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At least 19 recordsLinked to original sources
USGS2015

Advancing the science of microbial symbiosis to support invasive species management: a case study on Phragmites in the Great Lakes

A growing body of literature supports microbial symbiosis as a foundational principle for the competitive success of invasive plant species. Further exploration of the relationships between invasive species and their associated microbiomes, as well as the interactions with the microbiomes of native species, can lead to key new insights into invasive success and potentially new and effective control approaches. In this manuscript, we review microbial relationships with plants, outline steps necessary to develop invasive species control strategies that are based on those relationships, and use the invasive plant species Phragmites australis (common reed) as an example of how development of microbial-based control strategies can be enhanced using a collective impact approach. The proposed science agenda, developed by the Collaborative for Microbial Symbiosis and Phragmites Management, contains a foundation of sequential steps and mutually-reinforcing tasks to guide the development of microbial-based control strategies for Phragmites and other invasive species. Just as the science of plant-microbial symbiosis can be transferred for use in other invasive species, so too can the model of collective impact be applied to other avenues of research and management.

Frontiers in Microbiology↗
USGS2004

The role of fungal symbiosis in the adaptation of plants to high stress environments

All plants studied in natural ecosystemsare symbiotic with fungi that either resideentirely (endophytes) or partially(mycorrhizae) within plants. Thesesymbioses appear to adapt to biotic andabiotic stresses and may be responsible forthe survival of both plant hosts and fungalsymbionts in high stress habitats. Here wedescribe the role of symbiotic fungi inplant stress tolerance and present astrategy based on adaptive symbiosis topotentially mitigate the impacts of globalchange on plant communities.

Mitigation and Adaptation Strategies for Global Ch↗
USGS2008

Stress tolerance in plants via habitat-adapted symbiosis

We demonstrate that native grass species from coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively. Symbiotically conferred stress tolerance is a habitat-specific phenomenon with geothermal endophytes conferring heat but not salt tolerance, and coastal endophytes conferring salt but not heat tolerance. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not confer these stress tolerances. Moreover, fungal endophytes from agricultural crops conferred disease resistance and not salt or heat tolerance. We define habitat-specific, symbiotically-conferred stress tolerance as habitat-adapted symbiosis and hypothesize that it is responsible for the establishment of plants in high-stress habitats. The agricultural, coastal and geothermal plant endophytes also colonized tomato (a model eudicot) and conferred disease, salt and heat tolerance, respectively. In addition, the coastal plant endophyte colonized rice (a model monocot) and conferred salt tolerance. These endophytes have a broad host range encompassing both monocots and eudicots. Interestingly, the endophytes also conferred drought tolerance to plants regardless of the habitat of origin. Abiotic stress tolerance correlated either with a decrease in water consumption or reactive oxygen sensitivity/generation but not to increased osmolyte production. The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural and native plant communities.The ISME Journal (2008) 2, 404-416; doi:10.1038/ismej.2007.106; published online 7 February 2008. ?? 2008 International Society for Microbial Ecology All rights reserved.

ISME Journal↗
USGS2001

Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader?

Plant symbiotic fungi are generally thought to express a single lifestyle that might increase (mutualism), decrease (parasitism), or have no influence (commensalism) on host fitness. However, data are presented here demonstrating that plant pathogenic Colletotrichum species are able to asymptomatically colonize plants and express nonpathogenic lifestyles. Experiments were conducted in growth chambers and plant colonization was assessed by emergence of fungi from surface sterilized plant tissues. Expression of symbiotic lifestyles was assessed by monitoring the ability of fungi to confer disease resistance, drought tolerance and growth enhancement. Several pathogenic Colletotrichum species expressed either mutualistic or commensal lifestyles in plants not known to be hosts. Mutualists conferred disease resistance, drought tolerance, and/or growth enhancement to host plants. Lifestyle-altered mutants expressing nonpathogenic lifestyles had greater host ranges than the parental wildtype isolate. Successive colonization studies indicated that the ability of a symbiont to colonize a plant was dependent on previous colonization events and the lifestyles expressed by the initial colonizing fungus. The results indicate that the outcome of symbiosis is controlled by the plant's physiology. ?? New Phytologist.

