苹果属植物种间水分利用效率的差异及其机理研究
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摘要
干旱半干旱地区水分不足是限制农业生产的主要因素,因此干旱环境条件下的农业生产必须以水分高效利用为中心,而提高植物自身的水分利用效率(WUE)是实现节水和增产的重要途径之一。本文以我国10个苹果(Malus)砧木为试材,采用盆栽方式研究了不同砧木碳同位素组成(δ~(13)C)、长期水分利用效率(WUE_L)、瞬时水分利用效率(WUE_i)、耗水量和耐旱性的差异,分析了苹果属植物种间WUE差异的形态和生理基础。在此基础上,以WUE差异显著的新疆野苹果(M. sieverii (Ledeb) Roem.)和平邑甜茶(M. hupehensis (Pamp) Rehd.)为材料研究了水孔蛋白与植物WUE(WUE_i)的关系,以及外源脱落酸(ABA)和施肥处理对新疆野苹果和平邑甜茶WUE的影响,分析了气孔和光合能力对WUE的调节。
主要研究结果如下:
1.正常供水和干旱条件下,苹果属植物种间WUE都存在显著差异,而且这种差异在两种水分条件下表现出一致性。综合分析不同砧木的WUE、耐旱性和耗水量表明:楸子(M. prunifolia(Willd)Borkh.)WUE高、耐旱性强、耗水量大,八棱海棠(M. robusta Rehd.)WUE高、耗水量大、耐旱性中等,新疆野苹果和西府海棠(M. micromalus Hemsl.)WUE中等、耗水量低、耐旱性强,平邑甜茶和变叶海棠(M. toringoides (Rehd) Hughes.)WUE和耐旱性均较低。苹果属植物种间叶片的δ~(13)C差异显著,随土壤含水量的降低δ~(13)C显著增加。两种水分条件下,δ~(13)C都与WUE_L和WUE_i表现出显著的正相关性,种和处理对δ~(13)C没有互作效应,说明δ~(13)C可以用于苹果属植物WUE的评价。
2.苹果属植物的WUE受形态特征、生理因子及其交互作用的影响。正常供水和干旱条件下,不同砧木的整株干重、根/冠比和叶面积比与δ~(13)C之间均不存在显著的相关性,δ~(13)C与根系蒸腾速率、叶面积蒸腾速率呈显著的负相关关系。这说明可以选育同时具有高WUE和生长快的苹果砧木,与生物量的分配方式相比,叶和根的生理活动对苹果属植物WUE的影响更大。两种水分条件下,δ~(13)C与比叶面积、气孔长度、气孔导度(Gs)、蒸腾速率(Tr)和胞间CO2浓度呈显著的负相关关系,与气孔密度、叶片氮含量呈显著的正相关关系。光合速率(Pn)不是种间WUE差异的主要因素,但叶片氮含量通过Pn影响δ~(13)C。两种水分条件下,δ~(13)C与叶片内源激素ABA、GA、ZR、IAA、ABA/(ZR+IAA)均不存在显著的相关性。多元逐步回归分析表明,正常供水条件下,气孔密度和Gs是引起种间WUE差异的关键因素;干旱条件下,比叶面积和Gs是种间WUE差异的主要因素。
3.在1/2Hoagland营养液、20%PEG6000溶液、60μmol.L-1 ABA溶液中,分别用50μmol.L-1 HgCl2处理新疆野苹果和平邑甜茶幼苗。结果表明,水孔蛋白活性被抑制后两种砧木叶片WUE_i均显著降低。干旱条件下,新疆野苹果和平邑甜茶的盆栽苗WUE_i、叶和根中PIP1基因表达水平在胁迫初期都有所上升,新疆野苹果和平邑甜茶分别在第4 d和第2 d达到最大,之后随干旱胁迫程度的加重WUE_i和PIP1基因表达量开始下降。在mRNA水平上,新疆野苹果叶和根中PIP1表达量高于平邑甜茶。复水后新疆野苹果WUE_i和PIP1基因表达水平趋于恢复正常,平邑甜茶WUE_i和PIP1基因表达水平仍低于对照,但也表现出缓慢上升趋势。叶和根中ABA的变化与PIP1在mRNA水平上的表达量变化趋势一致。说明水孔蛋白可能参与了苹果属植物WUE_i的调控,叶和根中PIP1的表达有可能受ABA的诱导。
4.正常供水和干旱条件下,外源ABA均显著增加了一年生新疆野苹果和平邑甜茶的WUE_i、WUE_L、δ~(13)C、气孔密度、内源ABA含量,并且显著降低了气孔长度、Gs、Tr和Pn;同时外源ABA显著降低了两种砧木的株高、整株干重和总叶面积。但新疆野苹果对外源ABA更敏感,表现在有更大的Gs、Tr降低幅度,更高的生物量分配可塑性,以及更高的WUE、ABA含量增加幅度。这表明苹果砧木对外源ABA敏感性因种的不同而不同。两种水分条件下,外源ABA对两种砧木的最大光化学效率(FV/FM)、电子传递速率(ETR)、叶绿素含量和RuBPcase活性均不存在显著影响。说明外源ABA是通过气孔因素提高了苹果砧木的WUE,而对光合机构没有造成直接影响。研究结果还表明外源ABA增强了两种砧木的耐旱能力。
5.正常供水和干旱条件下,施肥均显著提高了新疆野苹果和平邑甜茶的WUE_i、WUE_L和δ~(13)C,水分充足条件下施肥效果更显著。与新疆野苹果相比,水分充足条件下,施肥使平邑甜茶的耗水量、总叶面积、整株干重、Pn、Tr增加幅度更大。正常供水条件下,施肥处理显著增加了Pn、Gs和Tr,但Gs和Tr增加幅度远低于Pn;干旱条件下,施肥对Gs和Tr没有显著影响,而Pn显著增加。两种水分条件下,施肥处理均显著增加了两种砧木的光饱和点、叶片氮含量、叶绿素含量、RuBPcase活性、FV/FM、光化学猝灭系数(qP)和ETR,显著降低了非光化学猝灭系数(qN)和光补偿点。表明施肥处理使叶片的PSⅡ活性升高,光合电子传递速率加快,光合能力增强。施肥处理可能主要是通过改变光合碳同化效率来提高苹果砧木的WUE。
