提高罗伦隐球酵母拮抗效力的途径及其机理的研究
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摘要
果实采后真菌性病害造成了巨大的经济损失。利用具有拮抗活性的酵母菌种开展生物防治是最有希望替代化学杀菌剂的方法之一。罗伦隐球酵母(Cryptococcus laurentii)是国内外研究较多的采后拮抗酵母。但目前拮抗酵母对采后果实病害的防治效力与化学杀菌剂相比仍有较大的差距。如何提高拮抗酵母的生物学活性，及如何通过与其他非杀菌剂方法的有效整合来提高其对采后果实病害的控制水平，是影响拮抗酵母商业化和推广应用的关键性因素。本论文主要从以下几个角度出发探讨提高罗伦隐球酵母控制效力的可行性及其机理：1)与激发果实采后抗性方法结合；2)与延缓果实采后衰老的方法结合；3)与壳聚糖等具有抑菌性能的天然物质结合；4)通过几丁质等诱导物激发罗伦隐球酵母的拮抗效力。并在以上研究的基础上，进一步开展对苹果、梨、葡萄、水蜜桃、油桃、番茄、柿子和柑橘等果实生物防腐保鲜技术的研究。
试验结果表明：
1、水杨酸(SA)、细胞分裂素(6-BA)、吲哚-3-乙酸(IAA)、赤霉酸(GA_3)、CaCl_2等激发子在合适的浓度下能显著增强C.laurentii对苹果和梨果实主要真菌病害的控制效力。这些激发子除较高浓度(500～2000μg／ml)6-BA外，一般不具有直接抑菌性能；但能通过诱导果实抗性或／和延缓果实组织衰老在C.laurentii拮抗活力的基础上促进对真菌病害的控制。此外，以上部分激发子和茉莉酸还能不同程度的提高C.laurentii对桃扩展青霉、柿子柿盘多毛孢和柑橘指状青霉的控制水平。
2、壳聚糖具有直接抑制扩展青霉在果实伤口侵染的效力，但其效力随着病原菌接种后时间的延长而显著下降。0.1％或0.5％壳聚糖能显著提高C.laurentii对苹果或梨青霉病的控制效力，且壳聚糖粘度越低，效果越好；而且添加CaCl_2能进一步提高壳聚糖和C.laurentii组合对梨果实青霉病的控制。此外，壳聚糖还能显著提高C.laurentii对桃青霉病和软腐病、对樱桃番茄自然腐烂的控制。
3、通过正交试验表明，以0.2％壳聚糖、1％CaCl_2和20μg／ml SA作为复合佐剂能进一步提高C.laurentii对苹果和梨的青霉病、梨软腐病的控制，其效力与化学杀菌剂接近或基本相当。
4、C.laurentii对葡萄果实灰霉病有一定的抑制作用，但其效力尚不能达到商业化的水平。热处理、壳聚糖、CaCl_2、碳酸氢钠等能不同程度的提高C.laurentii对葡萄病害的生物防治效力。而15％乙醇、1％CaCl_2和0.2％壳聚糖的复合处理能有效控制葡萄果实病害的发生和发展，其效果与SO_2的效力相当。
5、通过几丁质或壳聚糖诱导培养显著提高C.laurentii对扩展青霉的拮抗效力，其机理可能与诱导培养后，能促进C.laurentii在果实伤口处的生长、刺激酵母几丁质酶分泌和增强酵母对果实抗性的诱导等有关。并通过ProteomeLab~(TM) PF-2D目标蛋白快速分离系统对酵母蛋白进行了分离和比较研究。
综上所述，通过激发果实采后抗性、延缓果实采后衰老、与壳聚糖等具有抑菌性能的天然物质结合等方法能有效提高C.laurentii对多种果实主要真菌性病害的控制效力，其中部分方法已接近或达到化学杀菌剂的效力；通过几丁质或壳聚糖诱导培养，也能显著提升C.laurentii的生物学活性。以上研究结果将为进一步提高C.laurentii效力提供新的途径。
Postharvest fungal diseases cause substantial economic losses world-widely. In view of the fungicidetoxicity on the environment and human health, and the development of fungicide resistance bypathogens, great efforts have been made to exploit alternatives to the synthetic fungicides. Thebiological control by using antagonistic yeasts has been considered to be one of the most promisingnon-fungicidal methods. Strains of Cryptococcus laurentii are well known as postharvest biocontrolyeasts, which have been shown to have high antagonistic activity in various fruit. Unfortunately, atpresent, the effectiveness and stability of yeast antagonists have not been reached an adequate controllevel when compared with the synthetic fungicides. Therefore, the objective of this research was toexplore the potential utilization of such ways as delaying harvested fruit senescence, inducing harvestedfruit resistance, using natural bioactive substance or stimulating yeast physiology for improving theefficacy ofC. laurentii in inhibiting the postharvest fungal diseases in harvested fruit.
