菠菜对海水胁迫响应的生理机制研究
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摘要
海洋面积占地球表面积的70%,蓄水量达1.34×1018m3,约为地球水资源的96.8%,利用海水进行作物生产,是解决人类食物问题的有效途径。菠菜(Spinacia oleranceaL.)是一种中等耐盐作物,其耐盐临界值为2ds·m-1,利用海水栽培菠菜的可行性较大。本文以2个耐性性不同的菠菜品种为试材,采用水培方法,研究了菠菜对海水胁迫响应的生理机制。主要结果如下：
在14个供试菠菜品种中,‘荷兰3号’对海水胁迫的耐性最强,而‘圆叶菠菜’最敏感；40%的海水浓度是鉴定菠菜耐海水能力的适宜浓度。用含40%海水的营养液栽培菠菜,菠菜的综合品质没有明显变化。
海水胁迫对‘荷兰3号’单株干重影响不大,而显著降低‘圆叶菠菜’的单株干重；并使2个品种植株的叶片和根系丙二醛(MDA)含量增加,质膜透性增大,叶片光合色素含量降低,但‘荷兰3号’的变化幅度(叶片MDA除外)小于‘圆叶菠菜’。海水胁迫下,短期内2个品种由于气孔限制引起叶片胞间C02浓度(Ci)降低,净光合速率(Pn)下降；长期胁迫下,‘荷兰3号’Pn恢复到对照水平,而‘圆叶菠菜’同化力下降,Pn降低。叶绿素荧光动力学分析表明,海水胁迫对‘荷兰3号’光化学猝灭系数(qP)影响不大,实际光化学效率(ΦPSⅡ)明显升高,而使‘圆叶菠菜’qP和ΦPSⅡ下降；‘荷兰3号’初始荧光(F0)的下降幅度和非光化学猝灭系数(qN)上升幅度比‘圆叶菠菜’大；2个菠菜品种的最大光化学效率(Fv/Fm)均下降,但‘荷兰3号’光抑制程度(1-qP/qN)的升高幅度比圆叶菠菜小。这些结果说明,海水胁迫下,2个耐性不同的菠菜品种植株都产生了光合作用的光抑制和光氧化伤害,使膜质过氧化和叶绿素(Chl)含量降低,但海水胁迫对耐性强的品种影响较小
海水胁迫下,菠菜植株的表观量子效率(AQY)和饱和光强下的Pn均显著下降,天线耗散能量(D)的比率和非光化学瘁灭系数(NPQ)上升；NPQ和叶黄素脱环氧化状态(DES)的动态变化、日变化随海水胁迫时间的延长及光合有效辐射(PAR)的变化而呈现先升高后降低的趋势,并且二者之间具有多项式回归关系；抗坏血酸(AsA)处理显著提高了菠菜叶片的NPQ和DES,而二硫苏糖醇(DTT)处理却使其显著降低；且海水敏感品种‘圆叶菠菜’叶片的AQY和饱和光强下Pn的降低幅度大于耐海水品种‘荷兰3号’,而D. NPQ和DES的升高幅度小于后者。这些结果说明,海水胁迫下菠菜植株受到了光合作用的光抑制,非辐射能量耗散增强,叶黄素循环是其热耗散的主要途径；耐海水品种‘荷兰3号’由于叶黄素循环活性较高,能够将较多的过剩光能耗散,有效降低了过剩光能对光合器官的损害。
海水胁迫下,2个菠菜品种叶绿体内超氧阴离子自由基(O2-)、过氧化氢(H2O2)等ROS大量积累,MDA含量升高,膜系统受到了损伤；耐海水品种‘荷兰3号’叶绿体内清除ROS主要依赖于超氧化物歧化酶(SOD)、抗坏血酸过氧化物酶(APX)和谷胱甘肽还原酶(GR),对ROS的清除能力较强,并且氧化型谷胱甘肽(GSSG)还原为还原型谷胱甘肽(GSH)运转正常,维持了叶绿体内合适的氧化还原环境；而海水敏感品种‘圆叶菠菜’叶绿体清除ROS主要依赖SOD和过氧化物酶(POD),清除能力有限,从而造成ROS大量积累,对叶绿体的伤害较大,并且叶绿体内GSH/GSSG显著下降,适宜的氧化还原环境被破坏,耐性降低。
海水胁迫下,菠菜叶绿体内ROS积累,ROS通过降低胆色素原脱氨酶(PBGD)活性,使Chl生物合成步骤的胆色素原(PBG)向尿卟啉原Ⅲ(UroⅢ)的转化受阻,从而导致菠菜叶片Chl含量降低。海水胁迫下,耐海水品种‘荷兰3号’由于叶黄素循环活性较高,可以将较多的过剩光能以非辐射能量的方式耗散,降低了光系统Ⅱ(PSⅡ)反应中心由激发态能量诱发的ROS对Chl合成的阻抑作用,并且对叶绿素酶(Chlase)活性没有明显影响；而海水敏感品种‘圆叶菠菜’叶黄素循环活性较低,ROS对Chl合成的阻抑作用较大,并且Chlase活性显著升高,加速了Chl降解,进一步降低了Chl含量,表明较高的叶黄素循环活性通过降低叶绿体内ROS水平来减轻对Chl合成的阻抑程度,并防止了Chlase活性升高,从而使Chl含量维持在较高的水平。