Water availability is a major determinate of agricultural productivity in arid and semi-arid regions of the world. Therefore, higher water use efficience should be center of the agricultural production in these regions. One solution to the problem is to improve water use efficiency (WUE) of plants themselves. In this study, we examined the differences of carbon isotope composition (δ~(13)C), long-term water use efficiency (WUE_L), instantaneous water use efficiency (WUE_i), total water consumption and drought tolerance in ten Malus rootstocks, and elucidated morphological and physiological traits in relation to this variation in WUE. In addition, in order to gain a better understanding on the regulation of stomatal and photosynthetic capacity on WUE, M. sieverii and M. hupehensis were used to study the relationships of WUE (WUE_i) and aquaporin gene expression, and to investigate the effects of long-term exogenous abscisic acid (ABA) application and fertilization on WUE.
The results were as follows:
1. There was large variation in the WUE of Malus under both well-watered and drought-stressed conditions, the ranking and degree of response in WUE of the different species generally remained the same under both watering regimes. Analysis of WUE, drought resistance and total water consumption of different Malus rootstocks showed that M. prunifolia had high WUE, high drought resistance and large total water consumption, M. robusta had high WUE and total water comsuption but moderate drought tolerance, M. sieverii and M. micromalus had moderate WUE level, low total water consumption and high tolerance to drought stress, while M. hupehensis and M. toringoides had low WUE and drought resistant capability. Theδ~(13)C value in Malus differed significantly. Foliarδ~(13)C values increased significantly with the decreasing total soil water content. There was a positive correlation betweenδ~(13)C and both WUE_i and WUE_L, while the species×treatment interaction was non-significant forδ~(13)C, suggesting that it should be possible to useδ~(13)C as a surrogate for WUE and to select Malus rootstock for high WUE.
