核黄素及核黄素结合蛋白对拟南芥抗病抗逆调控作用的初步研究
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摘要
核黄素及其衍生物FMN和FAD在植物的生长发育过程中发挥着极其重要的作用。FMN和FAD作为黄素蛋白的辅基在植物的线粒体电子传递,光合作用,脂肪酸以及某些氨基酸等的代谢中发挥着重要的作用。尤其需要强调的是,它们广泛参与调控了植物细胞内活性氧(ROS)以及氧还平衡代谢调控。
ROS代谢以及氧还平衡调控在植物的生长发育以及抗病抗逆境胁迫中发挥着极其重要的作用。而在植物抵抗非生物胁迫的过程中,早期阶段胁迫诱导的ROS上升起到一种信号分子作用,诱导植物合成更多的ROS清除物质。
体外喷洒核黄素的水溶液能诱导植物增强对多种病原菌的抗性。体内核黄素含量改变也能导致植物相应地改变对多种病原菌的抗性。这说明核黄素在植物应答病害侵染上有着重要的作用。
核黄素结合蛋白是一类能与核黄素特异结合的动物蛋白,对于它们的功能特点,在动物体内已经有较深入的研究。然而在植物体内,目前尚未发现能与核黄素特异性结合的蛋白,也未见类似功能基因被克隆的报道。这可能与动物和植物采用了不同的核黄素调控机制有关。
我们实验室通过转基因技术将中华鳖体内的核黄素结合蛋白基因TsRfBP转入野生型拟南芥Col-0后,得到一系列能表达该结合蛋白的转基因植株。在这个现有的转基因材料的基础上,本文主要对其在抗病抗逆上的功能进行了初步的研究,得到了一些有意义的实验结果。此外,对植物进行核黄素体外喷洒实验,也是对核黄素抗病研究的有益且必要的补充。以下是我们的主要实验结果。
1.转TsRfBP拟南芥增强对假单胞菌番茄变种DC3000的抗性但降低对大白菜软腐病的抗性
在这一工作中,我们首先利用免疫胶体金和Northern杂交技术进一步验证了核黄素结合蛋白(RfbP)只在转基因植株K11(相对于野生型Col-0和空白对照RfbPi)中进行表达。在其应答两种不同营养类型病原物侵染上的初步研究中发现,与野生型(以及空白对照RfbPi)相比,开花提前(2-3周)而相对更成熟的K11植株对活体营养菌如Pseudomonas syringae subsp tomato DC3000的抗性增强但对死体营养菌如大白菜软腐病Pectobactor carotovora sp carotovora的抗性则削弱,而且这种趋势随年龄增长而有进一步增强(DC3000)或削弱(Pcc)的趋势。在进一步的研究中发现,K11植株有早衰趋势,它的叶片细胞更容易死亡,能积累更多的的H202,以及更严重的氧化损伤。在讨论中,我们发现用“年龄相关的抗性(Age-Related Resistance, ARR)”理论(即成熟植株或叶片比年幼植株或叶片抗病力强或弱)似乎能较好地解释这一现象。这主要是基于K11植株(与Co1-0对比)成熟更快和活性氧较高的特点而提出这个假说的。当然,该假说需要进一步的实验论证。
2.转TsRfBP拟南芥既能促进生长又具有显著增强的干旱适应能力
在这一工作中,我们主要比较了转基因植株K11和Co1-0的干旱适应能力并发现前者抗旱能力显著增强。考虑到核黄素代谢以及植物抗旱都与抗氧化应答有密切关系,所以这里主要从这个角度对其进行了比较研究。发现在正常条件下,K11虽然拥有较高的抗氧化酶(SOD,CAT,APX和GR酶)活力以及较高含量的抗氧化物质(抗坏血酸和谷胱甘肽)积累,然而其ROS积累较多,氧化损伤(离子渗漏和脂类氧化损伤)也更严重,其氧还平衡值(ASC/DHA和GSH/GSSG)也更低。然而有趣的是,在干旱胁迫处理下,与Co1-0相比我们发现其氧化损伤较轻,相应地其抗氧化能力下降较慢,其氧化平衡状态能保持较稳定的水平,从而表现出更强的干旱抗性或适应能力。然而K11比Col-0开花提前,成熟早,生长速度快。这似乎与通常所见的植物“抗旱-生长矛盾”现象(即抗旱往往生长较慢,生长快的往往抗旱较差)相悖。我们在讨论中提出“胁迫逃逸(stress escape)"的新假说(类似干旱逃逸)似乎能较好地解释黄素(即FMN和FAD)相对不足情况下,植物可能为了逃避这种因核黄素结合蛋白表达而导致的核黄素不足以及可能由此引发的轻度氧胁迫而加快植物生长并提前开花,从而避免因核黄素的进一步不足而可能导致的更严重后果(如植物死亡)出现。这一假说若能成立,将为指导今后培养优质抗旱农作物提供新思路。即只要将植物引入一种类似干旱逃逸的“胁迫逃逸”状态中,则“抗旱与促生长”这一对矛盾则有可能会同时得到解决。
3.体外喷洒核黄素能降低拟南芥对盐害等非生物胁迫的抗性
