中国红脂大小蠹伴生菌的系统发育及其生物生态学习性
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摘要
随着全球化的进程，生物入侵成为显著影响全球环境变化的重要因子之一。外来入侵物种在基因水平、物种水平和生态系统水平上对环境和社会经济造成重大影响。入侵物种也给我国的生物多样性、生态环境和社会经济造成危害。红脂大小蠹(Dendroctonus valens)作为近年来入侵我国农林业的重要有害生物之一，给北方油松林生态系统带来了巨大损失。该入侵物种在适应当地自然环境条件后表现出更强的危害性，与其一系列个体及种群的生态学习性改变有直接关系。自然界，真菌，尤其是长喙壳类真菌(ophiostomatoid fungi)与小蠹虫普遍能够形成稳定的共生关系。基于伴生真菌在影响昆虫种群建立、协同克服寄主抗性和造成寄主树木病害等方面具有显著作用，开展了本项研究，以期进一步探讨红脂大小蠹入侵的油松林大面积异常性死亡的原因，及合理的防治策略。
经过对红脂大小蠹发生的全面调查和标准样地的设置后，系统采集了红脂大小蠹危害寄主组织标本，进行了伴生真菌的分离鉴定。超过30个属多样性的真菌区系栖居在红脂大小蠹入侵危害的我国北方油松林生态系统内。对其中最主要的类群长喙壳真菌的系统研究，包括生物学、生理学、生态学和系统发育分析，明确了与红脂大小蠹伴生的长喙壳真菌区系组成。基于长喙壳真菌区系和红脂大小蠹之间的紧密伴生关系，以及长喙壳真菌的致病性测定，推测了这类真菌在油松林衰退死亡中的可能作用。
通过形态学和基于ITS2&LSU，β-tubulin基因和EF 1-α基因序列的系统发育分析，首先发现一个长喙壳真菌新种。由于该物种与Leptographium procerum形态相似、亲缘关系接近，定名该种为Leptographium sinoprocerum Lu，Decock，et Maraite sp. nov.，并给予正式描述。在MEA培养基上，该种很容易形成大量的直立分生孢子梗，孢子梗较长，着生于基质和气生菌丝上，梗基部具明显的根状分枝。产孢器官的初级分枝2—3个，无明显中央膨大分枝。大量分生孢子产于孢子梗顶端，形成黏性的分生孢子团。与现有Leptographium属内形态近似种可以从菌落特征(颜色、同心圆、气生菌丝等)、生长速度、分生孢子梗着生方式、长度、基部根状结构、产孢器官，以及菌丝壁形态等多个方面得以区分。
在红脂大小蠹伴生的长喙壳真菌区系内，还发现了Leptographium procerum，这是该种在我国的首次报道。值得指出的是该种的分生孢子梗长度可达3900μm以上，该长度在Leptographium属内十分罕见。分析推测L. procerum可能是由红脂大小蠹从北美携带进入我国，并定殖蔓延。作为一种重要的松树根部病害和引起松林衰退症的病原物，在我国的影响值得特别予以关注。
组成该长喙壳真菌区系的种类还包括Leptographium alethinum、L. koreanum、L.truncatum、Pesotum aureum和P. pini。由于L. koreanum和日本、韩国的测试菌株可以配对交配产生子囊及成熟的子囊孢子，证明其属于生物种Ophiostoma koreanum。提出新组合Grosmannia koreana comb. nov.。无论从真菌区系的优势种，还是区系的组成，长喙壳真菌都表现出与红脂大小蠹的发生危害程度明显相关。
对4种主要伴生菌的致病性测定表明，低浓度野外接种成年油松可以造成寄主不同程度的内韧皮部、形成层和木质部边材等组织的显著性坏死。4种供试真菌的致病性为两个水平，高致病力的G. koreanum、L. truncatum和低致病力的L. procerum、L. sinoprocerum。两个水平的致病力和体外培养的生长速率有明确的相关性。同时表明不同健康状况下的林分对长喙壳真菌表现出不同的感病性。
初步离体的平板对峙培养发现红脂大小蠹伴生真菌区系内，多种真菌对长喙壳真菌具有拮抗作用，能够形成拮抗带，显著抑制长喙壳真菌的生长。这种拮抗关系的发现有助于理解真菌区系的组成及其功能，同时这些菌株具备作为生物防治资源的潜力。
鉴于长喙壳真菌与红脂大小蠹的发生、危害的紧密关系，以及这些伴生菌表现出较强的致病性，结合红脂大小蠹攻击寄主行为习性的改变可能有利于增强这些伴生菌毒力的分析，与红脂大小蠹伴生的长喙壳真菌，在降低油松的抗性及其生长势上起到重要的作用。这些伴生菌协同红脂大小蠹，以及异常气候条件的诱因等多种因素的共同作用下，导致寄主死亡。
Biological invasions have been thought to be a significant component of globalenvironmental change. Invasive alien species can cause considerable irreversibleenvironmental and socio-economic impact at the genetic, species and ecosystem levels. InChina, a numerous well-know invasive forest pests have caused extensively economical, socialand ecological damage. Dendroctonus valens is a recent introduced pest in coniferous forestsof northern China. On the contrary to the situation in North America where the beetle hasexhibited as a secondary pest originally, the outbreak of this introduced beetle has beensuspected to be responsible for the death of more than 3 million P. tabuliformis trees in China.This abnormal phenomenon has been thought closely related to the changes in the beetleautecology and synecology resulting in an increase of aggressiveness.