New Phytologist↗
USGS2011

Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: A strategy for mitigating impacts of climate change

Climate change and catastrophic events have contributed to rice shortages in several regions due to decreased water availability and soil salinization. Although not adapted to salt or drought stress, two commercial rice varieties achieved tolerance to these stresses by colonizing them with Class 2 fungal endophytes isolated from plants growing across moisture and salinity gradients. Plant growth and development, water usage, ROS sensitivity and osmolytes were measured with and without stress under controlled conditions. The endophytes conferred salt, drought and cold tolerance to growth chamber and greenhouse grown plants. Endophytes reduced water consumption by 20–30% and increased growth rate, reproductive yield, and biomass of greenhouse grown plants. In the absence of stress, there was no apparent cost of the endophytes to plants, however, endophyte colonization decreased from 100% at planting to 65% compared to greenhouse plants grown under continual stress (maintained 100% colonization). These findings indicate that rice plants can exhibit enhanced stress tolerance via symbiosis with Class 2 endophytes, and suggest that symbiotic technology may be useful in mitigating impacts of climate change on other crops and expanding agricultural production onto marginal lands.

PLoS ONE↗
USGS2008

More than 400 million years of evolution and some plants still can't make it on their own: Plant stress tolerance via fungal symbiosis

All plants in natural ecosystems are thought to be symbiotic with mycorrhizal and/or endophytic fungi. Collectively, these fungi express different symbiotic lifestyles ranging from parasitism to mutualism. Analysis of Colletotrichum species indicates that individual isolates can express either parasitic or mutualistic lifestyles depending on the host genotype colonized. The endophyte colonization pattern and lifestyle expression indicate that plants can be discerned as either disease, non-disease, or non-hosts. Fitness benefits conferred by fungi expressing mutualistic lifestyles include biotic and abiotic stress tolerance, growth enhancement, and increased reproductive success. Analysis of plant-endophyte associations in high stress habitats revealed that at least some fungal endophytes confer habitat-specific stress tolerance to host plants. Without the habitat-adapted fungal endophytes, the plants are unable to survive in their native habitats. Moreover, the endophytes have a broad host range encompassing both monocots and eudicots, and confer habitat-specific stress tolerance to both plant groups. ?? The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.

Conference Paper↗
USGS2007

A virus in a fungus in a plant: Three-way symbiosis required for thermal tolerance

A mutualistic association between a fungal endophyte and a tropical panic grass allows both organisms to grow at high soil temperatures. We characterized a virus from this fungus that is involved in the mutualistic interaction. Fungal isolates cured of the virus are unable to confer heat tolerance, but heat tolerance is restored after the virus is reintroduced. The virus-infected fungus confers heat tolerance not only to its native monocot host but also to a eudicot host, which suggests that the underlying mechanism involves pathways conserved between these two groups of plants.

Science↗
USGS1984

Seed predation due to the yucca moth symbiosis

All species of Yucca (Agavaceae) require the pollinator services of a species of moth in the genus Tegeticula ( Lepidoptera : Incurvariidae). These moths oviposit in the ovary of the plants and the larvae are entirely dependent upon Yucca seeds for food. The extent and distribution of larval seed predation was examined in nine Yucca species in the southwestern United States. The proportion of seeds destroyed by the yucca moth ranged from 3 % in Y. schidigera from coastal southern California to 45 % in one population of Y. angustissima from southern Utah. This sampling was done in 1979 at which time the Y. schidigera population averaged 0.6 larvae per fruit and the population of Y. angustissima averaged 9.3 larvae per fruit. A second sampling of these populations in 1982 averaged 0.5 for Y. schidigera and 5.6 for Y. angustissima . Several species showed significant differences between populations in the number of larvae per fruit. Contrary to expectation, based on the dogma that fruit production is dependent upon Tegeticula pollination (which is always followed by oviposition), a large number of fruits were found without larvae. The proportion varied greatly between populations but was as high as two thirds of all fruits in some populations. Observations suggested that these flowers had been pollinated by Tegeticula and the moths had oviposited in them but that the eggs failed to hatch.

