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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

Arbuscular mycorrhizal fungi associated with Populus-Salix stands in a semiarid riparian ecosystem

??? This study examined the activity, species richness, and species composition of the arbuscular mycorrhizal fungal (AMF) community of Populus-Salix stands on the Verde River (Arizona, USA), quantified patterns of AMF richness and colonization along complex floodplain gradients, and identified environmental variables responsible for structuring the AMF community. ??? Samples from 61 Populus-Salix stands were analyzed for AMF and herbaceous composition, AMF colonization, gravimetric soil moisture, soil texture, per cent organic matter, pH, and concentrations of nitrate, bicarbonate phosphorus and exchangeable potassium. ??? AMF species richness declined with stand age and distance from and elevation above the channel and was positively related to perennial species cover and richness and gravimetric soil moisture. Distance from and elevation above the active channel, forest age, annual species cover, perennial species richness, and exchangeable potassium concentration all played a role in structuring the AMF community in this riparian area. ??? Most AMF species were found across a wide range of soil conditions, but a subset of species tended to occur more often in hydric areas. This group of riparian affiliate AMF species includes several not previously encountered in the surrounding Sonoran desert. ?? New Phytologist (2006).

New Phytologist

Divergence in an obligate mutualism is not explained by divergent climatic factors

Adaptation to divergent environments creates and maintains biological diversity, but we know little about the importance of different agents of ecological divergence. Coevolution in obligate mutualisms has been hypothesized to drive divergence, but this contention has rarely been tested against alternative ecological explanations. Here, we use a well-established example of coevolution in an obligate pollination mutualism, Yucca brevifolia and its two pollinating yucca moths, to test the hypothesis that divergence in this system is the result of mutualists adapting to different abiotic environments as opposed to coevolution between mutualists. ??? We used a combination of principal component analyses and ecological niche modeling to determine whether varieties of Y. brevifolia associated with different pollinators specialize on different environments. ??? Yucca brevifolia occupies a diverse range of climates. When the two varieties can disperse to similar environments, they occupy similar habitats. ??? This suggests that the two varieties have not specialized on distinct habitats. In turn, this suggests that nonclimatic factors, such as the biotic interaction between Y. brevifolia and its pollinators, are responsible for evolutionary divergence in this system. ?? New Phytologist (2009).

New Phytologist

Disentangling the complexities of how legumes and their symbionts regulate plant nitrogen access and storage

Nitrogen (N) availability strongly influences the structure and function of ecosystems (e.g. Vitousek & Howarth, 1991), but only a relatively small number of microbial groups have the ability to convert the N 2 in our atmosphere into biologically available forms.This process, N 2 fixation, is the dominant source of new N to the biosphere outside of anthropogenic inputs (Vitousek et al., 2013).Some N 2 -fixing microorganisms live independently on plant leaves, on decomposing organic material, and in soil (Reed et al.,2011), while others have co-evolved with a few higher plant taxa to form symbioses that fix N 2 in root nodules (e.g. Sprent & Raven,1985). The relationship between these legumes and their root nodule symbionts (rhizobia) is one of the most well studied plant –microbe symbioses. Yet, many important questions about the controls, interactions, and implications of legume N 2 fixation remain unanswered. In this issue of New Phytologist (pp. 690–699),Wolf, Funk, & Menge elegantly address a fundamental set of questions about N 2 fixation in their examination of how herbaceous legumes, their symbionts, and external N availability interact to govern legume access and storage of N.