在这一工作中,我们的目的除了想了解体外施加核黄素能否诱导植物增强对非生胁迫的抗性外,还想了解在增强抗病的同时是否会有其它负面影响(如削弱对非生物胁迫的抗性)?这也是对其广谱抗病研究的一个补充。用不同浓度(抗病处理所用浓度)的核黄素水溶液预处理拟南芥7天后,发现作为能诱导植物增强对多种病原菌抗性的核黄素,不但不能同时诱导对盐害等非生物的抗性,反而增强了处理植株对这些胁迫的敏感性。这表现在处理植物氧化损伤加剧,抗氧化酶活力下降,氧还平衡值下降,H2O2积累上升。在进一步的实验中,我们通过对经核黄素预处理7天的植物叶片的抗氧化酶相关基因(MSD1,CAT1,APX1,GR1,GST1)的表达进行分子检测后发现,这些基因的表达都不同程度地下降了。在讨论中,我们认为核黄素介导的ROS(主要是单线态氧)可能是主要因素。文献报道中认为的单线态氧与H2o2/O2-在调控基因表达相拮抗的(后者能诱导植物增强对多种非生物胁迫抗性),这个结论与我们的观察和推测是一致的。这可能暗示着核黄素在应答非生物胁迫上可能主要通过其光敏产物之一的单线态氧发挥作用的(注：核黄素的其它光解产物无此功能),当然这一推测有待进一步的实验证据支持。
综上所述,我们的研究工作显示外源的核黄素结合蛋白基因TsRfBP在拟南芥Col-0中表达后,可以通过影响植物体内核黄素及其衍生物FMN和FAD的含量,从而对其生长发育产生深刻的影响,并通过影响细胞内的氧化还原状态的调控和活性氧的代谢而进一步导致其对生物胁迫(此处主要是两类不同营养类型的病原细菌)和非生物胁迫(此处为干旱胁迫)的应答发生了显著的改变。而其中的促生长与抗旱性状的同时获得无疑为我们培育优质的抗旱农作物新品种提供了全新的思路和策略。而体外喷洒核黄素虽然能诱导植物增强增强对多种病原菌的抗性(前人报道),然而其造成的抗盐抗旱能力削弱的副作用也必需引起注意。此外,核黄素介导的活性氧(主要是单线态氧)可能是其在生物胁迫和非生物胁迫应答调控中的关键因素,而其有别于H202等活性氧的功能特点,为我们进一步研究活性氧作为信号分子参与调控植物对病害和逆境胁迫应答的机理解析提供了新的思路。
Riboflavin is the precursor of FMN and FAD, which play key roles in plant development and growth. They are required for many metabolism reactions such as mitochondrial electron transport, photosynthesis, fatty acid degradation and redox regulation. As for the redox homeostasis modulation, FAD is an indispensable component of many ROS-scavenging enzymes, such as glutathione reductase, monodehydrogen ascorbate reductase, and NADPH-dependent thiol reductase. Interestingly, FAD or FMN is also required for many ROS-generating enzymes, such as the NADPH-oxidase, glycolate oxidase and certain amine oxidases. In addition, riboflavin can generate singlet oxygen in the presence of light in vitro or in vivo.
Reactive oxygen species (ROS) is an unavoidable toxic by-product of plant metabolism under favorable or adverse conditions. These ROS, such as superoxide anion, hydrogen peroxide, hydroxyl radical and singlet oxygen, also can function as signaling molecules in plant defense against pathogen attack and abiotic stress challenge. For example, H2O2is required for the hypersensitive response (HR) in pathogen resistance. In addition, the early increase of ROS content also plays an "alarm" role in plant for response the abiotic stress challenge.
