钾素提高玉米（Zea mays L.）茎腐病抗性的营养与分子生理机制
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摘要
玉米茎腐病是世界玉米产区普遍发生的一种土传病害,严重影响到玉米的产量。近年来,由于耕作制度(如保护性耕作,秸秆还田等)及气候的影响,茎腐病在我国有逐年加重的趋势。应用化学手段很难完全控制该病,而且会对环境产生负面影响。研究发现,施钾能显著降低茎腐病的发病率,但是关于钾抑制玉米茎腐病发生的机制尚不清楚。本研究将田间试验和砂培试验相结合,研究了钾素对玉米各生育期干物质和氮磷钾积累与转运的影响;采用生理生化和分子生物学方法研究了钾素对接菌后玉米茎髓和幼根中酚类代谢产物总酚和木质素含量、酚类代谢关键酶活性及其基因表达的影响,研究了钾素对玉米碳水化合物分配及病原菌入侵后玉米幼根糖代谢产物和糖代谢关键酶活性及其基因表达的影响;利用扫描电镜和透射电镜观察了施钾后玉米茎髓组织和接菌后施钾和不施钾幼根根尖细胞超微结构的变化。主要结果如下:
1)施钾能显著降低玉米茎腐病的发病率。通过两年的试验结果分析,钾素对茎腐病的防治效果达35%-50%。玉米各生育期的根系、茎秆、叶片、叶鞘等营养体器官的钾素含量与茎腐病的发病率存在极显著的负相关。钾素能够促进玉米对干物质和氮磷钾的积累和转运,缺钾条件下,干物质和氮磷钾养分的积累速率过早下降,积累量减少,难以满足植株生育后期的需求。容易导致植株生育后期光合产物和养分供应不足,造成根系及茎秆的提前早衰,不利于植株健康生长。
2)在钾素对玉米酚代谢的影响方面,钾素不仅有利于提高玉米茎髓固有木质素的含量,而且还有利于病原菌入侵后茎髓诱导木质素和总酚含量的增加。施钾能促进接菌后茎髓和幼根中酚代谢相关酶:苯丙氨酸解氨酶(PAL)、过氧化物酶(POD)、多酚氧化酶(PPO)活性的提高,且对酶活性的峰值其及出现的时间影响最为明显。充足供钾处理中,茎髓PAL的活性在接菌3 d后达到最大值;而幼根PAL活性最大值出现于接菌后48 h。且施钾处理中PAL活性的峰值显著高于不施钾处理。从基因表达上看,在充足供钾的幼根中,受病原诱导产生的pal表达量高于不施钾处理。钾素还可以在基因水平调节pod基因的表达,缺钾导致了pod基因表达量的下降和表达时间的延迟。充足供钾,玉米茎髓和幼根受病原菌入侵后,POD活性被迅速诱导至最大。钾素还有利于接菌后茎髓和幼根PPO活性的增加。病原菌入侵幼根后,施钾处理中ppo的表达量在24 h内增加至接菌前的4倍多,显著高于不施钾处理。总之,钾素营养能从基因水平影响pal、pod、ppo基因的表达,促进受病原菌入侵后PAL、POD、PPO三种防御酶诱导活性的提高,调节植株酚代谢水平,增强玉米对茎腐病的抗性。此外,接菌后施钾处理中,根系对阿魏酸和绿原酸的分泌量显著增加,降低了病原菌与寄主的识别机率。
3)在钾素对玉米糖代谢的影响方面,缺钾导致叶片中糖的积累,而施钾有利于糖由“源”器官向“库”器官运输,促进玉米生育后期光合产物向茎秆中分配,提高茎秆中糖含量。灌浆期和成熟期时,玉米茎秆中的糖含量与茎腐病发病率呈显著负相关。受病原菌侵染后,施钾还有利于增加幼根组织ss和sps基因表达量,提高SS和SPS活性,保持蔗糖和葡萄糖含量的稳定。不施钾导致幼根ss和sps基因表达量的减少,sps基因表达时间的延迟,从酶活性的变化上看,不施钾处理中,接菌后SPS活性降低,SS活性变化不大,造成幼根蔗糖供应明显不足,玉米幼根中蔗糖和葡萄糖含量均显著降低,且蔗糖含量的下降速率高于葡萄糖含量的下降速率,葡萄糖和蔗糖比值显著增加。总之,钾素能从基因水平影响ss、sps的表达,调节受侵染部位SS和SPS的活性,影响蔗糖和葡萄糖含量,维持受侵染部位正常的糖代谢水平。
4)在钾素对玉米细胞超微结构的影响方面,缺钾处理的玉米茎髓薄壁细胞,结构不规则,长边较长,上下相邻细胞间连接壁破裂。而不缺钾处理茎髓细胞结构规则,呈长方形,整齐排列。缺钾导致维管束间的薄壁细胞破裂,致使茎髓中维管束间失去连接细胞,支撑能力变差。另外,施钾有利于寄主表皮细胞排列紧密而整齐,细胞壁增厚,有效阻碍病原菌的入侵。而且施钾处理细胞中拥有丰富的高尔基体,可以产生大量分泌物将菌丝降解。钾素还有利于菌丝入侵部位乳突的形成及高电子致密物的积累,以阻止菌丝的扩展。总之,钾素能通过稳定细胞结构,防止细胞间隙的扩大,来降低病原菌侵入的机率;通过积累酚类等化合物,加固细胞壁;通过形成位于胞间及胞内的闭塞物来限制病原物在寄主细胞的进一步发展。
综上所述,钾素不仅是植物生长所必需的营养元素,还是一种抗性元素。钾素一方面能够通过调控植物防御基因的表达,参与酚类物质的生理代谢过程,产生抑菌物质,稳定细胞结构,加固细胞壁,阻止病原菌的入侵和扩展;另一方面钾素还能促进营养物质的运输,并能通过调控受侵染部位糖代谢相关基因的表达,参与该部位糖类物质的转化,维持正常的糖代谢水平,为防御反应提供充足的能量和原料。可见,钾素可同时对植物次生代谢和初生代谢进行调节,起到抗病作用。
Stalk rot is a serious and widespread soil-borne disease in maize, which reduces both yield and quality. Moreover, recently, because the changes of cultivation practices (conservation tillage, straw returning etc) and climatic conditions, stalk rot of maize aggravated year by year in China. Using chemicals to control the disease can not control it completely, and it often cause environment pollution. It has been found that application of potassium (K) fertilizer can result in reduction of maize stalk rot. However, the mechanism of maize resistance to this disease due to K fertilizer application has not been completely understood. Both field experiment and sand-culture experiment were conducted to study the effect of maize K nutrition status on dry matter and NPK accumulation and translocation at entire growth stage of maize; the