New Phytologist

Biocrust science and global change

Global environmental changes such as climate and land‐use change affect ecosystems worldwide, and this New Phytologist Virtual Issue brings together fundamental research questions and novel approaches associated with the study of biological soil crusts in the context of such shifts. In a changing world, organisms can display a limited set of responses that will determine their persistence over varied spatial and temporal scales. Specifically, organisms might tolerate the change – for example, via phenotypic plasticity – and remain present in local communities. Alternatively, organisms might shift or retract their range to match their historical niche, they may adapt to the directional selection pressures imposed by change, or they could be driven to local (and possibly global) extinction. Efforts to understand which of these responses particular plant species or assemblages will exhibit are necessary for predicting changes in ecosystem functioning and trophic interactions under global change scenarios, and for managing and supporting sustainable terrestrial ecosystems. Accordingly, the assessment of plant responses to global change has become a significant research focus. Despite this impressive effort, our understanding and combined work to measure the responses to global change for species and communities of nonvascular autotrophs, such as the cyanobacteria, lichens, and bryophytes that form biological soil crusts (Fig. 1), remain rare compared with the large focus on vascular plants (Fig. 2; Reed et al., 2016). Nevertheless, these nonvascular photosynthetic communities and their responses to change could have critical implications for determining ecosystem structure and function at the global‐scale (Elbert et al., 2012; Ferrenberg et al., 2017; Rodriguez‐Caballero et al., 2018).

New Phytologist

Leaf conductance decreased under free-air CO2 enrichment (FACE) for three perennials in the Nevada desert

A common response of plants to elevated atmospheric CO 2 concentration (CO 2 ) is decreased leaf conductance. Consequently, leaf temperature is predicted to increase under elevated CO 2 . Diurnal patterns of leaf conductance and temperature were measured for three desert perennials, the C 3 shrub Larrea tridentata , C 3 tussock grass Achnatherum hymenoides and C 4 tussock grass Pleuraphis rigida , at the Nevada Desert FACE facility. Measurements were made on ambient and c . 550 µmol mol −1 CO 2 plots through both a wet and dry year. Reductions in conductance were 35%, 20% and 13% for Pleuraphis , Achnatherum and Larrea , respectively. Decreased conductance occurred throughout the day only for Pleuraphis . Both C 3 species had smaller CO 2 effects during dry periods than wet. Leaf temperature did not differ significantly between elevated and ambient CO 2 for any species. Comparisons of blower-control and nonring plots indicated that the FACE apparatus did not confound our results. All three species exhibited decreased leaf conductance under elevated CO 2 , although reductions were not uniform during the day or among years. Nonetheless, leaf energy balance was only minimally changed for these microphyllous desert perennials.

Nevada

Root growth and function of three Mojave Desert grasses in response to elevated atmospheric CO2 concentration

Root growth and physiological responses to elevated CO 2 were investigated for three important Mojave Desert grasses: the C 3 perennial Achnatherum hymenoides , the C 4 perennial Pleuraphis rigida and the C 3 annual Bromus madritensis ssp. rubens . Seeds of each species were grown at ambient (360 μl l −1 ) or elevated (1000 μl l −1 ) CO 2 in a glasshouse and harvested at three phenological stages: vegetative, anthesis and seed fill. Because P. rigida did not flower during the course of this study, harvests for this species represent three vegetative stages. Primary productivity was increased in both C 3 grasses in response to elevated CO 2 (40 and 19% for A. hymenoides and B. rubens , respectively), but root biomass increased only in the C 3 perennial grass. Neither above-ground nor below-ground biomass of the C 4 perennial grass was significantly affected by the CO 2 treatment. Elevated CO 2 did not significantly affect root surface area for any species. Total plant nitrogen was also not statistically different between CO 2 treatments for any species, indicating no enhanced uptake of N under elevated CO 2 . Physiological uptake capacities for NO 3 and NH 4 were not affected by the CO 2 treatment during the second harvest; measurements were not made for the first harvest. However, at the third harvest uptake capacity was significantly decreased in response to elevated CO 2 for at least one N form in each species. NO 3 uptake rates were lower in A. hymenoides and P. rigida , and NH 4 uptake rates were lower in B. rubens at elevated CO 2 . Nitrogen uptake on a whole root-system basis (NO 3 +NH 4 uptake capacity × root biomass) was influenced positively by elevated CO 2 only for A. hymenoides after anthesis. These results suggest that elevated CO 2 may result in a competitive advantage for A. hymenoides relative to species that do not increase root-system N uptake capacity. Root respiration measurements normalized to 20 °C were not significantly affected by the CO 2 treatment. However, specific root respiration was significantly correlated with either root C∶N ratio or root water content when all data per species were included within a simple regression model. The results of this study provide little evidence for up-regulation of root physiology in response to elevated CO 2 and indicate that root biomass responses to CO 2 are species-specific.

