花后高温对水稻胚乳淀粉合成与蛋白积累的影响机理
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摘要
花后高温是影响稻米品质的主要气候因子,同时也是制约许多高产品种产量潜力发挥与品质稳定的逆境因素之一。本文在前期研究工作的基础上,以品质性状的生态表现具有代表性(高温敏感和高温钝感)、且生育期和其他农艺性状相仿的两个早籼稻品种(嘉935和嘉353)为材料,利用大田异季种植和人工气候箱控温处理试验,对不同温度处理下稻米胚乳的淀粉粒径、链长精细结构和贮藏蛋白(蛋白亚基、氨基酸组分等)等品质理化指标的差异变化进行比较分析,并结合cDNA微阵列、定量RT-PCR和蛋白表达分析等技术,对花后高温胁迫下水稻胚乳淀粉合成与蛋白积累代谢途径的相关基因表达模式与表达谱进行了检测,以揭示花后高温对水稻胚乳淀粉精细结构与贮藏蛋白组分影响的效应机理。主要结果如下：
1、花后高温所导致的稻米蒸煮食味品质变劣现象(如糊化温度升高和胶稠度下降等),与不同温度处理下稻米淀粉的粒径分布差异、链长精细结构之间存在着密切联系。花后高温胁迫对稻米淀粉粒粒径的影响表现为：导致小型淀粉粒和中型淀粉粒的数量与相对比例降低,大型淀粉粒的数量与相对比例显著增大,淀粉粒的平均粒径增大,这是稻米糊化温度与糊化热焓值明显升高的重要因素。此外,花后高温会导致稻米直链淀粉的聚合度降低、支链淀粉长B链组分(B3链,DP≥37)的比例上升,短B链组分(B1链,DP13-24)的比例有所下降。与稻米表观直链淀粉含量(AC)的品种类型间差异相似,花后高温胁迫对稻米B2链(DP25-36)与短A链(DP5-12)也表现出一定的品种类型差异。低AC类型品种嘉935在花后高温下的B2链比例上升、短A链比例下降,而高AC类型品种嘉353呈相反趋势。
2、花后高温下发育胚乳中的蔗糖转运体(SUT)和蔗糖合成酶(SuSy)主要同工型基因(SUT1, SUT2, SuSy2和SuSy3)的相对表达量降低,但质体转化酶基因(CIN2和CIN7)的相对表达量上升,高温胁迫破坏发育胚乳糖卸载代谢环节两个关键蔗糖合成酶和质体转化酶间的平衡,降低蔗糖的卸载效率；此外,高温胁迫下己糖激酶类的几个主要功能基因(HxKI和HxKⅡ等)上调表达,而果糖激酶类和糖信号作用蛋白的相关功能基因(FrK Ⅰ和FrKⅡ)下调表达,两类基因(HxK类和FrK类)在高温胁迫下的相对表达量呈“此消彼长”变化,说明花后高温抑制己糖磷酸化代谢途径,并改变发育胚乳中的有关糖信号途径及其应答机制,不利于淀粉的合成代谢。
3、花后高温对水稻胚乳淀粉精细结构的影响效应涉及到淀粉合成代谢途径多个功能基因及相应同工型的特异性表达。淀粉合成酶基因(如SSS Ⅰ、SSSⅢa、SSSⅣa等)呈上调表达,淀粉合成酶与分支酶基因(如SSS Ⅱa、SBE Ⅰ、SBEⅢ等)呈下调表达,异淀粉酶基因ISA1的相对表达量上升,普鲁兰酶基因PUL的相对表达量下降,花后高温对稻米淀粉精细结构的影响效应(例如,B3链比例上升、B1链比例下降,等)受上述功能基因与同工型的共同调控,而SSS Ⅰ、SSS ⅡaQ两同工型基因对支链淀粉链长合成的催化作用最为明显。此外,GBSS Ⅰ是在发育胚乳中相对表达量较高的颗粒结合型淀粉合成酶基因同工型,高温胁迫下,GBSS Ⅰ在低直链淀粉品种嘉935胚乳中的相对表达量下降,而高直链淀粉品种嘉353中则呈相反趋势,这与不同温度处理下两水稻品种胚乳中的直链淀粉含量变化趋势是一致的。
4、水稻籽粒糊粉层临时淀粉的正常降解,对胚乳淀粉合成所需的碳源和能量保障具有重要意义。花后高温胁迫对临时淀粉降解代谢(包括磷酸化降解和非磷酸化降解两条途径)相关基因的影响主要表现为：“上游基因”(如GWD、AMY3和SEX4等)在高温胁迫下呈上调表达,导致代谢中间产物的快速累积；而“下游基因”(如ISA3、PUL和MEX1等)大多呈下调表达,抑制淀粉降解中间产物进一步分解。“上游基因”和“下游基因”的表达模式引起淀粉降解中间产物在糊粉层的过量累积,影响稻米糊粉层的营养转运功能,这可能是导致花后高温胁迫下胚乳淀粉合成所需的碳源和能量供应不足,并引起总淀粉积累量降低的重要原因。
5、花后高温胁迫下,水稻籽粒中的蛋白和氨基酸组分含量在灌浆前期普遍上升；醇溶蛋白含量在灌浆后期下降,蛋白和氨基酸组分含量差异主要表现在灌浆后期。高温加速蛋白体的形成,改变谷蛋白和醇溶蛋白亚基的相对含量,其中,醇溶蛋白13kDa亚基相对含量略微降低,17-19kDa亚基相对含量上升,谷蛋白亚基和谷蛋白前体相对含量均上升。水稻胚乳蛋白积累不仅受蛋白亚基前体基因的调控,同时还受到蛋白质修饰相关基因的调控。与蛋白亚基前体基因相比,蛋白质修饰调控和逆境防御相关基因对高温胁迫更为敏感。其中,内质网细胞腔结合蛋白基因(BiP)在高温下的上调表达有利于醇溶蛋白的折叠与聚集,加速蛋白体1的形成：蛋白质二硫同分异构酶基因(PDI)、水稻碱性亮氨酸拉链蛋白基因／醇溶谷蛋白框结合蛋白基因(RISBZ1/RPBF)组合的上调表达与高温胁迫下的蛋白前体聚合过程和逆境防御代谢有关。
High temperature during reproductive period is one of the crucial factors influencing rice yield and grain quality; Base on the former research work, two early non-waxy indica rice cultivars (J935and J353) differing in cooking and eating quality were chosen to investigate the effects of high temperature on the fine structure of amylopectin, protein body formation and starchy granule distribution by a field experiment of different sowing-date and the controlled temperature treatments in chambers, respectively. In current study, the cDNA microarrays, RT-PCR, protein expression analysis were used to elucidate the underlying metabolisms involved in starchy biosynthesis and storage protein accumulation, as well as their relations to rice grain quality when subjected to high temperature. The main results were showed as follows:
1. The high temperature stress at filling stage could deteriorate cooking and eating quality, which was closely related to rice starch granule size distribution as well as starch fine structure. High temperature increased rice starch granule average diameter, caused the percentage of large starch granule increasing, but small and medium-sized starch granule presented with an opposite way. The Phenomenon of starch granule size, affected by high temperature, was one of the explanations for rice starch gelatinization properties involved in high temperature at filling stage. In addition, great changes were also found in rice starch fine structure (chain length) when treated with two temperatures. Among different amylopectin components, long B chain (B3chain, DP≥37) increased significantly with B1chain (DP13-24) components decreasing under high temperature treatment. B3and B1chain presented a similar trend between the two variety, while B2chain (DP25-36) and A chain (DP5-12) differed by variety under high temperature stress. The proportion of B2chain increased in J935, a high quality variety, but decreased in J353. A chain was just opposite to B2chain. For different components in grain developing stage, the short A chain presented a higher proportion at initial stage relative to the other components, but gradually decreased as filling stage. On the contrary with A chain, B1, B2chain and B3chain showed lower proportion at initial stage and higher at later stage.
2. The high temperature stress at filling stage may inhibit the relative expression amount to main isoform genes (SUT1and SUT2) for Sucrose Transporter (SUT), implying sucrose transport pathway might be inhibited by high temperature. In addition, the main isoform genes (SuSy2and SuSy3) for sucrose synthase (SuSy) were down-regulation, which indicated sucrose unloading in rice endosperm impaired by high temperature treatment, however, the genes (CIN2and CIN7) related to plasmid-invertase in rice endosperm induced by high temperature. It was showed that high temperature broke the balance between sucrose synthase and plasmid-invertase, and Limited sucrose unloading efficiency. For sugar signal transduction procedure, the gene referred to fructokinase and hexokinase played important role at sugar signal transduction in rice endosperm, the "shift" phenomenon of fructokinase (FrK Ⅰand FrK Ⅱ) and hexokinase (HxK Ⅰand HxK Ⅱ) in the fructose phosphorylation might be an adaptation mechanism to high temperature stress in rice. High temperature can inhibit some signal transduction pathways.