Bark beetles infesting conifers are commonly associated with ophiostomatoid fungi,which contribute to success or failure of beetle establishment, tree disease, and/or wooddiscoloration, and thus to economical losses. The relationships between bark beetles andophiostomatoid fungi are often thought as a mutualistic symbiosis resulting in tree mortality.The association of D. valens with ophiostomatoid fungi, and their role in the decline of P.tabuliformis in northern China remained unknown, however. The present study aimed atinventorying the ophiostomatoid species associated with the D. valens attack, and to evaluatetheir possible role in tree mortality.
Fungi were recovered from and around the gallery system of D. valens attacking P.tabuliformis and P. bungeana. Over 30 genera of fungi were isolated during the sampling.Except Penicillium the ophiostomatoid fungi were isolated most frequently. In order to identifythese fungi, morphological and physiological observation, mating compatibility, multiple DNAsequences comparisons and phylogenetic analyses were conducted. The pathogenicity of someof these fungi was assessed based on inoculation on mature trees in forest stands.
Seven species of ophiostomatoid fungi were isolated from and around D. valens galleries.They are Leptographium alethinum, Grosmannia koreana comb. nov. (teleomorph of L. koreanum), L. procerum, L. sinoprocerum sp. nov., L. truncatum, Pesotum aureum and P. pini.Besides of the new species, all are recorded for the first time in China.
Leptographium sinoprocerum is a species closely related to L. procerum morphologicallyand phylogenetically. Although the phylogenetic analysis based on ITS&LSU sequence doesnot support the L. sinoprocerum clade confidentially (only one base difference from L.procerum), the phylogenetic analyses ofβ-tubulin gene and EF 1-αgene sequences, as well ascritical morphological comparisons, clearly evidence L. sinoprocerum as a new species. Thisspecies can be distinguished from resembling species in a combination of morphologicalcharacters.
As a dominant species of ophiostomatoid fungi, Leptographium procerum was also foundassociated with D. valens in P. tabuliformis ecosystem and its distribution is across the beetleoccurrence. The identity of the fungus was confused by its extra long stipe of conidiophore,reaching up to 3900μm frequently. And confusion also partly resulted from the reference DNAsequences deposited at GenBank, where the identical sequences of multiple genes are in nameof L. terebrantis, another virulent pathogen closely associated with D. valens in North America.However, the morphological characters corresponding to the species description and theidentical sequences ofβ-tubulin gene and EF 1-αgene to an authentic strain made the decisionof L. procerum recorded in China. Because the fungus has been documented commonly inassociation with D. valens in North America, it is suspected introduced to China by the meansof D. valens vector from North America. As an important pathogen of root disease andinvolving in pine decline, the introduced L. procerum is noteworthy to inspect extensively andintensively in future.
The community of ophiostomatoid fungi associated with D. valens in P. tabuliformisecosystem in northern China is positively linked to attack intensities of D. valens, whichperhaps indicates a mutualistic symbiotic relationship between the fungi and D. valens.
The pathogenicity of four ophiostomatoid fungi was tested on mature P. tabuliformis treesin low-density stem inoculation. All inoculated strains caused significant necrotic lesion ofinner bark. Grosmannia koreanum and L. truncatum were more virulent than L. procerum andL. sinoprocerum, which correlated with their growth rate differences in vitro. Meanwhile, thelower vigor of the stand is also linked to stronger pathogenicity expression of the studied fungi.
A preliminary study on the antagonism between the ophiostomatoid fungi and othermember strains of mycobiota associated with D. valens showed several strains effectivelyreduced the growth of the ophiostomatoid fungi in duel cultures. This suggests it is worth infuture to explore the interaction among fungal communities and potential biological controlagency to D. valens and its associated fungi.