New Phytologist

Attenuated total reflectance spectroscopy of plant leaves: A tool for ecological and botanical studies

??? Attenuated total reflectance (ATR) spectra of plant leaves display complex absorption features related to organic constituents of leaf surfaces. The spectra can be recorded rapidly, both in the field and in the laboratory, without special sample preparation. ??? This paper explores sources of ATR spectral variation in leaves, including compositional, positional and temporal variations. Interspecific variations are also examined, including the use of ATR spectra as a tool for species identification. ??? Positional spectral variations generally reflected the abundance of cutin and the epicuticular wax thickness and composition. For example, leaves exposed to full sunlight commonly showed more prominent cutin- and wax-related absorption features compared with shaded leaves. Adaxial vs. abaxial leaf surfaces displayed spectral variations reflecting differences in trichome abundance and wax composition. Mature vs. young leaves showed changes in absorption band position and intensity related to cutin, polysaccharide, and possibly amorphous silica development on and near the leaf surfaces. ??? Provided that similar samples are compared (e.g. adaxial surfaces of mature, sun-exposed leaves) same-species individuals display practically identical ATR spectra. Using spectral matching procedures to analyze an ATR database containing 117 individuals, including 32 different tree species, 83% of the individuals were correctly identified. ?? The Authors (2006).

New Phytologist

Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought?

Severe droughts have been associated with regional-scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, prediction remains difficult because the physiological mechanisms underlying drought survival and mortality are poorly understood. We developed a hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality. Multiple mechanisms may cause mortality during drought. A common mechanism for plants with isohydric regulation of water status results from avoidance of drought-induced hydraulic failure via stomatal closure, resulting in carbon starvation and a cascade of downstream effects such as reduced resistance to biotic agents. Mortality by hydraulic failure per se may occur for isohydric seedlings or trees near their maximum height. Although anisohydric plants are relatively drought-tolerant, they are predisposed to hydraulic failure because they operate with narrower hydraulic safety margins during drought. Elevated temperatures should exacerbate carbon starvation and hydraulic failure. Biotic agents may amplify and be amplified by drought-induced plant stress. Wet multidecadal climate oscillations may increase plant susceptibility to drought-induced mortality by stimulating shifts in hydraulic architecture, effectively predisposing plants to water stress. Climate warming and increased frequency of extreme events will probably cause increased regional mortality episodes. Isohydric and anisohydric water potential regulation may partition species between survival and mortality, and, as such, incorporating this hydraulic framework may be effective for modeling plant survival and mortality under future climate conditions.

New Phytologist

Fungal endophytes: diversity and functional roles

All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.

New Phytologist

Sensitivity of leaf size and shape to climate: Global patterns and paleoclimatic applications

Paleobotanists have long used models based on leaf size and shape to reconstruct paleoclimate. However, most models incorporate a single variable or use traits that are not physiologically or functionally linked to climate, limiting their predictive power. Further, they often underestimate paleotemperature relative to other proxies. Here we quantify leaf–climate correlations from 92 globally distributed, climatically diverse sites, and explore potential confounding factors. Multiple linear regression models for mean annual temperature (MAT) and mean annual precipitation (MAP) are developed and applied to nine well‐studied fossil floras. We find that leaves in cold climates typically have larger, more numerous teeth, and are more highly dissected. Leaf habit (deciduous vs evergreen), local water availability, and phylogenetic history all affect these relationships. Leaves in wet climates are larger and have fewer, smaller teeth. Our multivariate MAT and MAP models offer moderate improvements in precision over univariate approaches (± 4.0 vs 4.8°C for MAT) and strong improvements in accuracy. For example, our provisional MAT estimates for most North American fossil floras are considerably warmer and in better agreement with independent paleoclimate evidence. Our study demonstrates that the inclusion of additional leaf traits that are functionally linked to climate improves paleoclimate reconstructions. This work also illustrates the need for better understanding of the impact of phylogeny and leaf habit on leaf–climate relationships.