3. There were numerous genes involved in starch synthesis, as well as starch fine structure, in rice endosperm exposed to high temperature at filling stage. Among different gene isoform, some genes for starch synthase (SSS Ⅰ, SSS Ⅲa and SSS Ⅳa) was shown up-regulation when exposed to high temperature, but SSS Ⅱa, SBE Ⅰ, SB Ⅵ, which for starch synthase and starch branching synthase presented down-regulation. For starch debranching synthase genes, ISA1showed up-regulation, while PUL presented down-regulation under high temperature stress. Different expression patterns of genes for the three enzymes co-governed amylecptin, and determined its fine structure at high temperture. SSS Ⅰ,SSSⅡa was the two gene isoforms, which was the most important in starch fine structure. Concerned as GBSS Ⅰ, which mainly acted on amylase content, presented up-regulation in J353and down-regulation in J935. The change of GBSS Ⅰ expression pattern was coincide with amylose content when exposed to different temperature treatments at filling stage.
4. Transition starch degradation, what always occur in rice grain aleurone, played an important role in supplying carbon source and energy to starch synthesis in rice endosperm. Effect of high temperature on starch degradation metabolism (including phosphorylated degradation pathway and non-phosphorylated degradation pathway) in rice endosperm at filling stage presented similar features:"upstream genes"(like GWD, AMY3and SEX4) showed up-regulation pattern responsible to high temperature stress, which resulted in a rapid accumulation of intermediate product from starch degradation. However,"downstream genes"(like ISA3, PUL and MEX1) mostly inhibited by high temperature, which impaired successive degradation of intermediate product. The expression patterns of "upstream genes" and "downstream genes" under high temperature results in excess accumulation of intermediate product in rice aleurone, which might restrict carbon and energy supply, reduce total starch content in rice endosperm.
5. High temperature stress increased the accumulation of all classes of storage proteins and amino acid at early filling stage but decreased the accumulation of prolamin at later stage. High temperature not only accelerated the formation process of protein body (PB Ⅰ and PBⅡ), but also changed relative proportion of storage protein subunit in rice endosperm. For prolamin, high temperature resulted in slightly decreasing of13kDa prolamin subunits with a slight extent, and significantly increasing17-19kDa subunits. For Glutelin, high temperature cause higher content for α-subunit and β-subunit than those to lower temperature. The accumulation of storage protein in rice endosperm was not only regulated by gene related to protein subunit or precursor, but also controlled by the gene involving in protein modification and stress-defense. Compared with the former, the latter was much more sensitive to high temperature. For example, luminal-binding protein precursor gene (BiP), which contributed to prolamin fold and aggregation, as well as protein body Ⅰ (PB Ⅰ) formation, was up-regulation under high temperature. In addition, the genes for protein modification like Protein disulfide isomerase (PDI) and rice basic leucine Zipper factor/rice prolamin box binding factor(RISBZ1/RPBF) were up-regulation when exposed to high temperature.
1、花后高温所导致的稻米蒸煮食味品质变劣现象(如糊化温度升高和胶稠度下降等),与不同温度处理下稻米淀粉的粒径分布差异、链长精细结构之间存在着密切联系。花后高温胁迫对稻米淀粉粒粒径的影响表现为：导致小型淀粉粒和中型淀粉粒的数量与相对比例降低,大型淀粉粒的数量与相对比例显著增大,淀粉粒的平均粒径增大,这是稻米糊化温度与糊化热焓值明显升高的重要因素。此外,花后高温会导致稻米直链淀粉的聚合度降低、支链淀粉长B链组分(B3链,DP≥37)的比例上升,短B链组分(B1链,DP13-24)的比例有所下降。与稻米表观直链淀粉含量(AC)的品种类型间差异相似,花后高温胁迫对稻米B2链(DP25-36)与短A链(DP5-12)也表现出一定的品种类型差异。低AC类型品种嘉935在花后高温下的B2链比例上升、短A链比例下降,而高AC类型品种嘉353呈相反趋势。
