycle, and enhancing CO₂ utility efficiency. (2) Under saline-alkali stress, the activities of α-amylase and sucrose phosphate synthase were significantly increased and the contents of starch and reducing sugar and neutral invertase activities were significantly decreased in A. nude leaves on the 7th day after spraying NaHS. On the 14th day, the contents of total soluble sugar and reducing sugar, and the activities of sucrose synthase and sucrose phosphate synthase decreased significantly, and the activity of neutral invertase increased significantly. The contents of glucose, fructose and galactose on the 7th and 14th days increased to varying degrees, and the content of raffinose decreased significantly, while the activities of total amylase, β-amylase, starch phosphorylase, adenosine diphosphate glucose pyrophosphorylase and acid invertase and the contents of fucose, trehalose and sucrose did not change significantly. These changes suggested that exogenous H₂S was involved in the regulation of starch and sucrose metabolism and the conversion between polysaccharides and oligosaccharides in A. nude under saline-alkali stress. (3) Spraying NaHS had no significant effect on plant height, spike numbers per plant, boll numbers per spike, thousand-grain weight and biological yield per plant of A. nude under salt-alkali stress, while grain numbers per spike and grain yield per plant were increased significantly. In summary, exogenous H₂S participates in the regulation of photosynthetic carbon metabolism in A. nude under salt-alkali stress, and it can enhance the tolerance of A. nude to saline-alkali stress.

Key words: hydrogen sulfide, Avena nude, saline-alkali stress, photosynthetic parameter, fluorescence parameter, carbon metabolism, yield component

刘建新, 刘瑞瑞, 刘秀丽, 贾海燕, 卜婷, 李娜. 外源硫化氢对盐碱胁迫下裸燕麦光合碳代谢的调控. 植物生态学报, 2023, 47(3): 374-388. DOI: 10.17521/cjpe.2022.0032

LIU Jian-Xin, LIU Rui-Rui, LIU Xiu-Li, JIA Hai-Yan, BU Ting, LI Na. Regulation of exogenous hydrogen sulfide on photosynthetic carbon metabolism in Avena nude under saline-alkaline stress. Chinese Journal of Plant Ecology, 2023, 47(3): 374-388. DOI: 10.17521/cjpe.2022.0032

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0032

https://www.plant-ecology.com/CN/Y2023/V47/I3/374

图/表 9

图1 外源H2S对盐碱胁迫下裸燕麦叶片SPAD值(A)和Hill反应活力(B)的影响(平均值±标准差)。CK, 对照; NaHS, 单独喷NaHS; SA, 盐碱胁迫下喷蒸馏水; SA + NaHS, 盐碱胁迫下喷NaHS。不同小写字母表示同一时间不同处理间差异显著(p < 0.05)。

Fig. 1 Effect of exogenous H2S on the SPAD value (A) and Hill’s reaction activity (B) in Avena nude leaves under saline-alkali stress (mean ± SD). CK, control; NaHS, spraying NaHS only; SA, spraying water under salt-alkali stress; SA + NaHS, spraying NaHS under salt-alkali stress. Different lowercase letters indicate significant differences among treatments for the same time (p < 0.05).

图2 外源H2S对盐碱胁迫下裸燕麦叶片光合气体交换参数的影响(平均值±标准差)。CK, 对照; NaHS, 单独喷NaHS; SA, 盐碱胁迫下喷蒸馏水; SA + NaHS, 盐碱胁迫下喷NaHS。不同小写字母表示同一时间不同处理间差异显著(p < 0.05)。

Fig. 2 Effect of exogenous H2S on photosynthetic gas exchange parameters in Avena nude leaves under saline-alkali stress (mean ± SD). CK, control; NaHS, spraying NaHS only; SA, spraying water under salt-alkali stress; SA + NaHS, spraying NaHS under salt-alkali stress. Ci, intercellular CO2 concentration; CUE, apparent CO2 utility efficiency; Gs, stomatal conductance; Ls, stomatal limitation value; Pn, net photosynthetic rate; Tr, transpiration rate. Different lowercase letters indicate significant differences among treatments at the same time (p < 0.05).

