Functional Ecology ( IF 4.6 ) Pub Date : 2022-08-11 , DOI: 10.1111/1365-2435.14159 Carla Vázquez‐González 1, 2 , Laura Pombo‐Salinas 2 , Lucía Martín‐Cacheda 2 , Sergio Rasmann 3 , Gregory Röder 3 , Luis Abdala‐Roberts 4 , Kailen A. Mooney 1 , Xoaquín Moreira 2
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1 INTRODUCTION
Research has shown that plants can perceive and respond to complex blends of above- and below-ground volatile organic compounds (‘VOCs’ hereafter) emitted by conspecific or heterospecific neighbours, a phenomenon termed ‘plant communication’ (Heil & Karban, 2010; Karban et al., 2014). This form of plant–plant signalling frequently involves either priming or induction of defences in undamaged ‘receiver’ plants when exposed to VOCs released by herbivore-induced neighbours (‘emitters’), which results in increased induced resistance against herbivory in receiver plants (Karban, 2015). Several non-mutually exclusive hypotheses have been proposed to explain the ecological and evolutionary role of plant communication. Among those, kin selection has been proposed as a key mechanism driving the origin and maintenance of plant communication among conspecifics (Karban et al., 2013; Karban & Shiojiri, 2009). Namely, communication between unrelated individuals would come at high costs for the emitter plants, as they would increase competitors' fitness at the expense of their own fitness (Heil & Karban, 2010; Heil & Ton, 2008). Another hypothesis argues that inter-plant signalling arose as a by-product of plants using volatiles for efficient intra-plant signalling (Frost et al., 2007; Heil & Silva Bueno, 2007). That said, and while these explanations provide a useful framework for understanding the evolutionary relevance of plant communication, we still lack mechanistic data for understanding ecological variation in plant communication. Thus, while VOCs emissions have been amply shown to drive this phenomena, how biotic and abiotic factors interact with VOCs induction and perception to drive variation in communication needs to be elucidated (Bouwmeester et al., 2019; Turlings & Erb, 2018).
Recent advances point to several key factors that determine the strength of plant–plant signalling through VOCs (Moreira & Abdala-Roberts, 2019). Notably, the total amount of volatiles emitted as well as the blends of compounds and the abundance of individual compounds present in emissions depend on multiple biotic and abiotic factors, leading to specificity and context dependency in plant communication (Moreira & Abdala-Roberts, 2019). For example, recent work has shown that communication is strongly contingent upon the identity of the attacking herbivore, whereby resistance in receivers is only boosted when emitters and receivers are attacked by the same insect (Moreira et al., 2018). In addition, though much less studied, plant communication is likely contingent on abiotic factors such as soil nutrients, salinity or water availability, as these often affect plant defence induction in response to herbivory, including VOCs (Gouinguené & Turlings, 2002; Moreira et al., 2015; Quijano-Medina et al., 2021; Sampedro et al., 2011; Suárez-Vidal et al., 2019). There are at least two non-exclusive mechanisms by which abiotic conditions could affect plant communication. First, abiotic factors can modulate the inducibility of VOCs in response to herbivory in emitter plants (Gouinguené & Turlings, 2002; Holopainen & Gershenzon, 2010; Scott et al., 2019; Vallat et al., 2005). Second, these factors can shape receiver responses to emitter VOCs such as the physiological priming of defences and subsequent induced resistance in response to damage (Martinez-Medina et al., 2016; Ton et al., 2007; Wilkinson et al., 2019). Accordingly, studies that simultaneously address abiotic effects on emitters and receivers are needed to advance our understanding of the mechanisms that underlie context dependency of plant communication in response to herbivory.
Despite research on water availability effects on plant defences in both natural and cultivated species, including VOCs, its effects on plant–plant signalling are poorly understood. To date, only two studies have evaluated the effects of water availability on plant communication (Catola et al., 2018; Pezzola et al., 2017). First, Catola et al. (2018) investigated the individual and combined effects of emitter water stress and aphid feeding on the emission of VOCs in tomato Solanum lycopersicum and whether reception of VOCs from stressed emitters increased the attraction of parasitic wasps (i.e. indirect resistance by natural enemies) in receiver plants. They found that both factors (aphid feeding and water stress), individually or in combination, significantly induced VOCs emission. Correspondingly, receivers exposed to VOCs from stressed emitters exhibited increased indirect resistance by parasitic wasps, independently of whether abiotic (water availability) or biotic (aphid feeding) effects on emitters where considered individually or in combination. Second, Pezzola et al. (2017) similarly found that VOCs from damage-induced sagebrush Artemisia tridentata plants boosted receiver resistance to generalist grasshoppers but this effect was not contingent on the level of water availability, which in this case was manipulated for receiver plants. These studies together suggest that signalling is resilient to effects of water availability in both systems. However, more studies are needed to understand the commonness and abiotic context-dependency in plant signalling, particularly in cases where abiotic stress impairs VOCs induction. In particular, manipulations of water availability for both emitters and receivers (i.e. emission vs reception components) coupled with detailed assessments of quantitative vs. qualitative changes in VOCs are needed to unveil the mechanisms of abiotic effects on signalling.
