摘要
当植物叶片吸收的光能超过自身利用能力时就会产生过剩光能,引发光合作用光抑制的发生。自然条件下光抑制的发生是不可避免的,因此植物在进化过程中形成了一系列光破坏防御机制,包括热耗散、环式电子传递、水-水循环以及活性氧清除系统等。这些叶绿体内部光破坏防御途径已被进行了广泛的研究,而对叶绿体外部光破坏防御途径却知之甚少。随着研究的深入,人们发现叶绿体中过剩的还原力NADPH可以通过细胞中的穿梭机制(如苹果酸-草酰乙酸穿梭机制)运输到线粒体中被交替氧化酶(AOX)呼吸途径所氧化。人们推测,逆境条件下线粒体AOX呼吸途径可以通过快速氧化叶绿体输出的过剩NADPH以防止光合电子传递链的过度还原从而缓解光合作用的光抑制。然而目前为止仍没有详细的数据证明AOX呼吸途径的光破坏防御作用,更没有文献阐明AOX呼吸途径防御植物光抑制的作用机理。本文详细验证了杂交酸模(Rumex K-1)叶片中AOX呼吸途径的光破坏防御作用并阐明了其光破坏防御的机理,同时对AOX呼吸途径的光调控机制也进行了细致的讨论。主要结果如下:
(1)抑制AOX呼吸途径后导致杂交酸模叶片光合速率受到明显的抑制。当AOX呼吸途径被抑制后叶片气孔导度并没有发生明显变化,而细胞间隙CO_2浓度却明显上升,说明AOX呼吸途径被抑制后光合碳同化的降低是由于非气孔限制造成的。高CO_2浓度下抑制AOX呼吸途径后,杂交酸模叶片的光合速率与对照一样,说明抑制AOX呼吸途径后,杂交酸模叶片光合碳同化速率的下降与光呼吸有关。
光呼吸途径中甘氨酸到丝氨酸的脱羧过程发生于线粒体中,该过程伴随着大量NADH的产生。抑制AOX呼吸途径后,NAD~+的快速周转受抑致使甘氨酸的脱羧过程受抑、甘氨酸/丝氨酸明显升高,从而限制了光呼吸的运行。抑制AOX呼吸途径后,光呼吸甘氨酸脱羧过程的抑制导致的RuBP(1,5-二磷酸核酮糖)的再生的限制可能是抑制光合碳同化的原因之一;同时过量乙醛酸已被证明可以通过降低Rubisco(核酮糖-1,5-二磷酸羧化酶/加氧酶)的活化状态来抑制光合碳同化速率,光呼吸甘氨酸脱羧过程的抑制导致的乙醛酸的积累可能是抑制光合碳同化的另一原因。
(2)光照处理后杂交酸模叶片中苹果酸-草酰乙酸穿梭机制的两种关键酶NADP-苹果酸脱氢酶(NADP-MDH)和NAD-苹果酸脱氢酶(NAD-MDH)活性以及AOX呼吸途径的活性明显升高表明叶绿体产生的过剩还原性物质通过苹果酸-草酰乙酸穿梭机制转运出了叶绿体并通过AOX呼吸途径进行了消耗。光下抑制AOX呼吸途径后,苹果酸-草酰乙酸穿梭明显下调势必造成叶绿体中还原性物质NADPH的过度积累,进一步导致光合电子传递链的过度还原和光合电子传递推动力DF_(ABS)的下降。光合电子传递推动力DF_(ABS)的下降则进一步抑制了光合线性电子传递。线性电子传递受阻必将减少跨类囊体膜质子梯度的构建,这样NPQ(非光化学淬灭)的主要组分qE(依赖跨膜质子梯度的热耗散,NPQ的快组分)的诱导受到抑制。同时,与低浓度CO_2(1mM NaHCO_3)相比,在高浓度CO_2(20mM NaHCO_3)下抑制AOX呼吸途径后,光合电子传递链的变化较小同时NPQ的变化也较小,这说明光抑制条件下AOX呼吸途径具有诱导NPQ的作用。因此,光抑制条件下AOX呼吸途径通过消耗叶绿体产生的NADPH来维持光合线性电子传递的顺利进行,继而构建跨类囊体膜质子梯度以诱导NPQ,防止过剩光能的大量产生,保护植物免遭光破坏。
(3)在弱光下,抑制AOX呼吸途径后,杂交酸模叶片的Φ_(PSⅡ)以及光合放氧速率显著性下降,非还原性Q_B显著升高,这表明,即使在弱光下,AOX呼吸途径受到抑制之后,也会导致光抑制发生。但由于环式电子传递、米勒反应以及活性氧清除机制等其它光破坏防御途径的上调,一定程度上缓解了光抑制,没有导致叶绿体内活性氧的爆发。在强光条件下,当AOX呼吸途径受到抑制时,杂交酸模叶片的光抑制更为严重,而叶绿体内其他光破坏防御机制在强光下则不能完全替代AOX的作用,最终导致叶片内活性氧的爆发。上述结果表明,在弱光下叶绿体内其它光破坏防御机制可以部分缓解由于AOX呼吸途径受抑所造成的光抑制,而在强光下,AOX呼吸途径的光破坏防御作用是叶绿体内其他光破坏防御途径所不能完全代替的。
(4)与对照相比,强光下抑制AOX呼吸途径后,杂交酸模叶片的最大光化学效率φ_(Po)、反应中心捕获的光能用于电子传递的效率ψ_0及天线吸收的光能用于电子传递的效率φ_(Eo)明显下降,说明抑制AOX呼吸途径后杂交酸模叶片受到了更严重的光抑制;然而在用D1蛋白合成抑制剂氯霉素抑制光破坏修复过程的前提下,抑制AOX呼吸途径后,杂交酸模叶片的光抑制程度与对照相比没有显著性差异,说明AOX呼吸途径并不能减轻过剩激发能对光合机构的直接破坏作用,而是通过减缓活性氧等因素对光破坏修复的抑制起作用。
(5)杂交酸模叶片中苹果酸-草酰乙酸的关键酶NADP-MDH活性在照光后1min即已达到最大活性的75%,说明光合启动过程中过剩还原性物质NADPH输出了叶绿体。当抑制AOX呼吸途径后引起了苹果酸-草酰乙酸穿梭的明显下调及P700的氧化状态的下降,说明PSI受体侧过度还原,引起了PSII反应中心的关闭和光合线性电子传递受阻。光合启动过程中,与对照相比,抑制AOX呼吸途径后杂交酸模叶片反应中心吸收的光能(ABS/RC)和反应中心捕获的光能(TR_0/RC)并未发生显著变化,说明此过程中天线对光能的吸收及反应中心对光能的捕获并未受到影响,此时线性电子传递受阻势必导致光能吸收与利用的失衡。同时由于线性电子传递受阻导致跨类囊体膜质子梯度的构建受抑,这不可避免地抑制NPQ的启动。光合启动过程中,杂交酸模叶片光能吸收和利用的失衡及NPQ诱导的抑制不可避免地使PSII反应中心过度激发从而诱导活性氧的产生。此外,与对照相比,抑制AOX呼吸途径后,叶片的光合碳同化的光诱导速率明显变慢,外施ATP后被抑制的光合碳同化的光诱导得到部分恢复,说明光合启动过程中AOX呼吸途径可以通过促进ATP的合成从而加速卡尔文相关的酶尤其是Rubisco的活化,这主要是因为AOX呼吸途径可以促进光合线性电子传递从而增加了跨类囊体膜质子梯度。因此,即使是在光合启动过程中,AOX呼吸途径也可以通过消耗光合作用产生的过剩NADPH以维持光合线性电子传递顺利进行,既可以防止光合电子传递链的过度还原和反应中心的过度激发以防止活性氧的产生,又可以促进ATP的生成,从而加速卡尔文相关的酶尤其是Rubisco的快速活化。
