Biology subjects

Waterman, J. M.

Publications and source records attributed to Waterman, J. M..

8 recordsLinked to original sources

bioRxiv2025

Quantitative modelling of biological response dynamics reveals novel patterns in plant volatile signalling

Biological responses to environmental stimuli are inherently dynamic. Recent technological advances enable detailed time-resolved measurements of such responses. However, a standard for quantitative characterisation of dynamics is lacking, thus limiting biological insights and comparisons. We developed an unbiased mathematical model structure that allows for the quantification of biological response curve dynamics without a priori knowledge of underlying biochemical mechanisms. Using the model to quantify the dynamics of stress-induced plant volatiles, we uncover a range of novel patterns in volatile signalling, including i) a strong light-independent impact of the time of day of wounding on the onset, duration and shape of the volatile induction responses, ii) an accentuation of volatile-specific induction curve shapes by herbivory-associated molecular patterns (HAMPs) and iii) independent regulation of the strength and duration of volatile induction across genotypes. The model performs well across biochemically diverse responses, suggesting broad applicability to inducible responses. The model is also robust to partial response curves, low resolution data and complex multi-modal responses arising from overlapping stimuli, enabling identification of priming events from otherwise convoluted curves. As all responses measured conform to a common model structure, yet parameter values diverge markedly, we conclude that biologically meaningful information is ignored when dynamics are not quantified. The presented approach will pave the way to identifying new biological response patterns, and their function, across the tree of life.

plant biology↗

bioRxiv2025

Volatile-suppressed peptide signaling enhances volatile responses in plant-plant interactions

Plant volatiles shape plant-plant interactions by acting as defense regulators and response factors. While plant volatile biosynthesis is well understood, how their emission is regulated remains largely elusive. Here, we show that small peptide signaling regulates induced volatile release in maize. Following herbivore attack, green leaf volatiles such as (Z)-3-hexenyl acetate (HAC) are released and induce terpene and indole emissions from neighboring plants. This process is accompanied by reduced expression of the ZmCLE1E9 gene and the ZmBAM1A, ZmBAM1B and ZmBAM3C receptor genes in HAC-exposed plants. Exogenous ZmCLE1E9 peptide inhibits HAC-triggered volatile release by limiting stomatal aperture. This inhibition disappears in the Zmbam1a/Zmbam1b/Zmbam3c triple mutant. Molecular docking supports ZmCLE1E9 and ZmBAMs as ligand-receptor pairs. Furthermore, Zmcle1e9 and Zmbams triple mutants show increased volatile emissions upon HAC exposure. In summary, we show that upon HAC perception, maize plants enhance their capacity to release terpenes and indole via the suppression of CLE1E9 signaling. This behavior allows maize plants to rapidly deploy volatile cues in response to stress volatiles and thus shape the infochemical dynamics of multitrophic environments.

plant biology↗

bioRxiv2024

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↗

bioRxiv2023

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↗

bioRxiv2023

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↗

bioRxiv2020

Exploring the role of life history traits and introduction effort in understanding invasion success in mammals: A case study of Barbary ground squirrels

Invasive species -species that have successfully overcome the barriers of transport, introduction, establishment, and spread- are a risk to biodiversity and ecosystem function. Introduction effort is one of the main factors underlying invasion success, but life history traits are also important as they influence population growth. In this contribution, we first investigated life history traits of the Barbary ground squirrel, Atlantoxerus getulus, a species with a very low introduction effort. We then studied if their invasion success was due to a very fast life history profile by comparing their life history traits to those of other successful invasive mammals. Next, we examined whether the number of founders and/or a fast life history influences the invasion success of squirrels. Barbary ground squirrels were on the fast end of the "fast-slow continuum", but their life history was not the only contributing factor to their invasion success, as the life history profile is comparable to other invasive species that do not have such a low introduction effort. We also found that neither life history traits nor the number of founders explained the invasion success of introduced squirrels in general. These results contradict the concept that introduction effort is the main factor explaining invasion success, especially in squirrels. Instead, we argue that invasion success can be influenced by multiple aspects of the new habitat or the biology of the introduced species.

ecology↗

bioRxiv2020

Evidence for an extreme founding effect in a highly successful invasive species

The adaptive potential of invasive species is thought to decrease during founding events due to reduced genetic diversity, limiting the new populations ability to colonize novel habitats. Barbary ground squirrels (Atlantoxerus getulus) were purportedly introduced as a single breeding pair to the island of Fuerteventura but have expanded to over a million individuals spread across the island in just over 50 years. We estimated the number of founders and measured the level of genetic diversity in this population using the mitochondrial displacement loop and microsatellite markers. Island samples (n = 19) showed no variation in the d-loop, suggesting a single founding female, while Moroccan samples (n = 6) each had unique mitochondrial haplotypes. The microsatellite data of the island population (n = 256 individuals) revealed a small effective population size, low levels of heterozygosity, and high levels of inbreeding, supporting a founding population size of two to three individuals. Our results suggest that A. getulus has undergone an intense genetic bottleneck during their colonization of the island. They are one of the few species where introduction effort does not explain invasion success, although further investigation may explain how they have avoided the worst expected effects following an extreme genetic bottleneck.

evolutionary biology↗

bioRxiv2020

Synchronizing vigilance or taking turns as sentinels? The importance of testing coordination

Coordinated behavior, such as hunting in lions and coordinated vigilance as antipredator behavior, are examples of benefits of group-living. Instead of asynchronous vigilance, some social species synchronize their vigilance bouts or take turns acting as sentinels. To increase our knowledge on the evolution of vigilance behavior, we studied whether vigilance is coordinated in Barbary ground squirrels, Atlantoxerus getulus. We show that vigilance was synchronized instead of taking turns. Multiple non-mutually exclusive hypotheses could explain synchronization: Barbary ground squirrels may perch because 1) neighbors are perched (copying effect), 2) perch synchrony may be an emergent property of the ecology as all squirrels may be satiated at the same time (collective behavior), or 3) the benefits are large in terms of evading ambush predators and scanning effectiveness (watch each others back). Particularly, in habitats where the field of view is obstructed by man-made structures and multiple individuals may be necessary to watch for terrestrial predators, synchronized vigilance may have greater fitness benefits than sentinel behavior. We conclude that it is essential to test assumptions of coordination and, thus, to analyze coordination to describe sentinel systems. Significance StatementVigilance behavior can be vital to an animals survival. Taking turns acting as sentinels or synchronizing vigilance bouts reduces the cost of the trade-off between feeding and predation risk. A sentinel system assumes that sentinels are vigilant from raised positions, warn group members of danger, and alternate vigilance bouts. However, the assumption of alternating vigilance bouts remains poorly tested. We tested this assumption in invasive Barbary ground squirrels. We found that instead of alternating, individuals synchronized their vigilance bouts. Perch synchrony may be 1) a response to perching group members (copying effect), 2) an emergent property of the species ecology, and 3) an adaptation to anthropogenically altered habitats (watch each others back).

animal behavior and cognition↗