A persistent major mutation in canonical jasmonate signaling is embedded in an herbivory-elicited gene network

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.

The Key Role of Plant Hormone Signaling Transduction and Flavonoid Biosynthesis Pathways in the Response of Chinese Pine (Pinus tabuliformis) to Feeding Stimulation by Pine Caterpillar (Dendrolimus tabulaeformis)

“…Because mechanical damage alone is insufficient to induce a complete response, and the elicitors present in oral secretions can enhance this response, the application of oral secretions (OSs) to tobacco plants grown in the field triggers an outbreak of JA-Ile [ 26 ]. Thus, during the induction of plant resistance, certain substances are expressed in the early stage to act on oxidative stress, leading to the formation of resistance.…”

Phytohormones in a universe of regulatory metabolites: lessons from jasmonate

“…JAR1 is a member of the GH3 family of acyl acid amido synthetases, which conjugate amino acids to many phytohormones and likely other regulatory metabolites as well ( Staswick and Tiryaki 2004 ; Westfall et al 2012 ). Interestingly, a natural sequence polymorphism abrogating the expression of JAR1 accounts for much of the variation in induced defense responses within wild populations of Nicotiana attenuata ( Ray et al 2023 ).…”

Prezygotic mate selection is only partially correlated with the expression of NaS‐like RNases and affects offspring phenotypes

“…Selected recombinant inbred lines (RILs) of a 26-parent Multiparent Advanced Generation Inter-Cross (MAGIC) population were used, including one replicate of the entire population (650 lines). The population is 99% homozygous and has minimal population structure and high phenotypic and genetic diversity (Ray et al, 2023). Additionally, a UtWT inbred line silenced in the expression of NaS-like-RNase1 (irSL-R1/UT, pSOL8SRN1, A-17-091-7), and an AzWT inbred line silenced in the expression of NaS-like-RNase2 (irSLR2/AZ, pSOL8SRN2, A-17-059-6; Guo et al, 2019) were used.…”