低温胁迫下番茄紫黄质脱环氧化酶基因的表达和功能研究
|
摘要
光作为植物光合作用的唯一能源是植物生命活动的基础。然而,当植物吸收的光能超过其电子传递所需时,过剩的光能便会造成光合效率和光合功能的降低,引起光抑制,严重时还会发生光氧化破坏。植物除了在强光下会产生光抑制外,在低温弱光、高温、干旱、盐碱等逆境下由于CO2的固定受到限制,使得植物对光能的利用减少而导致光抑制。高等植物体内存在着多种防御机制以避免或减少光抑制,其中叶黄素循环被认为是逆境下保护植物光合机构免受过剩光能破坏的一种重要的机制。叶黄素循环是指植物吸收的光能过剩时,双环氧的紫黄质(V)在紫黄质脱环氧化酶(VDE)的催化下,经过中间物单环氧的花药黄质(A)转化为无环氧的玉米黄质(Z);在暗处,则在玉米黄质环氧化酶(ZE)的作用下朝相反的方向进行,将Z重新环氧化为V,形成一个循环。依赖于叶黄素循环的非光化学猝灭(NPQ)能够保护植物光合机构免受过剩激发能的破坏。有过剩光能存在时,由紫黄质(V)脱环氧化而积累的玉米黄质(Z)也被人们普遍认为对光合机构起到至关重要的保护作用。
本研究从番茄叶片中分离到番茄紫黄质脱环氧化酶基因,并对该基因的表达和功能进行了分析。结果表明,该基因的表达并受光强、温度和昼夜节律的影响。过量表达该基因可减轻番茄植株对光抑制的敏感性,而抑制该基因表达可加重番茄植株在低温弱光胁迫下的光抑制程度。主要结果如下:
1.利用同源序列设计简并引物,通过RT-PCR的方法从番茄叶片克隆到紫黄质脱环氧化酶基因的中间片段,通过5’-RACE和3’-RACE分别克隆到5’和3’片段,拼接后设计特异引物扩增到全长cDNA。命名为LeVDE(FJ648424)。该基因全长为1670bp,ORF为1437bp,编码478个氨基酸,分子量约为53 kDa。同源序列比较发现,番茄紫黄质脱环化酶基因的序列与拟南芥、烟草、菠菜、莴苣、水稻的紫黄质脱环化酶基因的序列同源性较高。结构同源性分析表明LeVDE有三个特征结构域,block I为-端半胱氨酸富集区,有活性的VDE中N-端含有11-13个半胱氨酸,是VDE的抑制剂DTT作用的区域,低浓度DTT只能部分抑制VDE的活性,说明N-端的半胱氨酸形成不止一个二硫键。block II为脂质运载蛋白特征区,结合和转运疏水小分子的区域,为疏水底物A和Z的结合区。block III是C-端谷氨酸富集区,含有大量的负电荷,是VDE与类囊体膜结合的部位。
2. Northern杂交结果表明,LeVDE基因呈非特异性表达,在叶绿素含量高的组织中表达量较高。同时,该基因在弱光和强光处理的24小时昼夜周期中都存在着相似的双峰表达模式,并部分受低温的抑制。Southern杂交结果表明,LeVDE基因在番茄基因组中是单拷贝的。
3.将获得的LeVDE基因与含有35S启动子的pBI121载体重组,分别构建了正义和反义表达载体,利用农杆菌介导的叶盘法转化番茄,用PCR及Northern杂交的方法对带卡那抗性的转基因番茄植株进一步检测,结果证明成功地获得了转正义和反义基因的番茄植株。与野生型植株相比,过量表达LeVDE基因的番茄叶片中A和Z的含量增加,而V的含量减少,脱环氧化状态较野生型高。LeVDE基因表达受到抑制的番茄植株中V量积累,而A和Z含量非常低,脱环氧化状态保持较低的水平
4.构建了原核表达载体pET-LeVDE,并在大肠杆菌BL21中表达融合蛋白,将强诱导带切下,溶于PBS获得抗原,免疫小白鼠,其抗血清效价为1: 500。Western杂交表明,转正义植株中LeVDE基因已在蛋白水平过量表达。另外,分别对低温弱光和强光处理的野生型番茄进行了Western杂交分析。结果表明,LeVDE在蛋白水平的表达始终处在稳定的水平,基本不受光强和温度的影响。
5.在低温弱光(4℃,100μmol m~(-2) s~(-1))和强光(1200μmol m~(-2) s~(-1))胁迫条件下,野生型和转正义基因株系T1-7和T1-10株系的NPQ及叶黄素循环脱环氧化状态(A+Z)/(V+A+Z)都增加,但野生型的增加更为明显。在低温弱光及强光胁迫条件下,依赖叶黄素循环的NPQ能够耗散过剩激发能,而转基因株系比野生型耗散能力加强。强光处理过程中,野生型比转正义基因株系的Fv/Fm降低更明显,且转基因株系的Fv/Fm恢复较快,野生型的Fv/Fm恢复较慢。与在强光下类似,T1-7和T1-10株系的Fv/Fm在低温胁迫过程中降低的程度比野生型小,而恢复较慢。这表明LeVDE的过量表达减轻了PSII的光抑制程度,与转基因番茄相比,野生型的PSII反应中心受伤害较严重。强光胁迫12 h,野生型和转基因番茄的净光合速率降低非常显著,但野生型下降程度明显大于转基因株系。这表明由于LeVDE的过量表达增强了低温弱光和强光胁迫下PSII反应中心的稳定性,使光合机构所受到的伤害减轻。
在低温弱光处理过程中转正义基因植株与野生型的氧化态P700都降低,且野生型降低幅度大于转正义基因植株。经过12 h的处理,T1-7,T1-10和野生型的O_2~(-|-)含量分别增加了52.3 %,59.8%和81.1 %, H2O2含量分别增加了40.1%,42.3 %和61.3 %。野生型中O2和H2O2含量增加的程度明显高于转基因株系。另外,在低温处理过程中,转正义基因植株和野生型的MDA含量都增加,但转正义基因植株的MDA含量增加的较少。
6.抑制LeVDE的表达使得过剩光能胁迫下的NPQ减少。在转反义基因植株中V大量积累而Z和A的含量非常低。在强光和低温弱光胁迫后,转反义基因植株脱环氧化状态始终保持较低的水平。在强光和低温胁迫过程中野生型和转反义基因植株的NPQ都上升,且胁迫12 h后转反义基因植株的NPQ低于野生型。这表明抑制Z的生成使得依赖于叶黄素循环的能量耗散减弱。
7.在强光胁迫下野生型和转反义基因植株的Fv/Fm都降低,但是转反义基因植株降低幅度大于野生型。低温弱光胁迫下野生型与转反义基因植株的Fv/Fm均下降,转反义基因植株下降更为明显,低温处理后,(-)2,(-)9和野生型植株的Fv/Fm分别下降了20.1%,17.9%,12.1%。在低温弱光处理过程中转反义基因植株与野生型的氧化态P700都降低,转反义基因株系植株P700的下降更为显著。
低温处理后,(-)2,(-)9和野生型植株中O_2~(-|-)含量分别增加了79.1%,76.4%和62.7%。经低温弱光处理后,野生型和转反义基因植株中MDA含量都增加,转反义基因植株中MDA含量增加更为显著,低温胁迫12小时后野生型,(-)2和(-)9中MDA含量分别增加到138.5 %,159.1 %和161.7%。
综上所述,LeVDE的表达受温度、光强和昼夜节律的影响。过量表达该基因减轻了PSII和PSI对光抑制的敏感性。抑制该基因的表达加重了强光和低温弱光胁迫下的光抑制。
Photosynthesis is important for plant growth and survival. On a daily as well as seasonal basis most plants receive more sunlight than they could actually use for photosynthesis. If the excessive light energy which has been absorbed by photosynthetic apparatus can not be dissipated rapidly, it may reduce the photosynthetic efficiency and result in photoinhibition, even photooxidative damage to the photosynthetic reaction center. The environmental stresses such as low and high temperatures, drought and salinity enhance photoinhibition. Photoinhibition occurs in the field in plants exposed to conditions of high light. The combination of low temperature with irradiance also has the potential to induce chronic photoinhibition of PSII. This is partly because lower temperature generally reduces the rates of biological reactions particularly carbon dioxide reduction and photorespiration, and therefore limits the sinks for the absorbed excitation energy. Among the short-term mechanisms, the xanthophyll cycle has been conceived to play a key role in photoprotection. The xanthophyll cycle exists in the thylakoid membranes of all higher plants, ferns, mosses and algae. Its pigments have been demonstrated to be associated with all light-harvesting components, including LHCI. It comprises intercoversions of three carotenoid pigments, violaxanthin, antheraxanthin and zeaxanthin, which catalysed by two enzyme, violaxanthin de-epoxidase (VDE, EC:1.10.99.3) and zeaxanthin epoxidase (ZE, EC:1.14.13.90). When light energy is excessive, violaxanthin is catalysed to zeaxanthin via antheraxanthin catalysed by violaxanthin de-epoxidase (VDE). However, when light stress disappeared, epoxidation of zeaxanthin to antheraxanthin and violaxanthin is catalysed by another enzyme, zeaxanthin epoxidase (ZE). The xanthophyll cycle and the associated non-photochemical quenching (NPQ) exert their protective role by thermal dissipation of excess light energy. Zeaxanthin is thought to be the main photoprotector in chloroplasts. Many studies show zeaxanthin can directly quench the 1Chl* state and some reactive oxygen species. So the photosynthetic apparatus can be protected from photooxidation. However, there are other researches which support that the xanthophyll pigments protect the thylakoid membrane by an indirect process. They can allosterically regulate the quenching process inside the LHCII. Zeaxanthin is a allosteric activator of this process and violaxanthin is a inhibitor.
In this study, we isolated and characterized violaxanthin de-epoxidase gene from tomato using homological clone. The functional analysis showed that expression of the gene was induced by diurnal rhythm, light intensity and temperature. It is interesting that overexpression of LeVDE increased the level of de-epoxidation and thermal dissipation capacity. It is suggested that the overexpression of LeVDE could alleviate photoinhibition of PSII and PSI under high light and chilling stress. However, the suppression of LeVDE enhanced the photoinhibition of tomato plants under low temperature. The main results are as follows:
1. Two degenerate primers were designed to amplify specific DNA fragment using cDNA prepared from tomato leaves according to the homologous sequences from other plants. The middle fragment of interested cDNA was obtained by RT-PCR. The 5’and 3’fragment of the cDNA was isolated by 5’and 3’RACE. The clone was named LeVDE (Acession numeber: FJ648424), contains 1670bp nucleotides with an open reading frame (ORF) of 1437bp, comprising 478 amino acid residues with the predicted molecular mass of 53 kDa. The deduced amino acid sequence showed high identities with VDE from Arabidopsis thaliana, Nicotiana tabacum,Oryza sativa, Spinacia oleracea, Lactuca sativa. Amino acid sequence alignment revealed that the plant members contained the previously defined regions. The cysteine-rich domain in block I, the lipocalin signature domain in block II and the C-terminal glutamate-rich domain in block III, all of which have been shown to form a catalytically essential site in VDE, are absolutely conserved. The cysteine-rich domain in block I was suggested to be the active site of VDE. The lipocalin signature domain could be a possible binding site for violaxanthin and MGDG which was the substrate for VDE. At the C-terminal region, the glutamate-rich domain in block III was thought to be involved in binding of VDE to the thylakoid membrane.
2. Northern blot analysis showed that LeVDE constitutively expressed in roots, leaves, fruits, stems and calyxes of wild type (WT) plants. The transcripts were high in the tissues abundant of chlorophyll. LeVDE transcript level was similar for extracts from plants treated with high light and low light condition, and exhibited a diurnal rhythm expression pattern. Furthermore, the LeVDE transcript level was inhibited by both light intensity and low temperature. Southern blot analysis showed that LeVDE gene was a single copy in tomato genome.
3. The full-length LeVDE cDNA was subcloned into the expression vector pBI121 downstream of the 35S-CaMV promoter to form sense and antisense constructs. The constructs were first introduced into Agrobacterium tumefaciens LBA4404 by the freezing transformation method and verified by PCR and northern blot. It was indicated that the LeVDE gene had been recombined into tomato genome and both sense and antisense transgenic tomato plants were obtained. A lower content of V and higher content of A and Z were detected in sense transgenic plants compared with WT plants. The de-epoxidation ratio of xanthophyll cycle pigments (A+Z)/(V+A+Z) of sense transgenic plants was higher than that of WT. Suppression of LeVDE in tomato decreased the content of Z and A. But V accumulated in antisense transgenic plants compared to that of WT plants.