In this study, we investigated whether VOC-mediated airborne communication in potato Solanum tuberosum plants in response to leaf herbivory by the generalist insect Spodoptera exigua was contingent on water availability effects on both emitter and receiver plants (interactive effects of emitter herbivory and water availability in the emitter and receiver), and evaluated qualitative and quantitative changes in emitter VOCs emissions to gain insight on the mechanism behind such effects. For this, we carried out a greenhouse experiment where we paired potato plants (i.e. emitters and receivers) and induced half of the emitters with S. exigua larvae. We subjected emitter and receiver plants to one of two water availability treatments: high (i.e. well-watered) vs. low (i.e. reduced watering) water availability. We measured total emission and composition of VOCs in emitter plants and then conducted a caterpillar bioassay on receiver plants to test for effects on the amount of leaf area consumed by S. exigua (i.e. induced resistance). We hypothesized that low water availability in emitters would hamper the inducibility of VOCs in response to herbivory, resulting in weaker (or null) airborne signalling effects on receiver resistance. Similarly, we hypothesized that low water availability in receivers would hamper the physiological priming and subsequent induced resistance boosted by perception of VOCs from herbivore-induced emitters. Our work provides insights into the effects of water availability on both the emission and reception of herbivore-induced VOCs and their implications for plant communication. This knowledge may not only inform and optimize sustainable methods that make use of plant volatiles to boost crop resistance (Pickett & Khan, 2016; Stenberg et al., 2015; Turlings & Erb, 2018), but also contribute to mechanistic research on the multiplicity of ecological roles of plant VOCs. We do so first, by investigating the mechanisms that underlie plant communication and second, by investigating the abiotic context dependency and potential effects of reduced water availability on induced resistance in plants via VOCs.
中文翻译：
水分供应对马铃薯植物间挥发性介导的昆虫食草通讯的影响
1 简介
