College of Science
117 Unraveling the Role of Volatiles in Plant Immunity
Alyssa Curtis and Heejin Yoo
Abstract
Plant volatiles, organic compounds emitted by various plant tissues, play a crucial role in plant immunity by serving as chemical signals that repel herbivores, attract their predators, and inhibit the growth of pathogenic microorganisms. Moreover, some volatiles act as signaling molecules to neighboring plants, priming them for defense activation. Despite their significance, the regulatory mechanisms connecting plant volatiles to immunity remain largely unexplored. This research aims to investigate the effects of specific plant volatiles – such as linalool, 1,8-cineole, and α-terpineol – for plant immunity. Building upon the established knowledge that certain monoterpenes, such as 1,8-cineole and α-terpineol, exhibit significant antimicrobial activity, our goal is to elucidate their impact on inhibiting bacterial pathogen growth and the underlying regulatory mechanisms. To explore the effects of volatiles on different plant species, we used diverse array of plants, such as Ocimum basilicum (Basil), Brassica napus, and the model plant Arabidopsis thaliana (Arabidopsis). Our aim is to elucidate the molecular mechanisms underlying the influence of these volatiles on plant immunity. This research aims to advance our understanding of the regulatory links between plant volatiles and immunity. This advancement seeks to pave the way for the development of innovative strategies that fortify plant immunity, potentially protecting crops from pests and diseases. Such strategies hold the promise of significantly impacting agriculture by enhancing both crop yield and quality, ultimately advocating for the adoption of sustainable agricultural practices.
Introduction
Take a moment to visualize a plant, perhaps it is a blossoming bluebonnet swaying gently in a meadow or a resilient cactus in the harsh heat of a desert landscape. Now extend your visualization to the plant’s immediate environment and the creatures who also dwell there.
Within its microbiome, this plant faces an array of external dangers, from pathogens to voracious parasites or herbivores, each capable of jeopardizing its existence. However, unlike humans, plants cannot simply get up and move to avoid such attacks. Instead, they have evolved intricate defense mechanisms to fortify themselves against these assaults. At the heart of this botanical arsenal are plant volatiles, or volatile organic compounds (VOCs), emitted by plant tissues to orchestrate tailored responses to the plant’s immediate needs (Ninovic et al., 2020). VOC emissions act as messengers that can attract beneficial organisms or repel pests and parasites, thus safeguarding the plant as well as notifying neighboring plants of potential threats.
Several studies have suggested that volatile organic compounds (VOCs) emitted by neighboring plants can affect plant defense mechanisms. However, it is largely unknown which specific VOCs trigger these responses and the mechanisms involved. To answer this question, several researchers have conducted experiments using a specific class of VOCs known as monoterpenes. One such study by Riedlmeier et al. (2017) explores how the specific monoterpenes α-pinene, β-pinene, and camphene play a role in SAR in plants.
During the experiment, the researchers fumigated wild-type Arabidopsis thaliana and several mutant lines with these monoterpenes in gas-tight containers and then infected them with P. syringae pv. tomato (Pst) (Riedlmeier et al., 2017). They found that these monoterpenes significantly reduced Pst growth and that mutant plants that lacked the SA signaling pathway had reduced resistance to Pst (Riedlmeier et al., 2017). These findings highlight the importance of SA biosynthesis and signaling in plant defense mechanisms triggered by these volatiles (Riedlmeier et al., 2017). This study also observed an increased expression of the SA marker gene PR1 in plants that were exposed to pinenes, indicating that pinene induces SA signaling and leads to an enhanced plant immune response (Riedlmeier et al., 2017). Additionally, the research highlights the role of specific genes like AZI1, EARLI1, and others in mediating resistance mechanisms induced by monoterpene exposure (Riedlmeier et al., 2017).
Similar to the research conducted by Riedlmeier et al. (2017), another project by Wenig et al. (2019) aimed to elucidate how plants activate their innate immune responses through SA when exposed to volatile monoterpenes. These researchers also used the model plant A. thaliana and several mutant lines, similarly, inoculating them with the pathogen Pst (Wenig et al., 2019). They conducted plant-to-plant (PTP) experiments, infecting “sender plants” and placing them alongside healthy “receiver plants” in separate vacuum containers with desiccators. These containers were opened at predetermined intervals to facilitate air exchange between the two, enabling the researchers to investigate whether the healthy receiver plants were priming their defenses with the monoterpenes released by the sender plants, potentially affecting their response to subsequent infections (Wenig et al., 2019). As a result of the PTP experiment, they found that receiver plants showed enhanced resistance against the bacterial pathogen Pst (Wenig et al., 2019). They further discovered that exposure to α-pinene and β-pinene enhanced the plants’ resistance to pathogen growth (Wenig et al., 2019). Both Wenig et al. (2019) and Riedlmeier et al. (2017) findings suggested that monoterpene emission can potentially promote plant volatile defense cues between and within plant leaves.
Although studying how monoterpenes strengthen plants might seem specialized research field, its implications extend widely, especially for those concerned about the safety and quality of their food supply. Agricultural practices, whether involving genetically modified crops or the widespread use of pesticides and herbicides, are often subject to debate.