effect of K nutrition status on phenolic metabolism products ( total phenol and lignin ), the activity of related enzyme and expression of related genes of inoculated stalk pith and young root of maize; the effect of K nutrition status on carbohydrate distribution and sugar metabolism products, the activity of related enzyme and expression of related genes of inoculated young root. Scanning electron microscope and transmission electron microscope were used to observe the effect of K on the ultrastructure of maize stalk pith tissue and young root tip cell influenced by K and pathogen. The main results are summarized as follows:
1) Potassium application to maize could reduce the incidence of stalk rot significantly. According to the results from two years field experiments, the control efficiency of K to stalk rot reached to 35%-50%. The K content in vegetative organs, such as root, stalk, leaf, sheath had negative correlation with stalk rot incidence. Potassium application stimulated the accumulation, translocation and distribution of dry matter and NPK. Under K deficient condition, dry matter and NPK accumulation rate declined early, and the amount of nutrients accumulated reduced, resulting in shortage of nutrients supply at later growth stage. Therefore, early senescence occurred in roots and stems when photosynthate and nutrients were deficiency, which limited healthy growth and development of plant.
2) Potassium application not only improved the inherent lignin content, but also increased induced lignin and phenol content of stalk pith. K could enhance the activities of phenolic metabolism related enzymes (phenylalanine ammonia-lyase, PAL; peroxidase, POD; polyphenoloxidase, PPO), especially had significant influence on the peak and its appearance time of the enzyme activity. In treatment with K application (+K), the activity of PAL in stalk pith reached maximum at 3 days after inoculation; and the activity of PAL in young root reached peak at 48 h after inoculation. Moreover, the inoculated root in +K treatment had higher pal transcripts as compared with no K treatment (-K). Potassium status in maize plants could also regulate pod gene expression. After inoculation, pod gene expressed later and lower in K deficient root. POD activity of stalk pith and young root induced rapidly to the maximum in K abundant treatment. Moreover, in +K treatment, the transcripts of ppo after inoculation increased 4-folds, which was higher than in–K treatment. When inoculated, K also enhanced PPO activity in both stalk pith and young root. Therefore, K could increase the resistant ability to maize stalk rot, through affecting the expression of pal, pod, ppo, promoting PAL, PPO, POD activities, and meliorating phenol metabolism. In addition, the ferulic acid and chlorogenic acid excreted by root increased significantly in +K treatment after inoculation, which reduced the identification probability between host and pathogen.