2. WUE of Malus was affected by morphological and physiological properties.δ~(13)C did not correlated with total dry weight, root/shoot ratio and leaf area ratio either in the well-watered condition or in the dry treatment. This result opens a way for selecting Malus rootstock combining large WUE and high relative growth rate. In addition, these results showed that the specific activities of leaves and roots were more important in determining the water use of the plant than the allocation to leaves and roots. Under both well-watered and drought-stressed conditions,δ~(13)C was negatively correlated with transpiration per plant weight, transpiration per leaf area, special leaf area, stomatal length, stomatal conductance (Gs), transpiration rate (Tr) and intercellular CO2 concentration, and positively correlated with stomatal density and leaf nitrogen content. Pn was not primarily responsible for differences inδ~(13)C. However, the positively relationship betweenδ~(13)C and leaf nitrogen content could re?ect the fact that the diversity forδ~(13)C may also be partly driven by Pn. Under both well-watered and drought-stressed conditions,δ~(13)C were not correlated with ABA, ZR, IAA, GA and ABA/(ZR+IAA). Multiple stepwise regression analysis showed that stomatal density and Gs were key determinants of difference in WUE under well-watered condition, and that the diversity for WUE was mainly driven by special leaf area and Gs under drought-stressed condition.
3. Under three conditions (1/2Hoagland solution, 20%PEG6000, 60μmol.L-1 ABA), WUE_i of seedlings of M. sieverii and M. hupehensis markedly decreased after HgCl2’s inhibition to the activities of aquaporins. Under drought stress, WUE_i and gene expression of PIP1 in roots and leaves of potted apple plants of M. sieverii and M. hupehensis increased with the continuance of drought stress. WUE_i and gene expression of PIP1 of M. sieverii and M. hupehensis reached the highest at 4d and 2d, respectively, followed by an obvious decline with further increasing of drought level. At the mRNA level, the leaf and root PIP1 expression level of M. sieverii. were higher than that of M. hupehensis. After re-watering, WUE_i and PIP1 expression level began to reverse, but M. hupehensis still lower than control. ABA content in leaves and roots showed the similar changes as PIP1 expression levels. Our results showed that aquaporins may regulate WUE (WUE_i) of Malus rootstocks. The PIP1 expression of leaves and roots may be triggered by ABA.
4. For M. sieverii and M. hupehensis, long-term exogenous ABA application significantly increased WUE_i, WUE_L,δ~(13)C, endogenous ABA concentration, stomatal density, and root/shoot ratio, and markedly decreased total dry weight, stomatal length, Pn, Gs and Tr under both well-watered and drought-stressed conditions. However, M. sieverii was more responsive to exogenous ABA application than M. hupehensis, as indicated by the strong stomata closure and by greater plasticity of biomass allocation, as well as by higher WUE and ABA content. We concluded that sensitivity to exogenous ABA application is species dependent in Malus.Under both well-watered and drought-stressed conditions, maximal efficiency of PSⅡ(FV/FM), electron transport rate (ETR), Chlorophyll content and RuBPcase activity of two contrasting Malus rootstocks were unaffected by exogenous ABA application. These results showed that ABA applied to leaf surfaces of two contrasting Malus rootstocks improved WUE and produced leaves with much-increased stomatal density and potential stomatal conductance, but had not a direct effect on photosynthetic apparatus. In addition, application of exogenous ABA appears to enhance the tolerance of two Malus species to drought-stress.
5. Under both well-watered and drought-stressed conditions, fertilization increased the WUE_i, WUE_L andδ~(13)C of M. sieverii and M. hupehensis. However, fertilization treatment had evident promoting effect on WUE under well-watered conditions. Under well-watered and fertilization treatment, the changes trends of total water consumption, total leaf area, total dry weight, Pn and Tr were consistent in M. sieverii and M. hupehensis seedlings, but the increased extent of them in M. hupehensis were more than that of M. sieverii. Under well-watered condition, treatment of fertilization increased Pn, Gs and Tr, but the increased extent of Gs and Tr were less than Pn. Fertilization treatment caused no significant changes in Gs and Tr under drought condition. However, under both well-watered and drought-stressed conditions, fertilization treatment significantly increased Pn, light saturation point, leaf nitrogen content, Chlorophyll content, RuBPcase activity, FV/FM, qP and ETR, and significantly decreased qN and light compensation point. These results indicated that application of fertilization could increase the light energy conversion efficiency, the potential activity of photosynthetic reaction center which can prevent leaf photosynthetic apparatus from damage of environmental stress. Fertilization treatment may improve WUE of Malus rootstocks through changes in carbon assimilation.
