Expression-environment associations in transcriptomic heat stress responses for a global plant lineage.

The increasing frequency and severity of heatwaves will intensify stress on plants. Given regional variation in heatwave exposure and expected differences in thermal tolerance between species it is unlikely that all plant species will be affected equally by climate change. However, little is currently known about variation in the responses of plants to heat stress, or how those responses differ among closely related species adapted to different environments. Here we quantify the response of 17 Acacia species (175 RNA-seq libraries), from across Australia's diverse biomes, to a multi-day experimental heatwave treatment to identify variation in transcriptomic and physiological responses to heat stress. Genes with known heat response functions showed consistent responses across Acacia species. Up to 10% of all genes and over 100 gene families showed significant clinal variation in the magnitude of their expression plasticity across species. Specifically, gene families linked to the temperature stress response were overrepresented among significant relationships with home range temperature conditions. Gene expression responses seen on the first day of the heatwave were more frequently associated with home range climates, while expression responses by day four were more commonly related to photosystem II acclimation. Comparative transcriptomics on non-model species has the potential to provide key information on stress response plasticity, especially when linked with our understanding of model species. Our study indicates that the pressing challenge to identifying potentially vulnerable species to climate change could be benefited by the further exploration of clinal variation in transcriptome plasticity.

Global dominance of lianas over trees is driven by forest disturbance, climate and topography.

Growing evidence suggests that liana competition with trees is threatening the global carbon sink by slowing the recovery of forests following disturbance. A recent theory based on local and regional evidence further proposes that the competitive success of lianas over trees is driven by interactions between forest disturbance and climate. We present the first global assessment of liana-tree relative performance in response to forest disturbance and climate drivers. Using an unprecedented dataset, we analysed 651 vegetation samples representing 26,538 lianas and 82,802 trees from 556 unique locations worldwide, derived from 83 publications. Results show that lianas perform better relative to trees (increasing liana-to-tree ratio) when forests are disturbed, under warmer temperatures and lower precipitation and towards the tropical lowlands. We also found that lianas can be a critical factor hindering forest recovery in disturbed forests experiencing liana-favourable climates, as chronosequence data show that high competitive success of lianas over trees can persist for decades following disturbances, especially when the annual mean temperature exceeds 27.8°C, precipitation is less than 1614 mm and climatic water deficit is more than 829 mm. These findings reveal that degraded tropical forests with environmental conditions favouring lianas are disproportionately more vulnerable to liana dominance and thus can potentially stall succession, with important implications for the global carbon sink, and hence should be the highest priority to consider for restoration management.

Des preuves de plus en plus nombreuses suggèrent que la competition entre lianes et les arbres menace le puits de carbone mondial en ralentissant la récupération des forêts après une perturbation. Une théorie récente, fondée sur des observations locales et régionales, propose en outre que le succès compétitif des lianes sur les arbres est dû aux interactions entre la perturbation forestière et le climat. Nous présentons la première évaluation mondiale de la performance relative des lianes par rapport aux arbres en réponse aux perturbations forestières et aux facteurs climatiques. En utilisant un ensemble de données sans précédent, nous avons analysé 651 échantillons de végétation représentant 26,538 lianes et 82,802 arbres, issus de 556 emplacements uniques dans le monde entier, tirés de 83 publications. Les résultats montrent que les lianes ont de meilleure performances par rapport aux arbres (augmentation du ratio liane-arbre) lorsque les forêts sont perturbées, sous des zones chaudes aves précipitations faibles, et vers les basses altitudes tropicales. Nous avons également constaté que les lianes peuvent être un facteur critique entravant la récupération des forêts dans les forêts perturbées connaissant des climats favorables aux lianes, car les données de chronoséquence montrent que le succès compétitif élevé des lianes sur les arbres peut persister pendant des décennies après les perturbations, surtout lorsque la température annuelle moyenne dépasse 27.8°C, que les précipitations sont inférieures à 1614 mm et que le déficit hydrique climatique est supérieur à 829 mm. Ces découvertes révèlent que les forêts tropicales dégradées avec des conditions environnementales favorables aux lianes sont disproportionnellement plus vulnérables à la dominance des lianes, et peuvent ainsi potentiellement entraver la succession, avec d'importantes implications pour le puits de carbone mondial et devraient donc être la plus haute priorité à considérer pour la gestion de la restauration.

Transcriptome Mining Expands Knowledge of RNA Viruses across the Plant Kingdom.