3) Potassium deficiency caused sugar accumulation in leaf, and K application stimulated sugar translocation from sink organ to source organ. Potassium application also promoted photosynthate distributed to stalk at the later growth stage of maize, and increased sugar content in stalk. At grain filling and maturity stages, the sugar content in maize stalk had negative correlation to stalk rot incidence. Potassium application also increased ss and sps expression in young root after inoculation, enhanced SS and SPS activity, and kept sucrose and glucose content steadily. In–K treatment, ss and sps expressed lower and sps expressed later than that with +K treatment. After inoculation, SPS activity decreased, but SS had little change, resulting in sucrose deficiently in roots. Both sucrose and glucose content reduced in maize root and the reduced rate of sucrose was higher than glucose, so the glucose/sucrose ratio increased significantly. Therefore, K application could increase the resistant ability to maize stalk rot, through affecting the expression of ss and sps, regulating SS and SPS activity, influencing sucrose and glucose content, and maintaining normal sugar metabolism in infected position.
4) Potassiun application helped to maintain an integrated cell structure with rectangle arrangement of stem pith. In K deficient treatment, parenchyma cells of stalk pith had abnormity structure and the cell wall between upper and lower adjacent cell was broken, resulting in the loss of connections between vascular cells and bad supporting capacity. In addition, improved K nutrition also helped in keeping a quite tight arrangement of root cell with thick cell wall, prevent the invading of pathogen effectively. Moreover, K treated root cell had abundant golgi apparatus, which could excrete large amount of secretions to degrade mycelium. Papillary and highly electronic intensity dot were accumulated in the invading point to prevent the development of the mycelium. Therefore, improved K nutrition could increase the resistant ability of maize plant to stalk rot, through keeping cell structure stability and preventing the expansion of intracellular space to reduce the chances of pathogen invasions; through accumulation of phenolic compounds to reinforce cell wall; through formation intercellular and intracellular material to restrict pathogen further development in host cell.
In conclusion, K is not only a necessary nutrient element for plant growth, but also a resistance element. On the one hand, K helped in control in the expression of plant defense genes involved in phenolic metabolism, produce antibacterial substances, keep cell structure stable, and reinforce cell wall to prevent the invasion and expansion of pathogen; on the other hand, K could also enhance the translocation of dry matter and NPK, regulate the expression the sugar metabolism related genes in invaded site, participate in the conversion of carbohydrate, and maintain sugar metabolism normally, to provide adequate energy and raw materials for defensive reaction. Consequently, K can regulate both plant secondary metabolism and primary metabolism, playing an important role in disease resistance.
1)施钾能显著降低玉米茎腐病的发病率。通过两年的试验结果分析,钾素对茎腐病的防治效果达35%-50%。玉米各生育期的根系、茎秆、叶片、叶鞘等营养体器官的钾素含量与茎腐病的发病率存在极显著的负相关。钾素能够促进玉米对干物质和氮磷钾的积累和转运,缺钾条件下,干物质和氮磷钾养分的积累速率过早下降,积累量减少,难以满足植株生育后期的需求。容易导致植株生育后期光合产物和养分供应不足,造成根系及茎秆的提前早衰,不利于植株健康生长。