The main research findings were summarized as follows:
1. Salicylic acid (SA) had little direct antifungal activity against Penicillium expansum and Botrytiscinerea in vivo. However, SA at 10μ/ml or 100μg/ml could enhance the efficacy of C. laurentii inreducing the blue and gray mold rots in apple or pear fruit, which might be supposed to be related to thefruit natural resistance induced by SA. Moreover, the application of SA at 10μg/ml or together with C.laurentii resulted in inhibition of the ethylene production but in promotion of the activities ofsuperoxide dismutase, catalase, peroxidase, phenylalanine amonialyase, polyphenol oxidase andlipoxygenase of apple fruit. On the other hand, treatment of pear fruit with SA at 100μg/ml was alsofound to elicit the fruit peroxidase activity. Anyway, SA at 10μg/ml or 100μg/ml had no influence onthe growth of C. laurentii in apple or pear fruit wounds.
2. Cytokinin (N~6-benzyladenine, 6-BA) at 500 to 2000μg/ml was effective in inhibiting the P.expansum infections in apple or pear fruit wounds, but its efficacy was declining rapidly with theincubation time. Integrated application of C. laurentii and 6-BA at 20μg/ml or 1000μg/ml broughtabout a more effective inhibition of the blue and gray mold rots in apple or pear fruit wounds than thatof the 6-BA or C. laurentii alone. Moreover, 6-BA at 20μg/ml or together with C. laurentii stimulatedthe superoxide dismutase activity but it inhibited the increase of the peroxidase activity of apple fruit.On the other hand, treatments of pears with 6-BA at 1000μg/ml or with C. laurentii led to an increasein the catalase activity but in an inhibition of the activities of both peroxidase and lipoxygenase as well as the ethylene production. Similarily, 6-BA from 20 to 2000μg/ml did not affect the population growthof C. laurentii in apple or pear fruit wounds.
3. Auxins including indole-3-acetic acid (IAA), indole-3-buyric acid (IBA) and2, 4-dichlorophenoxyacetic acid (2, 4-D) were shown to have little direct antifungal activity against P.expansum and B. cinerea in vivo. However, IAA at 20μg/ml or 100μg/ml augmented the efficacy of C.laurentii in reducing the blue and gray mold rots in apple or pear fruit. Moreover, it was found that IAAcould induce the apple and pear fruit resistance to molds infection, which was dependent on the IAAconcentration, the time interval between the IAA treatment and fungal pathogens inoculation, thepathogen inoculum concentration and the incubation time. In the apple wounds, IAA at the optimalconcentration (20μg/ml) and the optimal time interval (24 h) significantly inhibited the sporegermination of P. expansum and the initial mold infections, however, its efficacy was decreasing withthe increase of both of the pathogen inoculum concentration and the incubation time. The results fromthe present paper also revealed that IAA at 20μg/ml alone or together with C. laurentii could stimulatethe superoxide dismutase, catalase, peroxidase activities, whereas it inhibited the lipoxygenase activityof apple fruit. Just the same, IAA at 100μg/ml or together with C. laurentii also motivated the catalase,peroxidase and polyphenol oxidase activities of pear fruit. In addition, IAA at 20μg/ml or lower wasnot found to have any influence on the population growth of C. laurentii in fruit wounds but IAA wasshown to have toxic effect on C. laurenn'i when its concentration was increased to 200μg/ml or abovein vitro and in vivo.