研究表明，植物可以感知并响应由同种或异种邻居排放的地上和地下挥发性有机化合物（以下简称“VOC”）的复杂混合物，这种现象被称为“植物交流”（Heil & Karban， 2010 年；Karban等人， 2014 年）。这种形式的植物-植物信号传递通常涉及在未受损的“接收器”植物暴露于由食草动物诱导的邻居（“发射器”）释放的 VOC 时引发或诱导防御，这导致接收器植物对食草动物的诱导抗性增加（Karban , 2015）。已经提出了几个非互斥的假设来解释植物交流的生态和进化作用。其中，亲属选择被认为是驱动同种间植物交流起源和维持的关键机制（Karban et al., 2013 ; Karban & Shiojiri, 2009）。也就是说，不相关的个体之间的交流对排放植物来说会付出高昂的代价，因为它们会以牺牲自己的适应度为代价来增加竞争对手的适应度（Heil & Karban, 2010 ; Heil & Ton, 2008）。另一种假设认为，植物间信号传导是植物使用挥发物进行有效植物内信号传导的副产品（Frost 等人， 2007; 海尔和席尔瓦布埃诺， 2007 年）。也就是说，虽然这些解释为理解植物交流的进化相关性提供了一个有用的框架，但我们仍然缺乏了解植物交流中生态变异的机制数据。因此，虽然 VOCs 排放已被充分证明可以推动这一现象，但需要阐明生物和非生物因素如何与 VOCs 诱导和感知相互作用以推动交流的变化（Bouwmeester 等人， 2019 年；Turlings & Erb， 2018 年）。
最近的进展指出了通过 VOC 确定植物-植物信号强度的几个关键因素（Moreira 和 Abdala-Roberts， 2019 年）。值得注意的是，排放的挥发物总量以及化合物的混合物和排放中存在的单个化合物的丰度取决于多种生物和非生物因素，从而导致植物交流中的特异性和环境依赖性（Moreira 和 Abdala-Roberts， 2019 年） . 例如，最近的研究表明，交流在很大程度上取决于攻击草食动物的身份，因此只有当发射器和接收器受到同一昆虫的攻击时，接收器的抵抗力才会增强（Moreira 等， 2018）。此外，尽管研究较少，植物交流可能取决于非生物因素，如土壤养分、盐度或水的有效性，因为这些因素通常会影响植物对草食性的防御诱导，包括 VOCs (Gouinguené & Turlings, 2002 ; Moreira et al .， 2015 年；Quijano-Medina 等人， 2021 年；Sampedro 等人， 2011 年；Suárez-Vidal 等人， 2019 年）。至少有两种非排他性的机制可以使非生物条件影响植物的交流。首先，非生物因素可以调节 VOCs 对辐射植物中草食性的反应（Gouinguené 和 Turlings， 2002 年；Holopainen 和 Gershenzon， 2010 年）; 斯科特等人， 2019；Vallat 等人， 2005 年）。其次，这些因素可以影响接收器对发射器 VOC 的响应，例如防御的生理启动和随后对损伤的诱导抵抗（Martinez-Medina 等人， 2016 年；Ton 等人， 2007 年；Wilkinson 等人， 2019 年） . 因此，需要同时解决对发射器和接收器的非生物影响的研究，以促进我们对植物通讯响应草食性的背景依赖性机制的理解。
尽管研究了水对自然和栽培物种（包括挥发性有机化合物）植物防御的影响，但人们对其对植物-植物信号传导的影响却知之甚少。迄今为止，只有两项研究评估了水资源可用性对植物交流的影响（Catola 等人， 2018 年；Pezzola 等人， 2017 年）。首先，卡托拉等人。( 2018 ) 研究了排放源水分胁迫和蚜虫取食对番茄中 VOCs 排放的单独和综合影响Solanum lycopersicum以及从受压力的发射器接收 VOC 是否会增加接收植物中寄生蜂的吸引力（即天敌的间接抵抗力）。他们发现，这两个因素（蚜虫摄食和水分胁迫）单独或联合显着诱导 VOCs 排放。相应地，暴露于来自受压发射器的 VOC 的接收器表现出寄生蜂的间接抵抗力增加，与单独或组合考虑对发射器的非生物（水可用性）或生物（蚜虫取食）影响无关。其次，Pezzola 等人。( 2017 ) 同样发现，损伤诱导的山艾蒿中的 VOCs植物提高了接收器对通才蚱蜢的抵抗力，但这种影响并不取决于可用水的水平，在这种情况下，它是为接收器植物操纵的。这些研究共同表明，信号对两个系统中可用水的影响具有弹性。然而，需要更多的研究来了解植物信号传导中的共性和非生物环境依赖性，特别是在非生物胁迫损害 VOC 诱导的情况下。特别是，需要控制发射器和接收器的可用水量（即发射与接收组件），以及对 VOC 的定量与定性变化的详细评估，以揭示非生物效应对信号的影响机制。
在这项研究中，我们调查了马铃薯植物中 VOC 介导的空中传播是否响应通才昆虫Spodoptera exigua的叶子食草行为取决于对发射器和接收器植物的水可用性影响（发射器食草和水可用性的交互效应发射器和接收器），并评估了发射器 VOCs 排放的定性和定量变化，以深入了解这些影响背后的机制。为此，我们进行了一个温室实验，我们将马铃薯植物（即发射器和接收器）配对，并用S. exgua诱导一半的发射器幼虫。我们对发射器和接收器工厂进行了两种可用水量处理之一：高（即充分浇水）与低（即减少浇水）可用水量。我们测量了发射器植物中 VOC 的总排放量和组成，然后对接收器植物进行了毛虫生物测定，以测试对S. exigua消耗的叶面积量的影响（即感应电阻）。我们假设发射器中的低水可用性会阻碍 VOC 对食草动物的诱导性，从而导致对接收器阻力的空气传播信号影响较弱（或无效）。同样，我们假设接收器中的低水可用性会阻碍生理启动和随后的诱导阻力，这些阻力由草食动物诱导的发射器对 VOC 的感知增强。我们的工作提供了关于水的可用性对草食动物引起的 VOC 的排放和接收的影响及其对植物交流的影响的见解。这些知识不仅可以告知和优化利用植物挥发物提高作物抗性的可持续方法（Pickett & Khan, 2016 ; Stenberg et al., 2015; Turlings & Erb， 2018 年），但也有助于对植物 VOC 的多重生态作用进行机理研究。我们首先通过研究植物交流的机制，其次通过研究非生物环境依赖性和水可用性减少对通过 VOCs 诱导植物抗性的潜在影响来做到这一点。
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