American Midland Naturalist↗
USGS2019

Evidence for widespread microbivory of endophytic bacteria in roots of vascularplants through oxidative degradation in root cell periplasmic spaces

In this chapter we present a hypothesis, and data supporting it, that vascular plants in diverse families possess symbiotic/endophytic bacteria that frequently vector on or within their seeds; seedlings degrade symbiotic bacteria within roots. Evidence of widespread microbivory was found in a survey for intracellular bacteria that we conducted including seedlings in 36 species of vascular plants distributed in 20 plant families. Experiments indicate that when seeds germinate, bacteria colonize seedlings and internalize into root cells where they are oxidatively-degraded in the periplasmic spaces of cells. The process of degradation of microbes in roots has been termed “rhizophagy”, and “rhizophagy cycle” or “rhizophagy symbiosis” in the case of symbiotic bacteria that alternate between a free-living soil phase and intracellular/endophytic phase. We hypothesize that microbivory could account for a significant portion of nutrients acquired by plants from soils—with one estimate suggesting that as much as 30% of the nutrients acquired by seedlings may stem from rhizophagy symbiosis. Developing a better understanding of rhizophagy symbiosis could lead to new ways to cultivate crops without reliance on excessive agrochemical applications. Learning how to manipulate rhizophagy symbiosis could result in new technologies for reducing growth of weedy or invasive plant species by inhibiting rhizophagy symbiosis.

Book chapter↗
USGS2002

Field performance of cucurbit and tomato plants infected with a nonpathogenic mutant of Colletotrichum magna (teleomorph: Glomerella magna; Jekins and Winstead)

Path-1 is a UV-induced non-pathogenic mutant of a virulent Colletotrichum magna isolate that establishes mutualistic symbioses with cucurbit and tomato species. Under laboratory conditions, this mutualism results in plant growth enhancement, drought tolerance, and disease protection against fungal pathogens. This study focuses on the efficacy of this symbiosis and the symbiotic lifestyle expressed by path-1 under field conditions in the absence of disease stress. The effects of colonization by path-1 on fruit yields and growth was measured in field plots with four cucurbit species including four watermelon cultivars, and two tomato cultivars, over four growing seasons. The persistence of the symbiosis, extent of colonization, and path-1 transmission were also assessed. Yields from path-1 infected plants were equivalent to or greater than yields from non-inoculated control plants and path-1 systemically colonized plants throughout each growing season. Path-1 also increased the growth rates of tomato plants and was not transmitted to uncolonized plants. The results indicate that there are no metabolic costs of this symbiosis and the symbiosis is maintained under field conditions.

Symbiosis↗
USGS2026

Cnidarian–algal partnerships structure bacterial communities during strobilation in Cassiopea xamachana

Cnidarian–algal (Symbiodiniaceae) symbioses rely on complex interactions among the cnidarian host, algal symbionts, and associated bacterial communities. In the upside-down jellyfish Cassiopea xamachana , the polyp-to-medusa transition (strobilation) requires the establishment of symbiosis with Symbiodiniaceae algal partners, yet bacterial community dynamics during this developmental process remain unknown. Here, we experimentally induced symbiosis in aposymbiotic polyps using four algal treatments: xenic Symbiodinium microadriaticum (native symbiont), xenic Breviolum minutum , antibiotic-treated B. minutum , and a photosynthetically impaired B. minutum mutant. We combined 16S rRNA gene sequencing with measurements of photosynthetic efficiency, asexual budding, and algal surface N-glycan profiles to characterize holobiont assembly during symbiosis onset and strobilation. Algal treatment structured bacterial communities in both algal cultures and polyp tissues. Our analyses identified a set of amplicon sequence variants that consistently distinguished strobilating polyps from non-strobilating aposymbiotic and mutant polyps, in addition to potential bacterial biomarkers associated with successful metamorphosis. Strobilation was associated with the enrichment of bacterial communities putatively involved in sulfur and nitrogen cycling, whereas non-strobilating aposymbiotic and mutant polyps were characterized by opportunistic bacteria and increased community variability. Together, these results reveal coordinated changes in algal physiology, surface glycan profiles, and bacterial community structure associated with successful strobilation in C. xamachana and support a model in which tripartite host–alga–bacteria interactions influence cnidarian life stage transitions.

