Phloem anatomy predicts berry sugar accumulation across 13 wine-grape cultivars.

Introduction: Climate change is impacting the wine industry by accelerating ripening processes due to warming temperatures, especially in areas of significant grape production like California. Increasing temperatures accelerate the rate of sugar accumulation (measured in °Brix) in grapes, however this presents a problem to wine makers as flavor profiles may need more time to develop properly. To alleviate the mismatch between sugar accumulation and flavor compounds, growers may sync vine cultivars with climates that are most amenable to their distinct growing conditions. However, the traits which control such cultivar specific climate adaptation, especially for °Brix accumulation rate, are poorly understood. Recent studies have shown that higher rates of fruit development and sugar accumulation are predicted by larger phloem areas in different organs of the plant. Methods: Here we test this phloem area hypothesis using a common garden experiment in the Central Valley of Northern California using 18 cultivars of the common grapevine (Vitis vinifera) and assess the grape berry sugar accumulation rates as a function of phloem area in leaf and grape organs. Results: We find that phloem area in the leaf petiole organ as well as the berry pedicel is a significant predictor of °Brix accumulation rate across 13 cultivars and that grapes from warm climates overall have larger phloem areas than those from hot climates. In contrast, other physiological traits such as photosynthetic assimilation and leaf water potential did not predict berry accumulation rates. Discussion: As hot climate cultivars have lower phloem areas which would slow down brix accumulation, growers may have inadvertently been selecting this trait to align flavor development with sugar accumulation across the common cultivars tested. This work highlights a new trait that can be easily phenotyped (i.e., petiole phloem area) and be used for growers to match cultivar more accurately with the temperature specific climate conditions of a growing region to obtain satisfactory sugar accumulation and flavor profiles.

Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus, Vitis.

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these patterns remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlated with the average abiotic characteristics of each species' contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

Richness, not evenness, varies across water availability gradients in grassy biomes on five continents.

We sought to understand the role that water availability (expressed as an aridity index) plays in determining regional and global patterns of richness and evenness, and in turn how these water availability-diversity relationships may result in different richness-evenness relationships at regional and global scales. We examined relationships between water availability, richness and evenness for eight grassy biomes spanning broad water availability gradients on five continents. Our study found that relationships between richness and water availability switched from positive for drier (South Africa, Tibet and USA) vs. negative for wetter (India) biomes, though were not significant for the remaining biomes. In contrast, only the India biome showed a significant relationship between water availability and evenness, which was negative. Globally, the richness-water availability relationship was hump-shaped, however, not significant for evenness. At the regional scale, a positive richness-evenness relationship was found for grassy biomes in India and Inner Mongolia, China. In contrast, this relationship was weakly concave-up globally. These results suggest that different, independent factors are determining patterns of species richness and evenness in grassy biomes, resulting in differing richness-evenness relationships at regional and global scales. As a consequence, richness and evenness may respond very differently across spatial gradients to anthropogenic changes, such as climate change.

Structural and functional leaf diversity lead to variability in photosynthetic capacity across a range of Juglans regia genotypes.

Similar to other cropping systems, few walnut cultivars are used as scion in commercial production. Germplasm collections can be used to diversify cultivar options and hold potential for improving crop productivity, disease resistance and stress tolerance. In this study, we explored the anatomical and biochemical bases of photosynthetic capacity and response to water stress in 11 Juglans regia accessions in the U.S. department of agriculture, agricultural research service (USDA-ARS) National Clonal Germplasm. Net assimilation rate (An ) differed significantly among accessions and was greater in lower latitudes coincident with higher stomatal and mesophyll conductances, leaf thickness, mesophyll porosity, gas-phase diffusion, leaf nitrogen and lower leaf mass and stomatal density. High CO2 -saturated assimilation rates led to increases in An under diffusional and biochemical limitations. Greater An was found in lower-latitude accessions native to climates with more frost-free days, greater precipitation seasonality and lower temperature seasonality. As expected, water stress consistently impaired photosynthesis with the highest % reductions in lower-latitude accessions (A3, A5 and A9), which had the highest An under well-watered conditions. However, An for A3 and A5 remained among the highest under dehydration. J. regia accessions, which have leaf structural traits and biochemistry that enhance photosynthesis, could be used as commercial scions or breeding parents to enhance productivity.