New Phytologist

Stoichiometric patterns in foliar nutrient resorption across multiple scales

*Nutrient resorption is a fundamental process through which plants withdraw nutrients from leaves before abscission. Nutrient resorption patterns have the potential to reflect gradients in plant nutrient limitation and to affect a suite of terrestrial ecosystem functions. *Here, we used a stoichiometric approach to assess patterns in foliar resorption at a variety of scales, specifically exploring how N : P resorption ratios relate to presumed variation in N and/or P limitation and possible relationships between N : P resorption ratios and soil nutrient availability. *N : P resorption ratios varied significantly at the global scale, increasing with latitude and decreasing with mean annual temperature and precipitation. In general, tropical sites (absolute latitudes < 23°26′) had N : P resorption ratios of < 1, and plants growing on highly weathered tropical soils maintained the lowest N : P resorption ratios. Resorption ratios also varied with forest age along an Amazonian forest regeneration chronosequence and among species in a diverse Costa Rican rain forest. *These results suggest that variations in N : P resorption stoichiometry offer insight into nutrient cycling and limitation at a variety of spatial scales, complementing other metrics of plant nutrient biogeochemistry. The extent to which the stoichiometric flexibility of resorption will help regulate terrestrial responses to global change merits further investigation.

New Phytologist

Elevated CO2 does not offset greater water stress predicted under climate change for native and exotic riparian plants

In semiarid western North American riparian ecosystems, increased drought and lower streamflows under climate change may reduce plant growth and recruitment, and favor drought‐tolerant exotic species over mesic native species. We tested whether elevated atmospheric CO 2 might ameliorate these effects by improving plant water‐use efficiency. We examined the effects of CO 2 and water availability on seedlings of two native ( Populus deltoides spp. monilifera , Salix exigua ) and three exotic ( Elaeagnus angustifolia , Tamarix spp., Ulmus pumila ) western North American riparian species in a CO 2 ‐controlled glasshouse, using 1‐m‐deep pots with different water‐table decline rates. Low water availability reduced seedling biomass by 70–97%, and hindered the native species more than the exotics. Elevated CO 2 increased biomass by 15%, with similar effects on natives and exotics. Elevated CO 2 increased intrinsic water‐use efficiency (Δ 13 C leaf ), but did not increase biomass more in drier treatments than wetter treatments. The moderate positive effects of elevated CO 2 on riparian seedlings are unlikely to counteract the large negative effects of increased aridity projected under climate change. Our results suggest that increased aridity will reduce riparian seedling growth despite elevated CO 2 , and will reduce growth more for native Salix and Populus than for drought‐tolerant exotic species.

New Phytologist

Nonstructural leaf carbohydrates dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism

* Vegetation change is expected with global climate change, potentially altering ecosystem function and climate feedbacks. However, causes of plant mortality, which are central to vegetation change, are understudied, and physiological mechanisms remain unclear, particularly the roles of carbon metabolism and xylem function. * We report analysis of foliar nonstructural carbohydrates (NSCs) and associated physiology from a previous experiment where earlier drought-induced mortality of Pinus edulis at elevated temperatures was associated with greater cumulative respiration. Here, we predicted faster NSC decline for warmed trees than for ambient-temperature trees. * Foliar NSC in droughted trees declined by 30% through mortality and was lower than in watered controls. NSC decline resulted primarily from decreased sugar concentrations. Starch initially declined, and then increased above pre-drought concentrations before mortality. Although temperature did not affect NSC and sugar, starch concentrations ceased declining and increased earlier with higher temperatures. * Reduced foliar NSC during lethal drought indicates a carbon metabolism role in mortality mechanism. Although carbohydrates were not completely exhausted at mortality, temperature differences in starch accumulation timing suggest that carbon metabolism changes are associated with time to death. Drought mortality appears to be related to temperature-dependent carbon dynamics concurrent with increasing hydraulic stress in P. edulis and potentially other similar species.