ISME Communications↗
USGS2009

Symbiotic lifestyle expression by fungal endophytes and the adaptation of plants to stress: unraveling the complexities of intimacy

The fossil record indicates that fungal symbionts have been associated with plants since the Ordovician period (approximately 400 million years ago), when plants first became established on land (Pirozynski and Malloch, 1975; Redecker et al., 2000; Remy et al., 1994; Simon et al., 1993). Transitioning from aquatic to terrestrial habitats likely presented plants with new stresses, including periods of desiccation. Since symbiotic fungi are known to confer drought tolerance to plants (Bacon, 1993; Read and Camp, 1986), it has been suggested that fungal symbiosis was involved with or responsible for the establishment of land plants (Pirozynski and Malloch, 1975). Symbiosis was first defined by De Bary in 1879, and since that time, all plants in natural ecosystems have been found to be colonized with fungal and bacterial symbionts. It is clear that individual plants represent symbiotic communities with microorganisms associated in or on tissues below- and aboveground. There are two major classes of fungal symbionts associated with internal plant tissues: fungal endophytes that reside entirely within plants and may be associated with roots, stems leaves, or flowers; and mycorrhizal fungi that reside only in roots but extend out into the rhizosphere. In addition, fungal endophytes may be divided into two classes: (1) a relatively small number of fastidious species that are limited to a few monocot hosts (Clay and Schardl, 2002), and (2) a large number of tractable species with broad host ranges, including both monocots and eudicots (Stone et al., 2000). While significant resources and research have been invested in mycorrhizae and class 1 endophytes, comparatively little is known about class 2 endophytes, which may represent the largest group of fungal symbionts. This is partially because the symbiotic functionalities of class 2 endophytes have only recently been elucidated and shown to be responsible for the adaptation of some plants to high-stress environments (Redman et al., 1999, 2001, 2002a; Arnold et al., 2003; Dingle and McGee, 2003; Ernst et al., 2003). In this chapter, we focus on symbiotic interactions between class 2 endophytes and a variety of monocot and eudicot host species. Specifically, we will discuss the ability of endophytes to express more than one symbiotic lifestyle, fungal taxonomy vs. lifestyle expression, the adaptive nature of symbioses, mechanisms of symbiotically conferred stress tolerance, and the evolutionary implications of adaptive symbiosis. We will refer to class 2 endophytes as fungal endophytes throughout the text.

Book chapter↗
USGS2023

Fire modifies plant–soil feedbacks

Although plant–soil feedbacks (interactions between plants and soils, often mediated by soil microbes, abbreviated as PSFs) are widely known to influence patterns of plant diversity at local and landscape scales, these interactions are rarely examined in the context of important environmental factors. Resolving the roles of environmental factors is important because the environmental context may alter PSF patterns by modifying the strength or even direction of PSFs for certain species. One important environmental factor that is increasing in scale and frequency with climate change is fire, though the influence of fire on PSFs remains essentially unexamined. By changing microbial community composition, fire may alter the microbes available to colonize the roots of plants and thus seedling growth post-fire. This has potential to change the strength and/or direction of PSFs, depending on how such changes in microbial community composition occur and the plant species with which the microbes interact. We examined how a recent fire altered PSFs of two leguminous, nitrogen-fixing tree species in Hawaiʻi. For both species, growing in conspecific soil resulted in higher plant performance (as measured by biomass production) than growing in heterospecific soil. This pattern was mediated by nodule formation, an important process for growth for legume species. Fire weakened PSFs for these species and therefore pairwise PSFs, which were significant in unburned soils, but were nonsignificant in burned soils. Theory suggests that positive PSFs such as those found in unburned sites would reinforce the dominance of species where they are locally dominant. The change in pairwise PSFs with burn status shows PSF-mediated dominance might diminish after fire. Our results demonstrate that fire can modify PSFs by weakening the legume-rhizobia symbiosis, which may alter local competitive dynamics between two canopy dominant tree species. These findings illustrate the importance of considering environmental context when evaluating the role of PSFs for plants.

