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Abstract Plants produce defensive toxins to deter herbivores. In response, some specialized herbivores evolved resistance and even the capacity to sequester toxins, affecting interactions at higher trophic levels. Here, we test the hypothesis that potential natural enemies of specialized herbivores are differentially affected by plant toxins depending on their level of adaptation to the plant-herbivore system. We focus on toxic cardiac glycosides (CGs) from milkweeds (Asclepiasspp.), which inhibit animal Na⁺/K⁺-ATPases, and two CG-resistant insects, the large milkweed bugOncopeltus fasciatusand a CRISPR-editedDrosophila melanogaster. Both have CG-resistant Na⁺/K⁺-ATPases through a set of key amino acid substitutions, which facilitate CG sequestration. We conducted infection experiments with entomopathogenic nematodes (Steinernema carpocapsae,S. feltiae, andS. hermaphroditum) as natural enemies on host insects containing mixtures of milkweed-derived CGs or purified CGs (ouabain, digoxin, and digitoxin) that vary in toxicity. The nematodeS. carpocapsaeis known to occur in soil near milkweed plants and naturally has several of the same Na⁺/K⁺-ATPase substitutions as the milkweed bugO. fasciatusand ourDrosophilamutant. This nematode not only exhibited higher fecundity in hosts that carried CGs relative to the other nematode species (which have sensitive Na⁺/K⁺-ATPases), but also showed attraction to mixtures of CGs in milkweed root extracts and to purified ouabain when tested on agar plates. A coiling phenotype, which is a symptom of neurotoxicity, was observed more frequently inS. feltiaeandS. hermaphroditumupon exposure to milkweed root extracts than inS. carpocapsae. Nematode behavior was further tested in sand, and while attraction to CGs was found forS. carpocapsae, nematodes of the other species tended to migrate away from milkweed root chemicals. Thus,S. carpocapsaecan tolerate CGs and may use these as chemical cues to locate insect hosts that live on or around milkweed plants. 

Populations can adapt to stressful environments through changes in gene expression. However, the fitness effect of gene expression in mediating stress response and adaptation remains largely unexplored. Here, we use an integrative field dataset obtained from 780 plants of Oryza sativa ssp. indica (rice) grown in a field experiment under normal or moderate salt stress conditions to examine selection and evolution of gene expression variation under salinity stress conditions. We find that salinity stress induces increased selective pressure on gene expression. Further, we show that trans-eQTLs rather than cis-eQTLs are primarily associated with rice’s gene expression under salinity stress, potentially via a few master-regulators. Importantly, and contrary to the expectations, we find that cis-trans reinforcement is more common than cis-trans compensation which may be reflective of rice diversification subsequent to domestication. We further identify genetic fixation as the likely mechanism underlying this compensation/reinforcement. Additionally, we show that cis- and trans-eQTLs are under balancing and purifying selection, respectively, giving us insights into the evolutionary dynamics of gene expression variation. By examining genomic, transcriptomic, and phenotypic variation across a rice population, we gain insights into the molecular and genetic landscape underlying adaptive salinity stress responses, which is relevant for other crops and other stresses. 

Different plant species within the grasses were parallel targets of domestication, giving rise to crops with distinct evolutionary histories and traits1. Key traits that distinguish these species are mediated by specialized cell types2. Here, we compare the transcriptomes of root cells in three grass species—Zea mays (maize), Sorghum bicolor (sorghum), and Setaria viridis (Setaria). We first show that single-cell and single-nucleus RNA-seq provide complementary readouts of cell identity in both dicots and monocots, warranting a combined analysis. Cell types were mapped across species to identify robust, orthologous marker genes. The comparative cellular analysis shows that the transcriptomes of some cell types diverged more rapidly than others—driven, in part, by recruitment of gene modules from other cell types. The data also show that a recent whole genome duplication provides a rich source of new, highly localized gene expression domains that favor fast-evolving cell types. Together, the cell-by-cell comparative analysis shows how fine-scale cellular profiling can extract conserved modules from a pan transcriptome and shed light on the evolution of cells that mediate key functions in crops.