海水胁迫下,光氧化剂甲基紫精(MV)进一步使2个菠菜品种叶绿体内O2-产生速率加快、H2O2含量提高、膜质过氧化加重,活性氧清除剂AsA明显降低了菠菜叶绿体内ROS水平,缓解了由MV造成的严重的膜质过氧化伤害。海水胁迫下,2个菠菜品种叶片叶绿素b (Chlb)、叶绿素a(Chla)及其合成前体物质原叶绿素酸(Pchl)、镁原卟啉Ⅸ(Mg-ProtoⅨ)、原卟啉Ⅸ(ProtoⅨ)和尿卟啉原Ⅲ(UroⅢ)含量明显降低,而胆色素原(PBG)和6-氨基酮戊酸(ALA)积累,Chl合成受到阻碍,并且‘圆叶菠菜,的受阻程度大于‘荷兰3号’；MV进一步加剧了这种受阻程度,而AsA部分缓解了由海水胁迫和MV造成的阻碍作用。上述结果说明,由海水胁迫诱导的菠菜叶绿体内ROS与Chl代谢密切相关,不仅通过叶绿体膜的氧化伤害使Chl降解,而且使Chl合成的PBG向UroⅢ转化步骤受阻。耐海水品种‘荷兰3号’叶绿体清除ROS主要通过SOD和AsA-GSH循环系统,清除能力较强,减轻了ROS对叶绿体膜的氧化损伤和Chl合成的受阻程度,并且海水胁迫对其Chlase活性的影响较小；而海水敏感品种‘圆叶菠菜’叶绿体清除ROS主要依赖于SOD和POD,对ROS的清除能力有限,从而导致了ROS大量积累,叶绿体膜的氧化损伤和Chl合成的受阻程度严重,并且海水胁迫显著提高了Chlase活性,加剧了Chl降解。
海水胁迫下,菠菜植株体内的离子平衡被打破；可溶性糖、游离氨基酸和Cl-对2个菠菜品种植株渗透调节的相对贡献较大。耐海水品种‘荷兰3号’植株体内可溶性糖含量大量积累；根系和叶柄向叶片选择性运输较高含量的K+、Ca2+、Mg2+和SO42-而运输的Na+和Cl-较少；植株体内蛋白质分解和游离氨基酸积累量较低；甜菜碱和脯氨酸对维持根系和叶片渗透平衡中发挥了重要作用；质膜H+-ATPase和液泡膜H+-ATPase活性、叶绿体Ca2+-ATPase和Mg2+-ATPase活性维持较高水平,离子外排和区域化能力较强。而海水敏感品种‘圆叶菠菜’植株体内蛋白质分解,离子选择性吸收和运输比率较低,植株体内积累了大量的游离氨基酸、Na+和Cl-,并且胞内离子外排和区域化能力低。上述结果说明,根系和叶柄向叶片选择性运输较高含量的K+、Ca2+、Mg2+和SO42,是提高耐海水能力的离子选择性吸收策略；在应对海水诱导的渗透胁迫中,提高植株可溶性糖、甜菜碱和脯氨酸含量并降低可溶性蛋白降解和游离氨基酸含量,是菠菜提高耐性的有机渗透调节物质积累策略；而较强的离子外排和区域化能力是胞内离子环境调节策略。
Water resources in the ocean correspond to the capacity to be about 1.34×1018 m3 which is equivalent to 96.8% of total water of the earth. However, the freshwater on land has an inclination to be lacking. Now, researchers have attempted to cultivate crops by irrigation using seawater for food supply. Spinach (Spinacia olerancea L.) plants are a middle salt tolerant crop, which critical salt concentration is 2 d-S m-1. Therefore, it is supposed to be possible to cultivate spinach plants by using seawater. The physiological response to seawater stress was investigated using two cultivars plants cultured in the Hoagland's nutrients solution with or without seawater (40%). Main research results were as follows:
Spinach cultivar such as Helan No.3 was the greatest tolerant to seawater and cv. Yuanye was greatest sensitivity amony fourteen compared cultivars. The appropriate concentration identified was 10% of seawater. And the integrative quality of spinach plants was not enfluenced by nutrient solution with 40% seawater.