Ecology↗
USGS2010

Adaptation and survival of plants in high stress habitats via fungal endophyte conferred stress tolerance

From the Arctic to the Antarctic, plants thrive in diverse habitats that impose different levels of adaptive pressures depending on the type and degree of biotic and abiotic stresses inherent to each habitat (Stevens, 1989). At any particular location, the abundance and distribution of individual plant species vary tremendously and is theorized to be based on the ability to tolerate a wide range of edaphic conditions and habitat-specific stresses (Pianka, 1966). The ability of individual plant species to thrive in diverse habitats is commonly referred to as phenotypic plasticity and is thought to involve adaptations based on changes in the plant genome (Givnish, 2002; Pan et al., 2006; Robe and Griffiths, 2000; Schurr et al., 2006). Habitats that impose high levels of abiotic stress are typically colonized with fewer plant species compared to habitats imposing low levels of stress. Moreover, high stress habitats have decreased levels of plant abundance compared to low stress habitats even though these habitats may occur in close proximity to one another (Perelman et al., 2007). This is particularly interesting because all plants are known to perceive, transmit signals, and respond to abiotic stresses such as drought, heat, and salinity (Bartels and Sunkar, 2005; Bohnert et al., 1995). Although there has been extensive research performed to determine the genetic, molecular, and physiological bases of how plants respond to and tolerate stress, the nature of plant adaptation to high stress habitats remains unresolved (Leone et al., 2003; Maggio et al., 2003; Tuberosa et al., 2003). However, recent evidence indicates that a ubiquitous aspect of plant biology (fungal symbiosis) is involved in the adaptation and survival of at least some plants in high stress habitats (Rodriguez et al., 2008).

Book chapter↗
USGS2016

Coral calcification and ocean acidification

Over 60 years ago, the discovery that light increased calcification in the coral plant-animal symbiosis triggered interest in explaining the phenomenon and understanding the mechanisms involved. Major findings along the way include the observation that carbon fixed by photosynthesis in the zooxanthellae is translocated to animal cells throughout the colony and that corals can therefore live as autotrophs in many situations. Recent research has focused on explaining the observed reduction in calcification rate with increasing ocean acidification (OA). Experiments have shown a direct correlation between declining ocean pH, declining aragonite saturation state (Ωarag), declining [CO32_] and coral calcification. Nearly all previous reports on OA identify Ωarag or its surrogate [CO32] as the factor driving coral calcification. However, the alternate “Proton Flux Hypothesis” stated that coral calcification is controlled by diffusion limitation of net H+ transport through the boundary layer in relation to availability of dissolved inorganic carbon (DIC). The “Two Compartment Proton Flux Model” expanded this explanation and synthesized diverse observations into a universal model that explains many paradoxes of coral metabolism, morphology and plasticity of growth form in addition to observed coral skeletal growth response to OA. It is now clear that irradiance is the main driver of net photosynthesis (Pnet), which in turn drives net calcification (Gnet), and alters pH in the bulk water surrounding the coral. Pnet controls [CO32] and thus Ωarag of the bulk water over the diel cycle. Changes in Ωarag and pH lag behind Gnet throughout the daily cycle by two or more hours. The flux rate Pnet, rather than concentration-based parameters (e.g., Ωarag, [CO3 2], pH and [DIC]:[H+] ratio) is the primary driver of Gnet. Daytime coral metabolism rapidly removes DIC from the bulk seawater. Photosynthesis increases the bulk seawater pH while providing the energy that drives calcification and increases in Gnet. These relationships result in a correlation between Gnet and Ωarag, with both parameters being variables dependent on Pnet. Consequently the correlation between Gnet and Ωarag varies widely between different locations and times depending on the relative metabolic contributions of various calcifying and photosynthesizing organisms and local rates of carbonate dissolution. High rates of H+ efflux continue for several hours following the mid-day Gnet peak suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Model. DIC flux (uptake) tracks Pnet and Gnet and drops off rapidly after the photosynthesis-calcification maxima, indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H+. Predictive models of future global changes in coral and coral reef growth based on oceanic Ωarag must include the influence of future changes in localized Pnet on Gnet as well as changes in rates of reef carbonate dissolution. The correlation between Ωarag and Gnet over the diel cycle is simply the result of increasing pH due to photosynthesis that shifts the CO2-carbonate system equilibria to increase [CO32] relative to the other DIC components of [HCO3] and [CO2]. Therefore Ωarag closely tracks pH as an effect of Pnet, which also drives changes in Gnet. Measurements of DIC flux and H+ flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.

Book chapter↗