(6)虽然光可以诱导杂交酸模叶片AOX呼吸途径的上调,但是当用DCMU(3-(3,4-二氯苯基)-1,1-二甲基脲)抑制光合电子从Q_A到Q_B的传递后,光却未能诱导AOX呼吸途径的上调,这表明光是通过影响光合电子传递来调控AOX呼吸途径的。光下DCMU及MV(甲基紫精)预处理导致杂交酸模叶片超氧阴离子自由基(O2??)及过氧化氢(H_2O_2)等活性氧含量显著上升,但是显著增加的活性氧含量并未诱导AOX呼吸途径的上调,说明光并不是通过光合作用产生的活性氧来诱导AOX呼吸途径上调的。此外,因为DCMU和MV预处理减少了NADPH的产生,因此光对AOX呼吸途径的调控与NADPH的大量生成有关。黑暗中外施NADPH时并未诱导AOX呼吸途径的上调,而光下AOX呼吸途径的活性随着外施NADPH的增加而明显上升;同时黑暗中外施草酰乙酸(OAA)时并未诱导AOX呼吸途径的上调,而光下AOX呼吸途径的活性随着外施OAA的增加而明显上升。这些结果表明,光合作用产生的过剩NADPH并非诱导AOX呼吸途径上调的直接信号,可能在过剩的NADPH外运过程中生成某些中间产物间接诱导AOX呼吸途径。对照叶片中随着光强的升高,丙酮酸含量逐渐升高,而当用DCMU和MV预处理后,叶片中丙酮酸含量并未随光强的升高而升高;同时光处理后杂交酸模叶片中丙酮酸的含量随着NADPH及OAA预处理浓度的升高而逐渐升高,这些事实说明光很可能通过叶绿体中过剩NADPH外运而生成的丙酮酸来诱导AOX呼吸途径上调。
Excess light energy is harmful to plants and leads to photoinhibition. Since most plants cannot escape exposure to excess light, they have evolved defense systems that dissipate excess light energy. These systems include the thermal dissipation of light energy in pigment-protein complexes in the light-harvesting antennae, the cyclic electron flow around PSI and the water-water cycle. Though such intra-chloroplastic defense mechanisms have been studied extensively, little is known about the extra-chloroplastic defense mechanism. It has been presented that excess reducing equivalents generated in chloroplasts can be transported to mitochondria via shuttle machineries, and oxidized by the alternative oxidase (AOX) pathway. Therefore, it has been speculated that the AOX pathway might have a particular role in protection of plants from photoinhibition, but direct evidence for the role of AOX as a mechanism in protecting plants against photoinhibition is still limited. In this study, the physiological function of the AOX pathway in photoprotection of plants was confirmed in Rumex K-1 leaves. And the mechanism of up-regulation of AOX pathway by light was discussed. The main results obtained are as follows:
(1) A significant decrease in the rate of CO_2 assimilation in salicylhydroxamic acid (SHAM)-treated Rumex K-1 leaves was observed over a range of different light intensities. Gas exchange data further revealed that stomatal conductance was not significantly affected and the internal CO_2 concentration in Rumex K-1 leaves was enhanced by the inhibition of AOX pathway, suggesting that a reduction in stomatal density or aperture size was not responsible to the decreased photosynthetic rate. Furthermore, a reduction in Calvin cycle capacity and photochemical efficiency were not responsible to the decreased assimilation rate. And we measured photosynthetic rate under high concentrations of CO_2 conditions in which the oxygenase activity of Rubisco is minimized and photorespiration is not active. The photosynthetic rate in SHAM-treated leaves is not significantly different from than in the control leaves under non-photorespiratory conditions, strongly suggesting that the decrease in assimilation rate under ambient atmospheric conditions is linked to the photorespiratory restriction.
