Carla Vázquez González: Deciphering the context-dependency of plant communication: How does drought stress affect plant-plant signalling by volatile organic compounds?

In our latest post, Carla Vázquez González—a postdoctoral researcher from the University of California-Irvine—presents her last work ‘Effect of water availability on volatile-mediated communication between potato plants in response to insect herbivory’. In this post, she sheds new light on how plants communicate to overcome adversity, discusses the striking results in her paper, and shares her thought about the rough path early-career ecologists currently face.

About the paper

Plants perceive and respond to complex blends of above- or belowground volatile organic compounds (‘VOCs’) emitted by herbivore-damaged neighbours—a phenomenon termed ‘plant communication’. Such responses frequently involve either priming or induction of defences by “receiver” plants when exposed to incoming VOCs released by herbivore-damaged “emitter” plants, which ultimately results in heightened resistance against herbivory in these receivers.

 VOC sampling in experimental potato plants (credit: Lucia Martín-Cacheda).

Recent research suggests that variation in abiotic and biotic environmental conditions may lead to specificity and context-dependency in plant communication. For instance, previous studies demonstrated that chemical communication depends on plant sex, whereby females seem to be better ‘listeners’ compared to males. Similarly, other studies reported that the identity of the attacking herbivore can also modify the outcomes of plant communication and that effective signalling and concurrent resistance in receivers occurs only when both emitters and receivers are attacked by the same insect. Furthermore, abiotic factors that modulate defence inducibility—such as drought or water availability, salinity, and temperature—may potentially lead to variation in plant communication; however, their effects have been much less studied. Specifically, low water availability may hamper the inducibility of VOCs in response to herbivory in emitter plants, leading to weaker plant-to-plant signalling. Similarly, low water availably may negatively affect the induction of defences that mediate acquired resistance in receiver plants. Thus, water availability may play a key role at modulating plant communication by affecting both the chemical cues released by emitters, and the response to such cues by the eavesdropper receivers. To date, however, only a few studies have explored the effect of water availability on plant communication, and studies that did so did not consider the combined effects of water availability on both emitter and receiver plants. Therefore, in this study we designed a greenhouse experiment to simultaneously test the effects of drought (or low water availability) in emitters and receivers on the effectiveness of plant communication. To do this, we used potato (Solanum tuberosum) and the beet armyworm (Spodoptera exigua) as our model study system.

Paired emitter and receiver potato plants (credit: Lucia Martín-Cacheda).

This study on plant communication came up on a solid and long-lasting collaboration between four institutions (from Spain, Mexico, USA and Switzerland), which was focussed to a large extent on investigating how global change affects species interactions which are relevant to preserve biodiversity and human wellbeing. Specifically, ecological knowledge on plant-herbivore interactions and plant resistance underlies agricultural practices and policies, thus having enormous social implications. We still lack, however, a complete understanding of the processes and factors that drive standing ecological variation on plant defences and resistance. In relation to studies addressing the context-dependency of plant communication—to the extent that this variation is better understood—we will be able to exploit plant-plant signalling via VOCs as a tool for sustainable crop management. Within this context, our results are particularly relevant for the agriculture sector and policy makers.

About the research

Pest control in agroecosystems has relied heavily on the use of pesticides. However, the widespread use of agrochemicals has triggered severe environmental problems due to their persistence in the air, soil, water, and food, as well as the development of pest resistance. Presently, more than a quarter of all agricultural pesticides has been banned worldwide to mitigate these impacts, but pesticides continue to be heavily used. In response to this situation, over the last decade there has been a pressing need for developing environmentally friendly methods for pest management involving alternative biocontrol strategies. In this sense, the use of VOCs for pest management is in line with this challenge and holds great promise for lowering pesticide application in crops such as potato. Accordingly, research that addresses the context-dependency of VOC-mediated communication is warranted to successfully implement these methods. Furthermore, understanding the factors that determine the strength of plant-herbivore interactions has been an important research avenue in the last decades. In line with this, insights gained from studies on crop species such as potato can then be transferred to natural systems, contributing to understanding of how environmental variation in natural ecosystems, and in particular in factors associated with ongoing climate change, may affect plant communication in a broader ecological sense.

Potato is considered a drought-sensitive crop. Accordingly, one of the most surprising results was that despite water-stressed plants showing a weaker inducibility of VOCs in response to herbivory, this did not result in less effective communication. This means that while the chemical cue released by emitter plants (i.e., the message) was less strong when plants were under drought stress, water availability limitation did not affect the perception of the message by eavesdropper receivers, and the subsequent response in terms of induced resistance. This result somehow contradicts ecological theory on plant defences that predict that limited-resource conditions may constrain inducible responses. Finding no evidence of drought effects on plant communication in potato plants under the specific experimental conditions of our study, however, does not exactly mean that plant communication will not be compromised by changes in water availability under different circumstances. Accordingly, we think that further research testing the effects of variation in water availability on plant communication is warranted. Specifically, we think that the length of the water restriction treatment may play a key role at modulating defensive responses. In order to implement longer periods of water limitation on the experimental plants, other crops with longer vegetative cycles may be more suitable than potato plants.