Resprouting grasses are associated with less frequent fire than seeders.

Plant populations persist under recurrent fire via resprouting from surviving tissues (resprouters) or seedling recruitment (seeders). Woody species are inherently slow maturing, meaning that seeders are confined to infrequent fire regimes. However, for grasses, which mature faster, the relationships between persistence strategy and fire regime remain unknown. Globally, we analysed associations between fire regimes experienced by hundreds of grass species and their persistence strategy, within a phylogenetic context. We also tested whether persistence strategies are associated with morphological and physiological traits. Resprouters were associated with less frequent fire than seeders. Whilst modal fire frequencies were similar (fire return interval of 4-6 yr), seeders were restricted to regions with more frequent fire than resprouters, suggesting that greater competition with long-lived resprouters restricts seeder recruitment and survival when fire is rare. Resprouting was associated with lower leaf N, higher C:N ratios and the presence of belowground buds, but was unrelated to photosynthetic pathway. Differences between the life histories of grasses and woody species led to a contrasting prevalence of seeders and resprouters in relation to fire frequency. Rapid sexual maturation in grasses means that seeder distributions, relative to fire regime, are determined by competitive ability and recruitment, rather than time to reproductive maturity.

Digitally deconstructing leaves in 3D using X-ray microcomputed tomography and machine learning.

PREMISE: X-ray microcomputed tomography (microCT) can be used to measure 3D leaf internal anatomy, providing a holistic view of tissue organization. Previously, the substantial time needed for segmenting multiple tissues limited this technique to small data sets, restricting its utility for phenotyping experiments and limiting our confidence in the inferences of these studies due to low replication numbers. METHODS AND RESULTS: We present a Python codebase for random forest machine learning segmentation and 3D leaf anatomical trait quantification that dramatically reduces the time required to process single-leaf microCT scans into detailed segmentations. By training the model on each scan using six hand-segmented image slices out of >1500 in the full leaf scan, it achieves >90% accuracy in background and tissue segmentation. CONCLUSIONS: Overall, this 3D segmentation and quantification pipeline can reduce one of the major barriers to using microCT imaging in high-throughput plant phenotyping.

Extreme heat effects on perennial crops and strategies for sustaining future production.

Extreme heat events will challenge agricultural production and raise the risk of food insecurity. California is the largest agricultural producer in the United States, and climate change and extreme heat may significantly affect the state's food production. This paper provides a summary of the current literature on crop responses to extreme heat, with a focus on perennial agriculture in California. We highlight contemporary trends and future projections in heat extremes, and the range of plant responses to extreme heat exposure, noting the variability in plant tolerance and response across season, crop, and cultivar. We also review practices employed to mitigate heat damage and the capacity for those practices to serve as adaptation options in a warmer and drier future. Finally, we discuss current and future research directions aimed at increasing the adaptive capacity of perennial agriculture to the increased heat exposure anticipated with climate change. Collectively, the literature reviewed makes clear the need to understand crop responses and tolerances to heat within the context of climate change and climate extremes in order to sustain crop production, preserve agricultural communities, and bolster food security at local, national, and global scales.

Demystifying dominant species.