表1 外源H2S对盐碱胁迫下裸燕麦叶片叶绿素荧光参数的影响(平均值±标准差)

Table 1 Effect of exogenous H2S on the chlorophyll fluorescence parameters in leaves of Avena nude under saline-lkali stress (mean± SD)

图3 外源H2S对盐碱胁迫下裸燕麦叶片卡尔文循环关键酶活性的影响(平均值±标准差)。CK, 对照; NaHS, 单独喷NaHS; SA, 盐碱胁迫下喷蒸馏水; SA + NaHS, 盐碱胁迫下喷NaHS。FBA, 果糖-1,6-二磷酸醛缩酶; GAPDH, 3-磷酸甘油醛脱氢酶; RCA, Rubisco活化酶; Rubisco, 核酮糖-1,5-二磷酸羧化酶; SBPase, 景天庚酮糖-1,7-二磷酸酶; TK, 转酮醇酶。不同小写字母表示同一时间不同处理间差异显著(p < 0.05)。

Fig. 3 Effect of exogenous H2S on the activities of key enzymes in Calvin cycle in Avena nude leaves under saline-alkali stress (mean ± SD). CK, control; NaHS, spraying NaHS only; SA, spraying water under salt-alkali stress; SA + NaHS, spraying NaHS under salt-alkali stress. FBA, fructose-1,6-bisphosphate aldolase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; RCA, Rubisco activase; Rubisco, ribulose-1,5-bisphophate carboxylase; SBPase, sedoheptulose-1,7-bisphosphatase; TK, transketolase. Different lowercase letters indicate significant differences among treatments at the same time (p < 0.05).

表2 外源H2S对盐碱胁迫下裸燕麦叶片不同类型糖含量的影响(平均值±标准差)

Table 2 Effect of exogenous H2S on the contents of different sugars in leaves of Avena nude under saline-alkali stress (mean ±SD)

图4 外源H2S对盐碱胁迫下裸燕麦叶片淀粉和蔗糖代谢酶活性的影响(平均值±标准差)。ADPG, 腺苷二磷酸葡萄糖。CK, 对照; NaHS, 单独喷NaHS; SA, 盐碱胁迫下喷蒸馏水; SA + NaHS, 盐碱胁迫下喷NaHS。不同小写字母表示同一时间不同处理间差异显著(p < 0.05)。

Fig. 4 Effect of exogenous H2S on the metabolic enzyme activities of starch and sucrose in Avena nude leaves under saline-alkali stress (mean ± SD). ADPG, adenosine diphosphate glucose. CK, control; NaHS, spraying NaHS only; SA, spraying water under salt-alkali stress; SA + NaHS, spraying NaHS under salt-alkali stress. Different lowercase letters indicate significant differences among treatments at the same time (p < 0.05).

表3 外源H2S对盐碱胁迫下裸燕麦生长和产量性状的影响(平均值±标准差)

Table 3 Effect of exogenous H2S on the growth and yield traits of Avena nudes under saline-alkali stress (mean±SD)

图5 不同处理下裸燕麦叶片光合碳代谢隐结构正交投影判别分析(OPLS-DA)得分图及200次模型的置换检验。CK, 对照; NaHS, 单独喷NaHS; SA, 盐碱胁迫下喷蒸馏水; SA + NaHS, 盐碱胁迫下喷NaHS。

Fig. 5 Orthogonal projection to latent structure-discriminant analysis (OPLS-DA) score plot of photosynthetic carbon metabolism in leaves of Avena nude under different treatments and 200 permutation tests of the model. CK, control; NaHS, spraying NaHS only; SA, spraying water under salt-alkali stress; SA + NaHS, spraying NaHS under salt-alkali stress.