4. A recombinant of prokaryotic expression vector pET-LeVDE was constructed and transformed to E.Coli BL21 to express. The strong induced fusion protein bands were collected into PBS solution and used to immunize white mice to obtain antiserum. The value of antibody reaches 1: 500. Western blot revealed the presence of the strong positive protein signals corresponding to LeVDE in sense transgenic plants. Western blot analysis was carried out over the diurnal cycle. Unexpectedly, the LeVDE protein level remained constant in leaves. Moreover, there was no difference between leaves exposed to high light and chilling stress.
5. Although both NPQ and (A+Z)/(V+A+Z) of WT and sense transgenic plants increased markedly under chilling stress in the low irradiance (4℃, 100μmol m~(-2) s~(-1)) and high light stress (1200μmol m~(-2) s~(-1)), the increase of NPQ and (A+Z)/(V+A+Z) was more obvious in sense transgenic plants than in WT. Fv/Fm decreased in both WT and transgenic plants under high light stress, but the decrease of Fv/Fm in transgenic plants was more significant than that in WT. At the end of high light stress, Fv/Fm in WT, T1-10 and T1-7 lines decreased by 32.1%, 13.4 % and 11.2 %, respectively. When tomato plants were transferred to suitable condition of 25℃and a PFD of 100μmol m~(-2) s~(-1), Fv/Fm recovered in both WT and transgenic plants. However, the recovery of Fv/Fm in the transgenic plants was faster. Fv/Fm also decreased significantly in transgenic plants during chilling stress (4℃) relative to that in WT plants. At the end of chilling stress, Fv/Fm in the the WT and transgenic plants of T1-10 and T1-7 decreased about 12.1 %, 8.3 % and 7.1 %, respectively. The recovery of Fv/Fm in transgenic plants was also faster than that in WT. Under high light stress for 12 h, the Pn of WT and transgenic tomato plants obviously decreased. This decrease was more significant in WT than in transgenic plants.
The oxidizable P700 decreased significantly both in WT and sense transgenic plants under chilling stress in the low irradiance, and the decrease was more significant in WT than in transgenic plants. At the end of chilling stress, O_2~(-|-) content in leaves of T1-7, T1-10 and WT plants increased for about 52.3 %,59.8% and 81.1 % of initial values, respectively, and H2O2 content of T1-7, T1-10 and WT increased for about 40.1%,42.3 % and 61.3 % of initial values, respectively. The level of peroxide of membrane lipids was enlarged and the MDA contents of T1-7, T1-10 and WT plants increased to 115.1%, 121.7% and 140.5%, respectively.
7. Antisense-mediated suppression of LeVDE affected NPQ under light stress. V accumulated in antisense transgenic tomato plants, but Z and A content was very low. The de-epoxidation ratio of xanthophyll cycle pigments (A+Z)/(V+A+Z) in antisense transgenic plants sustained a very low level before and after high light and low temperature stress. Although both NPQ of WT and antisense transgenic plants increased markedly under chilling stress in the low irradiance and high light stress, the increase was more significant in WT than in transgenic plants. It was suggested that the suppression of LeVDE decreased the energy dissipation in PSII.
8. Fv/Fm decreased in both WT and antisense transgenic plants under chilling stress in the low irradiance, and WT showed the greater decrease. At the end of low temperature stress for 12 h, Fv/Fm in (-)2, (-)9 and WT decreased about 20.1%,17.9%,12.1%, respectively. The oxidizable P700 decreased significantly both in WT and antisense transgenic plants under chilling stress in the low irradiance, and the decrease of P700 was more obvious in WT than in antisense transgenic plants. O_2~(-|-) contents increased more markedly in antisense transgenic plants than in WT plants. At the end of chilling stress, O~(-|-) content in (-)2, (-)9 and WT plant leaves increased for about 79.1%,76.4% and 62.7%, respectively. The MDA contents of WT and antisense transgenic tomato plants increased under chilling stress in the low irradiance. The increase was more obvious in antisense transgenic plants than in the wild type. After 12 h stress, the MDA contents in WT, antisense transgenic lines (-)2 and (-)9 increased to about 138.5 %, 159.8 % and 161.7%, respectively.
In conclusion, we demonstrated that the expression of LeVDE was induced by light, temperature and diurnal rhythm and it was partially inhibited by chilling temperature. Overexpression of LeVDE increased the level of de-epoxidation and the thermal dissipation capacity under high light and chilling stress. The sensitivity of PSII and PSI photoinhibition to high light and chilling stress was therefore alleviated. The suppression of LeVDE affected NPQ under light stress and enchanced the photoinhibition of tomato plants under low temperature.
本研究从番茄叶片中分离到番茄紫黄质脱环氧化酶基因,并对该基因的表达和功能进行了分析。结果表明,该基因的表达并受光强、温度和昼夜节律的影响。过量表达该基因可减轻番茄植株对光抑制的敏感性,而抑制该基因表达可加重番茄植株在低温弱光胁迫下的光抑制程度。主要结果如下:
1.利用同源序列设计简并引物,通过RT-PCR的方法从番茄叶片克隆到紫黄质脱环氧化酶基因的中间片段,通过5’-RACE和3’-RACE分别克隆到5’和3’片段,拼接后设计特异引物扩增到全长cDNA。命名为LeVDE(FJ648424)。该基因全长为1670bp,ORF为1437bp,编码478个氨基酸,分子量约为53 kDa。同源序列比较发现,番茄紫黄质脱环化酶基因的序列与拟南芥、烟草、菠菜、莴苣、水稻的紫黄质脱环化酶基因的序列同源性较高。结构同源性分析表明LeVDE有三个特征结构域,block I为-端半胱氨酸富集区,有活性的VDE中N-端含有11-13个半胱氨酸,是VDE的抑制剂DTT作用的区域,低浓度DTT只能部分抑制VDE的活性,说明N-端的半胱氨酸形成不止一个二硫键。block II为脂质运载蛋白特征区,结合和转运疏水小分子的区域,为疏水底物A和Z的结合区。block III是C-端谷氨酸富集区,含有大量的负电荷,是VDE与类囊体膜结合的部位。
2. Northern杂交结果表明,LeVDE基因呈非特异性表达,在叶绿素含量高的组织中表达量较高。同时,该基因在弱光和强光处理的24小时昼夜周期中都存在着相似的双峰表达模式,并部分受低温的抑制。Southern杂交结果表明,LeVDE基因在番茄基因组中是单拷贝的。
3.将获得的LeVDE基因与含有35S启动子的pBI121载体重组,分别构建了正义和反义表达载体,利用农杆菌介导的叶盘法转化番茄,用PCR及Northern杂交的方法对带卡那抗性的转基因番茄植株进一步检测,结果证明成功地获得了转正义和反义基因的番茄植株。与野生型植株相比,过量表达LeVDE基因的番茄叶片中A和Z的含量增加,而V的含量减少,脱环氧化状态较野生型高。LeVDE基因表达受到抑制的番茄植株中V量积累,而A和Z含量非常低,脱环氧化状态保持较低的水平
4.构建了原核表达载体pET-LeVDE,并在大肠杆菌BL21中表达融合蛋白,将强诱导带切下,溶于PBS获得抗原,免疫小白鼠,其抗血清效价为1: 500。Western杂交表明,转正义植株中LeVDE基因已在蛋白水平过量表达。另外,分别对低温弱光和强光处理的野生型番茄进行了Western杂交分析。结果表明,LeVDE在蛋白水平的表达始终处在稳定的水平,基本不受光强和温度的影响。
5.在低温弱光(4℃,100μmol m~(-2) s~(-1))和强光(1200μmol m~(-2) s~(-1))胁迫条件下,野生型和转正义基因株系T1-7和T1-10株系的NPQ及叶黄素循环脱环氧化状态(A+Z)/(V+A+Z)都增加,但野生型的增加更为明显。在低温弱光及强光胁迫条件下,依赖叶黄素循环的NPQ能够耗散过剩激发能,而转基因株系比野生型耗散能力加强。强光处理过程中,野生型比转正义基因株系的Fv/Fm降低更明显,且转基因株系的Fv/Fm恢复较快,野生型的Fv/Fm恢复较慢。与在强光下类似,T1-7和T1-10株系的Fv/Fm在低温胁迫过程中降低的程度比野生型小,而恢复较慢。这表明LeVDE的过量表达减轻了PSII的光抑制程度,与转基因番茄相比,野生型的PSII反应中心受伤害较严重。强光胁迫12 h,野生型和转基因番茄的净光合速率降低非常显著,但野生型下降程度明显大于转基因株系。这表明由于LeVDE的过量表达增强了低温弱光和强光胁迫下PSII反应中心的稳定性,使光合机构所受到的伤害减轻。
在低温弱光处理过程中转正义基因植株与野生型的氧化态P700都降低,且野生型降低幅度大于转正义基因植株。经过12 h的处理,T1-7,T1-10和野生型的O_2~(-|-)含量分别增加了52.3 %,59.8%和81.1 %, H2O2含量分别增加了40.1%,42.3 %和61.3 %。野生型中O2和H2O2含量增加的程度明显高于转基因株系。另外,在低温处理过程中,转正义基因植株和野生型的MDA含量都增加,但转正义基因植株的MDA含量增加的较少。
6.抑制LeVDE的表达使得过剩光能胁迫下的NPQ减少。在转反义基因植株中V大量积累而Z和A的含量非常低。在强光和低温弱光胁迫后,转反义基因植株脱环氧化状态始终保持较低的水平。在强光和低温胁迫过程中野生型和转反义基因植株的NPQ都上升,且胁迫12 h后转反义基因植株的NPQ低于野生型。这表明抑制Z的生成使得依赖于叶黄素循环的能量耗散减弱。
7.在强光胁迫下野生型和转反义基因植株的Fv/Fm都降低,但是转反义基因植株降低幅度大于野生型。低温弱光胁迫下野生型与转反义基因植株的Fv/Fm均下降,转反义基因植株下降更为明显,低温处理后,(-)2,(-)9和野生型植株的Fv/Fm分别下降了20.1%,17.9%,12.1%。在低温弱光处理过程中转反义基因植株与野生型的氧化态P700都降低,转反义基因株系植株P700的下降更为显著。
低温处理后,(-)2,(-)9和野生型植株中O_2~(-|-)含量分别增加了79.1%,76.4%和62.7%。经低温弱光处理后,野生型和转反义基因植株中MDA含量都增加,转反义基因植株中MDA含量增加更为显著,低温胁迫12小时后野生型,(-)2和(-)9中MDA含量分别增加到138.5 %,159.1 %和161.7%。
综上所述,LeVDE的表达受温度、光强和昼夜节律的影响。过量表达该基因减轻了PSII和PSI对光抑制的敏感性。抑制该基因的表达加重了强光和低温弱光胁迫下的光抑制。
Photosynthesis is important for plant growth and survival. On a daily as well as seasonal basis most plants receive more sunlight than they could actually use for photosynthesis. If the excessive light energy which has been absorbed by photosynthetic apparatus can not be dissipated rapidly, it may reduce the photosynthetic efficiency and result in photoinhibition, even photooxidative damage to the photosynthetic reaction center. The environmental stresses such as low and high temperatures, drought and salinity enhance photoinhibition. Photoinhibition occurs in the field in plants exposed to conditions of high light. The combination of low temperature with irradiance also has the potential to induce chronic photoinhibition of PSII. This is partly because lower temperature generally reduces the rates of biological reactions particularly carbon dioxide reduction and photorespiration, and therefore limits the sinks for the absorbed excitation energy. Among the short-term mechanisms, the xanthophyll cycle has been conceived to play a key role in photoprotection. The xanthophyll cycle exists in the thylakoid membranes of all higher plants, ferns, mosses and algae. Its pigments have been demonstrated to be associated with all light-harvesting components, including LHCI. It comprises intercoversions of three carotenoid pigments, violaxanthin, antheraxanthin and zeaxanthin, which catalysed by two enzyme, violaxanthin de-epoxidase (VDE, EC:1.10.99.3) and zeaxanthin epoxidase (ZE, EC:1.14.13.90). When light energy is excessive, violaxanthin is catalysed to zeaxanthin via antheraxanthin catalysed by violaxanthin de-epoxidase (VDE). However, when light stress disappeared, epoxidation of zeaxanthin to antheraxanthin and violaxanthin is catalysed by another enzyme, zeaxanthin epoxidase (ZE). The xanthophyll cycle and the associated non-photochemical quenching (NPQ) exert their protective role by thermal dissipation of excess light energy. Zeaxanthin is thought to be the main photoprotector in chloroplasts. Many studies show zeaxanthin can directly quench the 1Chl* state and some reactive oxygen species. So the photosynthetic apparatus can be protected from photooxidation. However, there are other researches which support that the xanthophyll pigments protect the thylakoid membrane by an indirect process. They can allosterically regulate the quenching process inside the LHCII. Zeaxanthin is a allosteric activator of this process and violaxanthin is a inhibitor.