Dry weight per plant of cv. Helan No.3 was not obviously affected by seawater, but cv. Yuanye spinach was decreased remarkably. During exposure to stress of seawater, malondialdehyde (MDA) content and membrane permeability were both increased, but photo-pigment of leaves was reduced, and theirs change range of cv. Helan No.3 was little than cv. Yuanye spinach (except MDA content of leaves). Stomata limitation of two spinach cultivars induced decrease of intercellular CO2 concentration (Ci) and net photosynthetic rate (Pn) in short term on stress of seawater, however, in long term on stress of seawater, Pn of cv. Helan No.3 resumed to control level, but Pn of cv. Yuanye spinach continued to decrease as a result of assimilation decreased. The analyse of chlorohyll fluorescence kinetica parameters shows that there was little effect on photochemical quenching (qP) of cv.Helan No.3 but quantum yield of PSⅡphotochemisty rate (ΦPSⅡ) increased obviously under seawater stress, that of Yuanye spinach declined when exposure to stress seawater; Decrease amplitude and increase range of cv. Helan No.3 were greater than that of cv. Yuanye spinach; Maximal photochemical efficiency (Fv/Fm) of two spinach cultivars were declined, but the increase of photo-inhibition degree (1-qP/qN) of cv. Yuanye spinach was higher than cv. Helan No.3 under seawater stress. These results suggest that two spinach cultivars were injured by photo-inhibition and photo-oxidation on seawater stress, that lead lipid to peroxidize and chlorophyll (Chl) to decompose; however, tolerance cultivars such as cv. Helan No.3 applied more light energy to photochemical reaction, and caloric dissipation ability was strong, which was depended on xanthophylls cycle; degree of photo-inhibition was lower, reactive oxygen species (ROS), which was excited by excess light energy, were less destroyed membrane system and photopigment to maintained a higher level of Pn, there for, seawater stress had little effect on growth.
Apparent quanta yield (AQY) and Pn on saturation photo intensity were remarkably decreased but the allocation of dissipation energy (D) by antenna and non-fluorescence quenching coefficient (NPQ) were increased by the stress of seawater; daily and dynamic movements of NPQ and xanthophyll de-epoxidation state (DES) were presented trends to increased at first and then decreased with extend of stress time and photosynthetic active radiation (PAR) increased during exposure to seawater stress, furthermore, there were played some multinomial regress relationship between NPQ and DES; when treated with ascorbic acid (AsA), NPQ and DES were remarkably increased but decreased by 1, 4-dithiothreitol (DTT); during exposure to seawater stress, AQY and Pn under saturation photo intensity of Yuanye spinach was decrease more than that of cv. Helan No.3, and the increase of D, NPQ and DES were less than that of cv. Helan No.3. These results suggested that photo-inhibition was produced and non-radiant energy was enhanced, and xanthophyll cycle was major approach to thermal dissipation; cv. Helan No.3 has more high activity of de-epoxidation as a result of dissipating excessive energy to decease injury of photosynthesis organs.
The production rate of superoxide radical (O2-), content of hydrogen peroxide (H2O2) and MDA in chloroplasts of two spinach cultivars were remarkably increased by seawater with higher rate in cv. Yuanye; In seawater tolerant cultivar (cv. Helan No.3), the ROS elimination is mainly depended on superoxide dismutase (SOD) and ascorbic acid-reduced glutathione recycle system (AsA-GSH), which could alleviate oxidation injury of ROS to chloroplast membrane, and the conversion of glutathione (GSSG) into reduced glutathione (GSH) was maintained to keep correct oxidation and deoxidation circumstance in chloroplasts of spinach leaves during exposure to seawater; while in seawater sensitive cultivar (cv. Yuanye), it is mainly depended on SOD and peroxidase (POD), which has limited ability to eliminate ROS and lead to accumulate mass ROS to severe oxidation injury of chloroplast membrane, and the ratio of GSH/GSSG in chloroplasts was significant decreased by seawater, leading to disturbing of oxidation and deoxidation circumstance in chloroplasts, as a result of declination of seawater tolerance.
