Comparative analyses of responses to exogenous and endogenous antiherbivore elicitors enable a forward genetics approach to identify maize gene candidates mediating sensitivity to herbivore‐associated molecular patterns

Abstract

SUMMARY Crop damage by herbivorous insects remains a significant contributor to annual yield reductions. Following attack, maize (Zea mays) responds to herbivore‐associated molecular patterns (HAMPs) and damage‐associated molecular patterns (DAMPs), activating dynamic direct and indirect antiherbivore defense responses. To define underlying signaling processes, comparative analyses between plant elicitor peptide (Pep) DAMPs and fatty acid–amino acid conjugate (FAC) HAMPs were conducted. RNA sequencing analysis of early transcriptional changes following Pep and FAC treatments revealed quantitative differences in the strength of response yet a high degree of qualitative similarity, providing evidence for shared signaling pathways. In further comparisons of FAC and Pep responses across diverse maize inbred lines, we identified Mo17 as part of a small subset of lines displaying selective FAC insensitivity. Genetic mapping for FAC sensitivity using the intermated B73 × Mo17 population identified a single locus on chromosome 4 associated with FAC sensitivity. Pursuit of multiple fine‐mapping approaches further narrowed the locus to 19 candidate genes. The top candidate gene identified, termed FAC SENSITIVITY ASSOCIATED (ZmFACS), encodes a leucine‐rich repeat receptor‐like kinase (LRR‐RLK) that belongs to the same family as a rice (Oryza sativa) receptor gene previously associated with the activation of induced responses to diverse Lepidoptera. Consistent with reduced sensitivity, ZmFACS expression was significantly lower in Mo17 as compared to B73. Transient heterologous expression of ZmFACS in Nicotiana benthamiana resulted in a significantly increased FAC‐elicited response. Together, our results provide useful resources for studying early elicitor‐induced antiherbivore responses in maize and approaches to discover gene candidates underlying HAMP sensitivity in grain crops.

Influence of plant defense signaling and innate insect metabolic differences to the overall performance of fall armyworm (Spodoptera frugiperda) corn and rice strains on maize as a host

“…The putative switchgrass ( Panicum virgatum L.) homolog of AtWRKY72 was previously reported to be up-regulated in response to FAW feeding in two types of cultivars tested (Palmer et al 2019). Furthermore, Zm00001d039532 ( ZmWRKY56 in maize GDB, Arabidopsis ortholog AtWRKY72 ) and Zm00001d010399 ( ZmWRKY92 in maize GDB, Arabidopsis ortholog AtWRKY33 ) were recently reported to be up-regulated in response to Zmpep3 treatment along with a host of other ZmWRKY s that were induced (Poretsky et al 2021). In our experiments, Zm00001d017444 ( ZmWRKY128 in maize GDB, Arabidopsis ortholog AtWRKY12 ) and Zm00001d039532 were significantly up-regulated in the leaves subject to corn strain feeding, but only weakly induced in leaves subject to rice strain feeding.…”

Volatile uptake, transport, perception, and signaling shape a plant’s nose

“…Another Arabidopsis lectin receptor kinase LecRK-I.8 is critical for the defense triggered by phosphatidylcholines primarily with C16- to C18-fatty acyl chains [ 34 ]. The maize ZmFACS protein, a leucine-rich repeat (LRR) receptor kinase, mediates defense triggered by the fatty acid–amino acid conjugates (FACs) [ 35 ]. GLVs, as fatty acid derivatives, share certain biochemical properties with the molecular patterns mentioned above.…”

Immature leaves are the dominant volatile sensing organs of maize

“…Danger cues can be translocated as signals via the vasculature or as volatiles via the air The perception of danger signals then triggers anti-herbivore defenses via activation of the jasmonate signaling pathway (Howe and Jander, 2008; Erb et al, 2012). Recent years have seen considerable advances in understanding herbivory-derived cues as well as vascular and volatile defense signaling (Hu et al, 2019; Ye et al, 2019; Steinbrenner et al, 2020; Poretsky et al, 2021). However, how plants perceive volatile danger cues is still poorly understood.…”