quantifying-plant-soluble-protein-digestible-carbohydrate-content

Quantifying Plant Soluble Protein and Digestible Carbohydrate Content, Using Corn (<em>Zea mays</em>) As an Exemplar

Elemental data are commonly used to infer plant quality as a resource to herbivores. However, the ubiquity of carbon in biomolecules, the presence of ...

Texas A&M University

University of Minnesota

Interest in the field of epigenetics has increased rapidly over the last decade, with the term becoming more identifiable in biomedical research, scientific fields outside of the molecular sciences, such as ecology and physiology, and even mainstream culture. It has become increasingly clear, however, that different investigators ascribe different definitions to the term. Some employ epigenetics to explain changes in gene expression, others use it to refer to transgenerational effects and/or inherited expression states. This disagreement on a clear definition has made communication difficult, synthesis of epigenetic research across fields nearly impossible, and has in many ways biased methodologies and interpretations. This article discusses the history behind the multitude of definitions that have been employed since the conception of epigenetics, analyzes the components of these definitions, and offers solutions for clarifying the field and mitigating the problems that have arisen due to these definitional ambiguities. 

What do you mean, "epigenetic"?

Insect herbivores that ingest protein and carbohydrates in physiologically-optimal proportions and concentrations show superior performance and fitness. The first-ever study of protein-carbohydrate regulation in an insect herbivore was performed using the polyphagous agricultural pest Helicoverpa zea. In that study, experimental final instar caterpillars were presented two diets - one containing protein but no carbohydrates, the other containing carbohydrates but no protein - and allowed to self-select their protein-carbohydrate intake. The results showed that H. zea selected a diet with a protein-to-carbohydrate (p:c) ratio of 4:1. At about this same time, the geometric framework (GF) for the study of nutrition was introduced. The GF is now established as the most rigorous means to study nutrient regulation (in any animal). It has been used to study protein-carbohydrate regulation in several lepidopteran species, which exhibit a range of self-selected p:c ratios between 0.8 and 1.5. Given the economic importance of H. zea, and it is extremely protein-biased p:c ratio of 4:1 relative to those reported for other lepidopterans, we decided to revisit its protein-carbohydrate regulation. Our results, using the experimental approach of the GF, show that H. zea larvae self-select a p:c ratio of 1.6:1. This p:c ratio strongly matches that of its close relative, Heliothis virescens, and is more consistent with self-selected p:c ratios reported for other lepidopterans. Having accurate protein and carbohydrate regulation information for an insect herbivore pest such as H. zea is valuable for two reasons. First, it can be used to better understand feeding patterns in the field, which might lead to enhanced management. Second, it will allow researchers to develop rearing diets that more accurately reflect larval nutritional needs, which has important implications for resistance bioassays and other measures of physiological stress. 

Revisiting macronutrient regulation in the polyphagous herbivore Helicoverpa zea (Lepidoptera: Noctuidae): New insights via nutritional geometry.

The widespread global adoption of Bt crops elevates concerns about the evolution of Bt resistance in insect pest species. Current insecticide resistance management (IRM) strategies focus solely on genetic variation as a causal factor in the evolution of resistance, but ignore the role that environmental factors, such as nutrition, may play. In this opinion paper, we discuss the benefits that insect herbivores gain from consuming foods with protein-carbohydrate content that matches their self-selected protein-carbohydrate intake, and show that even within monocultures there is amply opportunity for insect herbivores to regulate their macronutrient intake. Next we review new data that show that dietary protein and carbohydrates can: firstly, have predictably strong effects on the survival and performance of caterpillars challenged with Bt toxins, and secondly, mediate plasticity in susceptibility to Cry1Ac, which can account for large differences in LC50 values. Nutrition-Bt interactions such as these have important implications for IRM, particularly given that diet-incorporated Bt bioassays commonly use artificial diets that vary substantially from their self-selected optimal diets, which likely results in underestimates of resistance in the field. Failing to bioassay larvae on ecologically-relevant diets can seriously confound the results of Bt resistance monitoring bioassays and undermine our ability to detect resistance in the field.

Nutrition as a neglected factor in insect herbivore susceptibility to Bt toxins.

Plant soluble protein and digestible carbohydrate content significantly affect insect herbivore fitness, but studies reporting plant protein and carbohydrate content are rare. Instead, the elements nitrogen and carbon often are used as surrogates for plant protein and digestible carbohydrate content, respectively. However, this is problematic for two reasons. First, carbon is found in all organic molecules, which precludes strong correlations with ecologically important dietary macronutrients (e.g., digestible carbohydrates, the primary energy source for most insect herbivores). Second, some elements (e.g., nitrogen) are present in both macronutrients (e.g., protein) and non-nutritive secondary compounds (e.g., alkaloids, protease inhibitors); in these cases N values would greatly overestimate protein available for an insect herbivore. Thus, the objective of this study was to explicitly document plant protein-carbohydrate content and assess its variation in cotton (Gossypium hirsutum and G. barbadense), which is a nutritional resource for a number of insect herbivores. We did this by measuring plant soluble protein (P) and digestible carbohydrate (C) content across seven plant tissues, five varieties, and two growing environments. Significant differences in P and C concentration, total macronutrient content (P + C), and P:C ratio were observed across plant tissues, plant age and environment; smaller differences were seen across plant genotype. Foliar tissues had higher total P + C content compared to reproductive tissues, except for developing seeds and developing flowers, which contained twice the total P + C content; these two tissues also had the highest P content. Our data show that even agricultural monocultures offer a highly heterogeneous protein-carbohydrate landscape for insect herbivores. Characterizing plant resources using nutritional currencies (e.g., protein and carbohydrates) that are ecologically and physiologically-relevant to insect herbivores can be used to enhance our understanding of plant-insect interactions.

Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar.

Pesticide resistance represents a major challenge to global food production. The spread of resistance alleles is the primary explanation for observations of reduced pesticide efficacy over time, but the potential for gene-by-environment interactions (plasticity) to mediate susceptibility has largely been overlooked. Here we show that nutrition is an environmental factor that affects susceptibility to Bt toxins. Protein and carbohydrates are two key macronutrients for insect herbivores, and the polyphagous pest Helicoverpa zea self-selects and performs best on diets that are protein-biased relative to carbohydrates. Despite this, most Bt bioassays employ carbohydrate-biased rearing diets. This study explored the effect of diet protein-carbohydrate content on H. zea susceptibility to Cry1Ac, a common Bt endotoxin. We detected a 100-fold increase in LC for larvae on optimal versus carbohydrate-biased diets, and significant diet-mediated variation in survival and performance when challenged with Cry1Ac. Our results suggest that Bt resistance bioassays that use ecologically- and physiologically-mismatched diets over-estimate susceptibility and under-estimate resistance.

Article	Year
What do you mean, "epigenetic"? Genetics\| PubMed ID: 25855649	2015
Revisiting macronutrient regulation in the polyphagous herbivore Helicoverpa zea (Lepidoptera: Noctuidae): New insights via nutritional geometry. Journal of insect physiology\| PubMed ID: 26141409	2015
Nutrition as a neglected factor in insect herbivore susceptibility to Bt toxins. Current opinion in insect science\| PubMed ID: 27436738	2016
Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar. Journal of chemical ecology\| PubMed ID: 27738861	2016
Nutrition affects insect susceptibility to Bt toxins. Scientific reports\| PubMed ID: 28045087	2017

Carrie A. Deans

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