Spinach plants with seawater were induced to oxidize metabolic substances and to accumulate ROS in chloroplasts of two cultivars to lower the activity of porphobilinogen deaminase (PBGD). Namely, the conversion of porphobilinogen (PBG) into uroporphyrinogenⅢ(UroⅢ) concerning in chlorophyll biosynthetic processes was inhibited by supplying seawater. In Helan No.3 spinach plants with seawater, higher activity of xanthophyll cycle in the leaves played a role of regulation to suppress more excess light energy in order to lower the levels of ROS in chloroplasts. Therefore, the chlorophyll biosynthesis in Helan No.3 leaves with seawater showed quite a weak inhibition and the activity of chlorophllase (Chlase) was not affected by seawater stress. However, more accumulation of ROS in chloroplasts of Yuanye leaves due to the lower activity of xanthophyll cycle severely inhibited the chlorophyll biosynthetic process and remarkably enhanced the activity of Chlase which aggravates the decomposition of chlorophyll. These results suggest that higher activity of xanthophyll cycle regulates to keep chlorophyll metabolic process by decreasing levels of ROS in chloroplasts of spinach plants cultured in the nutrient solution with seawater (40%).
The supplement of methyl viologen (MV), the photo-oxidant, enhanced the production rate of O2-, the content of H2O2 and MDA in chloroplast of two spinach cultivars, while the addition of AsA, the eliminator for ROS, decreased ROS level and alleviated oxidization of plasmolemma. The content of chlorophyll b (Chlb), chlorophyll a (Chla) and precursor of Chl such as protochlorophyll (Pchl), Mg-protoporphyrinⅨ(Mg-ProtoⅨ), protoporphyrinⅨ(ProtoⅨ) and uroorphyrinogenⅢ(UroⅢ) was remarkably decreased, but the content of porphobilinogen (PBG) andδ-aminolevulinic acid (ALA) was increased by the stress of seawater, which lead to inhibition for Chl synthesis, and the inhibition was aggravated by MV and eliminated by AsA. Chlorophyllase (Chlase) activity in the leaves of cv. Yuanye was improved while it was not influenced in the leaves of Helan No.3 under seawater stress. The Chlase activity in the leaves of cv. Yuanye was more greatly affected by MV treatment than that of Helan No.3, however, Chlase activity of two cultivars was not influenced by AsA. These results suggest that ROS is closely related to Chl metabolism, which not only injure plasmolemma but also inhibit the process of transformation of PBG to UroⅢas a result of Chl decomposition. In seawater tolerant cultivar (cv. Helan No.3), the ROS elimination is mainly depended on SOD and AsA-GSH system, which could alleviate oxidation injury of ROS to chloroplast membrane and inhibition of Chl synthesis, and Chlase activity was less influenced by seawater stress; while in seawater sensitive cultivar (cv. Yuanye), it is mainly depended on SOD and POD, which has limited ability to eliminate ROS and lead to accumulate mass ROS to severe oxidation injury of chloroplast membrane and inhibition of Chl synthesis, and Chlase activity was significantly improved by seawater stress, which enhanced Chl decomposition.
Ionic homeostasis in spinach plants was disturbed by the stress of seawater. Relative contribution of osmolytes such as soluble sugar, free amino acid and Cl- to osmotic adjustment was greater than that of others. In cv. Helan No.3 (tolerant cultivar), soluble sugar was mass accumulated during exposure to seawater, and the selective transport of K+, Ca2+, Mg2+ and SO42- from roots and petioles to leaves was more than that of Na+ and Cl-. Besides, decomposition of proteins and accumulation of free amino acids in seawater stressed plants of cv. Helan No.3 were lower than that in cv. Yuanye; under seawater stress, betaine and proline played a very important role in osmotic balance of roots and leaves, respectively. Plasma membrane H+ -adenosine-5'-triphosphate (H+-ATPase) and tonoplast H+-ATPase were remarkably enhanced, which effectively propelled excess ions to exclude out of cytoplasm and compartmentalized in vacuole, and the activity of Ca2+ -ATPase and Mg2+ -ATPase in chloroplasts were greater than that in cv. Yuanye under seawater stress, which help to propel excess Ca2+ and Mg2+ in cytoplasm transport into chloroplasts, therefore, the levels of Ca2+ and Mg2+ in cytoplasm was stabilized. However, decomposition of protein in leaves of cv. Yuanye (sensitive cultivar) was enhanced by seawater, and the selective transport of ions was lower, these resulted in accumulation of free amino acids, Na+ and Cl- by seawater. During seawater stress, lower ionic exclusion and compartmentalization of cv. Yuanye resulted in mass ionic accumulation in cytoplasm under seawater stress. Therefore, the damage to cells and chloroplasts of cv. Yuanye was more than that of cv. Helan No.3. In summary, greater ability of absorption to K+, Ca2+, Mg2+ and SO42- in leaves and compartmentalization to Na+ and Cl- in the roots and petioles to maintain higher ratio of K/Na, Mg/Na, Ca/Na and SO42-/Cl- and to protect the leaves from excessive Na+ and Cl- toxicity was strategy of ionic selective transportation and absorption against seawater stress; the higher efficiency of the compatible solute accumulation, lower decomposition of proteins and production of free amino acids can be considered as some factors responsible for its tolerance to seawater stress; and higher abilities of ionic exclusion and compartmentalization were regulatory strategy of intracellular ions cellular level against seawater stress.