In this study, we isolated and characterized violaxanthin de-epoxidase gene from tomato using homological clone. The functional analysis showed that expression of the gene was induced by diurnal rhythm, light intensity and temperature. It is interesting that overexpression of LeVDE increased the level of de-epoxidation and thermal dissipation capacity. It is suggested that the overexpression of LeVDE could alleviate photoinhibition of PSII and PSI under high light and chilling stress. However, the suppression of LeVDE enhanced the photoinhibition of tomato plants under low temperature. The main results are as follows:
1. Two degenerate primers were designed to amplify specific DNA fragment using cDNA prepared from tomato leaves according to the homologous sequences from other plants. The middle fragment of interested cDNA was obtained by RT-PCR. The 5’and 3’fragment of the cDNA was isolated by 5’and 3’RACE. The clone was named LeVDE (Acession numeber: FJ648424), contains 1670bp nucleotides with an open reading frame (ORF) of 1437bp, comprising 478 amino acid residues with the predicted molecular mass of 53 kDa. The deduced amino acid sequence showed high identities with VDE from Arabidopsis thaliana, Nicotiana tabacum,Oryza sativa, Spinacia oleracea, Lactuca sativa. Amino acid sequence alignment revealed that the plant members contained the previously defined regions. The cysteine-rich domain in block I, the lipocalin signature domain in block II and the C-terminal glutamate-rich domain in block III, all of which have been shown to form a catalytically essential site in VDE, are absolutely conserved. The cysteine-rich domain in block I was suggested to be the active site of VDE. The lipocalin signature domain could be a possible binding site for violaxanthin and MGDG which was the substrate for VDE. At the C-terminal region, the glutamate-rich domain in block III was thought to be involved in binding of VDE to the thylakoid membrane.
2. Northern blot analysis showed that LeVDE constitutively expressed in roots, leaves, fruits, stems and calyxes of wild type (WT) plants. The transcripts were high in the tissues abundant of chlorophyll. LeVDE transcript level was similar for extracts from plants treated with high light and low light condition, and exhibited a diurnal rhythm expression pattern. Furthermore, the LeVDE transcript level was inhibited by both light intensity and low temperature. Southern blot analysis showed that LeVDE gene was a single copy in tomato genome.
3. The full-length LeVDE cDNA was subcloned into the expression vector pBI121 downstream of the 35S-CaMV promoter to form sense and antisense constructs. The constructs were first introduced into Agrobacterium tumefaciens LBA4404 by the freezing transformation method and verified by PCR and northern blot. It was indicated that the LeVDE gene had been recombined into tomato genome and both sense and antisense transgenic tomato plants were obtained. A lower content of V and higher content of A and Z were detected in sense transgenic plants compared with WT plants. The de-epoxidation ratio of xanthophyll cycle pigments (A+Z)/(V+A+Z) of sense transgenic plants was higher than that of WT. Suppression of LeVDE in tomato decreased the content of Z and A. But V accumulated in antisense transgenic plants compared to that of WT plants.
4. A recombinant of prokaryotic expression vector pET-LeVDE was constructed and transformed to E.Coli BL21 to express. The strong induced fusion protein bands were collected into PBS solution and used to immunize white mice to obtain antiserum. The value of antibody reaches 1: 500. Western blot revealed the presence of the strong positive protein signals corresponding to LeVDE in sense transgenic plants. Western blot analysis was carried out over the diurnal cycle. Unexpectedly, the LeVDE protein level remained constant in leaves. Moreover, there was no difference between leaves exposed to high light and chilling stress.
5. Although both NPQ and (A+Z)/(V+A+Z) of WT and sense transgenic plants increased markedly under chilling stress in the low irradiance (4℃, 100μmol m~(-2) s~(-1)) and high light stress (1200μmol m~(-2) s~(-1)), the increase of NPQ and (A+Z)/(V+A+Z) was more obvious in sense transgenic plants than in WT. Fv/Fm decreased in both WT and transgenic plants under high light stress, but the decrease of Fv/Fm in transgenic plants was more significant than that in WT. At the end of high light stress, Fv/Fm in WT, T1-10 and T1-7 lines decreased by 32.1%, 13.4 % and 11.2 %, respectively. When tomato plants were transferred to suitable condition of 25℃and a PFD of 100μmol m~(-2) s~(-1), Fv/Fm recovered in both WT and transgenic plants. However, the recovery of Fv/Fm in the transgenic plants was faster. Fv/Fm also decreased significantly in transgenic plants during chilling stress (4℃) relative to that in WT plants. At the end of chilling stress, Fv/Fm in the the WT and transgenic plants of T1-10 and T1-7 decreased about 12.1 %, 8.3 % and 7.1 %, respectively. The recovery of Fv/Fm in transgenic plants was also faster than that in WT. Under high light stress for 12 h, the Pn of WT and transgenic tomato plants obviously decreased. This decrease was more significant in WT than in transgenic plants.
The oxidizable P700 decreased significantly both in WT and sense transgenic plants under chilling stress in the low irradiance, and the decrease was more significant in WT than in transgenic plants. At the end of chilling stress, O_2~(-|-) content in leaves of T1-7, T1-10 and WT plants increased for about 52.3 %,59.8% and 81.1 % of initial values, respectively, and H2O2 content of T1-7, T1-10 and WT increased for about 40.1%,42.3 % and 61.3 % of initial values, respectively. The level of peroxide of membrane lipids was enlarged and the MDA contents of T1-7, T1-10 and WT plants increased to 115.1%, 121.7% and 140.5%, respectively.
7. Antisense-mediated suppression of LeVDE affected NPQ under light stress. V accumulated in antisense transgenic tomato plants, but Z and A content was very low. The de-epoxidation ratio of xanthophyll cycle pigments (A+Z)/(V+A+Z) in antisense transgenic plants sustained a very low level before and after high light and low temperature stress. Although both NPQ of WT and antisense transgenic plants increased markedly under chilling stress in the low irradiance and high light stress, the increase was more significant in WT than in transgenic plants. It was suggested that the suppression of LeVDE decreased the energy dissipation in PSII.
8. Fv/Fm decreased in both WT and antisense transgenic plants under chilling stress in the low irradiance, and WT showed the greater decrease. At the end of low temperature stress for 12 h, Fv/Fm in (-)2, (-)9 and WT decreased about 20.1%,17.9%,12.1%, respectively. The oxidizable P700 decreased significantly both in WT and antisense transgenic plants under chilling stress in the low irradiance, and the decrease of P700 was more obvious in WT than in antisense transgenic plants. O_2~(-|-) contents increased more markedly in antisense transgenic plants than in WT plants. At the end of chilling stress, O~(-|-) content in (-)2, (-)9 and WT plant leaves increased for about 79.1%,76.4% and 62.7%, respectively. The MDA contents of WT and antisense transgenic tomato plants increased under chilling stress in the low irradiance. The increase was more obvious in antisense transgenic plants than in the wild type. After 12 h stress, the MDA contents in WT, antisense transgenic lines (-)2 and (-)9 increased to about 138.5 %, 159.8 % and 161.7%, respectively.
In conclusion, we demonstrated that the expression of LeVDE was induced by light, temperature and diurnal rhythm and it was partially inhibited by chilling temperature. Overexpression of LeVDE increased the level of de-epoxidation and the thermal dissipation capacity under high light and chilling stress. The sensitivity of PSII and PSI photoinhibition to high light and chilling stress was therefore alleviated. The suppression of LeVDE affected NPQ under light stress and enchanced the photoinhibition of tomato plants under low temperature.
引文
陈国祥,何兵,魏锦城等。低温下强光胁迫对小麦叶片光系统I结构与功能的影响。植物生理学报, 2000, 26(4): 337-342
陈少裕。膜脂过氧化对植物细胞的伤害。植物生理学通讯, 1991, 27(2): 84-90
董高峰,陈贻竹。植物叶黄素循环与非辐射能量耗散。植物生理学通讯, 1999, 35(2): 141-146
郭连旺,沈允钢。高等植物光合机构避免强光破坏的保护机制。植物生理学通讯, 1996, 32: 1-8
郭连旺,许大全,沈允钢。田间棉花叶片光合速率中午下降的原因。植物生理学报, 1995, 20: 360-366
刘鸿先,王以柔,郭俊彦。低温对植物细胞膜系统伤害机理的研究。中国科学院华南植物研究所集刊, 1989,第5集: 31-38
林荣呈,许长成,李良壁,匡廷云。叶黄素循环及其在光保护中的分子机理研究。植物学报,2002,44:379-383
李新国,段伟,孟庆伟,邹琦。PSI的低温光抑制。植物生理学通讯, 2002, 38(4): 375-381
李晓萍,陈贻竹。PSII光能耗散机制研究进展。生物化学与生物物理进展, 1996, 23(2): 145-149
谭新星,许大全,沈允钢。小麦叶片的状态转换涉及PSII向PSI激发能满溢的变化。植物生理学报, 1997, 23: 9-14
沈文飚,徐朗莱,叶茂炳,张荣铣。抗坏血酸过氧化物酶活性测定的探讨。植物生理学通讯, 1996, 32: 203-205
王爱国,罗广华。植物的超氧物自由基与羟胺反应的定量关系。植物生理学通讯, 1990, 6: 55-57
吴长艾,孟庆伟,邹琦。叶黄素循环及其调控。植物生理学通讯,2001,37:1-5
许大全。植物光合作用的光抑制。植物生理学通讯, 1992, 28(4): 237-243
许大全。光系统II反应中心的可逆失活及其生理意义。植物生理学通讯, 1999, 35(4): 273-276
阳成伟,陈贻竹。叶黄素循环酶。广西植物, 2002, 22(3): 264-267
叶济宇。叶绿体的电子传递。见:余叔文,汤章城主编.植物生理与分子生物学。北京:科学出版社, 1998, 198-211
赵世杰。植物生理学实验指导。北京:中国农业出版社, 1998, 161-165
赵世杰,许长成,孟庆伟等。植物组织中叶黄素循环组分的高效液相色谱分析法。植物生理学通讯,1995,31:438-442
Adams WW III, Demmig-Adams B, Logan BA. Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania Japonica And Smilax Australis, growing in the under storey of an open eucalyptus forest. Plant, Cell and Environment, 1999, 22: 125-136
Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH.‘Photoinhibition’during winter stress: Involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol, 1995, 22: 261-276
Allen DJ, Ort DR. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci, 2001, 6: 36-42
Alscher RG, Donahue JL, Cramer CL. Reactive oxygen species and antioxidants: Relationships in green cells. Physiol Plant, 1997, 100: 224-233
Anderson JM, Aro EM. Arana stacking and protection of photosystem II in thylakoid membranes of higher plant leavesunder sustained high irradiance. Photosynth Res, 1994, 41:315-326
Anderson JM, Osmond CB. Shade-sun responses: compromises between acclimation and photoinhibition. In Photoinhibition (eds D.J. Kyle, C.B. Osmond & C.J. Arntzen) pp. 1–38, 1987, Elsevier, Amsterdam, the Netherlands
Aro EM, Kettunen R, Tyystjrvi E. ATP and light regulated D1 protein modification and degradation. Role of D1 in photoinhibition. FEBS Lett, 1992, 297: 29-33
Aro EM, Virgin I, Andersson B. Photoinhibition of photosystem II: Inactivation, protein damage and turnover. Biochim Biophys Acta, 1993, 1143: 113–134
Arvidsson PO, Bratt CE, Carlsson M, ?kerlund HE. Purification and identification of the violaxanthin deepoxidase as a 43 kda protein. Photosynth Res, 1996, 49: 119–129
Arvidsson PO, Carlsson M, Stefánsson H, Albertsson P? and ?kerlund HE. Violaxanthin accessibility and temperature dependency for de-epoxidation in spinach thylakoid membranes. Photosynth Res, 1997, 52: 39-48
Asada K. Ascorbate peroxidase—a hydrogen peroxidescavenging enzyme in plants. Physiol Plant, 1992, 85: 235-241
Asada K. Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (ed). Cause of photooxidative Stress and Amelioration of Defense Systems in Plants. Boca Raton: CRC Press, 1994, 77-104
Asada K, Takahashi M. Production and scavenging of active oxygen in photosynthesis. In Photoinhibition (eds Kyle DJ, Osmond CB, Amtzen CJ). pp. 227-287, 1987, Elsevier Science Publishers, Amsterdam.
