红砂和柠条脱水复水过程中的生理生态特性研究
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摘要
红砂和柠条是具极强耐旱性的多年生灌木。研究发现，在中度干旱条件下(上层土壤含水量分别为22.6％和21.1％)，这两种植物大部分叶片枯黄：极端干旱时(土壤含水量分别为2.54％和2.9％)，植物叶片脱落即遇旱休眠，复水后又长出新叶继续生长，此类植物可称为“复苏植物”。本文以这两种植物为对象，研究干旱胁迫→遇水复苏过程中光合活性、叶片和茎中渗透物质、碳水化合物代谢和酶活性、植物叶肉细胞和叶绿体超微结构等的变化，以期阐明遇旱休眠的复苏植物忍耐极端干旱的生理生态机理。主要研究结果如下：
1．水分胁迫导致了红砂和柠条净光合速率(Pn)的下降，但内在水分利用效率(WUE)在中度干旱条件下却明显提高。PSⅡ的最大光化学效率(Fv／Fm)和非循环式电子传递效率(Φ_(PSⅡ))随着干旱程度的增加而减小，并表现出午间光抑制现象。在中度干旱胁迫下，红砂叶片叶绿素含量上升，在极端干旱条件下含量下降，在柠条叶片中随着干旱胁迫的加重而下降。红砂和柠条经过53天干旱处理后，土壤上下层含水量分别降低到2.54％、3.47％和2.9％、12.89％，茎中的相对含水量分别达到了4.66％和10.15％时，这两种植物的叶片死亡，但茎仍然保持活力，进行微弱的光合作用，随后植物进入休眠状态。复水后茎的光合能力还很弱，PSⅡ的最大光化学效率和非循环式电子传递效率也很低。等完全长出叶片后，光合和荧光参数恢复正常。因此，红砂和柠条具有剪去叶片而减少水分丢失并维持茎细胞的活力来度过极端干旱的能力。
2．红砂幼苗叶片、成熟的红砂和柠条叶片和茎中脯氨酸和丙二醛含量随着干旱胁迫强度的增加而增加，复水后下降。可溶性蛋白含量在红砂幼苗和成熟的红砂叶片、柠条叶片和茎中下降，在成熟的红砂茎中上升。复水后，无论在叶片还是在茎中都呈上升趋势。持续干旱是红砂幼苗、成熟的红砂和柠条叶片和茎中淀粉、可溶性糖、非结构糖、蔗糖和果糖的累积，在茎中累积量更大。复水后，成熟的红砂茎中可溶性糖、蔗糖和果糖、柠条茎中可溶性糖和蔗糖含量迅速下降，成熟的红砂茎中淀粉和非结构糖、柠条茎中果糖、淀粉和非结构糖的含量在未长出叶片之前上升，长出叶片后迅速下降。在叶片中的含量随着复水时间的延长变化很大。干旱和复水期间碳水化合物的变化表明，在极端干旱条件下，红砂和柠条在茎中积累大量的碳水化合物，在土壤水分适宜的情况下，茎中积累的碳水化合物能够促使茎萌发出新叶而继续生长。
3．干旱期间，过氧化氢酶活性变化为：在红砂幼苗叶片和成熟的红砂茎中先上升后下降，成熟的红砂和柠条叶片中基本保持不变，柠条茎中上升。复水后，成熟的红砂和柠条茎中先下降后保持不变，在叶片中持续上升。干旱过程中，α-淀粉酶和β-淀粉酶活性在红砂和柠条叶片和茎中都呈上升态势。复水后，红砂茎中β-淀粉酶活性先下降后保持不变，红砂茎中α-淀粉酶和柠条茎中α-淀粉酶和β-淀粉酶活性在未长出叶片之前上升，长出叶片后迅速下降。红砂和柠条叶片中α-淀粉酶活性先上升后下降，β-淀粉酶活性持续上升。以叶片萌芽过程中，成熟的红砂和柠条茎中淀粉含量的降低(57日、63日、69日、79日和86日含量分别减去63日、69日、79日和86日和96日含量)作为淀粉水解参数。求得淀粉迅速水解期间茎中淀粉酶活性和淀粉水解参数之间的相关关系后，发现α-淀粉酶活性与淀粉水解参数呈显著正相关(红砂为：r~2=0.856，P=0.005、柠条的为：r~2=0.873，P=0.005)。β-淀粉酶和淀粉水解参数之间相关关系小(红砂r~2=0.449，P=0.117、柠条r~2=0.3426，P=0.124)。
4．解剖结构研究表明，红砂和柠条茎的亚细胞组织中普遍含有叶绿体。正常条件下，无论是茎还是叶片的亚细胞组织，叶绿体紧贴细胞壁。叶绿体中的类囊体排列整体有序。随着干旱的加剧，叶绿体脱离细胞壁，向细胞中央靠近。严重干旱造成了叶片叶肉细胞和叶绿体结构的不可恢复性的破坏，包括外膜和膜片层结构，类囊体膜解体，淀粉粒消失，部分细胞器裂解成碎片。而茎中的亚细胞组织和叶绿体都保持完整。落叶后，茎叶绿体中淀粉粒含量增加。复水以后，红砂和柠条分别于复水后的第6天和第4天新的叶片完全伸展开，并且合成了大量的叶绿素，红砂叶片叶绿体中淀粉粒含量减少，柠条叶片叶绿体中淀粉粒含量增加。这样重新组织了光合细胞器，这些功能的恢复为植物生存打下了良好的基础。
以上分析表明，这两种植物对干旱胁迫的适应主要是依赖于光系统、物质代谢、形态和结构以及信号传递等方面的保护，表现出与其它复苏植物类似的干旱胁迫响应及遇水后复苏的机制。由此证明，复苏植物不仅存在于非洲的热带、亚热带地区，而且在温带地区也存在。