2、花后高温下发育胚乳中的蔗糖转运体(SUT)和蔗糖合成酶(SuSy)主要同工型基因(SUT1, SUT2, SuSy2和SuSy3)的相对表达量降低,但质体转化酶基因(CIN2和CIN7)的相对表达量上升,高温胁迫破坏发育胚乳糖卸载代谢环节两个关键蔗糖合成酶和质体转化酶间的平衡,降低蔗糖的卸载效率；此外,高温胁迫下己糖激酶类的几个主要功能基因(HxKI和HxKⅡ等)上调表达,而果糖激酶类和糖信号作用蛋白的相关功能基因(FrK Ⅰ和FrKⅡ)下调表达,两类基因(HxK类和FrK类)在高温胁迫下的相对表达量呈“此消彼长”变化,说明花后高温抑制己糖磷酸化代谢途径,并改变发育胚乳中的有关糖信号途径及其应答机制,不利于淀粉的合成代谢。
3、花后高温对水稻胚乳淀粉精细结构的影响效应涉及到淀粉合成代谢途径多个功能基因及相应同工型的特异性表达。淀粉合成酶基因(如SSS Ⅰ、SSSⅢa、SSSⅣa等)呈上调表达,淀粉合成酶与分支酶基因(如SSS Ⅱa、SBE Ⅰ、SBEⅢ等)呈下调表达,异淀粉酶基因ISA1的相对表达量上升,普鲁兰酶基因PUL的相对表达量下降,花后高温对稻米淀粉精细结构的影响效应(例如,B3链比例上升、B1链比例下降,等)受上述功能基因与同工型的共同调控,而SSS Ⅰ、SSS ⅡaQ两同工型基因对支链淀粉链长合成的催化作用最为明显。此外,GBSS Ⅰ是在发育胚乳中相对表达量较高的颗粒结合型淀粉合成酶基因同工型,高温胁迫下,GBSS Ⅰ在低直链淀粉品种嘉935胚乳中的相对表达量下降,而高直链淀粉品种嘉353中则呈相反趋势,这与不同温度处理下两水稻品种胚乳中的直链淀粉含量变化趋势是一致的。
4、水稻籽粒糊粉层临时淀粉的正常降解,对胚乳淀粉合成所需的碳源和能量保障具有重要意义。花后高温胁迫对临时淀粉降解代谢(包括磷酸化降解和非磷酸化降解两条途径)相关基因的影响主要表现为：“上游基因”(如GWD、AMY3和SEX4等)在高温胁迫下呈上调表达,导致代谢中间产物的快速累积；而“下游基因”(如ISA3、PUL和MEX1等)大多呈下调表达,抑制淀粉降解中间产物进一步分解。“上游基因”和“下游基因”的表达模式引起淀粉降解中间产物在糊粉层的过量累积,影响稻米糊粉层的营养转运功能,这可能是导致花后高温胁迫下胚乳淀粉合成所需的碳源和能量供应不足,并引起总淀粉积累量降低的重要原因。
5、花后高温胁迫下,水稻籽粒中的蛋白和氨基酸组分含量在灌浆前期普遍上升；醇溶蛋白含量在灌浆后期下降,蛋白和氨基酸组分含量差异主要表现在灌浆后期。高温加速蛋白体的形成,改变谷蛋白和醇溶蛋白亚基的相对含量,其中,醇溶蛋白13kDa亚基相对含量略微降低,17-19kDa亚基相对含量上升,谷蛋白亚基和谷蛋白前体相对含量均上升。水稻胚乳蛋白积累不仅受蛋白亚基前体基因的调控,同时还受到蛋白质修饰相关基因的调控。与蛋白亚基前体基因相比,蛋白质修饰调控和逆境防御相关基因对高温胁迫更为敏感。其中,内质网细胞腔结合蛋白基因(BiP)在高温下的上调表达有利于醇溶蛋白的折叠与聚集,加速蛋白体1的形成：蛋白质二硫同分异构酶基因(PDI)、水稻碱性亮氨酸拉链蛋白基因／醇溶谷蛋白框结合蛋白基因(RISBZ1/RPBF)组合的上调表达与高温胁迫下的蛋白前体聚合过程和逆境防御代谢有关。
High temperature during reproductive period is one of the crucial factors influencing rice yield and grain quality; Base on the former research work, two early non-waxy indica rice cultivars (J935and J353) differing in cooking and eating quality were chosen to investigate the effects of high temperature on the fine structure of amylopectin, protein body formation and starchy granule distribution by a field experiment of different sowing-date and the controlled temperature treatments in chambers, respectively. In current study, the cDNA microarrays, RT-PCR, protein expression analysis were used to elucidate the underlying metabolisms involved in starchy biosynthesis and storage protein accumulation, as well as their relations to rice grain quality when subjected to high temperature. The main results were showed as follows:
1. The high temperature stress at filling stage could deteriorate cooking and eating quality, which was closely related to rice starch granule size distribution as well as starch fine structure. High temperature increased rice starch granule average diameter, caused the percentage of large starch granule increasing, but small and medium-sized starch granule presented with an opposite way. The Phenomenon of starch granule size, affected by high temperature, was one of the explanations for rice starch gelatinization properties involved in high temperature at filling stage. In addition, great changes were also found in rice starch fine structure (chain length) when treated with two temperatures. Among different amylopectin components, long B chain (B3chain, DP≥37) increased significantly with B1chain (DP13-24) components decreasing under high temperature treatment. B3and B1chain presented a similar trend between the two variety, while B2chain (DP25-36) and A chain (DP5-12) differed by variety under high temperature stress. The proportion of B2chain increased in J935, a high quality variety, but decreased in J353. A chain was just opposite to B2chain. For different components in grain developing stage, the short A chain presented a higher proportion at initial stage relative to the other components, but gradually decreased as filling stage. On the contrary with A chain, B1, B2chain and B3chain showed lower proportion at initial stage and higher at later stage.
