| Title: | A persistent major mutation in canonical jasmonate signaling is embedded in an herbivory-elicited gene network |
| Author(s): | Ray R; Halitschke R; Gase K; Leddy SM; Schuman MC; Rodde N; Baldwin IT; |
| Address: | "Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14850. Department of Geography, University of Zurich, 8006 Zurich, Switzerland. Department of Chemistry, University of Zurich, 8006 Zurich, Switzerland. Institut national de recherche pour l'agriculture, l'alimentation et l'environnement, Centre National de Resources Genomiques Vegetales, French Plant Genomic Resource Center, Castanet Tolosan F-31326, France" |
| ISSN/ISBN: | 1091-6490 (Electronic) 0027-8424 (Print) 0027-8424 (Linking) |
| Abstract: | "When insect herbivores attack plants, elicitors from oral secretions and regurgitants (OS) enter wounds during feeding, eliciting defense responses. These generally require plant jasmonate (JA) signaling, specifically, a jasmonoyl-L-isoleucine (JA-Ile) burst, for their activation and are well studied in the native tobacco Nicotiana attenuata. We used intraspecific diversity captured in a 26-parent MAGIC population planted in nature and an updated genome assembly to impute natural variation in the OS-elicited JA-Ile burst linked to a mutation in the JA-Ile biosynthetic gene NaJAR4. Experiments revealed that NaJAR4 variants were associated with higher fitness in the absence of herbivores but compromised foliar defenses, with two NaJAR homologues (4 and 6) complementing each other spatially and temporally. From decade-long seed collections of natural populations, we uncovered enzymatically inactive variants occurring at variable frequencies, consistent with a balancing selection regime maintaining variants. Integrative analyses of OS-induced transcriptomes and metabolomes of natural accessions revealed that NaJAR4 is embedded in a nonlinear complex gene coexpression network orchestrating responses to OS, which we tested by silencing four hub genes in two connected coexpressed networks and examining their OS-elicited metabolic responses. Lines silenced in two hub genes (NaGLR and NaFB67) co-occurring in the NaJAR4/6 module showed responses proportional to JA-Ile accumulations; two from an adjacent module (NaERF and NaFB61) had constitutively expressed defenses with high resistance. We infer that mutations with large fitness consequences can persist in natural populations due to compensatory responses from gene networks, which allow for diversification in conserved signaling pathways and are generally consistent with predictions of an omnigene model" |
| Keywords: | *Gene Regulatory Networks *Herbivory/genetics Mutation MAGIC populations NaJAR4 jasmonate signaling natural mutations with large fitness effects plant defense; |
| Notes: | "MedlineRay, Rishav Halitschke, Rayko Gase, Klaus Leddy, Sabrina M Schuman, Meredith C Rodde, Nathalie Baldwin, Ian T eng Research Support, Non-U.S. Gov't 2023/08/22 Proc Natl Acad Sci U S A. 2023 Aug 29; 120(35):e2308500120. doi: 10.1073/pnas.2308500120. Epub 2023 Aug 22" |