The pattern of a few abundant species and many rarer species is a defining characteristic of communities worldwide. These abundant species are often referred to as dominant species. Yet, despite their importance, the term dominant species is poorly defined and often used to convey different information by different authors. Based on a review of historical and contemporary definitions we develop a synthetic definition of dominant species. This definition incorporates the relative local abundance of a species, its ubiquity across the landscape, and its impact on community and ecosystem properties. A meta-analysis of removal studies shows that the loss of species identified as dominant by authors can significantly impact ecosystem functioning and community structure. We recommend two metrics that can be used jointly to identify dominant species in a given community and provide a roadmap for future avenues of research on dominant species. In our review, we make the case that the identity and effects of dominant species on their environments are key to linking patterns of diversity to ecosystem function, including predicting impacts of species loss and other aspects of global change on ecosystems.

Change in dominance determines herbivore effects on plant biodiversity.

Herbivores alter plant biodiversity (species richness) in many of the world's ecosystems, but the magnitude and the direction of herbivore effects on biodiversity vary widely within and among ecosystems. One current theory predicts that herbivores enhance plant biodiversity at high productivity but have the opposite effect at low productivity. Yet, empirical support for the importance of site productivity as a mediator of these herbivore impacts is equivocal. Here, we synthesize data from 252 large-herbivore exclusion studies, spanning a 20-fold range in site productivity, to test an alternative hypothesis-that herbivore-induced changes in the competitive environment determine the response of plant biodiversity to herbivory irrespective of productivity. Under this hypothesis, when herbivores reduce the abundance (biomass, cover) of dominant species (for example, because the dominant plant is palatable), additional resources become available to support new species, thereby increasing biodiversity. By contrast, if herbivores promote high dominance by increasing the abundance of herbivory-resistant, unpalatable species, then resource availability for other species decreases reducing biodiversity. We show that herbivore-induced change in dominance, independent of site productivity or precipitation (a proxy for productivity), is the best predictor of herbivore effects on biodiversity in grassland and savannah sites. Given that most herbaceous ecosystems are dominated by one or a few species, altering the competitive environment via herbivores or by other means may be an effective strategy for conserving biodiversity in grasslands and savannahs globally.

Repeated evolution of vertebrate pollination syndromes in a recently diverged Andean plant clade.

Although specialized interactions, including those involving plants and their pollinators, are often invoked to explain high species diversity, they are rarely explored at macroevolutionary scales. We investigate the dynamic evolution of hummingbird and bat pollination syndromes in the centropogonid clade (Lobelioideae: Campanulaceae), an Andean-centered group of ∼550 angiosperm species. We demonstrate that flowers hypothesized to be adapted to different pollinators based on flower color fall into distinct regions of morphospace, and this is validated by morphology of species with known pollinators. This supports the existence of pollination syndromes in the centropogonids, an idea corroborated by ecological studies. We further demonstrate that hummingbird pollination is ancestral, and that bat pollination has evolved ∼13 times independently, with ∼11 reversals. This convergence is associated with correlated evolution of floral traits within selective regimes corresponding to pollination syndrome. Collectively, our results suggest that floral morphological diversity is extremely labile, likely resulting from selection imposed by pollinators. Finally, even though this clade's rapid diversification is partially attributed to their association with vertebrate pollinators, we detect no difference in diversification rates between hummingbird- and bat-pollinated lineages. Our study demonstrates the utility of pollination syndromes as a proxy for ecological relationships in macroevolutionary studies of certain species-rich clades.

Different clades and traits yield similar grassland functional responses.

Plant functional traits are viewed as key to predicting important ecosystem and community properties across resource gradients within and among biogeographic regions. Vegetation dynamics and ecosystem processes, such as aboveground net primary productivity (ANPP), are increasingly being modeled as a function of the quantitative traits of species, which are used as proxies for photosynthetic rates and nutrient and water-use efficiency. These approaches rely on an assumption that a certain trait value consistently confers a specific function or response under given environmental conditions. Here, we provide a critical test of this idea and evaluate whether the functional traits that drive the well-known relationship between precipitation and ANPP differ between systems with distinct biogeographic histories and species assemblages. Specifically, we compared grasslands spanning a broad precipitation gradient (∼200-1,000 mm/y) in North America and South Africa that differ in the relative representation and abundance of grass phylogenetic lineages. We found no significant difference between the regions in the positive relationship between annual precipitation and ANPP, yet the trait values underlying this relationship differed dramatically. Our results challenge the trait-based approach to predicting ecosystem function by demonstrating that different combinations of functional traits can act to maximize ANPP in a given environmental setting. Further, we show the importance of incorporating biogeographic and phylogenetic history in predicting community and ecosystem properties using traits.

