Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects.
Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects.
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DOI：
10.7554/elife.36268
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发表时间：
2018-07-17
期刊：
影响因子：
7.7
通讯作者：
Baldwin IT
中科院分区：
文献类型：
--
作者：
Brütting C;Crava CM;Schäfer M;Schuman MC;Meldau S;Adam N;Baldwin IT
内生昆虫提供了食草动物的教科书例子，这些食草动物操纵寄主植物的生理，通过转移细胞分裂素(CK)来创造增加被感染组织营养价值的“绿岛”，从而可能改变源/库关系。然而，缺乏关于CK转移的明确证据。在这里，我们证明了自由生活的草食动物Tupiocoris notatus取食烟草的特点是营养水平稳定，CK水平上升，以及受到攻击的叶片中CK相关转录水平的变化，这与内生昆虫有显著的相似之处。利用~(15)N同位素标记，我们证明了CK N6-异戊烯基腺嘌呤(IP)是通过昆虫的口腔分泌物转移到植物体内的。在田间，白纹伊蚊优先攻击CK水平升高的叶片；CK感知缺失的植物对T.notatus取食损害的耐受性较差。我们推断，这种自由生活的昆虫利用Cks来操纵源/汇关系，以提高食物质量，并将其摄食的健康后果降至最低。许多昆虫利用植物作为食物和庇护所。为了保护自己，植物通常会形成防御机制，以阻止或削弱攻击者，例如产生毒素或将营养储存在受攻击的组织之外。但一些昆虫设法对抗植物的防御反应。这类物种的流动性往往较小，它们一生中的很大一部分时间都在植物的有限区域度过，例如在植物组织内。这些昆虫也被称为内生动物，它们甚至可以操纵植物中的信号系统，例如一种名为细胞分裂素的植物激素，它有助于植物生长和发育种子以及储存营养的果实或幼叶。研究人员此前曾假设，内生动物以细胞分裂素为目标，因为它们被限制在植物内的特定区域生活，而且--与自由生活的昆虫不同--无法接触到其他可能更有营养的摄食部位。通过修改细胞分裂素，这种定位昆虫可以建立自己的“营养库”。到目前为止，昆虫是如何将细胞分裂素转移到植物上的，以及这种能力是否仅限于内生昆虫，目前还不清楚。为了进一步研究这一点，Bruüting，Crava等人。研究了郊狼烟草植株对一种自由生活的昆虫--吸液虫Tupiocoris notatus的反应。实验表明，即使昆虫是用人工饲料饲养的，昆虫体内也含有大量的细胞分裂素。Brüting，Crava等人。然后开发了一种方法，可以清楚地区分昆虫中存在的细胞分裂素和植物产生的细胞分裂素，以测试诺氏锥虫在取食过程中是否可以转移这些植物激素。结果表明，与内生昆虫相似，白纹伊蚊将细胞分裂素注入受侵袭的叶片中，可能是为了创造稳定的营养环境。昆虫代表着地球上最大和最多样化的有机体群体，包括许多农作物害虫。尽管杀虫剂对环境和农民的健康造成有害影响，但杀虫剂主要用于虫害防治。更好地了解昆虫如何利用细胞分裂素来增加叶子的营养价值，可能有助于我们找到提高作物对昆虫攻击的耐受性的方法。
Endophytic insects provide the textbook examples of herbivores that manipulate their host plant’s physiology, putatively altering source/sink relationships by transferring cytokinins (CK) to create ‘green islands’ that increase the nutritional value of infested tissues. However, unambiguous demonstrations of CK transfer are lacking. Here we show that feeding by the free-living herbivore Tupiocoris notatus on Nicotiana attenuata is characterized by stable nutrient levels, increased CK levels and alterations in CK-related transcript levels in attacked leaves, in striking similarity to endophytic insects. Using 15N-isotope labeling, we demonstrate that the CK N6-isopentenyladenine (IP) is transferred from insects to plants via their oral secretions. In the field, T. notatus preferentially attacks leaves with transgenically increased CK levels; plants with abrogated CK-perception are less tolerant of T. notatus feeding damage. We infer that this free-living insect uses CKs to manipulate source/sink relationships to increase food quality and minimize the fitness consequences of its feeding. Many insects use plants for food and for shelter. To protect themselves, plants often develop defense mechanisms that deter or debilitate their attackers, such as producing toxins or storing nutrients away from the attacked tissues. But some insects manage to counter the plants’ defense responses. Such species are often less mobile and spend a large part of their life in a restricted area of the plant, for example, inside plant tissues. Also known as ‘endophytic’ animals, these insects can even manipulate the signaling system in a plant, such as a class of plant hormones called cytokinins, which help plants to grow and to develop seeds and nutrient-storing fruits or young leaves. Researchers have previously assumed that endophytic animals target cytokinins because they are restricted to living in certain areas within the plant, and – unlike ‘free-living’ insects – lack access to other, potentially more nutritious feeding sites. By modifying cytokinins, the location-bound insects could create their own ‘nutrient pool’. Until now, it was unclear how insects transfer cytokinins to a plant and if this ability was restricted to endophytic insects. To investigate this further, Brütting, Crava et al. studied the response of coyote tobacco plants infested with a free-living insect, the sap-sucking bug Tupiocoris notatus. The experiments revealed that the insects’ bodies contained large quantities of a type of cytokinin, even when insects were raised on artificial diets. Brütting, Crava et al. then developed a method to clearly distinguish cytokinins present in the insects from those produced by the plants to test whether T. notatus can transfer these plant hormones during feeding. The results showed that similar to endophytic insects, T. notatus injects cytokinins into the attacked leaves, presumably to create a stable nutritious environment. Insects represent the largest and most diverse group of organisms on Earth, including many crop pests. Despite their detrimental impact on the environment and the health of the farmers, pesticides are used predominantly for pest control. A better understanding of how insects use cytokinins to increase the nutritional value of the leaves may help us to find ways to increase the crop’s tolerance to insect attacks.