In vitro experiment indicates that riboflavin is an important "elicitor" in plant pathogen resistance. In addition, the in vivo experiment (up-or down-regulate endogenous riboflavin content in plant) also shows riboflavin has a close correlation with pathogen resistance. In our experiment, a riboflavin-binding protein encoding gene TsRfBP was introduced into Arabidopsis thaliana Col-0and acquired transgenic plant with low free riboflavin availability. Riboflavin-binding protein was expressed in animal cells and there is no report of similar gene or protein in plant species.
Recently, riboflavin was applied on plant and acquired significant enhancement of pathogen defense capacity. For example, foliar spraying of riboflavin solution can confer Arabidopsis enhanced both biotrophic and necrotrophic pathogen resistance by trigger a noval signaling pathway. As for this broad-spectrum pathogen resistance, a "priming" hypothesis was proposed by our laboratory. Thus, we want to kow whether foliar application of riboflavin can also trigger abiotic stress tolerance.
1. Ectopic expression of riboflavin-binding protein gene TsRfBP incuces Pst DC3000resistance but impairs Pcc in transgenic Arabidopsis thaliana
Here, the TsRfBP was further identified in the transgenic plant K11with Northern blot and immunolocalization techniques. Then, we compared the pathogen resistance between the Col-0and the transgenic plant K11(carried riboflavin-binding protein) in two growth time points (20-day and40-day old). In compared with the Col-0, enhanced Pst DC3000(Pseudomonas syringae pv tomato DC3000, a biotrophic or facultative pathogen) and impaired Pcc (Pectobacter carotovora subsp. carotovora, a necrotrophic pathogen) resistance were observed in K11plant. Higher content of H2O2accumulation and severe cell death were monitored in K11over Col-0in the vegetative growth stages. In addition, accelerated senescence (or more matured growth state) was observed in K11over Col-0under our growth conditions. As for this interesting phenomenon, an "ARR-like" or Age-Related Response like mechanism was proposed to illustrate these two different trophic pathogen response, although more detailed experimental evidence was required to support this hypothesis.
2. Ectopic expression of riboflavin-binding protein gene TsRfBP paradoxically enhances both plant growth and drought tolerance in transgenic Arabidopsis thaliana
In the second chapter, we compared the antioxidant response of the Col-0and the transgenic plant K11under drought stress exposure. Under favorable conditions, higher accumulation of H2O2and TBARS, lower values of redox ratio were observed in K11over Col-0. However, enhanced drought tolerance was monitored in the K11over the Col-0coupled with higher accumulation of soluble sugar and free proline content. In consistent with these, lower decrease of antioxidant enzyme (SOD, CAT, APX and GR) activities and higher redox homeostasis were measured in K11over Col-0under stress exposure. In addition, faster growth rate, accelerated flowering and enhanced senescence are the basic features of "drought escape" strategy adopted by certain plant under gradual enhancement of drought stress. Here, we proposed a "stress escape" concept to illustrate the low riboflavin-mediated "both plant growth and drought tolerance enhancement" phenomenon observed in the K11plant over its Col-0counterparts. This work may help us to improve crop plant with higher growth rate and greater drought tolerance.
3. Exogenous riboflavin fails to induce salt stress tolerance in Arabidopsis thaliana
In the chapter Ⅲ, Arabidopsis thaliana were pretreated with different concentration (0,20μM,200μM and2mM) of riboflavin solution and their abiotic stress tolerance (such as salt, drought, and shade) were compared in this experiment. Reduced salt and drought tolerance were observed in the riboflavin-pretreated plants compared with the control (0μM riboflavin treated group). In line with these, enhanced oxidative damage, decreased antioxidant enzyme activities and redox ratio values were measured in the riboflavin-pretreated plant than these in the control Arabidopsis under salt conditions. Expression level of stress-related genes (MSD1, CAT1, APX1et al.) was down-regulated in the riboflavin-treated leaves over the control. In the discussion, we considered the riboflavin-mediated ROS production play a key role in the impaired abiotic stress tolerance observed in this experiment. In addition, it suggests that this abiotic stress tolerance impairement should be considered in the pathogen resistance with exogenous riboflavin application.