Reaumuria soongorica and Caragana korshinskii are perennial semi-shrubs. We found that under medium drought stress (when soil water content in the upper layers reached 22.6% and 21.1% respectively), a majority of leaves of those two species turned scorch. Under severe drought stress (when soil water content reached 2.54% and 2.9%), all leaves shedd and the plants have died away. After re-hydration, they can stimulate new leaves and regrowth. Those plants are resurrection plants. This paper presented the studies on the changes of photosynthetic activities, metabolic products enzyme activities, anatomy and chloroplast ultrastructure, in those two species during the period of progressive drought stress and the mergence of new leaves and regrowth after re-hydration. The studies were analyzed and discussed to elucidate further the mechanisms of adaptation to desiccation tolerance during water stress. The main results were summarized as follows:
1. Pn declined during drought stress in R. soongorica and C. korshinskii, but intrinsic water use efficiency (WUE) increased remarkably under medium drought stress. The maximal photochemical efficiency of PSII (Fv/Fm) and the quantum efficiency of noncyclic electric transport of PS II (Φ_(PSII)) decreased significantly under drought stress and exhibited an obvious phenomenon of photoinhibition at noon. The chlorophyll content in R. soongorica had increased under medium drought stress and dropped only under severe drought stress, but had progressive dropped during the drought stress period in C. korshinskii. When soil water content in the layers 0-10cm and 10-25cm reached 2.54%, 3.47% and 2.9%, 12.89% respectively and stem relative water content reached 4.66% and 10.15% in R. soongorica and C. korshinskii after 53 days of drought stress, the leaves died and abscised. But the stems photosynthesis remained and, afterward plants entered dormant state. Upon rewatering, the stems photosynthesis were very feeble and the maximal photochemical efficiency of PSII and the quantum efficiency of noncyclic electric transport of PS II were very low. After 4 to 6 days, the shoots reactivated and the plants developed new leaves, photosynthesis, Fv/Fm andΦ_(PS II) reached normal level. Therefore, R. soongorica and C. korshinskii have the ability to reduce water loss through leaf abscission and maintain the vigor of the stem cells to survive desiccation.