A possible link between mitochondrial coupling state and photosynthesis is the requirement for rapid oxidation of NADH produced in the mitochondrion during conversion of photorespiratory glycine to serine. A dramatic decrease in the rate of conversion of glycine to serine was observed when the AOX pathway was inhibited. These data demonstrate that the inhibition of AOX pathway restricts photorespiratory flux. The decrease in photosynthesis due to the inhibition of AOX pathway may be associated with a limitation in ribulose-1,5-bisphosphate regeneration in the Calvin cycle due to reduced glycollate-2-P recycling into glycerate-3-P via the photorespiratory pathway. Furthermore, glycine has been shown to accumulate in the light when AOX pathway was inhibited. This very high level of glycine could result in an accumulation of glyoxylate which was shown to inhibit photosynthesis by reducing the activation state of Rubisco.
(2) The observation that activities of malate-oxaloacetate shuttle and AOX pathway increased obviously under high light in Rumex K-1 leaves indicates that excess reducing equivalents generated by photosynthesis were transported from chloroplasts to mitochondria and oxidized by AOX pathway. Inhibition of AOX pathway by SHAM in Rumex K-1 leaves decreased the activity of malate-oxaloacetate shuttle, causing over-reduction of PSⅡacceptor side and the decrease in total driving forces for photosynthetic electron transport (DF_(ABS)) because of accumulation of excess reducing equivalents in chloroplasts. The decrease in total driving forces for photosynthetic electron transport (DF_(ABS)) restricted photosynthetic linear electron flow (ETR), which inevitably limited of generation of pH gradient across thylakoid and decreased the de-epoxidation of xanthophyll cycle pigments indicated by decrease inΔPRI. Therefore, formation of NPQ was suppressed due to the inhibition of AOX pathway. Moreover, effect of inhibition of AOX pathway on NPQ formation was lesser at higher CO_2 supply (20mM NaHCO_3) than that at lower CO_2 supply (1mM NaHCO_3). Therefore, AOX pathway plays an essential role in formation of NPQ under high light via the generation of pH gradient across thylakoid, protecting photosynthetic apparatus against photodamage.