In conclusion, drier climatic events during late 90ies in northern China might have placedP. tabuliforrnis under stress and predisposed them to attack by the RTB. The subsequentdevelopment of ophiostomatoid fungi could have contributed further to decrease the resistancecapacity of the stressed P. tabuliformis to both D. valens and soil humidity level. Thealternation of attack pattern to extensive root system in China was thought as favoring thebeetle's population establishment and its aggressiveness. Because this change could also bebeneficial to increasing the pathogens' virulence, such as L. procerurn, these ophiostomatoidfungi might play more important roles in the pine mortality in northern China.
经过对红脂大小蠹发生的全面调查和标准样地的设置后，系统采集了红脂大小蠹危害寄主组织标本，进行了伴生真菌的分离鉴定。超过30个属多样性的真菌区系栖居在红脂大小蠹入侵危害的我国北方油松林生态系统内。对其中最主要的类群长喙壳真菌的系统研究，包括生物学、生理学、生态学和系统发育分析，明确了与红脂大小蠹伴生的长喙壳真菌区系组成。基于长喙壳真菌区系和红脂大小蠹之间的紧密伴生关系，以及长喙壳真菌的致病性测定，推测了这类真菌在油松林衰退死亡中的可能作用。
通过形态学和基于ITS2&LSU，β-tubulin基因和EF 1-α基因序列的系统发育分析，首先发现一个长喙壳真菌新种。由于该物种与Leptographium procerum形态相似、亲缘关系接近，定名该种为Leptographium sinoprocerum Lu，Decock，et Maraite sp. nov.，并给予正式描述。在MEA培养基上，该种很容易形成大量的直立分生孢子梗，孢子梗较长，着生于基质和气生菌丝上，梗基部具明显的根状分枝。产孢器官的初级分枝2—3个，无明显中央膨大分枝。大量分生孢子产于孢子梗顶端，形成黏性的分生孢子团。与现有Leptographium属内形态近似种可以从菌落特征(颜色、同心圆、气生菌丝等)、生长速度、分生孢子梗着生方式、长度、基部根状结构、产孢器官，以及菌丝壁形态等多个方面得以区分。
在红脂大小蠹伴生的长喙壳真菌区系内，还发现了Leptographium procerum，这是该种在我国的首次报道。值得指出的是该种的分生孢子梗长度可达3900μm以上，该长度在Leptographium属内十分罕见。分析推测L. procerum可能是由红脂大小蠹从北美携带进入我国，并定殖蔓延。作为一种重要的松树根部病害和引起松林衰退症的病原物，在我国的影响值得特别予以关注。
组成该长喙壳真菌区系的种类还包括Leptographium alethinum、L. koreanum、L.truncatum、Pesotum aureum和P. pini。由于L. koreanum和日本、韩国的测试菌株可以配对交配产生子囊及成熟的子囊孢子，证明其属于生物种Ophiostoma koreanum。提出新组合Grosmannia koreana comb. nov.。无论从真菌区系的优势种，还是区系的组成，长喙壳真菌都表现出与红脂大小蠹的发生危害程度明显相关。
对4种主要伴生菌的致病性测定表明，低浓度野外接种成年油松可以造成寄主不同程度的内韧皮部、形成层和木质部边材等组织的显著性坏死。4种供试真菌的致病性为两个水平，高致病力的G. koreanum、L. truncatum和低致病力的L. procerum、L. sinoprocerum。两个水平的致病力和体外培养的生长速率有明确的相关性。同时表明不同健康状况下的林分对长喙壳真菌表现出不同的感病性。
初步离体的平板对峙培养发现红脂大小蠹伴生真菌区系内，多种真菌对长喙壳真菌具有拮抗作用，能够形成拮抗带，显著抑制长喙壳真菌的生长。这种拮抗关系的发现有助于理解真菌区系的组成及其功能，同时这些菌株具备作为生物防治资源的潜力。
鉴于长喙壳真菌与红脂大小蠹的发生、危害的紧密关系，以及这些伴生菌表现出较强的致病性，结合红脂大小蠹攻击寄主行为习性的改变可能有利于增强这些伴生菌毒力的分析，与红脂大小蠹伴生的长喙壳真菌，在降低油松的抗性及其生长势上起到重要的作用。这些伴生菌协同红脂大小蠹，以及异常气候条件的诱因等多种因素的共同作用下，导致寄主死亡。
Biological invasions have been thought to be a significant component of globalenvironmental change. Invasive alien species can cause considerable irreversibleenvironmental and socio-economic impact at the genetic, species and ecosystem levels. InChina, a numerous well-know invasive forest pests have caused extensively economical, socialand ecological damage. Dendroctonus valens is a recent introduced pest in coniferous forestsof northern China. On the contrary to the situation in North America where the beetle hasexhibited as a secondary pest originally, the outbreak of this introduced beetle has beensuspected to be responsible for the death of more than 3 million P. tabuliformis trees in China.This abnormal phenomenon has been thought closely related to the changes in the beetleautecology and synecology resulting in an increase of aggressiveness.