主要研究结果如下:
1.正常供水和干旱条件下,苹果属植物种间WUE都存在显著差异,而且这种差异在两种水分条件下表现出一致性。综合分析不同砧木的WUE、耐旱性和耗水量表明:楸子(M. prunifolia(Willd)Borkh.)WUE高、耐旱性强、耗水量大,八棱海棠(M. robusta Rehd.)WUE高、耗水量大、耐旱性中等,新疆野苹果和西府海棠(M. micromalus Hemsl.)WUE中等、耗水量低、耐旱性强,平邑甜茶和变叶海棠(M. toringoides (Rehd) Hughes.)WUE和耐旱性均较低。苹果属植物种间叶片的δ~(13)C差异显著,随土壤含水量的降低δ~(13)C显著增加。两种水分条件下,δ~(13)C都与WUE_L和WUE_i表现出显著的正相关性,种和处理对δ~(13)C没有互作效应,说明δ~(13)C可以用于苹果属植物WUE的评价。
2.苹果属植物的WUE受形态特征、生理因子及其交互作用的影响。正常供水和干旱条件下,不同砧木的整株干重、根/冠比和叶面积比与δ~(13)C之间均不存在显著的相关性,δ~(13)C与根系蒸腾速率、叶面积蒸腾速率呈显著的负相关关系。这说明可以选育同时具有高WUE和生长快的苹果砧木,与生物量的分配方式相比,叶和根的生理活动对苹果属植物WUE的影响更大。两种水分条件下,δ~(13)C与比叶面积、气孔长度、气孔导度(Gs)、蒸腾速率(Tr)和胞间CO2浓度呈显著的负相关关系,与气孔密度、叶片氮含量呈显著的正相关关系。光合速率(Pn)不是种间WUE差异的主要因素,但叶片氮含量通过Pn影响δ~(13)C。两种水分条件下,δ~(13)C与叶片内源激素ABA、GA、ZR、IAA、ABA/(ZR+IAA)均不存在显著的相关性。多元逐步回归分析表明,正常供水条件下,气孔密度和Gs是引起种间WUE差异的关键因素;干旱条件下,比叶面积和Gs是种间WUE差异的主要因素。
3.在1/2Hoagland营养液、20%PEG6000溶液、60μmol.L-1 ABA溶液中,分别用50μmol.L-1 HgCl2处理新疆野苹果和平邑甜茶幼苗。结果表明,水孔蛋白活性被抑制后两种砧木叶片WUE_i均显著降低。干旱条件下,新疆野苹果和平邑甜茶的盆栽苗WUE_i、叶和根中PIP1基因表达水平在胁迫初期都有所上升,新疆野苹果和平邑甜茶分别在第4 d和第2 d达到最大,之后随干旱胁迫程度的加重WUE_i和PIP1基因表达量开始下降。在mRNA水平上,新疆野苹果叶和根中PIP1表达量高于平邑甜茶。复水后新疆野苹果WUE_i和PIP1基因表达水平趋于恢复正常,平邑甜茶WUE_i和PIP1基因表达水平仍低于对照,但也表现出缓慢上升趋势。叶和根中ABA的变化与PIP1在mRNA水平上的表达量变化趋势一致。说明水孔蛋白可能参与了苹果属植物WUE_i的调控,叶和根中PIP1的表达有可能受ABA的诱导。
4.正常供水和干旱条件下,外源ABA均显著增加了一年生新疆野苹果和平邑甜茶的WUE_i、WUE_L、δ~(13)C、气孔密度、内源ABA含量,并且显著降低了气孔长度、Gs、Tr和Pn;同时外源ABA显著降低了两种砧木的株高、整株干重和总叶面积。但新疆野苹果对外源ABA更敏感,表现在有更大的Gs、Tr降低幅度,更高的生物量分配可塑性,以及更高的WUE、ABA含量增加幅度。这表明苹果砧木对外源ABA敏感性因种的不同而不同。两种水分条件下,外源ABA对两种砧木的最大光化学效率(FV/FM)、电子传递速率(ETR)、叶绿素含量和RuBPcase活性均不存在显著影响。说明外源ABA是通过气孔因素提高了苹果砧木的WUE,而对光合机构没有造成直接影响。研究结果还表明外源ABA增强了两种砧木的耐旱能力。
5.正常供水和干旱条件下,施肥均显著提高了新疆野苹果和平邑甜茶的WUE_i、WUE_L和δ~(13)C,水分充足条件下施肥效果更显著。与新疆野苹果相比,水分充足条件下,施肥使平邑甜茶的耗水量、总叶面积、整株干重、Pn、Tr增加幅度更大。正常供水条件下,施肥处理显著增加了Pn、Gs和Tr,但Gs和Tr增加幅度远低于Pn;干旱条件下,施肥对Gs和Tr没有显著影响,而Pn显著增加。两种水分条件下,施肥处理均显著增加了两种砧木的光饱和点、叶片氮含量、叶绿素含量、RuBPcase活性、FV/FM、光化学猝灭系数(qP)和ETR,显著降低了非光化学猝灭系数(qN)和光补偿点。表明施肥处理使叶片的PSⅡ活性升高,光合电子传递速率加快,光合能力增强。施肥处理可能主要是通过改变光合碳同化效率来提高苹果砧木的WUE。
