Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci.

Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci.
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DOI:
10.1371/journal.pgen.1003323
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发表时间:
2013
期刊:
影响因子:
4.5
通讯作者:
Zeng Z
Zeng Z
中科院分区:
生物学2区
文献类型:
--
作者:
Schardl CL;Young CA;Hesse U;Amyotte SG;Andreeva K;Calie PJ;Fleetwood DJ;Haws DC;Moore N;Oeser B;Panaccione DG;Schweri KK;Voisey CR;Farman ML;Jaromczyk JW;Roe BA;O'Sullivan DM;Scott B;Tudzynski P;An Z;Arnaoudova EG;Bullock CT;Charlton ND;Chen L;Cox M;Dinkins RD;Florea S;Glenn AE;Gordon A;Güldener U;Harris DR;Hollin W;Jaromczyk J;Johnson RD;Khan AK;Leistner E;Leuchtmann A;Li C;Liu J;Liu J;Liu M;Mace W;Machado C;Nagabhyru P;Pan J;Schmid J;Sugawara K;Steiner U;Takach JE;Tanaka E;Webb JS;Wilson EV;Wiseman JL;Yoshida R;Zeng Z

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真菌科包括植物共生体和寄生虫,它们能产生几种具有精神活性和生物保护作用的生物碱。该科包括表土支系(Eichloë和Neotyphdium种)中的草共生体,它们在寄主相互作用和生物碱组成上都非常不同。表皮藻产生四种不同类别的生物碱,所有这些生物碱都能阻止昆虫,其中一些--包括臭名昭著的麦角生物碱--对哺乳动物有很强的影响。上胚层的特殊化学类型多样性可能与它们广泛的寄主相互作用有关,其中一些是致病和传染性的,另一些是互惠和垂直传播的(种子传播),还有一些在致病或互惠行为上有所不同。我们对10种麦角菌、3种麦角菌(Clavicep种)、1种牵牛花共生体(Periglandula Ipomoeae)和1种竹子病原菌(针孢菌属)的生物碱进行了分析和测序,并比较了4类生物碱的基因簇。结果表明,生物碱基因座有一种强烈的趋势,即具有保守的核心,这些核心指定骨架结构和外围基因,这些基因决定了已知影响其药理特异性的化学变异。一般来说,基因在簇周的位置将它们定位在转座子衍生的富含AT的重复区块附近,这可能与基因丢失、复制和新的功能有关。上胚层中的生物碱位点具有不寻常的结构,充满了大的、复杂的和动态的重复块。这一特征并不反映基因组中重复内容的总体差异,也不是大多数其他专门化代谢基因座的特征。生物碱位点的组织和动态以及表土中丰富的重复区块表明,这些真菌是生物碱多样化的选择对象。我们认为,这种选择与表土动物多变的生活史,它们作为共生体的保护作用,以及它们与高度特殊和生态多样性的冷季草的联系有关。真菌科包括寄生在谷类作物穗部并在历史上造成大规模中毒的“麦角”真菌,以及“外生菌”,这是草类的共生体。许多上胚层是互惠共生体,但有些是致病的,另一些兼具互惠和致病的特性。大多数Clavempitaceae会产生“生物碱”,这是一种小分子物质,可以阻止昆虫、牲畜和野生动物以真菌或植物为食。表观生物碱对寄主具有保护作用,它们分别属于四个化学类别。在对10个表土真菌、3个麦角真菌和2个近缘真菌的全部DNA内容(基因组)进行测序后,我们比较了它们的生物碱生物合成基因簇。在上胚层中,这些簇包含非常大的高度重复的DNA块,这些DNA促进了基因丢失、突变,甚至新基因的进化。这些重复区块解释了表土中异常高的生物碱多样性,并可能与这些共生真菌的生态多样性有关。
The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some—including the infamous ergot alkaloids—have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses. The fungal family, Clavicipitaceae, includes “ergot” fungi that parasitize ears of cereals and have historically caused mass poisonings, as well as “epichloae,” which are symbionts of grasses. Many epichloae are mutualistic symbionts, but some are pathogenic, and others have both mutualistic and pathogenic characteristics. Most Clavicipitaceae produce “alkaloids,” small molecules that deter insects, livestock, and wildlife from feeding on the fungus or plant. Epichloae protect their hosts with diverse alkaloids belonging to four chemical classes. After sequencing the entire DNA contents (“genomes”) of ten epichloae, three ergot fungi, and two relatives, we compared their “clusters” of genes for alkaloid biosynthesis. In the epichloae, these clusters contained extraordinarily large blocks of highly repetitive DNA, which promote gene losses, mutations, and even the evolution of new genes. These repeat blocks account for the exceptionally high alkaloid diversity in the epichloae and may relate to the ecological diversity of these symbiotic fungi.
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