2. PRO and MDA increased in leaves of 2-year-old R. soogorica, in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii during progressive drought stress and decreased in re-hydration period. During progressive drought stress, protein content declined in leaves of 2-year-old, more than 8-year-old R. soogorica, in leaves and stems of C. korshinskii, but increased in stems of more than 8-year-old R. soogorica. During re-hydration period, protein content increased in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii. The progressive drought stress stimulated starch, solube carbohydrate, total nonstructural carbohydrate, sucrose and fructose accumulation in leaves of 2-year-old R. soogorica, in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii, which had a higher accumulation in the stems. After re-hydration, solube carbohydrate, sucrose and fructose content declined in stem of more than 8-year-old R. soogorica, solube carbohydrate and sucrose content declined in stem of C. korshinskii. The content of starch and total nonstructural carbohydrate in stem of more than 8-year-old R. soogorica, the content of fructose, starch and total nonstructural carbohydrate in stem of C. korshinskii increased before the emergence of new leaf, after that, which were declined. The carbohydrate content in leaf of more than 8-year-old R. soogorica and C. korshinskii has high fluctuation in 40 days after re-hydrtion. Changes of carbohydrate content during water stress and re-hydrtion period indicated that R. soogorica and C. korshinskii accumulate high carbohydrate content in stems under extremely drought stress which can stimulate emergence of new leaves and regrowth if the soil moisture reaches a new optimum level.
3. During progessive drought stress, activities of catalase increased at first and then declined in leaves of 2-year-old and in stems of more than 8-year-old R. soogorica, but increased in stems of C. korshinskii and kept constant in leaves of more than 8-year-old R. soogorica and C. korshinskii. After re-hydration, activities of catalase declined at first and then kept at constant level in stems and increased stablely in leaves in two species. Activities ofα-amylase andβ-amylase increased in leaves of 2-year-old R. soogorica, in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii during progessive drought stress. After re-hydration, activities ofβ-amylase declined at first and then kept at constant level in stems of more than 8-year-old R. soogorica. Activities ofα-amylase in stems of more than 8-year-old R. soogorica, and activities ofα-amylase andβ-amylase in stems of C. korshinskii increased before the emergence of new leaf, after that, which were declined. Activities ofα-amylase increased at first and then declined in leaves of two species and the activities ofβ-amylase increased stablely. During the energence of new leaf, the disappearance of starch in the stems of R. soogorica and C. korshinskii (starch at 57, 63, 69, 79 and 84 DAT minus starch at 63, 69, 79, 84 and 94 DAT, respectively) was calculated as mobilization parameters. The correlations of starch hydrolytic enzyme activies during a rapid period of starch mobilization in the stems with parameters were determined,α-amylase activity was significantly and positively correlated with the mobilization of starch (r~2=0.856, P=0.005 of R. soogorica and r~2=0.873, P=0.005 of C. korshinskii, respectively). Slight correlation ofβ-amylase activity was abserved with mobilization parameters (r~2=0.449, P=0.117 of R. soogorica and r~2=0.3426, P=0.124 of C. korshinskii, respectively).
4. The results of anatomical studies in R. soongorica and C. korshinskii indicated that in most case, choroplasts appeared in subcellular organization and choroplasts cling the cell wall. Chloroplasts surrounded by a persistent envelope and with abundant and ordered thylakoid system. With the ongoing of drought stress, Chloroplasts broke away from the cell wall and appeared in the center of cell. The mesophyll ultrastructure and Chloroplasts configuration in leaves were disturbed beyond retrieve in the leaves under severe drought, including the inner and outer membranes destroyed, hylakoid disintergrated, starch grain disappeared and parts of cell tissue dismantled into debris. But in stems, the mesophyll ultrastructure and Chloroplasts configuration remained completely. After leaf abscission, lots of starch grains appeared in choroplasts in stem. 6 days and 4 days after rewatering, the new leaves have already fully outspreaded in R. soongorica and C, korshinskii respectively and have resynthesized large quantities of chlorophyll. Compare with leaf of control, lots of starch grains appeared in choroplasts C. korshinskii and less of starch grains appeared in choroplasts in R. soongorica. The reorganization of the photosynthetic apparatus, whose functional recovery is essential for plant survival.
