An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores
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DOI:
10.1007/s00442-011-2015-z
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发表时间:
2011-11-01
期刊:
影响因子:
2.7
通讯作者:
Kliebenstein, Daniel
Kliebenstein, Daniel
中科院分区:
环境科学与生态学2区
文献类型:
--
作者:
Bidart-Bouzat, M. Gabriela;Kliebenstein, Daniel

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专家/多面手范式的一般预测表明,植物对昆虫食草动物的反应可能取决于昆虫进攻者的生态专门化程度。然而,一个温室实验评估了模式植物拟南芥对三种专家(小菜蛾、菜青虫和油菜夜蛾)和三种多面手(菜粉蝶、甜菜夜蛾和桃蚜)昆虫的反应,结果并不支持先前的预测。利用生态基因组学方法,我们从植食者诱导的全基因组基因表达的变化、与防御相关的途径和硫代葡萄糖苷(即十字花科植物中普遍存在的次生代谢物)浓度方面评估了植物的反应。我们的结果表明,植物的反应不受昆虫食草动物专化度的影响。相反,昆虫分类群(例如,蚜虫和鳞翅目昆虫)的反应更强烈,可能是因为它们的取食方式不同。有趣的是,同样的植食性昆虫物种在防御信号(茉莉酸途径)、脂肪硫代谢物(在基因表达和表型水平上)和全基因组反应方面都诱导了类似的植物反应模式。此外,植物对属于同一分类群的食草性昆虫(即四种鳞翅目昆虫)的反应不能用食草动物的专门化或系统发育历史来解释。总体而言,这项研究表明,昆虫类群的不同取食模式以及食草动物特有的植物反应,可能是由A.thaliana(或近亲)与每个鳞翅目物种之间不同的生态/进化相互作用造成的,这可能解释了为什么观察到的反应偏离了专家/多面手范式的预测。
A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.