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Cofer, T. M.

Publications and source records attributed to Cofer, T. M..

6 recordsLinked to original sources

Rapid green leaf volatile sensing allows intact plants to release induced volatiles earlier than wounded emitters

Organisms in the vicinity of attacked neighbors can respond to danger cues by activating their own defenses. However, the temporal dynamics of these interactions remain poorly resolved, despite their importance for the ensuing effects. Here, we investigated defense responses of maize plants that are exposed to induced volatiles from herbivory-induced neighbors in real time. These experiments revealed a surprising temporal paradox: Intact neighbors start emitting most induced volatiles 15-80 min earlier than the attacked plants themselves. This earlier responsiveness was not associated with earlier induction of defense hormones, volatile biosynthesis genes or within-leaf volatile accumulation. Instead, receiver plants kept their stomata open, while attacked sender plants rapidly closed them to combat water loss. Using different volatile deficient mutants, we demonstrate that the rapid responses in receivers are triggered by green leaf volatiles, which are released from the wound sites of sender plants within minutes independently of stomatal aperture. Thus, non-attacked neighbors can act as "unhindered observers" that activate some defenses more quickly than attacked organisms themselves, as they do not have to deal with wound trauma. The resulting plant volatile concatenation patterns expand our understanding of volatile signaling and have the potential to shape population-level multitrophic interactions.

plant biology↗

Leaf size determines damage- and herbivore-induced volatile emissions in maize

Stress-induced plant volatiles play an important role in mediating ecological interactions between plants and their environment. The timing and location of the inflicted damage is known to influence the quality and quantity of induced volatile emissions. However, how leaf characteristics and herbivore feeding behavior interact to shape volatile emissions is not well understood. Using a high-throughput volatile profiling system with high temporal resolution, we examined how mechanical damage and herbivore feeding on different leaves shapes plant-level volatile emission patterns in maize. We then tested feeding patterns and resulting consequences on volatile emissions with two generalist herbivores (Spodoptera exigua and Spodoptera littoralis), and assessed whether feeding preferences are associated with enhanced herbivore performance. We found maize seedlings emit more volatiles when larger leaves are damaged. Larger leaves emitted more volatiles locally, which was the determining factor for higher plant-level emissions. Surprisingly, both S. exigua and S. littoralis preferentially consumed larger leaves, and thus maximize plant volatile emission without apparent growth benefits. Together, these findings provide an ecophysiological and behavioral mechanism for plant volatile emission patterns, with potentially important implications for volatile-mediated plant-environment interactions.

plant biology↗

Insects visit Fusarium xyrophilum pseudoflowers on the host Xyris surinamensis (Xyridaceae) and carry fungal DNA on their bodies

The fungus Fusarium xyrophilum produces flower-like structures (i.e., pseudoflowers) that were recently discovered on yellow-eyed grasses (Xyris spp.) in Guyana. It is unknown whether these pseudoflowers, which are composed entirely of fungal tissue, are true mimics that attract insects as a means of fungal dispersal. We evaluated the potential of F. xyrophilum to affect insect visitation patterns to flowers and pseudoflowers by 1) documenting insect visitation to X. surinamensis in Guyana, 2) measuring the presence of F. xyrophilum DNA on insects, and 3) evaluating fluorescence and volatile production on flowers and pseudoflowers. We report for the first time Vespidae, Formicidae, Salticidae, Acrididae, and Tetrigidae visiting Xyris. Diverse insects, including Conocephalini spp. (meadow katydids; Tettigoniidae), Camponotus spp. (carpenter ants; Formicidae), and a Geometridae sp. (geometer moths) were found to visit flowers and pseudoflowers. Fusarium xyrophilum DNA was detected on 3/12 (25%) of captured insect bodies using conventional and quantitative PCR. Volatiles produced in the field by pseudoflowers and flowers were similar, except for the presence of a sesquiterpene, putatively identified here as -gurjunene, which was detected both in F. xyrophilum pure cultures and field-collected pseudoflower samples, but not from flowers. The production of this sesquiterpene by F. xyrophilum and the fluorescence of X. surinamensis peduncles represent potential signals involved in insect attraction for this system. These observations, along with the overlap in insect visitors of flowers and pseudoflowers and the detection of F. xyrophilum DNA on insect bodies, are consistent with insect visitors being vectors of Xyris pollen and F. xyrophilum propagules between host plants.

ecology↗

High-resolution kinetics of herbivore-induced plant volatile transfer reveal tightly clocked responses in neighboring plants

Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), with important consequences for community dynamics. However, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high- throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day : night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.

plant biology↗

The Arabidopsis thaliana carboxylesterase AtCXE12 converts volatile (Z)-3-hexenyl acetate to (Z)-3-hexenol

The green leaf volatiles (Z)-3-hexenal, (Z)-3-hexenol, and (Z)-3-hexenyl acetate are produced by nearly all plants in response to wounding and insect attack, can be transferred between plants, metabolized, and act as defense cues. If and how plant leaves convert exogenous (Z)-3-hexenyl acetate to (Z)-3-hexenol is unknown. We show that Arabidopsis leaves rapidly convert exogenous (Z)-3-hexenyl acetate to (Z)-3-hexenol. Inhibitor and fractionation experiments identified the carboxylesterases AtCXE5 and AtCXE12 as likely contributors to (Z)-3-hexenyl acetate esterase activity in Arabidopsis leaves. Heterologous expression of AtCXE5 and AtCXE12 revealed that both enzymes hydrolyze (Z)-3-hexenyl acetate to (Z)-3-hexenol in vitro, and assays using T-DNA insertion mutant plants showed that AtCXE12 significantly contributes to the conversion of (Z)-3-hexenyl acetate to (Z)-3-hexenol in planta. Lastly, we found that leaves from several other plant species possess (Z)-3-hexenyl acetate esterase activity, as well as homologs of AtCXE5 and AtCXE12 from Arabidopsis. Collectively, our study provides a better understanding of green leaf volatile biosynthesis and conversion dynamics, necessary for unraveling the potential functions of these compounds.

plant biology↗

Immature leaves are the dominant volatile (Z)-3-hexenyl acetate sensing organs of maize

Plants perceive herbivory induced volatiles and respond to them by upregulating their defenses. So far, the organs responsible for volatile perception remain poorly described. Here, we show that responsiveness to the herbivory induced green leaf volatile (Z)-3-hexenyl acetate (HAC) in terms of volatile emission, transcriptional regulation and defense hormone activation is largely constrained to younger maize leaves. Older leaves are much less sensitive to HAC. In a given leaf, responsiveness to HAC is high at immature developmental stages and drops off rapidly during maturation. Responsiveness to the non-volatile elicitor ZmPep3 shows an opposite pattern, demonstrating that hyposmia is not driven by defective canonical defense signaling. Neither stomatal conductance nor leaf cuticle composition explain the unresponsiveness of older leaves to HAC, suggesting perception mechanisms upstream of canonical defense signaling as driving factors. Finally, we show that hyposmia in older leaves is not restricted to HAC, and extends to the full blend of herbivory induced volatiles. In conclusion, our work identifies immature maize leaves as dominant stress volatile sensing organs. The tight spatiotemporal control of volatile perception may facilitate within-plant defense signaling to protect young leaves, and may allow plants with complex architectures to explore the dynamic odor landscapes at the outer periphery of their shoots.

plant biology↗