Complexity Untangled: For Plant Defenses, Pest Attack Order Matters
By Saumik Basu, Ph.D.
The order of arrival and feeding of different insect pests impact a plant’s ability to fight back by altering its defense response and nutritional quality. My colleagues and I have unfolded the complexity of these interactions in our research to understand potential implications in pest control strategies.
The Palouse region of eastern Washington and northern Idaho is home for cultivation of cool-season legumes such as peas, lentils, chickpeas, and fava beans. A piercing-sucking vector herbivore, pea aphid (Acyrthosiphon pisum) and an aphid-borne pathogen, pea enation mosaic virus (PEMV), have long worried farmers in the Palouse with crop yield loss ranging from 30–40 percent and major outbreaks of pea aphids reported every 6–9 years. In addition to the pea aphid-PEMV mediated pathosystem, a more innocuous-seeming, chewing, non-vector herbivore, the pea leaf weevil (Sitona lineatus), takes tiny feeding bites from pea leaves and has also been found to significantly affect plant susceptibility. These organisms co-occur in the Palouse region, and interactions between them can affect plant signaling pathways and nutritional status.
Pea leaf weevil adults overwinter outside of pea fields and migrate into fields in the late spring to lay eggs. After hatching of eggs, larvae burrow into the soil to feed and pupate before adults re-emerge in the summer and continue feeding on peas. First-generation pea leaf weevil adults typically attack plants before arrival of pea aphids and PEMV, but second-generation pea leaf weevils typically attack plants after pea aphid and PEMV have arrived. However, the responses of pea plants based on the number of stressors and their order of attack and the underlying molecular mechanisms that mediate these interactions are largely unknown.
Many studies have already investigated the effects of single pest on plants. But managing multiple pests concurrently is highly challenging. Our recent study published in August in Molecular Ecology is among the few published works that investigate complex plant-mediated interactions of multiple biotic stressors. To better understand plant responses to multiple stressors and to assess how these responses are affected by order of arrival of stressors and food web complexity, we investigated the response of pea plants to various attack sequences from these two pests and PEMV.
In a series of greenhouse experiments performed in collaboration with colleagues at Washington State University and Cornell University, we investigated what happens to pea plants when they face different sequences of pest attacks and virus exposure. We created experiments in which weevils and then pea aphids feasted on pea plants, and we contrasted the results with the reverse attack order. We also included scenarios where some pea plants were infected with PEMV while others remained uninfected. After removing the pests, we let the plants grow, and then we measured the plant’s defense phytohormone levels, expressions of associated defense genes, and nutritional status.
We found that, when pea leaf weevils feast on peas first, it enhances some of the anti-pathogen defense responses of the pea plants, helping them to become more resilient to PEMV infection. But, when the weevilsdine after the aphids, it lowers the anti-pathogen defenses, allowing the virus to spread more easily. In turn, PEMV-infected plants had stronger anti-herbivore defense responses, since they induce production of compounds that interfere with the pest feeding. Further complicating the issue, we also found in this study that, when weevils induced anti-pathogen defense responses, the nutritional quality of pea plants was lowered by decreasing the plant’s available amino acids.
We strongly believe that these complex interactions convey important implications to design sustainable pest- and pathogen-management strategies. If we know beforehand when these interactions are happening, that information will give farmers a best possible remedy to prevent their fields from these attacks by choosing proper timing, using appropriate pest control agents, and controlling the pests during the most susceptible stage of their life cycles. While using broad spectrum insecticides (e.g., pyrethroids) may enhance pest management efficiency against multiple pests in different attack orders, this approach comes with problems associated with non-target insects. Better understanding of the dynamics of pest-attack orders, however, can allow for more effective use of targeted approaches, such as biological control agents (e.g., lady beetles); pesticides that are less harmful to natural enemies, non-target insects, and pollinators; and biofertilizers (e.g., soil mutualistic rhizobia).
This study is a part of our ongoing series of investigations to assess complex interactions among many organisms that a plant may encounter in a food web ecosystem. Our earlier study published in May in Functional Ecology investigated the antagonistic relationship between PEMV and a root-colonizing and nitrogen-fixing bacteria called rhizobia. Our next study in this series looks at the interactions between the pea leaf weevil and soil rhizobia.
These complex relationships of multiple biotic stressors are crucial to understanding how plants respond to these attackers and are critical for developing sustainable management strategies against devastating pests and pathogens to boost crop yield and agroeconomy.
Saumik Basu, Ph.D., is a postdoctoral research associate in the Department of Entomology at Washington State University in Pullman, Washington. Email: firstname.lastname@example.org.