New Phytologist

How mangrove forests adjust to rising sea level

Mangroves are among the most well described and widely studied wetland communities in the world. The greatest threats to mangrove persistence are deforestation and other anthropogenic disturbances that can compromise habitat stability and resilience to sea-level rise. To persist, mangrove ecosystems must adjust to rising sea level by building vertically or become submerged. Mangroves may directly or indirectly influence soil accretion processes through the production and accumulation of organic matter, as well as the trapping and retention of mineral sediment. In this review, we provide a general overview of research on mangrove elevation dynamics, emphasizing the role of the vegetation in maintaining soil surface elevations (i.e. position of the soil surface in the vertical plane). We summarize the primary ways in which mangroves may influence sediment accretion and vertical land development, for example, through root contributions to soil volume and upward expansion of the soil surface. We also examine how hydrological, geomorphological and climatic processes may interact with plant processes to influence mangrove capacity to keep pace with rising sea level. We draw on a variety of studies to describe the important, and often under-appreciated, role that plants play in shaping the trajectory of an ecosystem undergoing change.

New Phytologist

Evolutionary ecology of resprouting and seeding in fire-prone ecosystems

There are two broad mechanisms by which plant populations persist under recurrent disturbances: resprouting from surviving tissues, and seedling recruitment. Species can have one of these mechanisms or both. However, a coherent framework explaining the differential evolutionary pressures driving these regeneration mechanisms is lacking. We propose a bottom-up approach in addressing this question that considers the relative survivorship of adults and juveniles in an evolutionary context, based on two assumptions. First, resprouting and seeding can be interpreted by analogy with annual versus perennial life histories; that is, if we consider disturbance cycles to be analogous to annual cycles, then resprouting species are analogous to the perennial life history with iteroparous reproduction, and obligate seeding species that survive disturbances solely through seed banks are analogous to the annual life history with semelparous reproduction. Secondly, changes in the selective regimes differentially modify the survival rates of adults and juveniles and thus the relative costs and benefits of resprouting versus seeding. Our approach provides a framework for understanding temporal and spatial variation in resprouting and seeding under crown-fire regimes. It accounts for patterns of coexistence and environmental changes that contribute to the evolution of seeding from resprouting ancestors.

New Phytologist

The unseen iceberg: Plant roots in arctic tundra

Plant roots play a critical role in ecosystem function in arctic tundra, but root dynamics in these ecosystems are poorly understood. To address this knowledge gap, we synthesized available literature on tundra roots, including their distribution, dynamics and contribution to ecosystem carbon and nutrient fluxes, and highlighted key aspects of their representation in terrestrial biosphere models. Across all tundra ecosystems, belowground plant biomass exceeded aboveground biomass, with the exception of polar desert tundra. Roots were shallowly distributed in the thin layer of soil that thaws annually, and were often found in surface organic soil horizons. Root traits &ndash; including distribution, chemistry, anatomy and resource partitioning &ndash; play an important role in controlling plant species competition, and therefore ecosystem carbon and nutrient fluxes, under changing climatic conditions, but have only been quantified for a small fraction of tundra plants. Further, the annual production and mortality of fine roots are key components of ecosystem processes in tundra, but extant data are sparse. Tundra root traits and dynamics should be the focus of future research efforts. Better representation of the dynamics and characteristics of tundra roots will improve the utility of models for the evaluation of the responses of tundra ecosystems to changing environmental conditions.

New Phytologist