From the above investigations of those two species, we concluded that the major adaptation mechanisms to desiccation depended on protective strategy in photosystem, products metabolism, morphological and anatomical changes and signal regulation. They have the response mechanisms of resurrection plants to drought stress and resurrection mechanisms to re-hydration. It is shown that resurrection plants not only exist in tropic and sub-tropic (Africa), but also exist in temperate zone.
1．水分胁迫导致了红砂和柠条净光合速率(Pn)的下降，但内在水分利用效率(WUE)在中度干旱条件下却明显提高。PSⅡ的最大光化学效率(Fv／Fm)和非循环式电子传递效率(Φ_(PSⅡ))随着干旱程度的增加而减小，并表现出午间光抑制现象。在中度干旱胁迫下，红砂叶片叶绿素含量上升，在极端干旱条件下含量下降，在柠条叶片中随着干旱胁迫的加重而下降。红砂和柠条经过53天干旱处理后，土壤上下层含水量分别降低到2.54％、3.47％和2.9％、12.89％，茎中的相对含水量分别达到了4.66％和10.15％时，这两种植物的叶片死亡，但茎仍然保持活力，进行微弱的光合作用，随后植物进入休眠状态。复水后茎的光合能力还很弱，PSⅡ的最大光化学效率和非循环式电子传递效率也很低。等完全长出叶片后，光合和荧光参数恢复正常。因此，红砂和柠条具有剪去叶片而减少水分丢失并维持茎细胞的活力来度过极端干旱的能力。
2．红砂幼苗叶片、成熟的红砂和柠条叶片和茎中脯氨酸和丙二醛含量随着干旱胁迫强度的增加而增加，复水后下降。可溶性蛋白含量在红砂幼苗和成熟的红砂叶片、柠条叶片和茎中下降，在成熟的红砂茎中上升。复水后，无论在叶片还是在茎中都呈上升趋势。持续干旱是红砂幼苗、成熟的红砂和柠条叶片和茎中淀粉、可溶性糖、非结构糖、蔗糖和果糖的累积，在茎中累积量更大。复水后，成熟的红砂茎中可溶性糖、蔗糖和果糖、柠条茎中可溶性糖和蔗糖含量迅速下降，成熟的红砂茎中淀粉和非结构糖、柠条茎中果糖、淀粉和非结构糖的含量在未长出叶片之前上升，长出叶片后迅速下降。在叶片中的含量随着复水时间的延长变化很大。干旱和复水期间碳水化合物的变化表明，在极端干旱条件下，红砂和柠条在茎中积累大量的碳水化合物，在土壤水分适宜的情况下，茎中积累的碳水化合物能够促使茎萌发出新叶而继续生长。
3．干旱期间，过氧化氢酶活性变化为：在红砂幼苗叶片和成熟的红砂茎中先上升后下降，成熟的红砂和柠条叶片中基本保持不变，柠条茎中上升。复水后，成熟的红砂和柠条茎中先下降后保持不变，在叶片中持续上升。干旱过程中，α-淀粉酶和β-淀粉酶活性在红砂和柠条叶片和茎中都呈上升态势。复水后，红砂茎中β-淀粉酶活性先下降后保持不变，红砂茎中α-淀粉酶和柠条茎中α-淀粉酶和β-淀粉酶活性在未长出叶片之前上升，长出叶片后迅速下降。红砂和柠条叶片中α-淀粉酶活性先上升后下降，β-淀粉酶活性持续上升。以叶片萌芽过程中，成熟的红砂和柠条茎中淀粉含量的降低(57日、63日、69日、79日和86日含量分别减去63日、69日、79日和86日和96日含量)作为淀粉水解参数。求得淀粉迅速水解期间茎中淀粉酶活性和淀粉水解参数之间的相关关系后，发现α-淀粉酶活性与淀粉水解参数呈显著正相关(红砂为：r~2=0.856，P=0.005、柠条的为：r~2=0.873，P=0.005)。β-淀粉酶和淀粉水解参数之间相关关系小(红砂r~2=0.449，P=0.117、柠条r~2=0.3426，P=0.124)。
4．解剖结构研究表明，红砂和柠条茎的亚细胞组织中普遍含有叶绿体。正常条件下，无论是茎还是叶片的亚细胞组织，叶绿体紧贴细胞壁。叶绿体中的类囊体排列整体有序。随着干旱的加剧，叶绿体脱离细胞壁，向细胞中央靠近。严重干旱造成了叶片叶肉细胞和叶绿体结构的不可恢复性的破坏，包括外膜和膜片层结构，类囊体膜解体，淀粉粒消失，部分细胞器裂解成碎片。而茎中的亚细胞组织和叶绿体都保持完整。落叶后，茎叶绿体中淀粉粒含量增加。复水以后，红砂和柠条分别于复水后的第6天和第4天新的叶片完全伸展开，并且合成了大量的叶绿素，红砂叶片叶绿体中淀粉粒含量减少，柠条叶片叶绿体中淀粉粒含量增加。这样重新组织了光合细胞器，这些功能的恢复为植物生存打下了良好的基础。
以上分析表明，这两种植物对干旱胁迫的适应主要是依赖于光系统、物质代谢、形态和结构以及信号传递等方面的保护，表现出与其它复苏植物类似的干旱胁迫响应及遇水后复苏的机制。由此证明，复苏植物不仅存在于非洲的热带、亚热带地区，而且在温带地区也存在。