4. A combination of C. laurentii and gibberellic acid (GA_3) at 200μg/ml or 2000μg/ml produced amore effective control of blue and gray mold rots in apple or pear wounds than C. laurentii alone,although GA_3 was not found to have toxic effect on P. expansum and B. cinerea as well as C. laurentiiin vivo. Moreover, it was shown that GA_3 at 2000μg/ml induced the pear fruit resistance to P.expansum infections, which was associated with the increased peroxidase and polyphenol oxidaseactivities and with the inhibition of the lipoxygenase activity and lipid peroxidation. On the other hand,in apple fruit, GA_3 at 200μg/ml alone or with C. laurentii enhanced the activities of both superoxidedismutase and catalase but inhibited the increase in peroxidase activity.
5. Application of CaCl_2 made C. laurentii more effective in delaying the blue and gray mold rots inpear fruit. Although CaCl_2 had little antifungal activity against P. expansum or B. cinerea as well as C.laurentii in vivo, it induced the fruit resistance to P. expansum in pear wounds and activated theperoxidase activity of pear fruit.
6. Furthermore, the results from the present research showed that a combination of 0.2％chitosan and 1％CaCl_2 and 20μg/ml SA was a most effective approach to improvement of the effectiveness andstability of C. laurentii against P. expansum and Rhizopus stolonifer in apple or pear fruit. Our resultsalso showed that jasmonic acid at 10μg/ml, IAA at 10μg/ml or GA_3 at100μg/ml could enhance theefficacy of C. laurentii against P. expansum infection in peach fruit. Application of CaCl_2 at 2％, SA at20μg/ml, GA_3 at 100μg/ml also enhanced the efficacy of C. laurentii against the fungus Pestalotiadiospyri infection in persimmon fruit.
7. Chitosan had the strength to inhibit the blue mold rot in apple or pear wounds, and its efficacywas shown to increase with the increase in its concentration and with the decrease in its viscosity, andalways declined with the incubation time. Combination of chitosan and C. laurentii exhibited asynergistic effect on the blue mold rot, which was the most effective at the optimal concentration ofchitosan at 0.1％or 0.5％in apple or pear fruit. Furthermore, an addition of CaCl_2 (1～2％) to thesuspension of C. laurentii with chitosan (0.5％) could further reduce the blue mold rot of pear fruit andthe blue and soft mold rots of peach or nectarine fruit. In addition, application of chitosan at 0.2％induced tomato fruit resistance to the fungus Alternaria alternate, and a combination of 0.2％chitosanand C. laurentii resulted in a synergistic inhibitive effect on the natural decay of tomato fruit.
8. In grape fruit, application of C. laurentii, heat treatment, chitosan or ethanol alone was shown tobe effective in reducing the decay of grape fruit. And heat treatment, chitosan, or calcium chloride couldimprove the efficacy of C. laurentii against B. cinerea infection. Moreover important, it was found thata most effective means of controlling the decay of grape was by using a combination of 15～30％ethanol,0.2％chitosan and 1～2％calcium chloride, which efficacy was shown to be equal to that of SO_2.
9. The physiology manipulation of biocontrol yeasts may also be a useful method of enhancingthe efficacy of postharvest biocontrol yeasts. The results from this research showed that application ofchitin or chitosan could induce C. laurentii antagonistic activity to P expansum infection in apple, pearor peach fruit after cultivation of the yeast in a liquid media amended with chitin at 1.0％or chitosan at0.002％, which might be related to enhancement of the population growth of C. laurentii in fruit wounds,stimulation of the chitinase activity and augment action of the capacity of inducing fruit naturalresistance after cultivation by chitin or chitosan. The proteomic analysis and comparison of C. laurentiiin response to chitin was analyzed based on two-dimensional liquid chromatography (ProteomeLabTMPF-2D).