In conclusion, riboflavin-binding protein mediated pathogen response and drought tolerance give us a noval insight of the roles of riboflavin in environmental stress response of plant. The exogenous riboflavin fails to induce abiotic stress tolerance indicates the riboflavin-mediated ROS (singlet oxygen) should play a different role in environmental stress challenge (including pathogen and salt stress et al. resistance).
ROS代谢以及氧还平衡调控在植物的生长发育以及抗病抗逆境胁迫中发挥着极其重要的作用。而在植物抵抗非生物胁迫的过程中,早期阶段胁迫诱导的ROS上升起到一种信号分子作用,诱导植物合成更多的ROS清除物质。
体外喷洒核黄素的水溶液能诱导植物增强对多种病原菌的抗性。体内核黄素含量改变也能导致植物相应地改变对多种病原菌的抗性。这说明核黄素在植物应答病害侵染上有着重要的作用。
核黄素结合蛋白是一类能与核黄素特异结合的动物蛋白,对于它们的功能特点,在动物体内已经有较深入的研究。然而在植物体内,目前尚未发现能与核黄素特异性结合的蛋白,也未见类似功能基因被克隆的报道。这可能与动物和植物采用了不同的核黄素调控机制有关。
我们实验室通过转基因技术将中华鳖体内的核黄素结合蛋白基因TsRfBP转入野生型拟南芥Col-0后,得到一系列能表达该结合蛋白的转基因植株。在这个现有的转基因材料的基础上,本文主要对其在抗病抗逆上的功能进行了初步的研究,得到了一些有意义的实验结果。此外,对植物进行核黄素体外喷洒实验,也是对核黄素抗病研究的有益且必要的补充。以下是我们的主要实验结果。
1.转TsRfBP拟南芥增强对假单胞菌番茄变种DC3000的抗性但降低对大白菜软腐病的抗性
在这一工作中,我们首先利用免疫胶体金和Northern杂交技术进一步验证了核黄素结合蛋白(RfbP)只在转基因植株K11(相对于野生型Col-0和空白对照RfbPi)中进行表达。在其应答两种不同营养类型病原物侵染上的初步研究中发现,与野生型(以及空白对照RfbPi)相比,开花提前(2-3周)而相对更成熟的K11植株对活体营养菌如Pseudomonas syringae subsp tomato DC3000的抗性增强但对死体营养菌如大白菜软腐病Pectobactor carotovora sp carotovora的抗性则削弱,而且这种趋势随年龄增长而有进一步增强(DC3000)或削弱(Pcc)的趋势。在进一步的研究中发现,K11植株有早衰趋势,它的叶片细胞更容易死亡,能积累更多的的H202,以及更严重的氧化损伤。在讨论中,我们发现用“年龄相关的抗性(Age-Related Resistance, ARR)”理论(即成熟植株或叶片比年幼植株或叶片抗病力强或弱)似乎能较好地解释这一现象。这主要是基于K11植株(与Co1-0对比)成熟更快和活性氧较高的特点而提出这个假说的。当然,该假说需要进一步的实验论证。
2.转TsRfBP拟南芥既能促进生长又具有显著增强的干旱适应能力
在这一工作中,我们主要比较了转基因植株K11和Co1-0的干旱适应能力并发现前者抗旱能力显著增强。考虑到核黄素代谢以及植物抗旱都与抗氧化应答有密切关系,所以这里主要从这个角度对其进行了比较研究。发现在正常条件下,K11虽然拥有较高的抗氧化酶(SOD,CAT,APX和GR酶)活力以及较高含量的抗氧化物质(抗坏血酸和谷胱甘肽)积累,然而其ROS积累较多,氧化损伤(离子渗漏和脂类氧化损伤)也更严重,其氧还平衡值(ASC/DHA和GSH/GSSG)也更低。然而有趣的是,在干旱胁迫处理下,与Co1-0相比我们发现其氧化损伤较轻,相应地其抗氧化能力下降较慢,其氧化平衡状态能保持较稳定的水平,从而表现出更强的干旱抗性或适应能力。然而K11比Col-0开花提前,成熟早,生长速度快。这似乎与通常所见的植物“抗旱-生长矛盾”现象(即抗旱往往生长较慢,生长快的往往抗旱较差)相悖。我们在讨论中提出“胁迫逃逸(stress escape)"的新假说(类似干旱逃逸)似乎能较好地解释黄素(即FMN和FAD)相对不足情况下,植物可能为了逃避这种因核黄素结合蛋白表达而导致的核黄素不足以及可能由此引发的轻度氧胁迫而加快植物生长并提前开花,从而避免因核黄素的进一步不足而可能导致的更严重后果(如植物死亡)出现。这一假说若能成立,将为指导今后培养优质抗旱农作物提供新思路。即只要将植物引入一种类似干旱逃逸的“胁迫逃逸”状态中,则“抗旱与促生长”这一对矛盾则有可能会同时得到解决。
3.体外喷洒核黄素能降低拟南芥对盐害等非生物胁迫的抗性