Reaumuria soongorica and Caragana korshinskii are perennial semi-shrubs. We found that under medium drought stress (when soil water content in the upper layers reached 22.6% and 21.1% respectively), a majority of leaves of those two species turned scorch. Under severe drought stress (when soil water content reached 2.54% and 2.9%), all leaves shedd and the plants have died away. After re-hydration, they can stimulate new leaves and regrowth. Those plants are resurrection plants. This paper presented the studies on the changes of photosynthetic activities, metabolic products enzyme activities, anatomy and chloroplast ultrastructure, in those two species during the period of progressive drought stress and the mergence of new leaves and regrowth after re-hydration. The studies were analyzed and discussed to elucidate further the mechanisms of adaptation to desiccation tolerance during water stress. The main results were summarized as follows:
1. Pn declined during drought stress in R. soongorica and C. korshinskii, but intrinsic water use efficiency (WUE) increased remarkably under medium drought stress. The maximal photochemical efficiency of PSII (Fv/Fm) and the quantum efficiency of noncyclic electric transport of PS II (Φ_(PSII)) decreased significantly under drought stress and exhibited an obvious phenomenon of photoinhibition at noon. The chlorophyll content in R. soongorica had increased under medium drought stress and dropped only under severe drought stress, but had progressive dropped during the drought stress period in C. korshinskii. When soil water content in the layers 0-10cm and 10-25cm reached 2.54%, 3.47% and 2.9%, 12.89% respectively and stem relative water content reached 4.66% and 10.15% in R. soongorica and C. korshinskii after 53 days of drought stress, the leaves died and abscised. But the stems photosynthesis remained and, afterward plants entered dormant state. Upon rewatering, the stems photosynthesis were very feeble and the maximal photochemical efficiency of PSII and the quantum efficiency of noncyclic electric transport of PS II were very low. After 4 to 6 days, the shoots reactivated and the plants developed new leaves, photosynthesis, Fv/Fm andΦ_(PS II) reached normal level. Therefore, R. soongorica and C. korshinskii have the ability to reduce water loss through leaf abscission and maintain the vigor of the stem cells to survive desiccation.