In conclusion, the results from the present paper showed that the biocontrol efficacy of C.laurentii could be improved by use of the methods of elicit of fruit resistance, retard of fruit senescenceor by chitosan, and combination of these approaches above and other non-fungicidal methods, such asheat treatment, sodium bicarbonate and ethanol could effectively control postharvest fungal diseases of various fruit. Moreover, the efficacy of C laurentii could be augmented by cultivation of chitin-orchitosan-amended liquid media, which might provided a novel strategy for enhancement of thebiological activity of C. laurentii against postharvest fungai pathogens.
试验结果表明：
1、水杨酸(SA)、细胞分裂素(6-BA)、吲哚-3-乙酸(IAA)、赤霉酸(GA_3)、CaCl_2等激发子在合适的浓度下能显著增强C.laurentii对苹果和梨果实主要真菌病害的控制效力。这些激发子除较高浓度(500～2000μg／ml)6-BA外，一般不具有直接抑菌性能；但能通过诱导果实抗性或／和延缓果实组织衰老在C.laurentii拮抗活力的基础上促进对真菌病害的控制。此外，以上部分激发子和茉莉酸还能不同程度的提高C.laurentii对桃扩展青霉、柿子柿盘多毛孢和柑橘指状青霉的控制水平。
2、壳聚糖具有直接抑制扩展青霉在果实伤口侵染的效力，但其效力随着病原菌接种后时间的延长而显著下降。0.1％或0.5％壳聚糖能显著提高C.laurentii对苹果或梨青霉病的控制效力，且壳聚糖粘度越低，效果越好；而且添加CaCl_2能进一步提高壳聚糖和C.laurentii组合对梨果实青霉病的控制。此外，壳聚糖还能显著提高C.laurentii对桃青霉病和软腐病、对樱桃番茄自然腐烂的控制。
3、通过正交试验表明，以0.2％壳聚糖、1％CaCl_2和20μg／ml SA作为复合佐剂能进一步提高C.laurentii对苹果和梨的青霉病、梨软腐病的控制，其效力与化学杀菌剂接近或基本相当。
4、C.laurentii对葡萄果实灰霉病有一定的抑制作用，但其效力尚不能达到商业化的水平。热处理、壳聚糖、CaCl_2、碳酸氢钠等能不同程度的提高C.laurentii对葡萄病害的生物防治效力。而15％乙醇、1％CaCl_2和0.2％壳聚糖的复合处理能有效控制葡萄果实病害的发生和发展，其效果与SO_2的效力相当。
5、通过几丁质或壳聚糖诱导培养显著提高C.laurentii对扩展青霉的拮抗效力，其机理可能与诱导培养后，能促进C.laurentii在果实伤口处的生长、刺激酵母几丁质酶分泌和增强酵母对果实抗性的诱导等有关。并通过ProteomeLab~(TM) PF-2D目标蛋白快速分离系统对酵母蛋白进行了分离和比较研究。
综上所述，通过激发果实采后抗性、延缓果实采后衰老、与壳聚糖等具有抑菌性能的天然物质结合等方法能有效提高C.laurentii对多种果实主要真菌性病害的控制效力，其中部分方法已接近或达到化学杀菌剂的效力；通过几丁质或壳聚糖诱导培养，也能显著提升C.laurentii的生物学活性。以上研究结果将为进一步提高C.laurentii效力提供新的途径。
Postharvest fungal diseases cause substantial economic losses world-widely. In view of the fungicidetoxicity on the environment and human health, and the development of fungicide resistance bypathogens, great efforts have been made to exploit alternatives to the synthetic fungicides. Thebiological control by using antagonistic yeasts has been considered to be one of the most promisingnon-fungicidal methods. Strains of Cryptococcus laurentii are well known as postharvest biocontrolyeasts, which have been shown to have high antagonistic activity in various fruit. Unfortunately, atpresent, the effectiveness and stability of yeast antagonists have not been reached an adequate controllevel when compared with the synthetic fungicides. Therefore, the objective of this research was toexplore the potential utilization of such ways as delaying harvested fruit senescence, inducing harvestedfruit resistance, using natural bioactive substance or stimulating yeast physiology for improving theefficacy ofC. laurentii in inhibiting the postharvest fungal diseases in harvested fruit.