在14个供试菠菜品种中,‘荷兰3号’对海水胁迫的耐性最强,而‘圆叶菠菜’最敏感；40%的海水浓度是鉴定菠菜耐海水能力的适宜浓度。用含40%海水的营养液栽培菠菜,菠菜的综合品质没有明显变化。
海水胁迫对‘荷兰3号’单株干重影响不大,而显著降低‘圆叶菠菜’的单株干重；并使2个品种植株的叶片和根系丙二醛(MDA)含量增加,质膜透性增大,叶片光合色素含量降低,但‘荷兰3号’的变化幅度(叶片MDA除外)小于‘圆叶菠菜’。海水胁迫下,短期内2个品种由于气孔限制引起叶片胞间C02浓度(Ci)降低,净光合速率(Pn)下降；长期胁迫下,‘荷兰3号’Pn恢复到对照水平,而‘圆叶菠菜’同化力下降,Pn降低。叶绿素荧光动力学分析表明,海水胁迫对‘荷兰3号’光化学猝灭系数(qP)影响不大,实际光化学效率(ΦPSⅡ)明显升高,而使‘圆叶菠菜’qP和ΦPSⅡ下降；‘荷兰3号’初始荧光(F0)的下降幅度和非光化学猝灭系数(qN)上升幅度比‘圆叶菠菜’大；2个菠菜品种的最大光化学效率(Fv/Fm)均下降,但‘荷兰3号’光抑制程度(1-qP/qN)的升高幅度比圆叶菠菜小。这些结果说明,海水胁迫下,2个耐性不同的菠菜品种植株都产生了光合作用的光抑制和光氧化伤害,使膜质过氧化和叶绿素(Chl)含量降低,但海水胁迫对耐性强的品种影响较小
海水胁迫下,菠菜植株的表观量子效率(AQY)和饱和光强下的Pn均显著下降,天线耗散能量(D)的比率和非光化学瘁灭系数(NPQ)上升；NPQ和叶黄素脱环氧化状态(DES)的动态变化、日变化随海水胁迫时间的延长及光合有效辐射(PAR)的变化而呈现先升高后降低的趋势,并且二者之间具有多项式回归关系；抗坏血酸(AsA)处理显著提高了菠菜叶片的NPQ和DES,而二硫苏糖醇(DTT)处理却使其显著降低；且海水敏感品种‘圆叶菠菜’叶片的AQY和饱和光强下Pn的降低幅度大于耐海水品种‘荷兰3号’,而D. NPQ和DES的升高幅度小于后者。这些结果说明,海水胁迫下菠菜植株受到了光合作用的光抑制,非辐射能量耗散增强,叶黄素循环是其热耗散的主要途径；耐海水品种‘荷兰3号’由于叶黄素循环活性较高,能够将较多的过剩光能耗散,有效降低了过剩光能对光合器官的损害。
海水胁迫下,2个菠菜品种叶绿体内超氧阴离子自由基(O2-)、过氧化氢(H2O2)等ROS大量积累,MDA含量升高,膜系统受到了损伤；耐海水品种‘荷兰3号’叶绿体内清除ROS主要依赖于超氧化物歧化酶(SOD)、抗坏血酸过氧化物酶(APX)和谷胱甘肽还原酶(GR),对ROS的清除能力较强,并且氧化型谷胱甘肽(GSSG)还原为还原型谷胱甘肽(GSH)运转正常,维持了叶绿体内合适的氧化还原环境；而海水敏感品种‘圆叶菠菜’叶绿体清除ROS主要依赖SOD和过氧化物酶(POD),清除能力有限,从而造成ROS大量积累,对叶绿体的伤害较大,并且叶绿体内GSH/GSSG显著下降,适宜的氧化还原环境被破坏,耐性降低。
海水胁迫下,菠菜叶绿体内ROS积累,ROS通过降低胆色素原脱氨酶(PBGD)活性,使Chl生物合成步骤的胆色素原(PBG)向尿卟啉原Ⅲ(UroⅢ)的转化受阻,从而导致菠菜叶片Chl含量降低。海水胁迫下,耐海水品种‘荷兰3号’由于叶黄素循环活性较高,可以将较多的过剩光能以非辐射能量的方式耗散,降低了光系统Ⅱ(PSⅡ)反应中心由激发态能量诱发的ROS对Chl合成的阻抑作用,并且对叶绿素酶(Chlase)活性没有明显影响；而海水敏感品种‘圆叶菠菜’叶黄素循环活性较低,ROS对Chl合成的阻抑作用较大,并且Chlase活性显著升高,加速了Chl降解,进一步降低了Chl含量,表明较高的叶黄素循环活性通过降低叶绿体内ROS水平来减轻对Chl合成的阻抑程度,并防止了Chlase活性升高,从而使Chl含量维持在较高的水平。