2. The high temperature stress at filling stage may inhibit the relative expression amount to main isoform genes (SUT1and SUT2) for Sucrose Transporter (SUT), implying sucrose transport pathway might be inhibited by high temperature. In addition, the main isoform genes (SuSy2and SuSy3) for sucrose synthase (SuSy) were down-regulation, which indicated sucrose unloading in rice endosperm impaired by high temperature treatment, however, the genes (CIN2and CIN7) related to plasmid-invertase in rice endosperm induced by high temperature. It was showed that high temperature broke the balance between sucrose synthase and plasmid-invertase, and Limited sucrose unloading efficiency. For sugar signal transduction procedure, the gene referred to fructokinase and hexokinase played important role at sugar signal transduction in rice endosperm, the "shift" phenomenon of fructokinase (FrK Ⅰand FrK Ⅱ) and hexokinase (HxK Ⅰand HxK Ⅱ) in the fructose phosphorylation might be an adaptation mechanism to high temperature stress in rice. High temperature can inhibit some signal transduction pathways.
3. There were numerous genes involved in starch synthesis, as well as starch fine structure, in rice endosperm exposed to high temperature at filling stage. Among different gene isoform, some genes for starch synthase (SSS Ⅰ, SSS Ⅲa and SSS Ⅳa) was shown up-regulation when exposed to high temperature, but SSS Ⅱa, SBE Ⅰ, SB Ⅵ, which for starch synthase and starch branching synthase presented down-regulation. For starch debranching synthase genes, ISA1showed up-regulation, while PUL presented down-regulation under high temperature stress. Different expression patterns of genes for the three enzymes co-governed amylecptin, and determined its fine structure at high temperture. SSS Ⅰ,SSSⅡa was the two gene isoforms, which was the most important in starch fine structure. Concerned as GBSS Ⅰ, which mainly acted on amylase content, presented up-regulation in J353and down-regulation in J935. The change of GBSS Ⅰ expression pattern was coincide with amylose content when exposed to different temperature treatments at filling stage.
4. Transition starch degradation, what always occur in rice grain aleurone, played an important role in supplying carbon source and energy to starch synthesis in rice endosperm. Effect of high temperature on starch degradation metabolism (including phosphorylated degradation pathway and non-phosphorylated degradation pathway) in rice endosperm at filling stage presented similar features:"upstream genes"(like GWD, AMY3and SEX4) showed up-regulation pattern responsible to high temperature stress, which resulted in a rapid accumulation of intermediate product from starch degradation. However,"downstream genes"(like ISA3, PUL and MEX1) mostly inhibited by high temperature, which impaired successive degradation of intermediate product. The expression patterns of "upstream genes" and "downstream genes" under high temperature results in excess accumulation of intermediate product in rice aleurone, which might restrict carbon and energy supply, reduce total starch content in rice endosperm.
5. High temperature stress increased the accumulation of all classes of storage proteins and amino acid at early filling stage but decreased the accumulation of prolamin at later stage. High temperature not only accelerated the formation process of protein body (PB Ⅰ and PBⅡ), but also changed relative proportion of storage protein subunit in rice endosperm. For prolamin, high temperature resulted in slightly decreasing of13kDa prolamin subunits with a slight extent, and significantly increasing17-19kDa subunits. For Glutelin, high temperature cause higher content for α-subunit and β-subunit than those to lower temperature. The accumulation of storage protein in rice endosperm was not only regulated by gene related to protein subunit or precursor, but also controlled by the gene involving in protein modification and stress-defense. Compared with the former, the latter was much more sensitive to high temperature. For example, luminal-binding protein precursor gene (BiP), which contributed to prolamin fold and aggregation, as well as protein body Ⅰ (PB Ⅰ) formation, was up-regulation under high temperature. In addition, the genes for protein modification like Protein disulfide isomerase (PDI) and rice basic leucine Zipper factor/rice prolamin box binding factor(RISBZ1/RPBF) were up-regulation when exposed to high temperature.
引文
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