Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?
Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?
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DOI：
10.1371/journal.ppat.1005790
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发表时间：
2016-08
期刊：
影响因子：
6.7
通讯作者：
Carr JP
中科院分区：
文献类型：
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作者：
Groen SC;Jiang S;Murphy AM;Cunniffe NJ;Westwood JH;Davey MP;Bruce TJ;Caulfield JC;Furzer OJ;Reed A;Robinson SI;Miller E;Davis CN;Pickett JA;Whitney HM;Glover BJ;Carr JP
植物挥发物在某些传粉者的引诱和食草性昆虫的寄主定位中起着重要作用。病毒感染会导致植物挥发性排放谱发生变化，这可以使植物对作为病毒载体的昆虫食草动物(如蚜虫)更具吸引力。然而，目前尚不清楚病毒诱导的挥发性产物的变化是否会影响植物与传粉者的相互作用。我们发现，感染黄瓜花叶病毒(CMV)的番茄(Solanum Lycopsicum)和拟南芥(Arabiopsis Thaliana)植株释放的挥发性物质改变了熊蜂(Bombus Terrestris)的觅食行为。用气相色谱-质谱法鉴定了番茄植株排放的挥发性有机化合物混合物中病毒诱导的量和质的变化。用不能表达2bRNA沉默抑制蛋白的CMV突变体和拟南芥沉默突变体的实验表明，microRNAs调节传粉者可感知的挥发物的释放。在番茄中，CMV侵染使植株释放出对大黄蜂有诱惑力的挥发性物质。大黄蜂通过‘嗡嗡’(超声波)花为番茄授粉，释放花粉，促进自花受精、种子生产和花粉输出。不进行蜂蜜授粉时，CMV侵染降低了种子产量，但对模拟接种和CMV感染植株的花进行蜂鸣授粉时，CMV感染植株的种子产量增加幅度与模拟接种植株相似。授粉者偏好的增加可能通过两种方式增加植物的繁殖成功：i)作为母本，通过增加胚珠受精的可能性；ii)作为父本，通过增加花粉输出。数学模型表明，在野外的广泛条件下，由于传粉者偏好增加而导致的受感染敏感植物后代数量的增加，可能会超过有利于病原菌抗性的潜在强大选择压力，从而使致病易感性基因在植物种群中持续存在。我们推测，为野生植物种群中受感染的个体提供增强的传粉者服务可能会为病毒及其敏感宿主提供互惠互利。黄瓜花叶病毒是番茄的重要病原，它会导致植物释放挥发性化学物质来吸引大黄蜂。大黄蜂是重要的番茄传粉者，但不会传播这种病毒。我们认为，在自然条件下，通过鼓励蜜蜂访问来帮助宿主繁殖可能是病毒对易受影响的宿主的“回报”。虽然番茄花可以通过自花授粉产生种子，但大黄蜂介导的“蜂群授粉”加强了这一点，增加了每个果实产生的种子数量。蜂鸣授粉通过促进花粉输出，进一步有利于植物的繁殖成功。数学模拟表明，如果受感染植物的自交以及从这些植物向周围植物的花粉转移(交叉受精)增加，这可能有利于感病植物的繁殖。这增加了这样一种可能性，即在自然条件下，一些病毒可能会增强敏感植物的竞争能力，并抑制抗病植物品系的出现。我们推测，通过增加对传粉者的吸引力来回报敏感宿主可能符合病毒的利益，这可能会提高受精率和敏感植物花粉的传播，并可能补偿感染病毒的植物种子产量的下降。
Plant volatiles play important roles in attraction of certain pollinators and in host location by herbivorous insects. Virus infection induces changes in plant volatile emission profiles, and this can make plants more attractive to insect herbivores, such as aphids, that act as viral vectors. However, it is unknown if virus-induced alterations in volatile production affect plant-pollinator interactions. We found that volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris). Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry. Experiments with a CMV mutant unable to express the 2b RNA silencing suppressor protein and with Arabidopsis silencing mutants implicate microRNAs in regulating emission of pollinator-perceivable volatiles. In tomato, CMV infection made plants emit volatiles attractive to bumblebees. Bumblebees pollinate tomato by ‘buzzing’ (sonicating) the flowers, which releases pollen and enhances self-fertilization and seed production as well as pollen export. Without buzz-pollination, CMV infection decreased seed yield, but when flowers of mock-inoculated and CMV-infected plants were buzz-pollinated, the increased seed yield for CMV-infected plants was similar to that for mock-inoculated plants. Increased pollinator preference can potentially increase plant reproductive success in two ways: i) as female parents, by increasing the probability that ovules are fertilized; ii) as male parents, by increasing pollen export. Mathematical modeling suggested that over a wide range of conditions in the wild, these increases to the number of offspring of infected susceptible plants resulting from increased pollinator preference could outweigh underlying strong selection pressures favoring pathogen resistance, allowing genes for disease susceptibility to persist in plant populations. We speculate that enhanced pollinator service for infected individuals in wild plant populations might provide mutual benefits to the virus and its susceptible hosts. Cucumber mosaic virus, an important pathogen of tomato, causes plants to emit volatile chemicals that attract bumblebees. Bumblebees are important tomato pollinators, but do not transmit this virus. We propose that under natural conditions, helping host reproduction by encouraging bee visitation might represent a ‘payback’ by the virus to susceptible hosts. Although tomato flowers can give rise to seed through self-fertilization, bumblebee-mediated ‘buzz-pollination’ enhances this, increasing the number of seeds produced per fruit. Buzz-pollination further favors reproductive success of a plant by facilitating pollen export. Mathematical modeling suggests that if self-fertilization by infected plants, as well as pollen transfer from these plants (cross-fertilization) to surrounding plants is increased, this might favor reproduction of susceptible over that of resistant plants. This raises the possibility that under natural conditions some viruses might enhance competitiveness of susceptible plants and inhibit the emergence of resistant plant strains. We speculate that it may be in a virus’ interest to pay back a susceptible host by enhancing its attractiveness to pollinators, which will likely increase fertilization rates and the dissemination of susceptible plant pollen and may compensate for a decreased yield of seeds on the virus-infected plants.