Audran C, Borel C, Frey A, Sotta B, Meyer C, Simonneau T, Marion-Poll A. Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol, 1998, 118: 1021–1028
Bailey S, Horton P, Walters RG. Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta, 2004, 218: 793–802
Bailey S, Walters RG., Jansson S, Horton P. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta, 2001, 213: 794–801.
Barber J, Andersson B. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci, 1992, 17: 61-66
Barber J. Molecular basis of the vulnerability of photosystem II to damage by light. Aust J Plant Physiol, 1995, 22:201-208
Barber J, Norris J, Morris EP, Zheleva D, Hankamer B. The structure, function and dynamics of photosystem two. Physiol Plant, 1997, 100: 817-828
Baroli I, Do AD, Yamane T, Niyogi KK. Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects chlamydomonas reinhardtii from photooxidative stress. Plant Cell, 2003, 15: 992-1008
Bertamini M, Muthuchelian K, Rubinigg M, Zorer R, Velasco R, Nedunchezhian N. Low-night temperature increased the photoinhibition of photosynthesis in grapevine (Vitis vinifera L. cv. Riesling) leaves. Environ Exp Bot, 2006, 57: 25-31
Bj?rkman O. Responses to different quantum flux densities.In Physiological Plant Ecology I: Responses to the Physical Environment (eds O.L. Lange, S. Nobel, C.B. Osmond, H. Ziegler) pp. 57–107, 1981, Springer-Verlag, Berlin, Germany
Boese SR, Hüner NPA. Developmental history affects the susceptibility of spinach leaves to in vivo low temperature photoinhibition. Physiol Plant, 1992, 99: 1141-1145
Büch K, Stransky H, Hager A. FAD is a further essential cofactor of the NAD(P)H and O2-dependent zeaxanthin-epoxidase. FEBS Lett, 1995, 376: 45-48
Bugos RC, Hieber D, Yamamoto HY. Xanthophyll cycle enzymes are members of the lipcolin finity, the first identified from plants. J Biol Chem, 1998, 273 (25): 15321-15324
Cakmak I, Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol, 1992, 98: 1222-1227
Campbell D, Bruce D, Carpenter C, Gustafsson P, ?quist G. Two forms of the Photosystem II D1 protein after energy dissipation and state transition in the cyanobacterium Synechocystis sp. PCC 7942. Photosynth Res, 1996, 47: 131-144
Chang SH, Bugos RC, Sun WH., Yamamoto HY. Antisense suppression of violaxanthin de-epoxidase in tobacco does not affect plant performance in controlled growth conditions. Photosynth Res, 2000, 64: 95–103
Cleland R, Melis A, Neale PJ. Mechanism of photoinhibition: photochemical reaction center inactivation in system II of chloroplasts. Photosynth Res, 1986, 9: 79-88
Conklin PL, Williams EH, Last RL. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proceedings of the National Academy of Sciences of the USA, 1996, 93: 9970–9974.
Cornic G, Bukhov NG, Wiese C et al., Flexible coupling between light-dependent electron and vectorial proton transport in illuminated leaves of C3 plant. Role of photosystem I-dependent proton pumping. Planta, 2000, 210: 468-477
Dalton DA, Hanus FJ, Russell SA, Evans HJ. Purification, properties, and distribution of ascorbate peroxidase in legume root nodules. Plant Physiol, 1987, 83: 789-794
Darkóé, Váradi G, Lemoine Y, Lehoczki E. Defensive strategies agaist high light stress in wild and D1 protein mutant biotypes of Erigeron canadensis. Aust J Plant Physiol, 2000, 27: 325-333
Demmig-Adams B, Adams WW III . Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol, 1992, 43: 599–626
Demmig-Adams B, Adams WW III. Harvesting light safely. Nature, 2000, 403 (27): 371-374
Demmig-Adams B, Adams WW III. Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta, 1996, 198: 460-470
Demmig-Adams B, Winter K, Czyger F. Photoinhibition and zeaxanthin formation in intactLeaves. Plant Physiol, 1987, 84:218-224
Demmig-Adams B, Winter K, Krger A, Czygan FC. Zeaxanthin synthesis, energy dissipation, and phototection of photosystem II at chilling temporation. Plant Physiol, 1989, 90:894-898
Demmig-Adams B. Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta, 1990, 1020: 1–24.
Durocher D, Jackson SP. The FHA domain. FEBS Lett, 2002, 513: 58-66
Eichelmann H and Laisk A. Cooperation of photosystems II and I in leaves as analyzed by simultaneous measurements of chlorophyll fluorescence and transmittance at 800nm. Plant Cell Physiol, 2000, 41: 138-147
Endo T, Shikanai T, Takabayashi A, Asada K, Sato F. The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett, 1999, 457: 5-8
Escoubas JM, Lomas M, Laroche J, Falkowski PG. Light intensity regulation of cab gene transcription is signaled by the redox state of plastoquinone pool. PNAS, 1995, 92: 10237-102341
Eskling M, Arvidsson PO, ?kerlund HE. The xanthophyll cycle, its regulation and components. Physiol Plant, 1997, 100: 806-816
Eskling M, Emanuelsson A, ?kerlund HE. Enzymes and mechanisms for violaxanthin-zeaxanthin conversion. In EM Aro and B Andersson, eds, Regulation of Photosynthesis, Kluwer Academic Publishers, The Netherlands, 2001, pp. 433-452
Feierabend J, Schaan C, Hertwig B. Photoinactivation of catalase occurs under both high-and low-temperature stress conditions and accompanies photoinhibition of photosystem II. Physiol Plant, 1992, 100: 1554-1561
Foyer CH, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta, 1976, 133: 21-25
Foyer CH, Lelandais M, Kunert KJ. Photooxidative stress in plants. Physiol Plant, 1994, 92: 696–717
Foyer CH, Lelandais M. A comparison of the relative rate of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. J Plant Physiol, 1996, 148: 391-398
Frommolt R, Goss R, Wilhelm C. The de-epoxidase and epoxidase reactions of Mantoniella squamata (Prasinophyceae) exhibit different substrate-specific reaction kinetics comparedto spinach. Planta, 2001, 213: 446-456
Gerber DW, Burris JE. Photoinhibition and P700 in the marine diatom Amphora sp. Plant Physiol, 1981, 68: 699-702
Giannopolitis CN, Ries SK. Superoxide Dismutases. I. Occurrence in higher plants. Plant Physiol, 1977, 59: 309-314
Gillham DJ, Dodge AD. Chloroplast superoxide and hydrogen peroxide scavenging systems from pea leaves: Seasonal variations. Plant Sci, 1987, 50: 105–109
Gilmore AM, Hazlett TL, Govindjee. Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: Formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci USA, 1995, 92: 2273-2277
Gilmore AM, Mohanty N, Yamamoto HY. Epoxidation of zeaxanthin and antheraxanthin reverses non-photochemical quenching of photosystem II chlorophyll a fluorescence in the presence of trans-thylakoid delta pH. FEBS Lett, 1994, 350: 271-274
Gilmore AM. Mechanistic aspects of xanthophylls cycle dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant, 1997, 99: 197-209
Gilmore AM. Xanthophyll cycle-dependent nonphotochemical quenching in photosystem II: Mechanistic insights gained from Arabidopsis thaliana L. mutants that lack violaxanthin deepoxidase activity and/or lutein. Photosynth Res, 2001, 67: 89-101
Golbeck JH. Structure and function of photosystem I. Annu Rev Plant Physiol Plant Mol Biol, 1992, 43:293-324
Golbeck JH. Structure, function and organization of the photosystem I reaction center complex. Biochim Biophys Acta, 1987, 895:167-204
Golbeck JH, Bryant DA. Photosystem I. Curr Top Bioenerg, 1991, 16: 3-177
Golden SS, Brusslan J, Haselkorn R. Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J, 1986, 5: 2789-2798
Goss R, Bohme K, Wilhelm C. The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: Consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta, 1998, 205: 613-621
Graβes T, Pesaresi P, Schiavon F, Varotto C, Salamini F, Jahns P, Leister D. The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against lightinduced damage in Arabidopsis thaliana. Plant Physiology and Biochemistry, 2002,40: 41–49
Greer GH, Berry JA, Bj?rkman O. Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature and requirement for chloroplast-protein synthesis during recovery. Planta, 1986, 168: 253-257
Gruszecki WI, Strzalka K. Does the xanthophyll cycle take part in the regulation of fluidity of the thylakoid membrane? Biochim Biophys Acta, 1991, 1060: 310-314
Hager A. Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta, 1969, 89: 224-243
Hager A. Die reversiblen, lichtabhangigen xanthophyll umwandlungen im chloroplasten. Ber Dtsch Bot Ges, 1975, 88: 27- 44
Hager A. The reversible, light-induced conversions of xanthophylls in the chloroplast. In FC Czygan, eds. Pigments in Plants. Fischer, Stuttgart, 1980, pp 57-79
Haldrup A, Jensen PE, Lunde C, Scheller HV. Balance of power: a view of the mechanism of photosynthetic state transitions. Tren Plant Sci, 2001, 6: 301-305
Hartel H, Lokstein H, Grimm B and Rank B. Kinetic studies on the xanthophyll cycle in barley leaves: Influence of antenna size and relations to nonphotochemical chlorophyll fluorescence quenching. Plant Physiol, 1996, 110: 471-482
Havaux M, Bonfils JP, Lütz C, Niyogi KK. Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin deepoxidase. Plant Physiol, 2000, 124: 273–284.
