Departments of Plant Biology and Entomology, and Institute of Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16663-8. doi: 10.1073/pnas.1220219110. Epub 2013 Sep 25.
Endoparasitism by gall-forming insects dramatically alters the plant phenotype by altering growth patterns and modifying plant organs in ways that appear to directly benefit the gall former. Because these morphological and physiological changes are linked to the presence of the insect, the induced phenotype is said to function as an extension of the parasite, albeit by unknown mechanisms. Here we report the gall-forming aphid-like parasite phylloxera, Daktulosphaira vitifoliae, induces stomata on the adaxial surface of grape leaves where stomata typically do not occur. We characterized the function of the phylloxera-induced stomata by tracing transport of assimilated carbon. Because induction of stomata suggests a significant manipulation of primary metabolism, we also characterized the gall transcriptome to infer the level of global reconfiguration of primary metabolism and the subsequent changes in downstream secondary metabolism. Phylloxera feeding induced stomata formation in proximity to the insect and promoted the assimilation and importation of carbon into the gall. Gene expression related to water, nutrient, and mineral transport; glycolysis; and fermentation increased in leaf-gall tissues. This shift from an autotrophic to a heterotrophic profile occurred concurrently with decreased gene expression for nonmevalonate and terpenoid synthesis and increased gene expression in shikimate and phenylpropanoid biosynthesis, secondary metabolite systems that alter defense status in grapes. These functional insect-induced stomata thus comprise part of an extended phenotype, whereby D. vitifoliae globally reprograms grape leaf development to alter patterns of primary metabolism, nutrient mobilization, and defense investment in favor of the galling habit.
昆虫在植物体内寄生会通过改变生长模式和修饰植物器官来显著改变植物表型，这些变化似乎直接有利于寄生物。由于这些形态和生理变化与昆虫的存在有关，因此诱导的表型被认为是寄生虫的一种延伸，尽管其机制尚不清楚。在这里，我们报告了一种类似于蚜虫的寄生叶蝉 Phylloxera vitifoliae，它会在葡萄叶的腹面诱导产生气孔，而通常情况下，葡萄叶的腹面是不会产生气孔的。我们通过追踪同化碳的运输来描述 Phylloxera 诱导的气孔的功能。由于诱导气孔表明对初级代谢的显著操纵，我们还对叶蝉转录组进行了特征描述，以推断初级代谢的全局重配置水平以及随后下游次生代谢的变化。叶蝉的取食诱导了在昆虫附近形成气孔，并促进了同化和导入碳到叶蝉中。与水、养分和矿物质运输、糖酵解和发酵相关的基因表达在叶-虫组织中增加。这种从自养到异养的转变伴随着非甲羟戊酸和萜类合成的基因表达减少，以及莽草酸和苯丙素生物合成的基因表达增加，这些次生代谢系统改变了葡萄的防御状态。因此，这些功能性的昆虫诱导气孔构成了扩展表型的一部分，其中 D. vitifoliae 会全局重新编程葡萄叶片的发育，以改变初级代谢、养分动员和防御投资的模式，从而有利于寄生习性。
