In this post, Pablo Urbaneja-Bernat, tenure track at Institute of Agrifood Research and Technology (Spain), presents his work ‘Not just candy: A herbivore-induced defense-related plant protein in honeydew enhances natural enemy fitness’. He talks about unexpected interactions in ecological communities, the application of ecological research to agricultural management and the importance of inclusivity to overcome the many challenges in the path of research.
About the paper
The paper explores the tri-trophic interaction between an herbivore, its natural enemy, and plant defenses. Specifically, it examines how herbivore-induced plant proteins affect these interactions. Contrary to conventional understanding, our research demonstrates that honeydew from the herbivore contains proteins with high nutritional value for its natural enemy. Additionally, among all the proteins identified, we found that superoxide dismutase (SOD), a protein related to plant defenses, is a common component in the honeydew of all tested phloem feeders.
The background of our paper focuses on the interactions within a tri-trophic system involving plant-derived food sources, herbivores, and their natural enemies. While it is well understood that herbivore-induced plant defenses primarily serve to deter herbivores and protect the plant, the effects these defenses have on honeydew and its specific components have not been thoroughly investigated. Our research aims to fill this gap by identifying proteins related to plant defenses, such as superoxide dismutase (SOD), in the honeydew. This provides new insights into the nutritional dynamics within this tri-trophic interaction.
The idea for this research emerged during my first postdoctoral study in the professor Alejandro Tena’s lab at IVIA, Spain. We were investigating the honeydew of the HLB vector, Trioza erytreae, and its impact on the fitness and parasitism of its main parasitoid, Tamarixia dryi (Urbaneja-Bernat et al., 2023). Our findings showed that parasitic wasps feeding on honeydew experienced a significant increase in fitness (longevity and egg load) compared to those on control diets with sugar and protein. Additionally, these honeydew-fed wasps exhibited a higher tendency to parasitize compared to those fed on other food sources. To our knowledge, this latter result had not been previously reported for any parasitoid species. Encouraged by these findings, we initiated studies with the primary subjects of this paper, the mealybug Planococcus citri and its primary parasitoid Anagyrus vladimiri, where we observed similar outcomes. These results prompted us to further investigate the topic, with a specific focus on the protein content of the honeydew.
Our research shows, for the first time, that plant proteins induced after herbivory accumulate in honeydew and are responsible of the increased fitness (longevity and fecundity) of natural enemies that feed on it. Proteomic and enzymatic analysis of honeydew demonstrated that a defense-plant protein, SOD, was present in the honeydew of the seven phloem-feeding insect species evaluated in this study. One of these proteins was also overexpressed in the phloem of infested plants, and its addition to a sugar-based diet increased the longevity and fecundity of natural enemy that feed on it.
Our paper is particularly relevant to entomologists, ecologists, and agricultural scientists who are focused on insect behavior, tri-trophic interactions, and IPM strategies. Additionally, biochemists interested in plant defenses and the biochemical composition of honeydew will find valuable insights. Environmental scientists studying the ecological impacts of agricultural practices, as well as policy makers and extension agents promoting sustainable agriculture, will also benefit from understanding the potential of natural enemies in pest control. Graduate students and academics seeking to expand their knowledge in these areas are encouraged to read our findings.
About the research
The broader impact of our paper lies in its potential to enhance biological control by improving the nutritional quality of honeydew, thereby increasing the effectiveness of natural enemies in pest management. Our findings highlight the role of plant defense proteins, such as superoxide dismutase (SOD), in supporting natural enemies, which could inspire new research in plant breeding and genetic engineering. Additionally, understanding these nutritional dynamics can provide insights into ecosystem functioning and contribute to the conservation of beneficial insects and biodiversity. By bridging multiple disciplines, our study encourages interdisciplinary research and offers a foundation for sustainable agriculture and ecosystem management.
We were indeed surprised by the findings during our research. One of the most unexpected results was the significant enhancement in the fecundity of the parasitoid Anagyrus vladimiri when fed on honeydew from the mealybug Planococcus citri. This was contrary to the conventional understanding that honeydew primarily serves as a carbohydrate source with limited nutritional value. Additionally, the discovery that honeydew contains proteins related to plant defenses, such as superoxide dismutase (SOD), and that these proteins can positively impact the fitness of natural enemies was quite surprising. This finding challenges the traditional view of plant-herbivore-natural enemy interactions and opens new avenues for understanding the nutritional dynamics within these complex ecological relationships.
Several big questions remain following our study, including understanding the mechanisms of protein transfer from plant phloem to honeydew, identifying a broader range of beneficial proteins, and determining if these effects extend to other natural enemies. Additionally, exploring the evolutionary dynamics of these interactions, translating laboratory findings to field applications, and investigating the potential for plant breeding and genetic engineering to enhance honeydew quality are crucial. Finally, understanding the broader ecological consequences and interactions with other plant defenses will provide a more comprehensive view of these complex tri-trophic relationships.
The next steps in this field should focus on investigating the biochemical pathways that transfer plant defense proteins to honeydew, conducting comprehensive proteomic analyses across various plant-insect systems, and validating these findings in field applications. Additionally, exploring genetic and breeding approaches to enhance beneficial protein production in plants, assessing the broader ecological impacts, studying the co-evolutionary dynamics, and understanding interactions with other plant defenses will provide a more holistic view of these complex tri-trophic relationships and improve sustainable pest control methods.
Schematic diagram summarizing key findings of our study (Credit: Lindsay Erndwein and the authors)
About The Author
My journey into ecology starts during my undergraduate studies in Entomology, field research projects allowed me to observe ecological processes firsthand, deepening my interest in plant-insect interactions and the role of natural enemies in regulating herbivore populations. This passion continued through my PhD, where I focused on tri-trophic interactions, highlighting the practical applications of ecological knowledge in sustainable agriculture and pest management. Also, during my postdoc with the professor Cesar Rodriguez-Saona’s lab I was deeply involved in chemical ecology driven by a desire to understand and contribute to the conservation and sustainable management of ecosystems. I am currently a tenure track researcher at IRTA (Institute of Agrifood Research and Technology) in Spain.
My greatest scientific inspiration comes from the intricate and dynamic relationships within ecosystems, especially the interactions between plants, herbivores, and their natural enemies. Additionally, my mentors and colleagues, who have guided and collaborated with me throughout my academic journey, have continually inspired me to delve deeper into the study of chemical and ecology, and contribute to the field with innovative and impactful research.
Like many in the scientific community, I have encountered several barriers in my career. One of the most significant challenges has been securing consistent funding for research. The competitive nature of grant applications and the limited availability of resources can make it difficult to sustain long-term projects and explore innovative ideas. Additionally, navigating the academic jobs can be challenging, with a limited number of positions available relative to the number of qualified candidates. Despite these obstacles, I have been fortunate to receive support and mentorship from colleagues and institutions that value diversity and innovation. This support has been crucial in overcoming barriers and continuing to pursue my passion for scientific research. Moving forward, I am committed to contributing to a more inclusive scientific community and advocating for policies and practices that support equitable opportunities for all researchers.
One piece of advice I would offer to someone in the field of ecology is to embrace interdisciplinary collaboration. Ecology is inherently a multidisciplinary science, and the most impactful research often comes from integrating knowledge and techniques from various fields such as genetics, chemistry, data science, and environmental policy. Building a diverse network of collaborators can provide new perspectives, enhance the robustness of your research, and open opportunities for innovative solutions to complex ecological problems. Additionally, stay curious and passionate about your work, as this will drive you to continually learn and adapt in this ever-evolving field.
Like the blog post? Read the paper here.
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