Havaux M, Dall'Osto L, CuinèS, Giuliano G, Bassi R. The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. J Biol Chem, 2004, 279: 13878-13888
Havaux M, Davaud A. Photoinhibition of photosynthesis in chilled potato leaves is not correlated with loss of photosysthem II activity. Preferential inactivation of Photosystem I. Photosynth Res, 1994, 40: 75-92
Havaux M, Gruszecki WI, Dupont I and Leblanc RM. Increased heat emission and its relationship to the xanthophylls cycle in pea leaves exposed to strong light stress. J Photochem Photobiol, 1991, 8: 361–370
Havaux M, Niyogi KK. The violaxanthin cycle protects plants from photooxidative damageby more than one mechanism. Proc Natl Acad Sci USA, 1999, 96: 8762-8767
Havaux M, Tardy F, Ravenel J, Parot P. Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochrochromic shift in intact potato leaves: influence of the xanthophyll content. Plant Cell Environ, 1996, 19: 1359-1368
Havaux M. Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci, 1998, 3: 147-151
Hieber AD, Robert C, Bugos RC, Harry Y, Yamamoto HY. Plant lipocalins: Violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta, 2000, 1482: 84-91
Hodges DM, Andrews CJ, Johnson DA. Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. J Exp Bot, 1997, 48:1105-1113
Hodgson RAL, Orr GR, Raison JK. Inhibition of photosynthesis by chilling in light. Plant Sci Lett, 1987, 49:75-81
Hong SS, Xu DQ. Light-induced increase in initial chlorophyll fluorescence Fo level and the reversible inactivation of PS II reaction centers in soybean leaves. Photosynth Res, 1999, 61: 269-280
Horton P, Ruban A, Walts RG. Regulation of light harvesting in green plants Indication by nonphotochemical quenching of chlorophyll fluorescence. Physiol Plant, 1994, 106: 415-420
Horton P, Ruban AV, Walters RG. Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol, 1996, 47: 655-684
Horton P. Nonphotochemical quenching of chlorophyll fluorescence. In Light as an Energy Source and Information Carrier in Plant Physiology, R.C. Jennings, ed (New York: Plenum Press), 1996, pp. 99–111
Huner NPA, ?quist G, Hurry VM et al., Photosynthesis, phtotoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res, 1993, 37:19-39
Hurry V, Andersson JM, Chow WS, Osmond CB. Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll quenching or sensitivity to photoinhibition in vivo. Plant Physiol, 1997, 113: 639-648
Inoue K, Fujii T, Yokoyama E. The photoinhibition site of photosystem I in isolated chloroplasts under extremely reducing conditions. Plant Cell Physiol, 1989, 30:65-71
Inoue K, Sakurai H, Hiyama T. Photoinactivation of photosystem I in isolated chloroplasts. Plant Cell Physiol, 1986, 27: 961-968
Ivanov AG, Krol M, Maxwell D, Huner NP. Abscisic acid induced protection against photoinhibition of PS II correlates with enhanced activity of the xanthophyll cycle. FEBS Lett, 1995, 371: 61-64
Jakob B, Heber U. Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and relation to photoinactivation of photosystem I and II. Plant Cell Physiol, 1996, 37: 629-635
Jansson C, Maenpaa P. Site-directed mutagenesis for structure-function analysis of the photosystem II reaction center protein D1. Progr Bot, 1997, 58: 352-367
Jiao S, Emmanuel H, Guikema JA. High light stress inducing photoinhibition and protein degradation of photosystem I in Brassica rapa. Plant Sci, 2004, 167: 733-741
Jiné, Yokthongwattana K, Polle JEW, Melis A. Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. Plant Physiol, 2003, 132: 352-364
Johnson N, Horton P. The dissipation of excess excitation energy in British plant species. Plant Cell Environ, 1993, 16: 673-679
Juhler RK, Andreasson E, Yu-SG et al., Composition of photosystem pigments in thyakoid membrane vesicles from spinach. Photosynth Res, 1993, 35: 171-178
Kanwischer M, Porfirova S, Bergmüller E, D?rmann P. Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition, and oxidative stress. Plant Physiol, 2005, 137: 713–723.
Krause GH, Weis E. Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol, 1991, 42: 313-349
Krieger A, Moya I, Weis E. Energy-dependent quenching chlorophyll a fluorescence: effect of pH on stationary fluorescence and picosecond relaxation kinetics in thylakoid membranes and photosystem II preparations. Biochim Biophys Acta, 1992, 1102: 167
Külheim C, ?gren J, Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science, 2002, 297: 91–93.
Latowski D, Grzyb J, Strzalka K. The xanthophyll cycle—molecular mechanism and physiological significance. Acta Physiol Plant, 2004, 26: 197-212
Lee HY, Hong YN, Chow WS. Photoinactivation of photosystem II complex and photoprotection by non-functional neighbours in Capsicum annuum L. Leaves. Planta, 2001, 212: 332-342
Li XG, Duan W, Meng QW, Zou Q, Zhao SJ. The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant Cell Physiol, 2004, 45: 103-108
Li XG, Meng QW, Jiang GQ, Zou Q. The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. Photosynthetica, 2003, 41(2): 259-265
Li XP, Bj?rkman O, Grossman AR. A pigment binding protein essential for regulation of photosynthetic light harvesting. Nature, 2000, 403(27): 391-395
Li XP, Müller P, Gilmore AM, Niyogi KK. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proceedings of the National Academy of Sciences of the USA, 2002, 99: 15222–15227.
Liu P, Meng QW, Zou Q. Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. Photosynthetica, 2001, 39:467-472
Long SP, East TM, Baker NR. Chilling damage to photosynthesis in young Zea mays I. Effects of light and temperature variation on photosynthetic CO2 assimilation. J Exp Bot, 1983, 34:177-188
Long SP, Humphries S, Falkowski PG. Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol, 1994, 45: 633-662
Lunde C, Jnesen PE, Haldrup A. The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature, 2000, 408: 613-615
Maeda H, Sakuragi Y, Bryant DA, DellaPenna D. Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiol. 2005, 138: 1422–1435.
Marin E, Arvidsson PO, ?kerlund HE. The xanthophyll cycle, its regulation and components. Physiol Plant, 1997, 100: 806-816
Marin E, Nusssaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion PA. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J, 1996, 15: 2331-2342
Mattoo AK, Edelman M. Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci USA, 1987, 84: 1497-1501
Mead JF. Free radical mechanism of lipid damage, a consequence for cellular membranes. In Free Radical in Biology Chapter 2 (eds Pryor WA). Academic Press, New York, 1976
Miyake C, Asada K. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol, 1992, 33: 541-553
Müller P, Golan T, Niyogi KK. Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol, 2004, 134: 1163–1172
Müller P, Havaux M, Niyogi KK. Zeaxanthin deficiency enhances the light sensitivity of an ascorbate-deficient mutant of Arabidopsis thaliana. Plant Physiol, 2003, 133: 748–760
Müller P, Li XP, Niyogi KK. Non-photochemical quenching. A response to excess light energy. Plant Physiol, 2001, 125: 1558-1566
Murata N, Sato N, Takahashi N. Compositions and positional distributions of fatty acids in phospholipids from leaves of chilling-sensitive and chilling-resistant plants. Plant Cell Physiol, 1982, 23: 1071-1079
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta, 2007, 1767: 414-421
Niyogi KK, Grossman AR, Bj?rkman O. Arabidopsisi mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell, 1998, 10: 1121-1134
Niyogi KK, Bj?rkman O, Grossman AR. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell, 1997, 9: 1369-1380
Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Bjorkman O. Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res, 2001, 67: 139-145
Niyogi KK. Photoprotection revisited: Genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol, 1999, 50: 333-359
Noctor G, Foyer CH. Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol, 1998, 49: 249-279
North HM, Frey A, Boutin JP, Sotta B, Marion-Poll A. Analysis of xanthophyll cycle gene expression during the adaptation of Arabidopsis to excess light and drought stress: Changes in RNA steady-state levels do not contribute to short-term responses. Plant Sci,2005, 169: 115-124
Ogawa K, Kenematsu S, Takabe K Asada K. Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection by immuno-gold labelling after rapid freezing and substitution method. Plant Cell Physiol, 1995, 36: 565-573
?quist DG, Chow WS, Anderson JM. Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta, 1992, 186: 450-457
Ort DR, Yocum CF. Electron transfer transduction in photosynthesis: an overview. In: Ort DR, Yocum CF (eds). Oxygenic photosynthesis: the Light Reactions. Dordrecht, Kluwer Academic, 1996, 4: 1-9
Owens TG, Shreve AP, Albrecht AC. Dynamics and mechanism of singlet energy transfer between carotenoids and chlorophylls: light harvesting and nonphotochemical fluorescence quenching. In N Murata, eds, Research in Photosynthesis, Vol 4. Kluwer Academic Publishers, Dordrecht, The Netherlands, 1992, pp. 179-186
Pastenes C, Horton P. Effect of photosynthesis in beans. Plant Physiol, 1996, 112: 1253-1260
Pastenes C, Pimentel P, Lillo J. Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot, 2005, 56: 425-433
Pearcy RW, Sims DA. Photosynthetic acclimation to changing light environments: scaling from the leaf to the whole plant. In Exploitation of Environmental Heterogeneity by Plants: Ecophysiological Processes Above-and Below Ground (eds M.M. Caldwell & R.W. Pearcy) pp. 145–174, 1994, Academic Press, Inc., San Diego, CA, USA.
Pfündel E, Bilger W. Regulation and possible function of the violaxanthin cycle. Photosynth Res, 1994, 42: 89-109
Phillip Y and Young AJ. Occurrence of the carotenoid lactucaxanthin in higher plant LHCII. Photosynth Res, 1995, 43: 273-282
Pogson B, McDonald KA, Truong M, Britton G, DellaPenna D. Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell, 1996, 8: 1627-1639
Pogson BJ, Niyogi KK, Bj?rkman O. Altered xanthophylls compositions adversely affect chlorophyll accumulation and non-photo-chemical quenching in Arabisopsis mutant. Proc Natl Acad Sci USA, 1998, 95:13324-29
Powles SB. Photoinhibition of photosynthesis induced by visible light. Annu Rev PlantPhysiol, 1984, 35: 15–44
Prásil O, Adir N, Ohad I. Dynamics of Photosystem II: Mechanism of photoinhibition and recovery process. In: Barber NR, Bowyer JR (eds) Topics in photosynthesis, Vol 11, the photosystems: structure, function, and molecular biology. Oxford: Elsevier Scientific Publisher, 1992, 295-348
Quinones MA, Zeiger A. A putative role of the xanthophyll,zeaxanthin in blue light photoreaction of corn coleoptiles. Science, 1994, 264: 558-561.
Rock CD, Zeevaart JAD. The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci USA , 1991, 88: 7496-7499
Rockholm DC, Yamamoto H Y. Violaxanthin de-epoxidase. Plant Physiol, 1996, 110: 697-703
Ruban AV, Young AJ, Pasca AA. The effect of illumination on the xanthophyll composition of the photosystem II light harvesting complexes of spinach thylakoid membrane. Plant Physiol, 1994, 104:227-234
Sairam Pk, Srivastava GC. Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci, 2002, 162: 897-904
Salin ML. Toxic oxygen species and protective systems of the chloroplast. Physiol Plant, 1988, 72: 681-689
Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning. A Laboratory Manual, 2nd Edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989
Sarry JE, Montillet JL, Sauvire Y. The protective function of the xanthophylls cycle in photosynthesis. FEBS Lett, 1994, 353:147-150
Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D. Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell, 2004, 16: 1419-1432.
Schansker G, Srivastava A, Govindjee, Strasser RJ. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol, 2003, 30: 785-796
Schindler C and Lichtenthaler HK. Photosynthetic CO2-assimilation, chlorophyll fluorescence and zeaxanthin accumulation in field grown maple trees in the course of a sunny and a cloudy day. J Plant Physiol, 1996, 148: 399-412
Schoner S, Krause GH. Protective systems against active oxygen species in spinach:Response to cold acclimation in excess light. Planta, 1990, 180: 383-389
Schreiber U, Bilger W, Neubauer C. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze, E.D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. pp. 49-70, 1994, Springer-Verlag, Berlin
Shen JR, Terashima I, Katok S. Cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves. Plant Physiol, 1990, 93: 1354-1357
Shunichi Takahashi and Norio Murata (2008) How do environmental stresses accelerate photoinhibition? Trends in Plant Sci. 13: 178-182
Siefermann D, Yamamoto HY. Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts: a transmembrane model for the violaxanthin cycle. Biochim Biophys Acta, 1975a, 387: 149-158
Siefermann D, Yamamoto HY. NADPH and oxygen-dependent epoxidation of zeaxanthin in isolated chloroplasts. Biochem Biophys Res Commun, 1975b, 62: 456-461
Song XS, Hu WH, Mao WH, Ogweno JO, Zhou YH, Yu JQ. Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. Plant Physiol Biochem, 2005, 43: 1082-1088
Sonoike K. Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol, 1995, 36: 825-830
Sonoike K. Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: Possible involvement of active oxygen species. Plant Sci, 1996a, 115: 157-164
Sonoike K. Photoinhibition of photosystem I: Its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol, 1996b, 37: 239-247
Sonoike K, Kamo M, Hihara Y, Enami I. The mechanism of the degradation of psaB gene product, one of the photosynthetic reaction center subunits of photosystem I, upon photoinhibition. Photosynth Res, 1997, 53: 55-63
Sonoike K, Terashima I. Mechanism of photosystem I photoinhibition in leaves of Cucumis sativus L. Planta, 1994, 194: 287-293
Sonoike K, Terashima I, Iwaki M, Itoh S. Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett, 1995, 362: 235-238
Sujak A, Gabrielska J, Grudzinski W, Borc R, Mazurek P, Gruszecki WI. Lutein and zeaxanthin as protectorsof lipid membranes against oxidative damage: the structural aspects. Arch Biochem Biophys, 1999, 371: 301-307
Sukenik A, Wyman KD, Bennett J, Falkowski PG. A novel mechanism for regulating the excitation of photosystem II in a green alga. Nature, 1987, 327: 704-707.