2)在钾素对玉米酚代谢的影响方面,钾素不仅有利于提高玉米茎髓固有木质素的含量,而且还有利于病原菌入侵后茎髓诱导木质素和总酚含量的增加。施钾能促进接菌后茎髓和幼根中酚代谢相关酶:苯丙氨酸解氨酶(PAL)、过氧化物酶(POD)、多酚氧化酶(PPO)活性的提高,且对酶活性的峰值其及出现的时间影响最为明显。充足供钾处理中,茎髓PAL的活性在接菌3 d后达到最大值;而幼根PAL活性最大值出现于接菌后48 h。且施钾处理中PAL活性的峰值显著高于不施钾处理。从基因表达上看,在充足供钾的幼根中,受病原诱导产生的pal表达量高于不施钾处理。钾素还可以在基因水平调节pod基因的表达,缺钾导致了pod基因表达量的下降和表达时间的延迟。充足供钾,玉米茎髓和幼根受病原菌入侵后,POD活性被迅速诱导至最大。钾素还有利于接菌后茎髓和幼根PPO活性的增加。病原菌入侵幼根后,施钾处理中ppo的表达量在24 h内增加至接菌前的4倍多,显著高于不施钾处理。总之,钾素营养能从基因水平影响pal、pod、ppo基因的表达,促进受病原菌入侵后PAL、POD、PPO三种防御酶诱导活性的提高,调节植株酚代谢水平,增强玉米对茎腐病的抗性。此外,接菌后施钾处理中,根系对阿魏酸和绿原酸的分泌量显著增加,降低了病原菌与寄主的识别机率。
3)在钾素对玉米糖代谢的影响方面,缺钾导致叶片中糖的积累,而施钾有利于糖由“源”器官向“库”器官运输,促进玉米生育后期光合产物向茎秆中分配,提高茎秆中糖含量。灌浆期和成熟期时,玉米茎秆中的糖含量与茎腐病发病率呈显著负相关。受病原菌侵染后,施钾还有利于增加幼根组织ss和sps基因表达量,提高SS和SPS活性,保持蔗糖和葡萄糖含量的稳定。不施钾导致幼根ss和sps基因表达量的减少,sps基因表达时间的延迟,从酶活性的变化上看,不施钾处理中,接菌后SPS活性降低,SS活性变化不大,造成幼根蔗糖供应明显不足,玉米幼根中蔗糖和葡萄糖含量均显著降低,且蔗糖含量的下降速率高于葡萄糖含量的下降速率,葡萄糖和蔗糖比值显著增加。总之,钾素能从基因水平影响ss、sps的表达,调节受侵染部位SS和SPS的活性,影响蔗糖和葡萄糖含量,维持受侵染部位正常的糖代谢水平。
4)在钾素对玉米细胞超微结构的影响方面,缺钾处理的玉米茎髓薄壁细胞,结构不规则,长边较长,上下相邻细胞间连接壁破裂。而不缺钾处理茎髓细胞结构规则,呈长方形,整齐排列。缺钾导致维管束间的薄壁细胞破裂,致使茎髓中维管束间失去连接细胞,支撑能力变差。另外,施钾有利于寄主表皮细胞排列紧密而整齐,细胞壁增厚,有效阻碍病原菌的入侵。而且施钾处理细胞中拥有丰富的高尔基体,可以产生大量分泌物将菌丝降解。钾素还有利于菌丝入侵部位乳突的形成及高电子致密物的积累,以阻止菌丝的扩展。总之,钾素能通过稳定细胞结构,防止细胞间隙的扩大,来降低病原菌侵入的机率;通过积累酚类等化合物,加固细胞壁;通过形成位于胞间及胞内的闭塞物来限制病原物在寄主细胞的进一步发展。
综上所述,钾素不仅是植物生长所必需的营养元素,还是一种抗性元素。钾素一方面能够通过调控植物防御基因的表达,参与酚类物质的生理代谢过程,产生抑菌物质,稳定细胞结构,加固细胞壁,阻止病原菌的入侵和扩展;另一方面钾素还能促进营养物质的运输,并能通过调控受侵染部位糖代谢相关基因的表达,参与该部位糖类物质的转化,维持正常的糖代谢水平,为防御反应提供充足的能量和原料。可见,钾素可同时对植物次生代谢和初生代谢进行调节,起到抗病作用。
Stalk rot is a serious and widespread soil-borne disease in maize, which reduces both yield and quality. Moreover, recently, because the changes of cultivation practices (conservation tillage, straw returning etc) and climatic conditions, stalk rot of maize aggravated year by year in China. Using chemicals to control the disease can not control it completely, and it often cause environment pollution. It has been found that application of potassium (K) fertilizer can result in reduction of maize stalk rot. However, the mechanism of maize resistance to this disease due to K fertilizer application has not been completely understood. Both field experiment and sand-culture experiment were conducted to study the effect of maize K nutrition status on dry matter and NPK accumulation and translocation at entire growth stage of maize; the effect of K nutrition status on phenolic metabolism products ( total phenol and lignin ), the activity of related enzyme and expression of related genes of inoculated stalk pith and young root of maize; the effect of K nutrition status on carbohydrate distribution and sugar metabolism products, the activity of related enzyme and expression of related genes of inoculated young root. Scanning electron microscope and transmission electron microscope were used to observe the effect of K on the ultrastructure of maize stalk pith tissue and young root tip cell influenced by K and pathogen. The main results are summarized as follows:
1) Potassium application to maize could reduce the incidence of stalk rot significantly. According to the results from two years field experiments, the control efficiency of K to stalk rot reached to 35%-50%. The K content in vegetative organs, such as root, stalk, leaf, sheath had negative correlation with stalk rot incidence. Potassium application stimulated the accumulation, translocation and distribution of dry matter and NPK. Under K deficient condition, dry matter and NPK accumulation rate declined early, and the amount of nutrients accumulated reduced, resulting in shortage of nutrients supply at later growth stage. Therefore, early senescence occurred in roots and stems when photosynthate and nutrients were deficiency, which limited healthy growth and development of plant.