(3) The inhibition of AOX pathway by SHAM decreasedΦ_(PSⅡ) and the O_2 evolution rate, and increased non-Q_B reducing reaction center, causing more severe photoinhibition even under low light in Rumex K-1 leaves. Under low light, the loss of the function of AOX pathway was compensated by up-regulation of other photoprotection pathways such as cyclic electron transport around PSI, water-water cycle and antioxidant enzymes, , which alleviated the accumulation of reactive oxygen species (ROS) when AOX pathway was inhibited. But under high light, it was not able to compensate the loss of the function of AOX pathway by the other photoprotection pathways when the AOX pathway was inhibited, leading to more severe accumulation of ROS. This result indicates that other photoprotection pathways were able to partially replace the function of AOX pathway under low light, but not under high light.
(4) Inhibition of AOX pathway decreased the maximum quantum yield for primary photochemistry (φ_(Po)), the excitation efficiency of electron transport beyong Q_A~- (Ψ_0) and the quantum yield of electron transport (φ_(Eo)), causing more severe photoinhibition under high light in Rumex K-1 leaves. However, the inhibition of AOX pathway did not change the level of photoinhibition under high light in the presence of the inhibitor of chloroplast D1 protein synthesis, chloramphenicol, indicating that the inhibition of the AOX pathway did not accelerate the photodamage to PSⅡdirectly. All of these results suggest that the AOX pathway plays an important role in the protection of plants against photoinhibition by minimiszing the inhibition of the repair of the photodamaged PSⅡ.
(5) It is noteworthy that activation state of malate-oxaloacetate shuttle increased very quickly upon irradiation in Rumex K-1 leaves, it increased to about 75% of full activation only 1min after irradiation, suggesting that malate-OAA shuttle was activated quickly to export excess reducing equivalents generated by photosynthesis to mitochondria and cytosol during photosynthetic induction. During photosynthetic induction, inhibition of AOX pathway by SHAM restricted light activation of malate-oxaloacetate shuttle, which caused over-reduction of PSI acceptor side and over-accumulation of Q_A~ˉ, thereby limited photosynthetic linear electron flow (ETR). The limitation of ETR without changing in light absorption (ABS/RC) and trapping (TR_0/RC) caused imbalance between light energy absorption and utilization during photosynthetic induction. The limitation of ETR also restricted formation of pH gradient across thylakoid indicated by decrease in de-epoxidation of xanthophyll cycle, restricting formation of non-photochemical quenching (NPQ). The imbalance between light energy absorption and utilization and the suppression of NPQ formation inevitably resulted in over-excitation of PSⅡreaction centres during photosynthetic induction. The induction of CO_2 assimilation was delayed by SHAM-treatment, which was reversed partly by exogenously-application of ATP, suggesting that the inhibition of AOX pathway delayed light activation of Calvin cycle enzymes due to the restriction of formation of pH gradient across thylakoid to generate ATP. Therefore, mitochondrial AOX pathway acts as a sink for electrons generated by photosynthesis, which protects photosynthetic apparatus against photoinhibition and accelerates induction of CO_2 assimilation during photosynthetic induction.
(6) Light increased the capacity of AOX pathway in Rumex K-1 leaves. But the capacity of AOX pathway did not increase when the photosynthetic electron transport from Q_A to Q_B was inhibited by DCMU in the light, which suggests that light regulates the AOX pathway through photosynthetic signals. The DCMU or MV-pretreatment, which induced more severe accumulation of O_2~- and H_2O_2 and inhibited the generation of NADPH, did not enhance the capacity of the AOX pathway under light, suggesting that the accumulation of NADPH rather than ROS generated by photosynthesis was involved in light-dependent increase in AOX pathway capacity.. Exogenously-application of NADPH and OAA did not change the capacity of AOX pathway in the dark. But the capacity of AOX pathway increased with the increase of NADPH or OAA concentration in the light, which suggests that NADPH was not the direct signal in light-dependent induction of AOX pathway.
Furthermore, it was observed that pyruvate content increased with the increase of light intensity in control leaves. And the pyruvate content increased with the increase of NADPH or OAA concentration in the light. Given that the excess NADPH can be transported from chloroplasts to mitochondria accompanied with formation of pyruvate, and the DCMU or MV-pretreatment did not enhance the formation of pyruvate in the light, it is reasonable to suggest that the pyruvate might play a major role in light-dependent up-regulation of AOX pathway.
引文
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