Tardy F, Havaux M. Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim Biophys Acta, 1997, 1330: 179-193
Tardy F, Havaux M. Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. J Photochem Photobiol B, 1996, 34: 87-94
Telfer A, Dhami S, Bishop SM, Phillips D, Barber J. Beta-carotene quenches singlet oxygen formed by isolated photosystem II reaction centers. Biochemistry, 1994, 33: 14469-14474
Terashima I, Funayama S, Sonoike K. The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not system II. Planta, 1994, 193: 300-306
Terashima I, Huang LR, Osmond CB. Effects of leaf chilling on thylakoid functions measured at room temperature in Cucumis sativus L. and Oryza sativa L. Plant Cell Physiol, 1989a, 30: 841-850
Terashima I, Shen JR, Katoh S. Chilling damage in cucumber (Cucumis sativus L.) thylakoids. In Plant Water Relations and Growth under Stress (eds. M Tazawa, M Katsumi, Y Masuda and H. Okamoto) Yamada Science Foundation, Osaka and My K K, Tokyo, 1989b, 470-472
Thayer SS, Bj?rkman O. Carotenoid distribution and deepoxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynth Res, 1992, 33: 213-225
Thiele A, Krause GH. Xanthophyll cycle and thermal energy dissipation in photosystem II: Relationship between zeaxanthin formation, energy dependent fluorescence quenching and photoinhibition. J Plant Physiol, 1994, 144: 324-332
Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB. Abscisic acid biosynthesis in tomato: Regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol, 2000, 42: 833-845
Tjus SE, Moller BL, Scheller HV. Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol, 1998, 116: 755-764
Tjus SE, Scheller HV, Andersson B, Moller BL. Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. Plant Physiol, 2001, 125: 2007-2015
van Kooten O, Snel JPH. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res, 1990, 25: 147-150
Verhoeven AS, Adams WW III, Demmig-Adams B, Croce R, Bassi R. Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major. Plant Physiol, 1999, 120: 727-738
Verhoeven AS, Bugos RC, Yamamoto HY. Transgenic tobacco with suppressed zeaxanthin formation is susceptible to stress-induced photoinhibition. Photosynth Res, 2001, 67: 27-39.
Walker DA. The use of O2 electrode and fluorescence probes in simple measurements of photosynthesis. Robert Hill Institute, University of Sheffield, UK, 1990
Walters RG, Horton P. Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus. Planta, 1994, 195: 248-256.
William W, Adams WW III, Demming-Adams B. The xanthophyll cycle, protein turnover, and the high tolerance of sun-acclimated leaves. Plant Physiol, 1993, 103: 1413-1420
Wise RR, Naylor AW. Chilling-enhanced photooxidation. Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol, 1987, 83:278-282
Woitsch S, R?mer S. Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol, 2003, 132: 1508-1517
Xu CC, Jeon YA, Lee CH. Relative contributions of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. Physiol Plant, 1999a, 107: 447-453
Xu CC, Kuang T, Li L, Lee CH. D1 protein turnover and carotene synthesis in relation to zeathanthin epoxidation in rice leaves during recovery from low temperature photoinhibition. Aust J Plant Physiol, 2000b, 27: 239-244
Xu CC, Lee HY, Lee CH. Recovery from low temperature photoinhibition is not governed by changes in the level of zeaxanthin in rice. J Plant Physiol, 1999b, 155: 755-761
Xu CC, Li L, Kuang T. Photoprotection in chilling-sensitive and–resistant plants illuminated at a chilling temperature: role of the xanthophyll cycle in the protection against lumen acidification. Aust J Plant Physiol, 2000a, 27: 669-675
Xu CC, Lin RC, Li LB, Kuang TY. Increase in resistance to low temperature photoinhibition following ascorbate feeding is attributable to an enhanced xanthophyll cycle activity in rice (Oryza sativa L.) leaves. Photosynthetica, 2000c, 38: 221-226
Yamamoto HY. Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem, 1979, 51: 639-648
Yamamoto HY, Higashi RM. Violaxanthin de-epoxidase lipid composition and substrate specificity. Arch Biochem Biophys, 1978, 190: 514-522
Yamamoto HY, Nakayama TOM, Chichester CO. Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys, 1962, 97: 168-173
Zhao SJ, Meng QW, Xu CC, Han HY, Zou Q. Analysis of xanthophyll cycle components in plant tissues by high performance liquid chromatography. Plant Physiol Commun, 1995, 31: 438-442
陈少裕。膜脂过氧化对植物细胞的伤害。植物生理学通讯, 1991, 27(2): 84-90
董高峰,陈贻竹。植物叶黄素循环与非辐射能量耗散。植物生理学通讯, 1999, 35(2): 141-146
郭连旺,沈允钢。高等植物光合机构避免强光破坏的保护机制。植物生理学通讯, 1996, 32: 1-8
郭连旺,许大全,沈允钢。田间棉花叶片光合速率中午下降的原因。植物生理学报, 1995, 20: 360-366
刘鸿先,王以柔,郭俊彦。低温对植物细胞膜系统伤害机理的研究。中国科学院华南植物研究所集刊, 1989,第5集: 31-38
林荣呈,许长成,李良壁,匡廷云。叶黄素循环及其在光保护中的分子机理研究。植物学报,2002,44:379-383
李新国,段伟,孟庆伟,邹琦。PSI的低温光抑制。植物生理学通讯, 2002, 38(4): 375-381
李晓萍,陈贻竹。PSII光能耗散机制研究进展。生物化学与生物物理进展, 1996, 23(2): 145-149
谭新星,许大全,沈允钢。小麦叶片的状态转换涉及PSII向PSI激发能满溢的变化。植物生理学报, 1997, 23: 9-14
沈文飚,徐朗莱,叶茂炳,张荣铣。抗坏血酸过氧化物酶活性测定的探讨。植物生理学通讯, 1996, 32: 203-205
王爱国,罗广华。植物的超氧物自由基与羟胺反应的定量关系。植物生理学通讯, 1990, 6: 55-57
吴长艾,孟庆伟,邹琦。叶黄素循环及其调控。植物生理学通讯,2001,37:1-5
许大全。植物光合作用的光抑制。植物生理学通讯, 1992, 28(4): 237-243
许大全。光系统II反应中心的可逆失活及其生理意义。植物生理学通讯, 1999, 35(4): 273-276
阳成伟,陈贻竹。叶黄素循环酶。广西植物, 2002, 22(3): 264-267
叶济宇。叶绿体的电子传递。见:余叔文,汤章城主编.植物生理与分子生物学。北京:科学出版社, 1998, 198-211
赵世杰。植物生理学实验指导。北京:中国农业出版社, 1998, 161-165
赵世杰,许长成,孟庆伟等。植物组织中叶黄素循环组分的高效液相色谱分析法。植物生理学通讯,1995,31:438-442
Adams WW III, Demmig-Adams B, Logan BA. Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania Japonica And Smilax Australis, growing in the under storey of an open eucalyptus forest. Plant, Cell and Environment, 1999, 22: 125-136
Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH.‘Photoinhibition’during winter stress: Involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol, 1995, 22: 261-276
Allen DJ, Ort DR. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci, 2001, 6: 36-42
Alscher RG, Donahue JL, Cramer CL. Reactive oxygen species and antioxidants: Relationships in green cells. Physiol Plant, 1997, 100: 224-233
Anderson JM, Aro EM. Arana stacking and protection of photosystem II in thylakoid membranes of higher plant leavesunder sustained high irradiance. Photosynth Res, 1994, 41:315-326
Anderson JM, Osmond CB. Shade-sun responses: compromises between acclimation and photoinhibition. In Photoinhibition (eds D.J. Kyle, C.B. Osmond & C.J. Arntzen) pp. 1–38, 1987, Elsevier, Amsterdam, the Netherlands
Aro EM, Kettunen R, Tyystjrvi E. ATP and light regulated D1 protein modification and degradation. Role of D1 in photoinhibition. FEBS Lett, 1992, 297: 29-33
Aro EM, Virgin I, Andersson B. Photoinhibition of photosystem II: Inactivation, protein damage and turnover. Biochim Biophys Acta, 1993, 1143: 113–134
Arvidsson PO, Bratt CE, Carlsson M, ?kerlund HE. Purification and identification of the violaxanthin deepoxidase as a 43 kda protein. Photosynth Res, 1996, 49: 119–129
Arvidsson PO, Carlsson M, Stefánsson H, Albertsson P? and ?kerlund HE. Violaxanthin accessibility and temperature dependency for de-epoxidation in spinach thylakoid membranes. Photosynth Res, 1997, 52: 39-48
Asada K. Ascorbate peroxidase—a hydrogen peroxidescavenging enzyme in plants. Physiol Plant, 1992, 85: 235-241
Asada K. Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (ed). Cause of photooxidative Stress and Amelioration of Defense Systems in Plants. Boca Raton: CRC Press, 1994, 77-104
Asada K, Takahashi M. Production and scavenging of active oxygen in photosynthesis. In Photoinhibition (eds Kyle DJ, Osmond CB, Amtzen CJ). pp. 227-287, 1987, Elsevier Science Publishers, Amsterdam.
Audran C, Borel C, Frey A, Sotta B, Meyer C, Simonneau T, Marion-Poll A. Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol, 1998, 118: 1021–1028
Bailey S, Horton P, Walters RG. Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta, 2004, 218: 793–802
Bailey S, Walters RG., Jansson S, Horton P. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta, 2001, 213: 794–801.
Barber J, Andersson B. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci, 1992, 17: 61-66
Barber J. Molecular basis of the vulnerability of photosystem II to damage by light. Aust J Plant Physiol, 1995, 22:201-208
Barber J, Norris J, Morris EP, Zheleva D, Hankamer B. The structure, function and dynamics of photosystem two. Physiol Plant, 1997, 100: 817-828
Baroli I, Do AD, Yamane T, Niyogi KK. Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects chlamydomonas reinhardtii from photooxidative stress. Plant Cell, 2003, 15: 992-1008
Bertamini M, Muthuchelian K, Rubinigg M, Zorer R, Velasco R, Nedunchezhian N. Low-night temperature increased the photoinhibition of photosynthesis in grapevine (Vitis vinifera L. cv. Riesling) leaves. Environ Exp Bot, 2006, 57: 25-31
Bj?rkman O. Responses to different quantum flux densities.In Physiological Plant Ecology I: Responses to the Physical Environment (eds O.L. Lange, S. Nobel, C.B. Osmond, H. Ziegler) pp. 57–107, 1981, Springer-Verlag, Berlin, Germany
Boese SR, Hüner NPA. Developmental history affects the susceptibility of spinach leaves to in vivo low temperature photoinhibition. Physiol Plant, 1992, 99: 1141-1145
Büch K, Stransky H, Hager A. FAD is a further essential cofactor of the NAD(P)H and O2-dependent zeaxanthin-epoxidase. FEBS Lett, 1995, 376: 45-48
Bugos RC, Hieber D, Yamamoto HY. Xanthophyll cycle enzymes are members of the lipcolin finity, the first identified from plants. J Biol Chem, 1998, 273 (25): 15321-15324
Cakmak I, Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol, 1992, 98: 1222-1227
Campbell D, Bruce D, Carpenter C, Gustafsson P, ?quist G. Two forms of the Photosystem II D1 protein after energy dissipation and state transition in the cyanobacterium Synechocystis sp. PCC 7942. Photosynth Res, 1996, 47: 131-144
Chang SH, Bugos RC, Sun WH., Yamamoto HY. Antisense suppression of violaxanthin de-epoxidase in tobacco does not affect plant performance in controlled growth conditions. Photosynth Res, 2000, 64: 95–103
Cleland R, Melis A, Neale PJ. Mechanism of photoinhibition: photochemical reaction center inactivation in system II of chloroplasts. Photosynth Res, 1986, 9: 79-88
Conklin PL, Williams EH, Last RL. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proceedings of the National Academy of Sciences of the USA, 1996, 93: 9970–9974.