Water availability is a major determinate of agricultural productivity in arid and semi-arid regions of the world. Therefore, higher water use efficience should be center of the agricultural production in these regions. One solution to the problem is to improve water use efficiency (WUE) of plants themselves. In this study, we examined the differences of carbon isotope composition (δ~(13)C), long-term water use efficiency (WUE_L), instantaneous water use efficiency (WUE_i), total water consumption and drought tolerance in ten Malus rootstocks, and elucidated morphological and physiological traits in relation to this variation in WUE. In addition, in order to gain a better understanding on the regulation of stomatal and photosynthetic capacity on WUE, M. sieverii and M. hupehensis were used to study the relationships of WUE (WUE_i) and aquaporin gene expression, and to investigate the effects of long-term exogenous abscisic acid (ABA) application and fertilization on WUE.
The results were as follows:
1. There was large variation in the WUE of Malus under both well-watered and drought-stressed conditions, the ranking and degree of response in WUE of the different species generally remained the same under both watering regimes. Analysis of WUE, drought resistance and total water consumption of different Malus rootstocks showed that M. prunifolia had high WUE, high drought resistance and large total water consumption, M. robusta had high WUE and total water comsuption but moderate drought tolerance, M. sieverii and M. micromalus had moderate WUE level, low total water consumption and high tolerance to drought stress, while M. hupehensis and M. toringoides had low WUE and drought resistant capability. Theδ~(13)C value in Malus differed significantly. Foliarδ~(13)C values increased significantly with the decreasing total soil water content. There was a positive correlation betweenδ~(13)C and both WUE_i and WUE_L, while the species×treatment interaction was non-significant forδ~(13)C, suggesting that it should be possible to useδ~(13)C as a surrogate for WUE and to select Malus rootstock for high WUE.