The main research findings were summarized as follows:
1. Salicylic acid (SA) had little direct antifungal activity against Penicillium expansum and Botrytiscinerea in vivo. However, SA at 10μ/ml or 100μg/ml could enhance the efficacy of C. laurentii inreducing the blue and gray mold rots in apple or pear fruit, which might be supposed to be related to thefruit natural resistance induced by SA. Moreover, the application of SA at 10μg/ml or together with C.laurentii resulted in inhibition of the ethylene production but in promotion of the activities ofsuperoxide dismutase, catalase, peroxidase, phenylalanine amonialyase, polyphenol oxidase andlipoxygenase of apple fruit. On the other hand, treatment of pear fruit with SA at 100μg/ml was alsofound to elicit the fruit peroxidase activity. Anyway, SA at 10μg/ml or 100μg/ml had no influence onthe growth of C. laurentii in apple or pear fruit wounds.
2. Cytokinin (N~6-benzyladenine, 6-BA) at 500 to 2000μg/ml was effective in inhibiting the P.expansum infections in apple or pear fruit wounds, but its efficacy was declining rapidly with theincubation time. Integrated application of C. laurentii and 6-BA at 20μg/ml or 1000μg/ml broughtabout a more effective inhibition of the blue and gray mold rots in apple or pear fruit wounds than thatof the 6-BA or C. laurentii alone. Moreover, 6-BA at 20μg/ml or together with C. laurentii stimulatedthe superoxide dismutase activity but it inhibited the increase of the peroxidase activity of apple fruit.On the other hand, treatments of pears with 6-BA at 1000μg/ml or with C. laurentii led to an increasein the catalase activity but in an inhibition of the activities of both peroxidase and lipoxygenase as well as the ethylene production. Similarily, 6-BA from 20 to 2000μg/ml did not affect the population growthof C. laurentii in apple or pear fruit wounds.
3. Auxins including indole-3-acetic acid (IAA), indole-3-buyric acid (IBA) and2, 4-dichlorophenoxyacetic acid (2, 4-D) were shown to have little direct antifungal activity against P.expansum and B. cinerea in vivo. However, IAA at 20μg/ml or 100μg/ml augmented the efficacy of C.laurentii in reducing the blue and gray mold rots in apple or pear fruit. Moreover, it was found that IAAcould induce the apple and pear fruit resistance to molds infection, which was dependent on the IAAconcentration, the time interval between the IAA treatment and fungal pathogens inoculation, thepathogen inoculum concentration and the incubation time. In the apple wounds, IAA at the optimalconcentration (20μg/ml) and the optimal time interval (24 h) significantly inhibited the sporegermination of P. expansum and the initial mold infections, however, its efficacy was decreasing withthe increase of both of the pathogen inoculum concentration and the incubation time. The results fromthe present paper also revealed that IAA at 20μg/ml alone or together with C. laurentii could stimulatethe superoxide dismutase, catalase, peroxidase activities, whereas it inhibited the lipoxygenase activityof apple fruit. Just the same, IAA at 100μg/ml or together with C. laurentii also motivated the catalase,peroxidase and polyphenol oxidase activities of pear fruit. In addition, IAA at 20μg/ml or lower wasnot found to have any influence on the population growth of C. laurentii in fruit wounds but IAA wasshown to have toxic effect on C. laurenn'i when its concentration was increased to 200μg/ml or abovein vitro and in vivo.