在这一工作中,我们的目的除了想了解体外施加核黄素能否诱导植物增强对非生胁迫的抗性外,还想了解在增强抗病的同时是否会有其它负面影响(如削弱对非生物胁迫的抗性)?这也是对其广谱抗病研究的一个补充。用不同浓度(抗病处理所用浓度)的核黄素水溶液预处理拟南芥7天后,发现作为能诱导植物增强对多种病原菌抗性的核黄素,不但不能同时诱导对盐害等非生物的抗性,反而增强了处理植株对这些胁迫的敏感性。这表现在处理植物氧化损伤加剧,抗氧化酶活力下降,氧还平衡值下降,H2O2积累上升。在进一步的实验中,我们通过对经核黄素预处理7天的植物叶片的抗氧化酶相关基因(MSD1,CAT1,APX1,GR1,GST1)的表达进行分子检测后发现,这些基因的表达都不同程度地下降了。在讨论中,我们认为核黄素介导的ROS(主要是单线态氧)可能是主要因素。文献报道中认为的单线态氧与H2o2/O2-在调控基因表达相拮抗的(后者能诱导植物增强对多种非生物胁迫抗性),这个结论与我们的观察和推测是一致的。这可能暗示着核黄素在应答非生物胁迫上可能主要通过其光敏产物之一的单线态氧发挥作用的(注：核黄素的其它光解产物无此功能),当然这一推测有待进一步的实验证据支持。
综上所述,我们的研究工作显示外源的核黄素结合蛋白基因TsRfBP在拟南芥Col-0中表达后,可以通过影响植物体内核黄素及其衍生物FMN和FAD的含量,从而对其生长发育产生深刻的影响,并通过影响细胞内的氧化还原状态的调控和活性氧的代谢而进一步导致其对生物胁迫(此处主要是两类不同营养类型的病原细菌)和非生物胁迫(此处为干旱胁迫)的应答发生了显著的改变。而其中的促生长与抗旱性状的同时获得无疑为我们培育优质的抗旱农作物新品种提供了全新的思路和策略。而体外喷洒核黄素虽然能诱导植物增强增强对多种病原菌的抗性(前人报道),然而其造成的抗盐抗旱能力削弱的副作用也必需引起注意。此外,核黄素介导的活性氧(主要是单线态氧)可能是其在生物胁迫和非生物胁迫应答调控中的关键因素,而其有别于H202等活性氧的功能特点,为我们进一步研究活性氧作为信号分子参与调控植物对病害和逆境胁迫应答的机理解析提供了新的思路。
Riboflavin is the precursor of FMN and FAD, which play key roles in plant development and growth. They are required for many metabolism reactions such as mitochondrial electron transport, photosynthesis, fatty acid degradation and redox regulation. As for the redox homeostasis modulation, FAD is an indispensable component of many ROS-scavenging enzymes, such as glutathione reductase, monodehydrogen ascorbate reductase, and NADPH-dependent thiol reductase. Interestingly, FAD or FMN is also required for many ROS-generating enzymes, such as the NADPH-oxidase, glycolate oxidase and certain amine oxidases. In addition, riboflavin can generate singlet oxygen in the presence of light in vitro or in vivo.
Reactive oxygen species (ROS) is an unavoidable toxic by-product of plant metabolism under favorable or adverse conditions. These ROS, such as superoxide anion, hydrogen peroxide, hydroxyl radical and singlet oxygen, also can function as signaling molecules in plant defense against pathogen attack and abiotic stress challenge. For example, H2O2is required for the hypersensitive response (HR) in pathogen resistance. In addition, the early increase of ROS content also plays an "alarm" role in plant for response the abiotic stress challenge.