Bark beetles infesting conifers are commonly associated with ophiostomatoid fungi,which contribute to success or failure of beetle establishment, tree disease, and/or wooddiscoloration, and thus to economical losses. The relationships between bark beetles andophiostomatoid fungi are often thought as a mutualistic symbiosis resulting in tree mortality.The association of D. valens with ophiostomatoid fungi, and their role in the decline of P.tabuliformis in northern China remained unknown, however. The present study aimed atinventorying the ophiostomatoid species associated with the D. valens attack, and to evaluatetheir possible role in tree mortality.
Fungi were recovered from and around the gallery system of D. valens attacking P.tabuliformis and P. bungeana. Over 30 genera of fungi were isolated during the sampling.Except Penicillium the ophiostomatoid fungi were isolated most frequently. In order to identifythese fungi, morphological and physiological observation, mating compatibility, multiple DNAsequences comparisons and phylogenetic analyses were conducted. The pathogenicity of someof these fungi was assessed based on inoculation on mature trees in forest stands.
Seven species of ophiostomatoid fungi were isolated from and around D. valens galleries.They are Leptographium alethinum, Grosmannia koreana comb. nov. (teleomorph of L. koreanum), L. procerum, L. sinoprocerum sp. nov., L. truncatum, Pesotum aureum and P. pini.Besides of the new species, all are recorded for the first time in China.
Leptographium sinoprocerum is a species closely related to L. procerum morphologicallyand phylogenetically. Although the phylogenetic analysis based on ITS&LSU sequence doesnot support the L. sinoprocerum clade confidentially (only one base difference from L.procerum), the phylogenetic analyses ofβ-tubulin gene and EF 1-αgene sequences, as well ascritical morphological comparisons, clearly evidence L. sinoprocerum as a new species. Thisspecies can be distinguished from resembling species in a combination of morphologicalcharacters.
As a dominant species of ophiostomatoid fungi, Leptographium procerum was also foundassociated with D. valens in P. tabuliformis ecosystem and its distribution is across the beetleoccurrence. The identity of the fungus was confused by its extra long stipe of conidiophore,reaching up to 3900μm frequently. And confusion also partly resulted from the reference DNAsequences deposited at GenBank, where the identical sequences of multiple genes are in nameof L. terebrantis, another virulent pathogen closely associated with D. valens in North America.However, the morphological characters corresponding to the species description and theidentical sequences ofβ-tubulin gene and EF 1-αgene to an authentic strain made the decisionof L. procerum recorded in China. Because the fungus has been documented commonly inassociation with D. valens in North America, it is suspected introduced to China by the meansof D. valens vector from North America. As an important pathogen of root disease andinvolving in pine decline, the introduced L. procerum is noteworthy to inspect extensively andintensively in future.
The community of ophiostomatoid fungi associated with D. valens in P. tabuliformisecosystem in northern China is positively linked to attack intensities of D. valens, whichperhaps indicates a mutualistic symbiotic relationship between the fungi and D. valens.
The pathogenicity of four ophiostomatoid fungi was tested on mature P. tabuliformis treesin low-density stem inoculation. All inoculated strains caused significant necrotic lesion ofinner bark. Grosmannia koreanum and L. truncatum were more virulent than L. procerum andL. sinoprocerum, which correlated with their growth rate differences in vitro. Meanwhile, thelower vigor of the stand is also linked to stronger pathogenicity expression of the studied fungi.
A preliminary study on the antagonism between the ophiostomatoid fungi and othermember strains of mycobiota associated with D. valens showed several strains effectivelyreduced the growth of the ophiostomatoid fungi in duel cultures. This suggests it is worth infuture to explore the interaction among fungal communities and potential biological controlagency to D. valens and its associated fungi.
In conclusion, drier climatic events during late 90ies in northern China might have placedP. tabuliforrnis under stress and predisposed them to attack by the RTB. The subsequentdevelopment of ophiostomatoid fungi could have contributed further to decrease the resistancecapacity of the stressed P. tabuliformis to both D. valens and soil humidity level. Thealternation of attack pattern to extensive root system in China was thought as favoring thebeetle's population establishment and its aggressiveness. Because this change could also bebeneficial to increasing the pathogens' virulence, such as L. procerurn, these ophiostomatoidfungi might play more important roles in the pine mortality in northern China.
引文
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