图6 不同处理下裸燕麦光合碳代谢隐结构正交投影判别分析(OPLS-DA)得分图(A、B、C)和变量投射重要度(VIP)图(平均值±标准差) (D、E、F)。CK, 对照; NaHS, 单独喷NaHS; SA, 盐碱胁迫下喷蒸馏水; SA + NaHS, 盐碱胁迫下喷NaHS。 Acid inver, 酸性转化酶; ADPG pyrop, 腺苷二磷酸葡萄糖焦磷酸化酶; α-amylase, α-淀粉酶; β-amylase, β-淀粉酶; α+β-amylas, (α+β)-淀粉酶; Ci, 胞间CO2浓度; CUE, 表观CO2利用效率; ETR, 电子传递速率; FBA, 果糖-1,6-二磷酸醛缩酶; Fm, 最大荧光; Fo, 初始荧光; Fru, 果糖; Fuc, 岩藻糖; Fv/Fm, 最大光化学效率; Fv′/Fm′, 有效光量子产量; Gal, 半乳糖; GAPDH, 3-磷酸甘油醛脱氢酶; Glc, 葡萄糖; Gs, 气孔导度; Hill, Hill反应活力; Ls, 气孔限制值; Neutral in, 中性转化酶; NPQ, 非光化学淬灭系数; Pn, 净光合速率; qL,光化学淬灭系数; Raf, 棉子糖; RCA, Rubisco活化酶; Reducing s, 还原性糖; Rubisco, 核酮糖-1,5-二磷酸羧化酶; SBPase, 景天庚酮糖-1,7-二磷酸酶; Soluble su, 可溶性糖; SPAD, 叶绿素相对含量; Starch, 淀粉; Starch pho, 淀粉磷酸化酶; Suc, 蔗糖; Sucrose sy, 蔗糖合成酶; Sucroseph, 蔗糖磷酸合成酶; TK, 转酮醇酶; Tr, 蒸腾速率; Tre, 海藻糖; Y(NO), 非调节性能量耗散量子产量; Y(NPQ), 调节性能量耗散量子产量; Y(II), 实际光化学量子产量。7和14分别表示第7天和第14天。

Fig. 6 Orthogonal projection to latent structure-discriminant analysis (OPLS-DA) score plot (A, B, C) and varibale importance for the projection (VIP)-plot (mean ± SD) (D, E, F) of photosynthetic carbon metabolism in leaves of Avena nude under different treatment. CK, control; NaHS, spraying NaHS only; SA, spraying water under salt-alkali stress; SA + NaHS, spraying NaHS under salt-alkali stress. Acid inver, acid invertase; ADPG pyrop, adenosine diphosphate glucose pyrophosphorylase; α+β-amylas, (α+β)-amylase; Ci, intercellular CO2 concentration; CUE, apparent CO2 utility efficiency; ETR, electron transport rate; FBA, fructose-1,6-bisphosphate aldolase; Fm, maximum fluorescence; Fo, initial fluorescence; Fru, fructose; Fuc, fucose; Fv/Fm, maximum photochemical efficiency; Fv′/Fm′, effective light quantum yield; Gal, galactose; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; Glc, glucose; Gs, stomatal conductance; Hill, Hill’s reaction activity; Ls, stomatal limitation value; Neutral in, neutral invertase; NPQ, non-photochemical quenching coefficient; Pn, net photosynthetic rate; qL, photochemical quenching coefficient; Raf, raffinose; RCA, Rubisco activase; Reducing s, reducing sugar; Rubisco, ribulose-1,5-bisphophate carboxylase; SBPase, sedoheptulose-1,7-bisphosphatase; Soluble su, soluble sugar; SPAD, chlorophyll relative content; Starch pho, starch phosphorylase; Suc, sucrose; Sucrose sy, sucrose synthase; Sucrose ph, sucrose phosphate synthase; TK, transketolase; Tr, transpiration rate; Tre, trehalose; Y(NO), non-adjusting energy dissipation quantum yield; Y(NPQ), adjusting energy dissipation quantum yield; Y(II), actual photochemical quantum yield. 7 and 14 represent the 7th and 14th day, respectively.

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