4. A combination of C. laurentii and gibberellic acid (GA_3) at 200μg/ml or 2000μg/ml produced amore effective control of blue and gray mold rots in apple or pear wounds than C. laurentii alone,although GA_3 was not found to have toxic effect on P. expansum and B. cinerea as well as C. laurentiiin vivo. Moreover, it was shown that GA_3 at 2000μg/ml induced the pear fruit resistance to P.expansum infections, which was associated with the increased peroxidase and polyphenol oxidaseactivities and with the inhibition of the lipoxygenase activity and lipid peroxidation. On the other hand,in apple fruit, GA_3 at 200μg/ml alone or with C. laurentii enhanced the activities of both superoxidedismutase and catalase but inhibited the increase in peroxidase activity.
5. Application of CaCl_2 made C. laurentii more effective in delaying the blue and gray mold rots inpear fruit. Although CaCl_2 had little antifungal activity against P. expansum or B. cinerea as well as C.laurentii in vivo, it induced the fruit resistance to P. expansum in pear wounds and activated theperoxidase activity of pear fruit.
6. Furthermore, the results from the present research showed that a combination of 0.2％chitosan and 1％CaCl_2 and 20μg/ml SA was a most effective approach to improvement of the effectiveness andstability of C. laurentii against P. expansum and Rhizopus stolonifer in apple or pear fruit. Our resultsalso showed that jasmonic acid at 10μg/ml, IAA at 10μg/ml or GA_3 at100μg/ml could enhance theefficacy of C. laurentii against P. expansum infection in peach fruit. Application of CaCl_2 at 2％, SA at20μg/ml, GA_3 at 100μg/ml also enhanced the efficacy of C. laurentii against the fungus Pestalotiadiospyri infection in persimmon fruit.
7. Chitosan had the strength to inhibit the blue mold rot in apple or pear wounds, and its efficacywas shown to increase with the increase in its concentration and with the decrease in its viscosity, andalways declined with the incubation time. Combination of chitosan and C. laurentii exhibited asynergistic effect on the blue mold rot, which was the most effective at the optimal concentration ofchitosan at 0.1％or 0.5％in apple or pear fruit. Furthermore, an addition of CaCl_2 (1～2％) to thesuspension of C. laurentii with chitosan (0.5％) could further reduce the blue mold rot of pear fruit andthe blue and soft mold rots of peach or nectarine fruit. In addition, application of chitosan at 0.2％induced tomato fruit resistance to the fungus Alternaria alternate, and a combination of 0.2％chitosanand C. laurentii resulted in a synergistic inhibitive effect on the natural decay of tomato fruit.
8. In grape fruit, application of C. laurentii, heat treatment, chitosan or ethanol alone was shown tobe effective in reducing the decay of grape fruit. And heat treatment, chitosan, or calcium chloride couldimprove the efficacy of C. laurentii against B. cinerea infection. Moreover important, it was found thata most effective means of controlling the decay of grape was by using a combination of 15～30％ethanol,0.2％chitosan and 1～2％calcium chloride, which efficacy was shown to be equal to that of SO_2.
9. The physiology manipulation of biocontrol yeasts may also be a useful method of enhancingthe efficacy of postharvest biocontrol yeasts. The results from this research showed that application ofchitin or chitosan could induce C. laurentii antagonistic activity to P expansum infection in apple, pearor peach fruit after cultivation of the yeast in a liquid media amended with chitin at 1.0％or chitosan at0.002％, which might be related to enhancement of the population growth of C. laurentii in fruit wounds,stimulation of the chitinase activity and augment action of the capacity of inducing fruit naturalresistance after cultivation by chitin or chitosan. The proteomic analysis and comparison of C. laurentiiin response to chitin was analyzed based on two-dimensional liquid chromatography (ProteomeLabTMPF-2D).
In conclusion, the results from the present paper showed that the biocontrol efficacy of C.laurentii could be improved by use of the methods of elicit of fruit resistance, retard of fruit senescenceor by chitosan, and combination of these approaches above and other non-fungicidal methods, such asheat treatment, sodium bicarbonate and ethanol could effectively control postharvest fungal diseases of various fruit. Moreover, the efficacy of C laurentii could be augmented by cultivation of chitin-orchitosan-amended liquid media, which might provided a novel strategy for enhancement of thebiological activity of C. laurentii against postharvest fungai pathogens.
引文
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