How megadrought causes extensive mortality in a deep-rooted shrub species normally resistant to drought-induced dieback: The role of a biotic mortality agent.

Southern California experienced unprecedented megadrought between 2012 and 2018. During this time, Malosma laurina, a chaparral species normally resilient to single-year intense drought, developed extensive mortality exceeding 60% throughout low-elevation coastal populations of the Santa Monica Mountains. We assessed the physiological mechanisms by which the advent of megadrought predisposed M. laurina to extensive shoot dieback and whole-plant death. We found that hydraulic conductance of stem xylem (Ks, native ) was reduced seven to 11-fold in dieback adult and resprout branches, respectively. Staining of stem xylem vessels revealed that dieback plants experienced 68% solid-blockage, explaining the reduction in water transport. Following Koch's postulates, persistent isolation of a microorganism in stem xylem of dieback plants but not healthy controls indicated that the causative agent of xylem blockage was an opportunistic endophytic fungus, Botryosphaeria dothidea. We inoculated healthy M. laurina saplings with fungal isolates and compared hyphal elongation rates under well-watered, water-deficit, and carbon-deficit treatments. Relative to controls, we found that both water deficit and carbon-deficit increased hyphal extension rates and the incidence of shoot dieback.

Plant communication across different environmental contexts suggests a role for stomata in volatile perception.

Plants can detect herbivore-induced plant volatiles (HIPVs) from their damaged neighbours and respond by enhancing or priming their defenses against future herbivore attack. Plant communication and defense priming by volatile cues has been well documented, however, the extent to which plants are able to perceive and respond to these cues across different environmental contexts remains poorly understood. We investigated how abiotic changes that modulate stomatal conductance and/or defense signalling affect the ability of maize plants to perceive HIPVs and respond by priming their defenses. During light exposure, when stomata were open and conditions allowed for defense signal biosynthesis, the individual compounds indole and (Z)-3-hexenyl acetate primed maize defenses. Neither compound primed defenses under environmental conditions that closed stomata and/or altered defense signalling. Moreover, plants were not primed when exposed to indole or (Z)-3-hexenyl acetate in darkness (while stomata were closed) and then subjected to simulated herbivory in the light, to ensure defense induction. The full blend of HIPVs primed maize defenses in light conditions but suppressed defense induction during dark exposure and wounding. These findings indicate that environmental context is important for plant communication and defense priming and suggest that stomata play a role in plant perception of HIPVs.

A Beneficial Plant-Associated Fungus Shifts the Balance toward Plant Growth over Resistance, Increasing Cucumber Tolerance to Root Herbivory.

Plants allocate their limited resources toward different physiological processes, dynamically adjusting their resource allocation in response to environmental changes. How beneficial plant-associated microbes influence this allocation is a topic that continues to interest plant biologists. In this study, we examined the effect of a beneficial fungus, Phialemonium inflatum, on investment in growth and anti-herbivore resistance traits in cucumber plants (Cucumis sativus). We inoculated cucumber seeds with P. inflatum spores and measured several growth parameters, including germination rate, above and belowground biomass, and number of flowers. We also examined plant resistance to adult and larval striped cucumber beetles (Acalymma vitattum), and quantified levels of defense hormones in leaves and roots. Our results indicate that P. inflatum strongly enhances cucumber plant growth and reproductive potential. Although fungus treatment did not improve plant resistance to cucumber beetles, inoculated plants were more tolerant to root herbivory, experiencing less biomass reduction. Together, these findings document how a beneficial plant-associated fungus shifts plant investment in growth over herbivore resistance, highlighting the importance of microbes in mediating plant-herbivore interactions. These findings also have important implications for agricultural systems, where beneficial microbes are often introduced or managed to promote plant growth or enhance resistance.

Chemical Cues from Entomopathogenic Nematodes Vary Across Three Species with Different Foraging Strategies, Triggering Different Behavioral Responses in Prey and Competitors.

Chemical cues play important roles in predator-prey interactions. Semiochemicals can aid predator foraging and alert prey organisms to the presence of predators. Previous work suggests that predator traits differentially influence prey behavior, however, empirical data on how prey organisms respond to chemical cues from predator species with different hunting strategies, and how foraging predators react to cues from potential competitors, is lacking. Furthermore, most research in this area has focused on aquatic and aboveground terrestrial systems, while interactions among belowground, soiling-dwelling organisms have received relatively little attention. Here, we assessed how chemical cues from three species of entomopathogenic nematodes (EPNs), each with a different foraging strategy, influenced herbivore (cucumber beetle) and natural enemy (EPN) foraging behavior. We predicted these cues could serve as chemical indicators of increased predation risk, prey availability, or competition. Our findings revealed that foraging cucumber beetle larvae avoided chemical cues from Heterorhabditis bacteriophora (active-foraging cruiser EPNs), but not Steinernema carpocapsae (ambusher EPNs) or Steinernema riobrave (intermediate-foraging EPNs). In contrast, foraging H. bacteriophora EPNs were attracted to cues produced by the two Steinernema species but not conspecific cues. Notably, the three EPN species produced distinct blends of olfactory cues, with only a few semi-conserved compounds across species. These results indicate that a belowground insect herbivore responds differently to chemical cues from different EPN species, with some EPN species avoiding prey detection. Moreover, the active-hunting EPNs were attracted to heterospecific cues, suggesting these cues indicate a greater probability of available prey, rather than strong interspecific competition.

Positive root pressure is critical for whole-plant desiccation recovery in two species of terrestrial resurrection ferns.

Desiccation-tolerant (DT) organisms can lose nearly all their water without dying. Desiccation tolerance allows organisms to survive in a nearly completely dehydrated, dormant state. At the cellular level, sugars and proteins stabilize cellular components and protect them from oxidative damage. However, there are few studies of the dynamics and drivers of whole-plant recovery in vascular DT plants. In vascular DT plants, whole-plant desiccation recovery (resurrection) depends not only on cellular rehydration, but also on the recovery of organs with unequal access to water. In this study, in situ natural and artificial irrigation experiments revealed the dynamics of desiccation recovery in two DT fern species. Organ-specific irrigation experiments revealed that the entire plant resurrected when water was supplied to roots, but leaf hydration alone (foliar water uptake) was insufficient to rehydrate the stele and roots. In both species, pressure applied to petioles of excised desiccated fronds resurrected distal leaf tissue, while capillarity alone was insufficient to resurrect distal pinnules. Upon rehydration, sucrose levels in the rhizome and stele dropped dramatically as starch levels rose, consistent with the role of accumulated sucrose as a desiccation protectant. These findings provide insight into traits that facilitate desiccation recovery in dryland ferns associated with chaparral vegetation of southern California.

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores.

There is increasing evidence that plant-associated microorganisms play important roles in shaping interactions between plants and insect herbivores. Studies of both pathogenic and beneficial plant microbes have documented wide-ranging effects on herbivore behavior and performance. Some studies, for example, have reported enhanced insect-repellent traits or reduced performance of herbivores on microbe-associated plants, while others have documented increased herbivore attraction or performance. Insect herbivores frequently rely on plant cues during foraging and oviposition, suggesting that plant-associated microbes affecting these cues can indirectly influence herbivore preference. We review and synthesize recent literature to provide new insights into the ways pathogenic and beneficial plant-associated microbes alter visual, olfactory, and gustatory cues of plants that affect host-plant selection by insect herbivores. We discuss the underlying mechanisms, ecological implications, and future directions for studies of plant-microbial symbionts that indirectly influence herbivore behavior by altering plant traits.