2. WUE of Malus was affected by morphological and physiological properties.δ~(13)C did not correlated with total dry weight, root/shoot ratio and leaf area ratio either in the well-watered condition or in the dry treatment. This result opens a way for selecting Malus rootstock combining large WUE and high relative growth rate. In addition, these results showed that the specific activities of leaves and roots were more important in determining the water use of the plant than the allocation to leaves and roots. Under both well-watered and drought-stressed conditions,δ~(13)C was negatively correlated with transpiration per plant weight, transpiration per leaf area, special leaf area, stomatal length, stomatal conductance (Gs), transpiration rate (Tr) and intercellular CO2 concentration, and positively correlated with stomatal density and leaf nitrogen content. Pn was not primarily responsible for differences inδ~(13)C. However, the positively relationship betweenδ~(13)C and leaf nitrogen content could re?ect the fact that the diversity forδ~(13)C may also be partly driven by Pn. Under both well-watered and drought-stressed conditions,δ~(13)C were not correlated with ABA, ZR, IAA, GA and ABA/(ZR+IAA). Multiple stepwise regression analysis showed that stomatal density and Gs were key determinants of difference in WUE under well-watered condition, and that the diversity for WUE was mainly driven by special leaf area and Gs under drought-stressed condition.
3. Under three conditions (1/2Hoagland solution, 20%PEG6000, 60μmol.L-1 ABA), WUE_i of seedlings of M. sieverii and M. hupehensis markedly decreased after HgCl2’s inhibition to the activities of aquaporins. Under drought stress, WUE_i and gene expression of PIP1 in roots and leaves of potted apple plants of M. sieverii and M. hupehensis increased with the continuance of drought stress. WUE_i and gene expression of PIP1 of M. sieverii and M. hupehensis reached the highest at 4d and 2d, respectively, followed by an obvious decline with further increasing of drought level. At the mRNA level, the leaf and root PIP1 expression level of M. sieverii. were higher than that of M. hupehensis. After re-watering, WUE_i and PIP1 expression level began to reverse, but M. hupehensis still lower than control. ABA content in leaves and roots showed the similar changes as PIP1 expression levels. Our results showed that aquaporins may regulate WUE (WUE_i) of Malus rootstocks. The PIP1 expression of leaves and roots may be triggered by ABA.
4. For M. sieverii and M. hupehensis, long-term exogenous ABA application significantly increased WUE_i, WUE_L,δ~(13)C, endogenous ABA concentration, stomatal density, and root/shoot ratio, and markedly decreased total dry weight, stomatal length, Pn, Gs and Tr under both well-watered and drought-stressed conditions. However, M. sieverii was more responsive to exogenous ABA application than M. hupehensis, as indicated by the strong stomata closure and by greater plasticity of biomass allocation, as well as by higher WUE and ABA content. We concluded that sensitivity to exogenous ABA application is species dependent in Malus.Under both well-watered and drought-stressed conditions, maximal efficiency of PSⅡ(FV/FM), electron transport rate (ETR), Chlorophyll content and RuBPcase activity of two contrasting Malus rootstocks were unaffected by exogenous ABA application. These results showed that ABA applied to leaf surfaces of two contrasting Malus rootstocks improved WUE and produced leaves with much-increased stomatal density and potential stomatal conductance, but had not a direct effect on photosynthetic apparatus. In addition, application of exogenous ABA appears to enhance the tolerance of two Malus species to drought-stress.
5. Under both well-watered and drought-stressed conditions, fertilization increased the WUE_i, WUE_L andδ~(13)C of M. sieverii and M. hupehensis. However, fertilization treatment had evident promoting effect on WUE under well-watered conditions. Under well-watered and fertilization treatment, the changes trends of total water consumption, total leaf area, total dry weight, Pn and Tr were consistent in M. sieverii and M. hupehensis seedlings, but the increased extent of them in M. hupehensis were more than that of M. sieverii. Under well-watered condition, treatment of fertilization increased Pn, Gs and Tr, but the increased extent of Gs and Tr were less than Pn. Fertilization treatment caused no significant changes in Gs and Tr under drought condition. However, under both well-watered and drought-stressed conditions, fertilization treatment significantly increased Pn, light saturation point, leaf nitrogen content, Chlorophyll content, RuBPcase activity, FV/FM, qP and ETR, and significantly decreased qN and light compensation point. These results indicated that application of fertilization could increase the light energy conversion efficiency, the potential activity of photosynthetic reaction center which can prevent leaf photosynthetic apparatus from damage of environmental stress. Fertilization treatment may improve WUE of Malus rootstocks through changes in carbon assimilation.
引文
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