2. PRO and MDA increased in leaves of 2-year-old R. soogorica, in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii during progressive drought stress and decreased in re-hydration period. During progressive drought stress, protein content declined in leaves of 2-year-old, more than 8-year-old R. soogorica, in leaves and stems of C. korshinskii, but increased in stems of more than 8-year-old R. soogorica. During re-hydration period, protein content increased in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii. The progressive drought stress stimulated starch, solube carbohydrate, total nonstructural carbohydrate, sucrose and fructose accumulation in leaves of 2-year-old R. soogorica, in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii, which had a higher accumulation in the stems. After re-hydration, solube carbohydrate, sucrose and fructose content declined in stem of more than 8-year-old R. soogorica, solube carbohydrate and sucrose content declined in stem of C. korshinskii. The content of starch and total nonstructural carbohydrate in stem of more than 8-year-old R. soogorica, the content of fructose, starch and total nonstructural carbohydrate in stem of C. korshinskii increased before the emergence of new leaf, after that, which were declined. The carbohydrate content in leaf of more than 8-year-old R. soogorica and C. korshinskii has high fluctuation in 40 days after re-hydrtion. Changes of carbohydrate content during water stress and re-hydrtion period indicated that R. soogorica and C. korshinskii accumulate high carbohydrate content in stems under extremely drought stress which can stimulate emergence of new leaves and regrowth if the soil moisture reaches a new optimum level.
3. During progessive drought stress, activities of catalase increased at first and then declined in leaves of 2-year-old and in stems of more than 8-year-old R. soogorica, but increased in stems of C. korshinskii and kept constant in leaves of more than 8-year-old R. soogorica and C. korshinskii. After re-hydration, activities of catalase declined at first and then kept at constant level in stems and increased stablely in leaves in two species. Activities ofα-amylase andβ-amylase increased in leaves of 2-year-old R. soogorica, in leaves and stems of more than 8-year-old R. soogorica and C. korshinskii during progessive drought stress. After re-hydration, activities ofβ-amylase declined at first and then kept at constant level in stems of more than 8-year-old R. soogorica. Activities ofα-amylase in stems of more than 8-year-old R. soogorica, and activities ofα-amylase andβ-amylase in stems of C. korshinskii increased before the emergence of new leaf, after that, which were declined. Activities ofα-amylase increased at first and then declined in leaves of two species and the activities ofβ-amylase increased stablely. During the energence of new leaf, the disappearance of starch in the stems of R. soogorica and C. korshinskii (starch at 57, 63, 69, 79 and 84 DAT minus starch at 63, 69, 79, 84 and 94 DAT, respectively) was calculated as mobilization parameters. The correlations of starch hydrolytic enzyme activies during a rapid period of starch mobilization in the stems with parameters were determined,α-amylase activity was significantly and positively correlated with the mobilization of starch (r~2=0.856, P=0.005 of R. soogorica and r~2=0.873, P=0.005 of C. korshinskii, respectively). Slight correlation ofβ-amylase activity was abserved with mobilization parameters (r~2=0.449, P=0.117 of R. soogorica and r~2=0.3426, P=0.124 of C. korshinskii, respectively).
4. The results of anatomical studies in R. soongorica and C. korshinskii indicated that in most case, choroplasts appeared in subcellular organization and choroplasts cling the cell wall. Chloroplasts surrounded by a persistent envelope and with abundant and ordered thylakoid system. With the ongoing of drought stress, Chloroplasts broke away from the cell wall and appeared in the center of cell. The mesophyll ultrastructure and Chloroplasts configuration in leaves were disturbed beyond retrieve in the leaves under severe drought, including the inner and outer membranes destroyed, hylakoid disintergrated, starch grain disappeared and parts of cell tissue dismantled into debris. But in stems, the mesophyll ultrastructure and Chloroplasts configuration remained completely. After leaf abscission, lots of starch grains appeared in choroplasts in stem. 6 days and 4 days after rewatering, the new leaves have already fully outspreaded in R. soongorica and C, korshinskii respectively and have resynthesized large quantities of chlorophyll. Compare with leaf of control, lots of starch grains appeared in choroplasts C. korshinskii and less of starch grains appeared in choroplasts in R. soongorica. The reorganization of the photosynthetic apparatus, whose functional recovery is essential for plant survival.
From the above investigations of those two species, we concluded that the major adaptation mechanisms to desiccation depended on protective strategy in photosystem, products metabolism, morphological and anatomical changes and signal regulation. They have the response mechanisms of resurrection plants to drought stress and resurrection mechanisms to re-hydration. It is shown that resurrection plants not only exist in tropic and sub-tropic (Africa), but also exist in temperate zone.
引文
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