Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming

Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming
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DOI:
10.3389/fpls.2011.00039
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发表时间:
2011-01-01
影响因子:
5.6
通讯作者:
Sonnewald, Uwe
Sonnewald, Uwe
中科院分区:
生物学2区
文献类型:
--
作者:
Voll, Lars Matthias;Horst, Robin Jonathan;Sonnewald, Uwe

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在与寄主植物相容的相互作用中,生物营养植物病原菌颠覆寄主新陈代谢,以确保定植的寄主细胞持续提供营养同化物。为了研究大麦白粉菌(Blumeria graminis f.sp.)的初级碳氮代谢对生养真菌侵染的响应是否能揭示共同的基序,我们对大麦白粉菌(Blumeria graminis f.sp.)三个完全不同的病原菌进行了代谢组和转录组的联合研究。玉米黑粉菌(Ustilago Maydis)和玉米炭疽菌(Colletotrichum Graminicola),后者是一种半营养生物,在其建立过程中只表现出最初的生物营养阶段。基于对42种水溶性代谢物的分析,我们能够通过层次聚类分析和主成分分析来区分早期生物营养和晚期生物营养相互作用,而与植物寄主无关。有趣的是,相应的转录组数据集不能区分这些生物营养阶段,无论使用的是中央代谢基因的转录本数据还是整个转录组数据集。在光合作用、糖酵解、TCA循环、脂类生物合成和细胞壁代谢的转录调控方面,不同的病原菌之间存在着显著的差异。然而,在所有相互作用的早期渗透后阶段,谷氨酰胺、天冬氨酸和葡萄糖的含量增加,而PEP和3-PGA的含量减少是共同的。在转录水平上,TCA循环、核苷酸能量代谢和氨基酸生物合成等基因在比较的生物营养相互作用中表现出一致的趋势,确定代谢能量需求和氨基酸池重排是生物营养早期共同的转录基序。代谢组和转录本数据被用来建立三个被研究的相互作用的早期生物营养期间的叶片初级代谢模型。
During compatible interactions with their host plants, biotrophic plant-pathogens subvert host metabolism to ensure the sustained provision of nutrient assimilates by the colonized host cells. To investigate, whether common motifs can be revealed in the response of primary carbon and nitrogen metabolism toward colonization with biotrophic fungi in cereal leaves, we have conducted a combined metabolome and transcriptome study of three quite divergent pathosystems, the barley powdery mildew fungus (Blumeria graminis f.sp. hordei), the corn smut fungus Ustilago maydis, and the maize anthracnose fungus Colletotrichum graminicola, the latter being a hemibiotroph that only exhibits an initial biotrophic phase during its establishment. Based on the analysis of 42 water-soluble metabolites, we were able to separate early biotrophic from late biotrophic interactions by hierarchical cluster analysis and principal component analysis, irrespective of the plant host. Interestingly, the corresponding transcriptome dataset could not discriminate between these stages of biotrophy, irrespective, of whether transcript data for genes of central metabolism or the entire transcriptome dataset was used. Strong differences in the transcriptional regulation of photosynthesis, glycolysis, the TCA cycle, lipid biosynthesis, and cell wall metabolism were observed between the pathosystems. However, increased contents of Gln, Asn, and glucose as well as diminished contents of PEP and 3-PGA were common to early post-penetration stages of all interactions. On the transcriptional level, genes of the TCA cycle, nucleotide energy metabolism and amino acid biosynthesis exhibited consistent trends among the compared biotrophic interactions, identifying the requirement for metabolic energy and the rearrangement of amino acid pools as common transcriptional motifs during early biotrophy. Both metabolome and transcript data were employed to generate models of leaf primary metabolism during early biotrophy for the three investigated interactions.