Cornic G, Bukhov NG, Wiese C et al., Flexible coupling between light-dependent electron and vectorial proton transport in illuminated leaves of C3 plant. Role of photosystem I-dependent proton pumping. Planta, 2000, 210: 468-477
Dalton DA, Hanus FJ, Russell SA, Evans HJ. Purification, properties, and distribution of ascorbate peroxidase in legume root nodules. Plant Physiol, 1987, 83: 789-794
Darkóé, Váradi G, Lemoine Y, Lehoczki E. Defensive strategies agaist high light stress in wild and D1 protein mutant biotypes of Erigeron canadensis. Aust J Plant Physiol, 2000, 27: 325-333
Demmig-Adams B, Adams WW III . Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol, 1992, 43: 599–626
Demmig-Adams B, Adams WW III. Harvesting light safely. Nature, 2000, 403 (27): 371-374
Demmig-Adams B, Adams WW III. Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta, 1996, 198: 460-470
Demmig-Adams B, Winter K, Czyger F. Photoinhibition and zeaxanthin formation in intactLeaves. Plant Physiol, 1987, 84:218-224
Demmig-Adams B, Winter K, Krger A, Czygan FC. Zeaxanthin synthesis, energy dissipation, and phototection of photosystem II at chilling temporation. Plant Physiol, 1989, 90:894-898
Demmig-Adams B. Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta, 1990, 1020: 1–24.
Durocher D, Jackson SP. The FHA domain. FEBS Lett, 2002, 513: 58-66
Eichelmann H and Laisk A. Cooperation of photosystems II and I in leaves as analyzed by simultaneous measurements of chlorophyll fluorescence and transmittance at 800nm. Plant Cell Physiol, 2000, 41: 138-147
Endo T, Shikanai T, Takabayashi A, Asada K, Sato F. The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett, 1999, 457: 5-8
Escoubas JM, Lomas M, Laroche J, Falkowski PG. Light intensity regulation of cab gene transcription is signaled by the redox state of plastoquinone pool. PNAS, 1995, 92: 10237-102341
Eskling M, Arvidsson PO, ?kerlund HE. The xanthophyll cycle, its regulation and components. Physiol Plant, 1997, 100: 806-816
Eskling M, Emanuelsson A, ?kerlund HE. Enzymes and mechanisms for violaxanthin-zeaxanthin conversion. In EM Aro and B Andersson, eds, Regulation of Photosynthesis, Kluwer Academic Publishers, The Netherlands, 2001, pp. 433-452
Feierabend J, Schaan C, Hertwig B. Photoinactivation of catalase occurs under both high-and low-temperature stress conditions and accompanies photoinhibition of photosystem II. Physiol Plant, 1992, 100: 1554-1561
Foyer CH, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta, 1976, 133: 21-25
Foyer CH, Lelandais M, Kunert KJ. Photooxidative stress in plants. Physiol Plant, 1994, 92: 696–717
Foyer CH, Lelandais M. A comparison of the relative rate of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. J Plant Physiol, 1996, 148: 391-398
Frommolt R, Goss R, Wilhelm C. The de-epoxidase and epoxidase reactions of Mantoniella squamata (Prasinophyceae) exhibit different substrate-specific reaction kinetics comparedto spinach. Planta, 2001, 213: 446-456
Gerber DW, Burris JE. Photoinhibition and P700 in the marine diatom Amphora sp. Plant Physiol, 1981, 68: 699-702
Giannopolitis CN, Ries SK. Superoxide Dismutases. I. Occurrence in higher plants. Plant Physiol, 1977, 59: 309-314
Gillham DJ, Dodge AD. Chloroplast superoxide and hydrogen peroxide scavenging systems from pea leaves: Seasonal variations. Plant Sci, 1987, 50: 105–109
Gilmore AM, Hazlett TL, Govindjee. Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: Formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci USA, 1995, 92: 2273-2277
Gilmore AM, Mohanty N, Yamamoto HY. Epoxidation of zeaxanthin and antheraxanthin reverses non-photochemical quenching of photosystem II chlorophyll a fluorescence in the presence of trans-thylakoid delta pH. FEBS Lett, 1994, 350: 271-274
Gilmore AM. Mechanistic aspects of xanthophylls cycle dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant, 1997, 99: 197-209
Gilmore AM. Xanthophyll cycle-dependent nonphotochemical quenching in photosystem II: Mechanistic insights gained from Arabidopsis thaliana L. mutants that lack violaxanthin deepoxidase activity and/or lutein. Photosynth Res, 2001, 67: 89-101
Golbeck JH. Structure and function of photosystem I. Annu Rev Plant Physiol Plant Mol Biol, 1992, 43:293-324
Golbeck JH. Structure, function and organization of the photosystem I reaction center complex. Biochim Biophys Acta, 1987, 895:167-204
Golbeck JH, Bryant DA. Photosystem I. Curr Top Bioenerg, 1991, 16: 3-177
Golden SS, Brusslan J, Haselkorn R. Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J, 1986, 5: 2789-2798
Goss R, Bohme K, Wilhelm C. The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: Consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta, 1998, 205: 613-621
Graβes T, Pesaresi P, Schiavon F, Varotto C, Salamini F, Jahns P, Leister D. The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against lightinduced damage in Arabidopsis thaliana. Plant Physiology and Biochemistry, 2002,40: 41–49
Greer GH, Berry JA, Bj?rkman O. Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature and requirement for chloroplast-protein synthesis during recovery. Planta, 1986, 168: 253-257
Gruszecki WI, Strzalka K. Does the xanthophyll cycle take part in the regulation of fluidity of the thylakoid membrane? Biochim Biophys Acta, 1991, 1060: 310-314
Hager A. Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta, 1969, 89: 224-243
Hager A. Die reversiblen, lichtabhangigen xanthophyll umwandlungen im chloroplasten. Ber Dtsch Bot Ges, 1975, 88: 27- 44
Hager A. The reversible, light-induced conversions of xanthophylls in the chloroplast. In FC Czygan, eds. Pigments in Plants. Fischer, Stuttgart, 1980, pp 57-79
Haldrup A, Jensen PE, Lunde C, Scheller HV. Balance of power: a view of the mechanism of photosynthetic state transitions. Tren Plant Sci, 2001, 6: 301-305
Hartel H, Lokstein H, Grimm B and Rank B. Kinetic studies on the xanthophyll cycle in barley leaves: Influence of antenna size and relations to nonphotochemical chlorophyll fluorescence quenching. Plant Physiol, 1996, 110: 471-482
Havaux M, Bonfils JP, Lütz C, Niyogi KK. Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin deepoxidase. Plant Physiol, 2000, 124: 273–284.
Havaux M, Dall'Osto L, CuinèS, Giuliano G, Bassi R. The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. J Biol Chem, 2004, 279: 13878-13888
Havaux M, Davaud A. Photoinhibition of photosynthesis in chilled potato leaves is not correlated with loss of photosysthem II activity. Preferential inactivation of Photosystem I. Photosynth Res, 1994, 40: 75-92
Havaux M, Gruszecki WI, Dupont I and Leblanc RM. Increased heat emission and its relationship to the xanthophylls cycle in pea leaves exposed to strong light stress. J Photochem Photobiol, 1991, 8: 361–370
Havaux M, Niyogi KK. The violaxanthin cycle protects plants from photooxidative damageby more than one mechanism. Proc Natl Acad Sci USA, 1999, 96: 8762-8767
Havaux M, Tardy F, Ravenel J, Parot P. Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochrochromic shift in intact potato leaves: influence of the xanthophyll content. Plant Cell Environ, 1996, 19: 1359-1368
Havaux M. Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci, 1998, 3: 147-151
Hieber AD, Robert C, Bugos RC, Harry Y, Yamamoto HY. Plant lipocalins: Violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta, 2000, 1482: 84-91
Hodges DM, Andrews CJ, Johnson DA. Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. J Exp Bot, 1997, 48:1105-1113
Hodgson RAL, Orr GR, Raison JK. Inhibition of photosynthesis by chilling in light. Plant Sci Lett, 1987, 49:75-81
Hong SS, Xu DQ. Light-induced increase in initial chlorophyll fluorescence Fo level and the reversible inactivation of PS II reaction centers in soybean leaves. Photosynth Res, 1999, 61: 269-280
Horton P, Ruban A, Walts RG. Regulation of light harvesting in green plants Indication by nonphotochemical quenching of chlorophyll fluorescence. Physiol Plant, 1994, 106: 415-420
Horton P, Ruban AV, Walters RG. Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol, 1996, 47: 655-684
Horton P. Nonphotochemical quenching of chlorophyll fluorescence. In Light as an Energy Source and Information Carrier in Plant Physiology, R.C. Jennings, ed (New York: Plenum Press), 1996, pp. 99–111
Huner NPA, ?quist G, Hurry VM et al., Photosynthesis, phtotoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res, 1993, 37:19-39
Hurry V, Andersson JM, Chow WS, Osmond CB. Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll quenching or sensitivity to photoinhibition in vivo. Plant Physiol, 1997, 113: 639-648
Inoue K, Fujii T, Yokoyama E. The photoinhibition site of photosystem I in isolated chloroplasts under extremely reducing conditions. Plant Cell Physiol, 1989, 30:65-71
Inoue K, Sakurai H, Hiyama T. Photoinactivation of photosystem I in isolated chloroplasts. Plant Cell Physiol, 1986, 27: 961-968
Ivanov AG, Krol M, Maxwell D, Huner NP. Abscisic acid induced protection against photoinhibition of PS II correlates with enhanced activity of the xanthophyll cycle. FEBS Lett, 1995, 371: 61-64
Jakob B, Heber U. Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and relation to photoinactivation of photosystem I and II. Plant Cell Physiol, 1996, 37: 629-635
Jansson C, Maenpaa P. Site-directed mutagenesis for structure-function analysis of the photosystem II reaction center protein D1. Progr Bot, 1997, 58: 352-367
Jiao S, Emmanuel H, Guikema JA. High light stress inducing photoinhibition and protein degradation of photosystem I in Brassica rapa. Plant Sci, 2004, 167: 733-741
Jiné, Yokthongwattana K, Polle JEW, Melis A. Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. Plant Physiol, 2003, 132: 352-364
Johnson N, Horton P. The dissipation of excess excitation energy in British plant species. Plant Cell Environ, 1993, 16: 673-679
Juhler RK, Andreasson E, Yu-SG et al., Composition of photosystem pigments in thyakoid membrane vesicles from spinach. Photosynth Res, 1993, 35: 171-178
Kanwischer M, Porfirova S, Bergmüller E, D?rmann P. Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition, and oxidative stress. Plant Physiol, 2005, 137: 713–723.
Krause GH, Weis E. Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol, 1991, 42: 313-349
Krieger A, Moya I, Weis E. Energy-dependent quenching chlorophyll a fluorescence: effect of pH on stationary fluorescence and picosecond relaxation kinetics in thylakoid membranes and photosystem II preparations. Biochim Biophys Acta, 1992, 1102: 167
Külheim C, ?gren J, Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science, 2002, 297: 91–93.
Latowski D, Grzyb J, Strzalka K. The xanthophyll cycle—molecular mechanism and physiological significance. Acta Physiol Plant, 2004, 26: 197-212
Lee HY, Hong YN, Chow WS. Photoinactivation of photosystem II complex and photoprotection by non-functional neighbours in Capsicum annuum L. Leaves. Planta, 2001, 212: 332-342
Li XG, Duan W, Meng QW, Zou Q, Zhao SJ. The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant Cell Physiol, 2004, 45: 103-108
Li XG, Meng QW, Jiang GQ, Zou Q. The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. Photosynthetica, 2003, 41(2): 259-265
Li XP, Bj?rkman O, Grossman AR. A pigment binding protein essential for regulation of photosynthetic light harvesting. Nature, 2000, 403(27): 391-395
Li XP, Müller P, Gilmore AM, Niyogi KK. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proceedings of the National Academy of Sciences of the USA, 2002, 99: 15222–15227.
Liu P, Meng QW, Zou Q. Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. Photosynthetica, 2001, 39:467-472
Long SP, East TM, Baker NR. Chilling damage to photosynthesis in young Zea mays I. Effects of light and temperature variation on photosynthetic CO2 assimilation. J Exp Bot, 1983, 34:177-188
Long SP, Humphries S, Falkowski PG. Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol, 1994, 45: 633-662
Lunde C, Jnesen PE, Haldrup A. The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature, 2000, 408: 613-615
Maeda H, Sakuragi Y, Bryant DA, DellaPenna D. Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiol. 2005, 138: 1422–1435.