Beet armyworm (Spodoptera exigua) feeding on a potato plant (credit: Lucia Martín-Cacheda).

Our findings provide a first glimpse at the complexity and variability of plant communication, and point at important sources of specificity that may lead to predictable outcomes. Potential future avenues of research that will allow us to better understand specificity of plant communication as a tool for sustainable crop management include assessing how domestication of species determines the outcomes of plant signalling. Research has shown that cultivated varieties are more susceptible to pests compared to their wild relatives—mainly as a result of selection for traits that increase productivity at the expense of defensive traits, or even selection directly aimed at reducing physical or chemical defences to increase palatability for human consumption. These domestication effects have also been shown to affect volatile emissions, frequently decreasing total production or altering blends and the abundances of specific compounds. As a result, domestication has likely altered or disrupted plant-plant signalling, but our understanding of such effects is still limited. Research evaluating domestication effects on plant communication can help understand whether and how changes in VOCs in domesticated varieties (relative to wild populations or relatives) have affected plant-plant signalling. We believe that these types of studies can provide the knowledge to manage or restore plant-plant signalling in crops.

From a broader ecological perspective, there is still a considerable knowledge gap at understanding the factors and mechanisms that promote and maintain variation in plant communication. Abiotic factors such as salinity, temperature, and nutrient availability are known to modulate induced responses in plants; however, their effects on plant communication have not been broadly addressed. Similarly, biotic interactions between emitter and receiver plants with other organisms can notably affect and modulate both the emission and perception of VOCs involved in this chemical signalling. For instance, beneficial associations between plants and a number of organisms from the soil microbiome play a key role at mediating the priming of defences and acquired resistance to antagonist organisms in plants. Finally, there is a need to decipher the specific responses that occur in receiver plants that mediate induced resistance. This includes understanding what type of defensive strategies are involved (direct vs. indirect defences) and what specific plant traits are primed and subsequently induced when receiver plants are attacked. For instance, perception of VOCs emitted by damaged plants can boost in eavesdropper neighbours the priming of plant secondary metabolites that act as a direct defence against insect herbivores, as well as traits that mediate indirect defence by herbivore predators and parasitoids, such as extrafloral nectaries or the emission of VOCs that act as a ‘cry for help’. These are all potential avenues of research that will help to decipher the language of plant communication.

About the author

The author, Carla Vázquez-González

I grew up in a small fishing village in Galicia, Northwest Spain. In my hometown, the household incomes of near a thousand families, including my own, depend directly on fish and seafood extraction. Having been in such close contact with a community that relies directly on the sustainable use of natural resources, I have always been aware of the necessity of ecosystem preservation to ensure social welfare—this was critical in my decision to get involved in ecological research. After graduating in Biology, I decided to study a Master’s in Fundamental Ecology and Conservation. I was fascinated by the intellectual challenge that fundamental ecological research represented to me, and how stimulating it was! Therefore, the most obvious next step was to enroll on a Ph.D. program in Ecology. During my Ph.D., I studied how genetics and environmental gradients affected natural variation in defences in pine trees. I remember reading about the ‘arms race’ theory, and coevolution stories between milkweeds and monarch butterflies that sounded almost like fantasy to me—this fuelled my interest in plant-herbivore interactions. I particularly enjoyed reading the pioneer work of Professor Richard Karban (University of California-Davis) and collaborators. Their studies on plant responses to herbivory and induced resistance have broadened our knowledge on how plants sense, react, and actively interact with their environment (including their responses to insect herbivores), and have inspired the scientific work of generations, including myself. Currently, I am a postdoctoral researcher at Professor Kailen Mooney’s lab at the University of California, Irvine. My current research aims at investigating plant-herbivore interactions from a broader ecological perspective, taking into account the complex biotic and abiotic context in which these interactions occur.

            Having the pleasure to experience and understand nature in its wildest form is a privilege that hooks me in ecological research. The feeling of fulfilment makes the scientific career worthy, in spite of the many obstacles we have to confront. In particular, being a woman working in academia can make the experience significantly harder, especially for those trying to reconcile work and family life. I am aware, however, that as a cisgender, white woman born and raised in the global north, I hold a privilege to pursue a career in academia that many others may not hold, and this needs to be acknowledged in order to make visible the discrimination that other social groups face. I am grateful for having had the opportunity to study in a public university and being granted with public funding during my education and my career as a researcher. Having a strong welfare state definitely makes an enormous contribution to equitable access to career opportunities, including research. There are still, however, enormous barriers our society needs to overcome in order to improve scientific research and careers in academia. Specifically, in my home country (Spain), as well as in other countries in Europe, low funding for research (especially for fundamental one) has generated a fierce competition among young scientists that has profound negative effects on our mental health and wellbeing. In this sense, my best piece of advice to those who try to build a career in academia is to prioritize inclusive collaboration over competition. This will allow us to increase the scientific impact of our contributions by including different perspectives, approaches, and sensibilities. Most importantly, it will help us to maintain healthy relationships with our peers and to preserve our own wellbeing.

Enjoyed the blogpost? Read the research here.

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