The joint evolution of traits and habitat: ontogenetic shifts in leaf morphology and wetland specialization in Lasthenia.

The interplay between functional traits and habitat associations drives species' evolutionary responses to environmental heterogeneity, including processes such as adaptation, ecological speciation, and niche evolution. Seasonal variation is an aspect of the environment that varies across habitats, and could result in adaptive shifts in trait values across the life cycle of a plant. Here, we use phylogenetic comparative methods to evaluate the joint evolution of plant traits and habitat associations in Lasthenia (Asteraceae), a small clade of predominantly annual plants that have differentiated into an ecologically diverse range of habitats, including seasonal ephemeral wetlands known as vernal pools. Our results support the hypothesis that there is a link between the evolution of leaf morphology and the ecohydrological niche in Lasthenia, and, in the formation of aerenchyma (air space), differentiation between vernal pool and terrestrial taxa is fine-tuned to specific stages of plant ontogeny that reflects the evolution of heterophylly. Our findings demonstrate how the relationships between traits and habitat type can vary across the development of an organism, while highlighting a carefully considered comparative approach for examining correlated trait and niche evolution in a recently diversified and ecologically diverse plant clade.

Convergent phylogenetic and functional responses to altered fire regimes in mesic savanna grasslands of North America and South Africa.

The importance of fire in the creation and maintenance of mesic grassland communities is well recognized. Improved understanding of how grasses--the dominant clade in these important ecosystems--will respond to alterations in fire regimes is needed in the face of anthropogenically driven climate and land-use change. Here, we examined how grass communities shift in response to experimentally manipulated fire regimes at multiple levels of community diversity--taxonomic, phylogenetic and functional--in C4-dominanted mesic savanna grassland sites with similar structure and physiognomy, yet disparate biogeographic histories. We found that the grass communities were similar in their phylogenetic response and aspects of their functional response to high fire frequency. Both sites exhibited phylogenetic clustering of highly abundant species in annually burned plots, driven by species of the Andropogoneae, and a narrow range of functional strategies associated with rapid post-fire regeneration in a high-light, nitrogen-limited environment. By examining multiple facets of diversity in a comparative context, we identified convergent phylogenetic and functional responses to altered fire regimes in two mesic savanna grasslands. Our results highlight the importance of a common filtering process associated with fire that is consistent across grasslands of disparate biogeographic histories and taxonomic representation.

Effect of local community phylogenetic structure on pollen limitation in an obligately insect-pollinated plant.

PREMISE OF THE STUDY: Pollination is a key aspect of ecosystem function in the majority of land plant communities. It is well established that many animal-pollinated plants suffer lower seed set than they are capable of, likely because of competition for pollinators. Previously, competition for pollinator services has been shown to be most intense in communities with the greatest plant diversity. In spite of the fact that community evolutionary relations have a demonstrated impact on many ecological processes, their role in competition for pollinator services has rarely been examined. METHODS: In this study, we explore relations among several aspects of the surrounding plant community, including species richness, phylodiversity, evolutionary distance from a focal species, and pollen limitation in an annual insect-pollinated plant. KEY RESULTS: We did not find a significant effect of species richness on competition for pollination. However, consistent with a greater role for facilitation than competition, we found that a focal species occurring in communities composed of species of close relatives, especially other members of the Asteraceae, was less pollen limited than when it occurred in communities composed of more distant relatives. CONCLUSIONS: Our results demonstrate that community phylodiversity is an important correlate of pollen limitation in this system and that it has greater explanatory power than species richness alone.