In vitro experiment indicates that riboflavin is an important "elicitor" in plant pathogen resistance. In addition, the in vivo experiment (up-or down-regulate endogenous riboflavin content in plant) also shows riboflavin has a close correlation with pathogen resistance. In our experiment, a riboflavin-binding protein encoding gene TsRfBP was introduced into Arabidopsis thaliana Col-0and acquired transgenic plant with low free riboflavin availability. Riboflavin-binding protein was expressed in animal cells and there is no report of similar gene or protein in plant species.
Recently, riboflavin was applied on plant and acquired significant enhancement of pathogen defense capacity. For example, foliar spraying of riboflavin solution can confer Arabidopsis enhanced both biotrophic and necrotrophic pathogen resistance by trigger a noval signaling pathway. As for this broad-spectrum pathogen resistance, a "priming" hypothesis was proposed by our laboratory. Thus, we want to kow whether foliar application of riboflavin can also trigger abiotic stress tolerance.
1. Ectopic expression of riboflavin-binding protein gene TsRfBP incuces Pst DC3000resistance but impairs Pcc in transgenic Arabidopsis thaliana
Here, the TsRfBP was further identified in the transgenic plant K11with Northern blot and immunolocalization techniques. Then, we compared the pathogen resistance between the Col-0and the transgenic plant K11(carried riboflavin-binding protein) in two growth time points (20-day and40-day old). In compared with the Col-0, enhanced Pst DC3000(Pseudomonas syringae pv tomato DC3000, a biotrophic or facultative pathogen) and impaired Pcc (Pectobacter carotovora subsp. carotovora, a necrotrophic pathogen) resistance were observed in K11plant. Higher content of H2O2accumulation and severe cell death were monitored in K11over Col-0in the vegetative growth stages. In addition, accelerated senescence (or more matured growth state) was observed in K11over Col-0under our growth conditions. As for this interesting phenomenon, an "ARR-like" or Age-Related Response like mechanism was proposed to illustrate these two different trophic pathogen response, although more detailed experimental evidence was required to support this hypothesis.
2. Ectopic expression of riboflavin-binding protein gene TsRfBP paradoxically enhances both plant growth and drought tolerance in transgenic Arabidopsis thaliana
In the second chapter, we compared the antioxidant response of the Col-0and the transgenic plant K11under drought stress exposure. Under favorable conditions, higher accumulation of H2O2and TBARS, lower values of redox ratio were observed in K11over Col-0. However, enhanced drought tolerance was monitored in the K11over the Col-0coupled with higher accumulation of soluble sugar and free proline content. In consistent with these, lower decrease of antioxidant enzyme (SOD, CAT, APX and GR) activities and higher redox homeostasis were measured in K11over Col-0under stress exposure. In addition, faster growth rate, accelerated flowering and enhanced senescence are the basic features of "drought escape" strategy adopted by certain plant under gradual enhancement of drought stress. Here, we proposed a "stress escape" concept to illustrate the low riboflavin-mediated "both plant growth and drought tolerance enhancement" phenomenon observed in the K11plant over its Col-0counterparts. This work may help us to improve crop plant with higher growth rate and greater drought tolerance.
3. Exogenous riboflavin fails to induce salt stress tolerance in Arabidopsis thaliana
In the chapter Ⅲ, Arabidopsis thaliana were pretreated with different concentration (0,20μM,200μM and2mM) of riboflavin solution and their abiotic stress tolerance (such as salt, drought, and shade) were compared in this experiment. Reduced salt and drought tolerance were observed in the riboflavin-pretreated plants compared with the control (0μM riboflavin treated group). In line with these, enhanced oxidative damage, decreased antioxidant enzyme activities and redox ratio values were measured in the riboflavin-pretreated plant than these in the control Arabidopsis under salt conditions. Expression level of stress-related genes (MSD1, CAT1, APX1et al.) was down-regulated in the riboflavin-treated leaves over the control. In the discussion, we considered the riboflavin-mediated ROS production play a key role in the impaired abiotic stress tolerance observed in this experiment. In addition, it suggests that this abiotic stress tolerance impairement should be considered in the pathogen resistance with exogenous riboflavin application.
In conclusion, riboflavin-binding protein mediated pathogen response and drought tolerance give us a noval insight of the roles of riboflavin in environmental stress response of plant. The exogenous riboflavin fails to induce abiotic stress tolerance indicates the riboflavin-mediated ROS (singlet oxygen) should play a different role in environmental stress challenge (including pathogen and salt stress et al. resistance).
引文
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