Marin E, Arvidsson PO, ?kerlund HE. The xanthophyll cycle, its regulation and components. Physiol Plant, 1997, 100: 806-816
Marin E, Nusssaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion PA. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J, 1996, 15: 2331-2342
Mattoo AK, Edelman M. Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci USA, 1987, 84: 1497-1501
Mead JF. Free radical mechanism of lipid damage, a consequence for cellular membranes. In Free Radical in Biology Chapter 2 (eds Pryor WA). Academic Press, New York, 1976
Miyake C, Asada K. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol, 1992, 33: 541-553
Müller P, Golan T, Niyogi KK. Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol, 2004, 134: 1163–1172
Müller P, Havaux M, Niyogi KK. Zeaxanthin deficiency enhances the light sensitivity of an ascorbate-deficient mutant of Arabidopsis thaliana. Plant Physiol, 2003, 133: 748–760
Müller P, Li XP, Niyogi KK. Non-photochemical quenching. A response to excess light energy. Plant Physiol, 2001, 125: 1558-1566
Murata N, Sato N, Takahashi N. Compositions and positional distributions of fatty acids in phospholipids from leaves of chilling-sensitive and chilling-resistant plants. Plant Cell Physiol, 1982, 23: 1071-1079
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta, 2007, 1767: 414-421
Niyogi KK, Grossman AR, Bj?rkman O. Arabidopsisi mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell, 1998, 10: 1121-1134
Niyogi KK, Bj?rkman O, Grossman AR. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell, 1997, 9: 1369-1380
Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Bjorkman O. Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res, 2001, 67: 139-145
Niyogi KK. Photoprotection revisited: Genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol, 1999, 50: 333-359
Noctor G, Foyer CH. Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol, 1998, 49: 249-279
North HM, Frey A, Boutin JP, Sotta B, Marion-Poll A. Analysis of xanthophyll cycle gene expression during the adaptation of Arabidopsis to excess light and drought stress: Changes in RNA steady-state levels do not contribute to short-term responses. Plant Sci,2005, 169: 115-124
Ogawa K, Kenematsu S, Takabe K Asada K. Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection by immuno-gold labelling after rapid freezing and substitution method. Plant Cell Physiol, 1995, 36: 565-573
?quist DG, Chow WS, Anderson JM. Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta, 1992, 186: 450-457
Ort DR, Yocum CF. Electron transfer transduction in photosynthesis: an overview. In: Ort DR, Yocum CF (eds). Oxygenic photosynthesis: the Light Reactions. Dordrecht, Kluwer Academic, 1996, 4: 1-9
Owens TG, Shreve AP, Albrecht AC. Dynamics and mechanism of singlet energy transfer between carotenoids and chlorophylls: light harvesting and nonphotochemical fluorescence quenching. In N Murata, eds, Research in Photosynthesis, Vol 4. Kluwer Academic Publishers, Dordrecht, The Netherlands, 1992, pp. 179-186
Pastenes C, Horton P. Effect of photosynthesis in beans. Plant Physiol, 1996, 112: 1253-1260
Pastenes C, Pimentel P, Lillo J. Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot, 2005, 56: 425-433
Pearcy RW, Sims DA. Photosynthetic acclimation to changing light environments: scaling from the leaf to the whole plant. In Exploitation of Environmental Heterogeneity by Plants: Ecophysiological Processes Above-and Below Ground (eds M.M. Caldwell & R.W. Pearcy) pp. 145–174, 1994, Academic Press, Inc., San Diego, CA, USA.
Pfündel E, Bilger W. Regulation and possible function of the violaxanthin cycle. Photosynth Res, 1994, 42: 89-109
Phillip Y and Young AJ. Occurrence of the carotenoid lactucaxanthin in higher plant LHCII. Photosynth Res, 1995, 43: 273-282
Pogson B, McDonald KA, Truong M, Britton G, DellaPenna D. Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell, 1996, 8: 1627-1639
Pogson BJ, Niyogi KK, Bj?rkman O. Altered xanthophylls compositions adversely affect chlorophyll accumulation and non-photo-chemical quenching in Arabisopsis mutant. Proc Natl Acad Sci USA, 1998, 95:13324-29
Powles SB. Photoinhibition of photosynthesis induced by visible light. Annu Rev PlantPhysiol, 1984, 35: 15–44
Prásil O, Adir N, Ohad I. Dynamics of Photosystem II: Mechanism of photoinhibition and recovery process. In: Barber NR, Bowyer JR (eds) Topics in photosynthesis, Vol 11, the photosystems: structure, function, and molecular biology. Oxford: Elsevier Scientific Publisher, 1992, 295-348
Quinones MA, Zeiger A. A putative role of the xanthophyll,zeaxanthin in blue light photoreaction of corn coleoptiles. Science, 1994, 264: 558-561.
Rock CD, Zeevaart JAD. The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci USA , 1991, 88: 7496-7499
Rockholm DC, Yamamoto H Y. Violaxanthin de-epoxidase. Plant Physiol, 1996, 110: 697-703
Ruban AV, Young AJ, Pasca AA. The effect of illumination on the xanthophyll composition of the photosystem II light harvesting complexes of spinach thylakoid membrane. Plant Physiol, 1994, 104:227-234
Sairam Pk, Srivastava GC. Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci, 2002, 162: 897-904
Salin ML. Toxic oxygen species and protective systems of the chloroplast. Physiol Plant, 1988, 72: 681-689
Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning. A Laboratory Manual, 2nd Edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989
Sarry JE, Montillet JL, Sauvire Y. The protective function of the xanthophylls cycle in photosynthesis. FEBS Lett, 1994, 353:147-150
Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D. Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell, 2004, 16: 1419-1432.
Schansker G, Srivastava A, Govindjee, Strasser RJ. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol, 2003, 30: 785-796
Schindler C and Lichtenthaler HK. Photosynthetic CO2-assimilation, chlorophyll fluorescence and zeaxanthin accumulation in field grown maple trees in the course of a sunny and a cloudy day. J Plant Physiol, 1996, 148: 399-412
Schoner S, Krause GH. Protective systems against active oxygen species in spinach:Response to cold acclimation in excess light. Planta, 1990, 180: 383-389
Schreiber U, Bilger W, Neubauer C. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze, E.D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. pp. 49-70, 1994, Springer-Verlag, Berlin
Shen JR, Terashima I, Katok S. Cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves. Plant Physiol, 1990, 93: 1354-1357
Shunichi Takahashi and Norio Murata (2008) How do environmental stresses accelerate photoinhibition? Trends in Plant Sci. 13: 178-182
Siefermann D, Yamamoto HY. Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts: a transmembrane model for the violaxanthin cycle. Biochim Biophys Acta, 1975a, 387: 149-158
Siefermann D, Yamamoto HY. NADPH and oxygen-dependent epoxidation of zeaxanthin in isolated chloroplasts. Biochem Biophys Res Commun, 1975b, 62: 456-461
Song XS, Hu WH, Mao WH, Ogweno JO, Zhou YH, Yu JQ. Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. Plant Physiol Biochem, 2005, 43: 1082-1088
Sonoike K. Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol, 1995, 36: 825-830
Sonoike K. Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: Possible involvement of active oxygen species. Plant Sci, 1996a, 115: 157-164
Sonoike K. Photoinhibition of photosystem I: Its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol, 1996b, 37: 239-247
Sonoike K, Kamo M, Hihara Y, Enami I. The mechanism of the degradation of psaB gene product, one of the photosynthetic reaction center subunits of photosystem I, upon photoinhibition. Photosynth Res, 1997, 53: 55-63
Sonoike K, Terashima I. Mechanism of photosystem I photoinhibition in leaves of Cucumis sativus L. Planta, 1994, 194: 287-293
Sonoike K, Terashima I, Iwaki M, Itoh S. Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett, 1995, 362: 235-238
Sujak A, Gabrielska J, Grudzinski W, Borc R, Mazurek P, Gruszecki WI. Lutein and zeaxanthin as protectorsof lipid membranes against oxidative damage: the structural aspects. Arch Biochem Biophys, 1999, 371: 301-307
Sukenik A, Wyman KD, Bennett J, Falkowski PG. A novel mechanism for regulating the excitation of photosystem II in a green alga. Nature, 1987, 327: 704-707.
Tardy F, Havaux M. Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim Biophys Acta, 1997, 1330: 179-193
Tardy F, Havaux M. Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. J Photochem Photobiol B, 1996, 34: 87-94
Telfer A, Dhami S, Bishop SM, Phillips D, Barber J. Beta-carotene quenches singlet oxygen formed by isolated photosystem II reaction centers. Biochemistry, 1994, 33: 14469-14474
Terashima I, Funayama S, Sonoike K. The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not system II. Planta, 1994, 193: 300-306
Terashima I, Huang LR, Osmond CB. Effects of leaf chilling on thylakoid functions measured at room temperature in Cucumis sativus L. and Oryza sativa L. Plant Cell Physiol, 1989a, 30: 841-850
Terashima I, Shen JR, Katoh S. Chilling damage in cucumber (Cucumis sativus L.) thylakoids. In Plant Water Relations and Growth under Stress (eds. M Tazawa, M Katsumi, Y Masuda and H. Okamoto) Yamada Science Foundation, Osaka and My K K, Tokyo, 1989b, 470-472
Thayer SS, Bj?rkman O. Carotenoid distribution and deepoxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynth Res, 1992, 33: 213-225
Thiele A, Krause GH. Xanthophyll cycle and thermal energy dissipation in photosystem II: Relationship between zeaxanthin formation, energy dependent fluorescence quenching and photoinhibition. J Plant Physiol, 1994, 144: 324-332
Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB. Abscisic acid biosynthesis in tomato: Regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol, 2000, 42: 833-845
Tjus SE, Moller BL, Scheller HV. Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol, 1998, 116: 755-764
Tjus SE, Scheller HV, Andersson B, Moller BL. Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. Plant Physiol, 2001, 125: 2007-2015
van Kooten O, Snel JPH. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res, 1990, 25: 147-150
Verhoeven AS, Adams WW III, Demmig-Adams B, Croce R, Bassi R. Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major. Plant Physiol, 1999, 120: 727-738
Verhoeven AS, Bugos RC, Yamamoto HY. Transgenic tobacco with suppressed zeaxanthin formation is susceptible to stress-induced photoinhibition. Photosynth Res, 2001, 67: 27-39.
Walker DA. The use of O2 electrode and fluorescence probes in simple measurements of photosynthesis. Robert Hill Institute, University of Sheffield, UK, 1990
Walters RG, Horton P. Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus. Planta, 1994, 195: 248-256.
William W, Adams WW III, Demming-Adams B. The xanthophyll cycle, protein turnover, and the high tolerance of sun-acclimated leaves. Plant Physiol, 1993, 103: 1413-1420
Wise RR, Naylor AW. Chilling-enhanced photooxidation. Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol, 1987, 83:278-282
Woitsch S, R?mer S. Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol, 2003, 132: 1508-1517
Xu CC, Jeon YA, Lee CH. Relative contributions of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. Physiol Plant, 1999a, 107: 447-453
Xu CC, Kuang T, Li L, Lee CH. D1 protein turnover and carotene synthesis in relation to zeathanthin epoxidation in rice leaves during recovery from low temperature photoinhibition. Aust J Plant Physiol, 2000b, 27: 239-244
Xu CC, Lee HY, Lee CH. Recovery from low temperature photoinhibition is not governed by changes in the level of zeaxanthin in rice. J Plant Physiol, 1999b, 155: 755-761
Xu CC, Li L, Kuang T. Photoprotection in chilling-sensitive and–resistant plants illuminated at a chilling temperature: role of the xanthophyll cycle in the protection against lumen acidification. Aust J Plant Physiol, 2000a, 27: 669-675
Xu CC, Lin RC, Li LB, Kuang TY. Increase in resistance to low temperature photoinhibition following ascorbate feeding is attributable to an enhanced xanthophyll cycle activity in rice (Oryza sativa L.) leaves. Photosynthetica, 2000c, 38: 221-226
Yamamoto HY. Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem, 1979, 51: 639-648
Yamamoto HY, Higashi RM. Violaxanthin de-epoxidase lipid composition and substrate specificity. Arch Biochem Biophys, 1978, 190: 514-522
Yamamoto HY, Nakayama TOM, Chichester CO. Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys, 1962, 97: 168-173
Zhao SJ, Meng QW, Xu CC, Han HY, Zou Q. Analysis of xanthophyll cycle components in plant tissues by high performance liquid chromatography. Plant Physiol Commun, 1995, 31: 438-442