海水胁迫下,光氧化剂甲基紫精(MV)进一步使2个菠菜品种叶绿体内O2-产生速率加快、H2O2含量提高、膜质过氧化加重,活性氧清除剂AsA明显降低了菠菜叶绿体内ROS水平,缓解了由MV造成的严重的膜质过氧化伤害。海水胁迫下,2个菠菜品种叶片叶绿素b (Chlb)、叶绿素a(Chla)及其合成前体物质原叶绿素酸(Pchl)、镁原卟啉Ⅸ(Mg-ProtoⅨ)、原卟啉Ⅸ(ProtoⅨ)和尿卟啉原Ⅲ(UroⅢ)含量明显降低,而胆色素原(PBG)和6-氨基酮戊酸(ALA)积累,Chl合成受到阻碍,并且‘圆叶菠菜,的受阻程度大于‘荷兰3号’；MV进一步加剧了这种受阻程度,而AsA部分缓解了由海水胁迫和MV造成的阻碍作用。上述结果说明,由海水胁迫诱导的菠菜叶绿体内ROS与Chl代谢密切相关,不仅通过叶绿体膜的氧化伤害使Chl降解,而且使Chl合成的PBG向UroⅢ转化步骤受阻。耐海水品种‘荷兰3号’叶绿体清除ROS主要通过SOD和AsA-GSH循环系统,清除能力较强,减轻了ROS对叶绿体膜的氧化损伤和Chl合成的受阻程度,并且海水胁迫对其Chlase活性的影响较小；而海水敏感品种‘圆叶菠菜’叶绿体清除ROS主要依赖于SOD和POD,对ROS的清除能力有限,从而导致了ROS大量积累,叶绿体膜的氧化损伤和Chl合成的受阻程度严重,并且海水胁迫显著提高了Chlase活性,加剧了Chl降解。
海水胁迫下,菠菜植株体内的离子平衡被打破；可溶性糖、游离氨基酸和Cl-对2个菠菜品种植株渗透调节的相对贡献较大。耐海水品种‘荷兰3号’植株体内可溶性糖含量大量积累；根系和叶柄向叶片选择性运输较高含量的K+、Ca2+、Mg2+和SO42-而运输的Na+和Cl-较少；植株体内蛋白质分解和游离氨基酸积累量较低；甜菜碱和脯氨酸对维持根系和叶片渗透平衡中发挥了重要作用；质膜H+-ATPase和液泡膜H+-ATPase活性、叶绿体Ca2+-ATPase和Mg2+-ATPase活性维持较高水平,离子外排和区域化能力较强。而海水敏感品种‘圆叶菠菜’植株体内蛋白质分解,离子选择性吸收和运输比率较低,植株体内积累了大量的游离氨基酸、Na+和Cl-,并且胞内离子外排和区域化能力低。上述结果说明,根系和叶柄向叶片选择性运输较高含量的K+、Ca2+、Mg2+和SO42,是提高耐海水能力的离子选择性吸收策略；在应对海水诱导的渗透胁迫中,提高植株可溶性糖、甜菜碱和脯氨酸含量并降低可溶性蛋白降解和游离氨基酸含量,是菠菜提高耐性的有机渗透调节物质积累策略；而较强的离子外排和区域化能力是胞内离子环境调节策略。
Water resources in the ocean correspond to the capacity to be about 1.34×1018 m3 which is equivalent to 96.8% of total water of the earth. However, the freshwater on land has an inclination to be lacking. Now, researchers have attempted to cultivate crops by irrigation using seawater for food supply. Spinach (Spinacia olerancea L.) plants are a middle salt tolerant crop, which critical salt concentration is 2 d-S m-1. Therefore, it is supposed to be possible to cultivate spinach plants by using seawater. The physiological response to seawater stress was investigated using two cultivars plants cultured in the Hoagland's nutrients solution with or without seawater (40%). Main research results were as follows:
Spinach cultivar such as Helan No.3 was the greatest tolerant to seawater and cv. Yuanye was greatest sensitivity amony fourteen compared cultivars. The appropriate concentration identified was 10% of seawater. And the integrative quality of spinach plants was not enfluenced by nutrient solution with 40% seawater.