Nevertheless, they all share a common aim: ensuring abundant and safe food production. Therefore, exploring the connection between monoterpenes and plant immunity opens doors to broader applications, particularly in crop cultivation. The studies conducted by Wenig et al. (2019) and Riedlmeier et al. (2017) underscore the potential of utilizing VOCs to enhance plant immunity, reducing dependence on harmful chemicals. This approach, as proposed by Wenig et al., involves triggering a plant’s natural defense mechanisms by increasing the production of specific monoterpenes. While this approach is great alternative, caution is necessary, as emphasized by Kessler & Baldwin (2002) in their study of plant responses to insect herbivory. They warn against the overuse of VOCs, which could diminish effectiveness over time. Just as the overuse of antibiotics has led to the rise of resistant bacteria, continuous exposure to VOCs could harmful, making the strategy ineffective. This highlights the importance of responsible regulation in utilizing VOC-based solutions. Finding a balance is essential to avoid this drawback. Therefore, a clear understanding of regulatory mechanisms is essential for sustainable implementation.
While certain monoterpenes are recognized for their contributions to plant immunity, much remains to be understood regarding the role of others in this context. Monoterpenes such as 1,8-cineole, linalool, and α-terpineol, commonly found in essential oils, have been subjects of investigation (Lackus et al., 2018; Ye et al., 2021; Taniguchi et al., 2013). Research by Lackus et al. (2018) suggests that 1,8-cineole may play a role in defense pathways by reducing pathogen growth in poplar trees and Arabidopsis plants. While 1,8- cineole demonstrates significant antimicrobial activity against plant pathogens and induces the expression of defense-related genes, the association between α-terpineol and plant immunity remains largely unexplored (Lackus et al., 2018; Ye et al., 2021). Ye et al. (2021) investigated α-terpineol, present in pine needles, through soil fumigation experiments assessing seed growth, pathogen activity, and beneficial microorganisms. Their findings suggest that α-terpineol fumigation decreases seed decay rates and targets harmful fungi while promoting beneficial bacteria growth (Ye et al., 2021). However, it remains unclear what the underlying molecular mechanism is. Taniguchi et al. (2013) found that linalool treatment induced resistance to fungal and bacterial pathogens in rice and A. thaliana plants, hinting at its role in enhancing plant defense mechanisms, albeit within the context of jasmonic acid signaling rather than salicylic acid signaling (Taniguchi et al., 2013).
While the regulatory mechanisms linking plant volatiles and immunity are crucial, they largely remain unclear, highlighting the need for thorough research to understand the impact of diverse plant volatiles on immunity. My thesis research focused on investigating the effects of specific plant volatiles—such as linalool, cineole, and terpineol—recognized for their antimicrobial properties against bacterial pathogens in crop species, offering promising avenues for further study. In addition to assessing phenotype changes through a comparative study of bacterial growth after pathogen infection, a more in-depth approach was undertaken to elucidate molecular mechanisms. Based on the significant inhibition of bacterial pathogen growth observed with linalool and terpineol in crop species, I am motivated to conduct experiments on Arabidopsis WT and SA biosynthetic mutants to uncover their underlying molecular mechanisms in future. Advancing our understanding of the regulatory connections between plant volatiles and immunity holds great potential for devising innovative strategies to strengthen plant immunity and protect crops against pests and diseases.
References
Kessler, A., & Baldwin, I. T. (2002). Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology, 53(1), 299–328. https://doi.org/10.1146/annurev.arplant.53.100301.135207
Lackus, N. D., Lackner, S., Gershenzon, J., Unsicker, S. B., & Köllner, T. G. (2018). The occurrence and formation of monoterpenes in herbivore-damaged poplar roots. Scientific Reports, 8(1). https://doi.org/10.1038/s41598-018-36302-6
Riedlmeier, M., Ghirardo, A., Wenig, M., Knappe, C., Koch, K., Georgii, E., Dey, S., Parker, J. E., Schnitzler, J.-P., & Vlot, A. C. (2017). Monoterpenes support systemic acquired resistance within and between plants. The Plant Cell, 29(6), 1440–1459. https://doi.org/10.1105/tpc.16.00898
Taniguchi, S., Hosokawa-shinonaga, Y., Tamoki, D., Yamada, S., Akimitsu, K., & Gomi, K. (2013). Jasmonate induction of the monoterpene linalool confers resistance to rice bacterial blight and its biosynthesis is regulated by jaz protein in Rice. Plant, Cell & Environment, 37(2), 451–461. https://doi.org/10.1111/pce.12169
Wenig, M., Ghirardo, A., Sales, J. H., Pabst, E. S., Breitenbach, H. H., Antritter, F., Weber, B., Lange, B., Lenk, M., Cameron, R. K., Schnitzler, J.-P., & Vlot, A. C. (2019). Systemic acquired resistance networks amplify airborne defense cues. Nature Communications, 10(1), 3813. https://doi-org.ezproxy.lib.utah.edu/10.1038/s41467-019-11798-2
Ye, C., Liu, Y., Zhang, J., Li, T., Zhang, Y., Guo, C., Yang, M., He, X., Zhu, Y., Huang, H., & Zhu, S. (2021). Α-terpineol fumigation alleviates negative plant-soil feedbacks of Panax Notoginseng via suppressing Ascomycota and enriching antagonistic bacteria. Phytopathology Research, 3(1). https://doi.org/10.1186/s42483-021-00090-1