2) Potassium application not only improved the inherent lignin content, but also increased induced lignin and phenol content of stalk pith. K could enhance the activities of phenolic metabolism related enzymes (phenylalanine ammonia-lyase, PAL; peroxidase, POD; polyphenoloxidase, PPO), especially had significant influence on the peak and its appearance time of the enzyme activity. In treatment with K application (+K), the activity of PAL in stalk pith reached maximum at 3 days after inoculation; and the activity of PAL in young root reached peak at 48 h after inoculation. Moreover, the inoculated root in +K treatment had higher pal transcripts as compared with no K treatment (-K). Potassium status in maize plants could also regulate pod gene expression. After inoculation, pod gene expressed later and lower in K deficient root. POD activity of stalk pith and young root induced rapidly to the maximum in K abundant treatment. Moreover, in +K treatment, the transcripts of ppo after inoculation increased 4-folds, which was higher than in–K treatment. When inoculated, K also enhanced PPO activity in both stalk pith and young root. Therefore, K could increase the resistant ability to maize stalk rot, through affecting the expression of pal, pod, ppo, promoting PAL, PPO, POD activities, and meliorating phenol metabolism. In addition, the ferulic acid and chlorogenic acid excreted by root increased significantly in +K treatment after inoculation, which reduced the identification probability between host and pathogen.
3) Potassium deficiency caused sugar accumulation in leaf, and K application stimulated sugar translocation from sink organ to source organ. Potassium application also promoted photosynthate distributed to stalk at the later growth stage of maize, and increased sugar content in stalk. At grain filling and maturity stages, the sugar content in maize stalk had negative correlation to stalk rot incidence. Potassium application also increased ss and sps expression in young root after inoculation, enhanced SS and SPS activity, and kept sucrose and glucose content steadily. In–K treatment, ss and sps expressed lower and sps expressed later than that with +K treatment. After inoculation, SPS activity decreased, but SS had little change, resulting in sucrose deficiently in roots. Both sucrose and glucose content reduced in maize root and the reduced rate of sucrose was higher than glucose, so the glucose/sucrose ratio increased significantly. Therefore, K application could increase the resistant ability to maize stalk rot, through affecting the expression of ss and sps, regulating SS and SPS activity, influencing sucrose and glucose content, and maintaining normal sugar metabolism in infected position.
4) Potassiun application helped to maintain an integrated cell structure with rectangle arrangement of stem pith. In K deficient treatment, parenchyma cells of stalk pith had abnormity structure and the cell wall between upper and lower adjacent cell was broken, resulting in the loss of connections between vascular cells and bad supporting capacity. In addition, improved K nutrition also helped in keeping a quite tight arrangement of root cell with thick cell wall, prevent the invading of pathogen effectively. Moreover, K treated root cell had abundant golgi apparatus, which could excrete large amount of secretions to degrade mycelium. Papillary and highly electronic intensity dot were accumulated in the invading point to prevent the development of the mycelium. Therefore, improved K nutrition could increase the resistant ability of maize plant to stalk rot, through keeping cell structure stability and preventing the expansion of intracellular space to reduce the chances of pathogen invasions; through accumulation of phenolic compounds to reinforce cell wall; through formation intercellular and intracellular material to restrict pathogen further development in host cell.
In conclusion, K is not only a necessary nutrient element for plant growth, but also a resistance element. On the one hand, K helped in control in the expression of plant defense genes involved in phenolic metabolism, produce antibacterial substances, keep cell structure stable, and reinforce cell wall to prevent the invasion and expansion of pathogen; on the other hand, K could also enhance the translocation of dry matter and NPK, regulate the expression the sugar metabolism related genes in invaded site, participate in the conversion of carbohydrate, and maintain sugar metabolism normally, to provide adequate energy and raw materials for defensive reaction. Consequently, K can regulate both plant secondary metabolism and primary metabolism, playing an important role in disease resistance.
引文
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