Dry weight per plant of cv. Helan No.3 was not obviously affected by seawater, but cv. Yuanye spinach was decreased remarkably. During exposure to stress of seawater, malondialdehyde (MDA) content and membrane permeability were both increased, but photo-pigment of leaves was reduced, and theirs change range of cv. Helan No.3 was little than cv. Yuanye spinach (except MDA content of leaves). Stomata limitation of two spinach cultivars induced decrease of intercellular CO2 concentration (Ci) and net photosynthetic rate (Pn) in short term on stress of seawater, however, in long term on stress of seawater, Pn of cv. Helan No.3 resumed to control level, but Pn of cv. Yuanye spinach continued to decrease as a result of assimilation decreased. The analyse of chlorohyll fluorescence kinetica parameters shows that there was little effect on photochemical quenching (qP) of cv.Helan No.3 but quantum yield of PSⅡphotochemisty rate (ΦPSⅡ) increased obviously under seawater stress, that of Yuanye spinach declined when exposure to stress seawater; Decrease amplitude and increase range of cv. Helan No.3 were greater than that of cv. Yuanye spinach; Maximal photochemical efficiency (Fv/Fm) of two spinach cultivars were declined, but the increase of photo-inhibition degree (1-qP/qN) of cv. Yuanye spinach was higher than cv. Helan No.3 under seawater stress. These results suggest that two spinach cultivars were injured by photo-inhibition and photo-oxidation on seawater stress, that lead lipid to peroxidize and chlorophyll (Chl) to decompose; however, tolerance cultivars such as cv. Helan No.3 applied more light energy to photochemical reaction, and caloric dissipation ability was strong, which was depended on xanthophylls cycle; degree of photo-inhibition was lower, reactive oxygen species (ROS), which was excited by excess light energy, were less destroyed membrane system and photopigment to maintained a higher level of Pn, there for, seawater stress had little effect on growth.
Apparent quanta yield (AQY) and Pn on saturation photo intensity were remarkably decreased but the allocation of dissipation energy (D) by antenna and non-fluorescence quenching coefficient (NPQ) were increased by the stress of seawater; daily and dynamic movements of NPQ and xanthophyll de-epoxidation state (DES) were presented trends to increased at first and then decreased with extend of stress time and photosynthetic active radiation (PAR) increased during exposure to seawater stress, furthermore, there were played some multinomial regress relationship between NPQ and DES; when treated with ascorbic acid (AsA), NPQ and DES were remarkably increased but decreased by 1, 4-dithiothreitol (DTT); during exposure to seawater stress, AQY and Pn under saturation photo intensity of Yuanye spinach was decrease more than that of cv. Helan No.3, and the increase of D, NPQ and DES were less than that of cv. Helan No.3. These results suggested that photo-inhibition was produced and non-radiant energy was enhanced, and xanthophyll cycle was major approach to thermal dissipation; cv. Helan No.3 has more high activity of de-epoxidation as a result of dissipating excessive energy to decease injury of photosynthesis organs.
The production rate of superoxide radical (O2-), content of hydrogen peroxide (H2O2) and MDA in chloroplasts of two spinach cultivars were remarkably increased by seawater with higher rate in cv. Yuanye; In seawater tolerant cultivar (cv. Helan No.3), the ROS elimination is mainly depended on superoxide dismutase (SOD) and ascorbic acid-reduced glutathione recycle system (AsA-GSH), which could alleviate oxidation injury of ROS to chloroplast membrane, and the conversion of glutathione (GSSG) into reduced glutathione (GSH) was maintained to keep correct oxidation and deoxidation circumstance in chloroplasts of spinach leaves during exposure to seawater; while in seawater sensitive cultivar (cv. Yuanye), it is mainly depended on SOD and peroxidase (POD), which has limited ability to eliminate ROS and lead to accumulate mass ROS to severe oxidation injury of chloroplast membrane, and the ratio of GSH/GSSG in chloroplasts was significant decreased by seawater, leading to disturbing of oxidation and deoxidation circumstance in chloroplasts, as a result of declination of seawater tolerance.
Spinach plants with seawater were induced to oxidize metabolic substances and to accumulate ROS in chloroplasts of two cultivars to lower the activity of porphobilinogen deaminase (PBGD). Namely, the conversion of porphobilinogen (PBG) into uroporphyrinogenⅢ(UroⅢ) concerning in chlorophyll biosynthetic processes was inhibited by supplying seawater. In Helan No.3 spinach plants with seawater, higher activity of xanthophyll cycle in the leaves played a role of regulation to suppress more excess light energy in order to lower the levels of ROS in chloroplasts. Therefore, the chlorophyll biosynthesis in Helan No.3 leaves with seawater showed quite a weak inhibition and the activity of chlorophllase (Chlase) was not affected by seawater stress. However, more accumulation of ROS in chloroplasts of Yuanye leaves due to the lower activity of xanthophyll cycle severely inhibited the chlorophyll biosynthetic process and remarkably enhanced the activity of Chlase which aggravates the decomposition of chlorophyll. These results suggest that higher activity of xanthophyll cycle regulates to keep chlorophyll metabolic process by decreasing levels of ROS in chloroplasts of spinach plants cultured in the nutrient solution with seawater (40%).
The supplement of methyl viologen (MV), the photo-oxidant, enhanced the production rate of O2-, the content of H2O2 and MDA in chloroplast of two spinach cultivars, while the addition of AsA, the eliminator for ROS, decreased ROS level and alleviated oxidization of plasmolemma. The content of chlorophyll b (Chlb), chlorophyll a (Chla) and precursor of Chl such as protochlorophyll (Pchl), Mg-protoporphyrinⅨ(Mg-ProtoⅨ), protoporphyrinⅨ(ProtoⅨ) and uroorphyrinogenⅢ(UroⅢ) was remarkably decreased, but the content of porphobilinogen (PBG) andδ-aminolevulinic acid (ALA) was increased by the stress of seawater, which lead to inhibition for Chl synthesis, and the inhibition was aggravated by MV and eliminated by AsA. Chlorophyllase (Chlase) activity in the leaves of cv. Yuanye was improved while it was not influenced in the leaves of Helan No.3 under seawater stress. The Chlase activity in the leaves of cv. Yuanye was more greatly affected by MV treatment than that of Helan No.3, however, Chlase activity of two cultivars was not influenced by AsA. These results suggest that ROS is closely related to Chl metabolism, which not only injure plasmolemma but also inhibit the process of transformation of PBG to UroⅢas a result of Chl decomposition. In seawater tolerant cultivar (cv. Helan No.3), the ROS elimination is mainly depended on SOD and AsA-GSH system, which could alleviate oxidation injury of ROS to chloroplast membrane and inhibition of Chl synthesis, and Chlase activity was less influenced by seawater stress; while in seawater sensitive cultivar (cv. Yuanye), it is mainly depended on SOD and POD, which has limited ability to eliminate ROS and lead to accumulate mass ROS to severe oxidation injury of chloroplast membrane and inhibition of Chl synthesis, and Chlase activity was significantly improved by seawater stress, which enhanced Chl decomposition.
Ionic homeostasis in spinach plants was disturbed by the stress of seawater. Relative contribution of osmolytes such as soluble sugar, free amino acid and Cl- to osmotic adjustment was greater than that of others. In cv. Helan No.3 (tolerant cultivar), soluble sugar was mass accumulated during exposure to seawater, and the selective transport of K+, Ca2+, Mg2+ and SO42- from roots and petioles to leaves was more than that of Na+ and Cl-. Besides, decomposition of proteins and accumulation of free amino acids in seawater stressed plants of cv. Helan No.3 were lower than that in cv. Yuanye; under seawater stress, betaine and proline played a very important role in osmotic balance of roots and leaves, respectively. Plasma membrane H+ -adenosine-5'-triphosphate (H+-ATPase) and tonoplast H+-ATPase were remarkably enhanced, which effectively propelled excess ions to exclude out of cytoplasm and compartmentalized in vacuole, and the activity of Ca2+ -ATPase and Mg2+ -ATPase in chloroplasts were greater than that in cv. Yuanye under seawater stress, which help to propel excess Ca2+ and Mg2+ in cytoplasm transport into chloroplasts, therefore, the levels of Ca2+ and Mg2+ in cytoplasm was stabilized. However, decomposition of protein in leaves of cv. Yuanye (sensitive cultivar) was enhanced by seawater, and the selective transport of ions was lower, these resulted in accumulation of free amino acids, Na+ and Cl- by seawater. During seawater stress, lower ionic exclusion and compartmentalization of cv. Yuanye resulted in mass ionic accumulation in cytoplasm under seawater stress. Therefore, the damage to cells and chloroplasts of cv. Yuanye was more than that of cv. Helan No.3. In summary, greater ability of absorption to K+, Ca2+, Mg2+ and SO42- in leaves and compartmentalization to Na+ and Cl- in the roots and petioles to maintain higher ratio of K/Na, Mg/Na, Ca/Na and SO42-/Cl- and to protect the leaves from excessive Na+ and Cl- toxicity was strategy of ionic selective transportation and absorption against seawater stress; the higher efficiency of the compatible solute accumulation, lower decomposition of proteins and production of free amino acids can be considered as some factors responsible for its tolerance to seawater stress; and higher abilities of ionic exclusion and compartmentalization were regulatory strategy of intracellular ions cellular level against seawater stress.
引文
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