Our current understanding of plant viruses stems largely from those affecting economically important plants. Yet plant species in cultivation represent a small and biased subset of the plant kingdom. Here, we describe virus diversity and abundance in 1,079 transcriptomes from species across the breadth of the plant kingdom (Archaeplastida) by analyzing open-source data from the 1000 Plant Transcriptomes Initiative (1KP). We identified 104 potentially novel viruses, of which 40% were single-stranded positive-sense RNA viruses across eight orders, including members of the Hepelivirales, Tymovirales, Cryppavirales, Martellivirales, and Picornavirales. One-third of the newly described viruses were double-stranded RNA viruses from the orders Durnavirales and Ghabrivirales. The remaining were negative-sense RNA viruses from the Rhabdoviridae, Aspiviridae, Yueviridae, and Phenuiviridae and the newly proposed Viridisbunyaviridae. Our analysis considerably expands the known host range of 13 virus families to include lower plants (e.g., Benyviridae and Secoviridae) and 4 virus families to include alga hosts (e.g., Tymoviridae and Chrysoviridae). More broadly, however, a cophylogeny analysis revealed that the evolutionary history of these families is largely driven by cross-species transmission events. The discovery of the first 30-kDa movement protein in a nonvascular plant suggests that the acquisition of plant virus movement proteins occurred prior to the emergence of the plant vascular system. Together, these data highlight that numerous RNA virus families are associated with older evolutionary plant lineages than previously thought and that the apparent scarcity of RNA viruses found in lower plants likely reflects a lack of investigation rather than their absence. IMPORTANCE Our knowledge of plant viruses is mainly limited to those infecting economically important host species. In particular, we know little about those viruses infecting basal plant lineages such as the ferns, lycophytes, bryophytes, and charophytes. To expand this understanding, we conducted a broad-scale viral survey of species across the breadth of the plant kingdom. We found that basal plants harbor a wide diversity of RNA viruses, including some that are sufficiently divergent to likely compose a new virus family. The basal plant virome revealed offers key insights into the evolutionary history of core plant virus gene modules and genome segments. More broadly, this work emphasizes that the scarcity of viruses found in these species to date most likely reflects the limited research in this area.

Insect pollination for most of angiosperm evolutionary history.

Most contemporary angiosperms (flowering plants) are insect pollinated, but pollination by wind, water or vertebrates occurs in many lineages. Though evidence suggests insect pollination may be ancestral in angiosperms, this is yet to be assessed across the full phylogeny. Here, we reconstruct the ancestral pollination mode of angiosperms and quantify the timing and environmental associations of pollination shifts. We use a robust, dated phylogeny and species-level sampling across all angiosperm families to model the evolution of pollination modes. Data on the pollination system or syndrome of 1160 species were collated from the primary literature. Angiosperms were ancestrally insect pollinated, and insects have pollinated angiosperms for c. 86% of angiosperm evolutionary history. Wind pollination evolved at least 42 times, with few reversals to animal pollination. Transitions between insect and vertebrate pollination were more frequent: vertebrate pollination evolved at least 39 times from an insect-pollinated ancestor with at least 26 reversals. The probability of wind pollination increases with habitat openness (measured by Leaf Area Index) and distance from the equator. Our reconstruction gives a clear overview of pollination macroevolution across angiosperms, highlighting the long history of interactions between insect pollinators and angiosperms still vital to biodiversity today.

Towards species-level forecasts of drought-induced tree mortality risk.

Predicting species-level responses to drought at the landscape scale is critical to reducing uncertainty in future terrestrial carbon and water cycle projections. We embedded a stomatal optimisation model in the Community Atmosphere Biosphere Land Exchange (CABLE) land surface model and parameterised the model for 15 canopy dominant eucalypt tree species across South-Eastern Australia (mean annual precipitation range: 344-1424 mm yr-1 ). We conducted three experiments: applying CABLE to the 2017-2019 drought; a 20% drier drought; and a 20% drier drought with a doubling of atmospheric carbon dioxide (CO2 ). The severity of the drought was highlighted as for at least 25% of their distribution ranges, 60% of species experienced leaf water potentials beyond the water potential at which 50% of hydraulic conductivity is lost due to embolism. We identified areas of severe hydraulic stress within-species' ranges, but we also pinpointed resilience in species found in predominantly semiarid areas. The importance of the role of CO2 in ameliorating drought stress was consistent across species. Our results represent an important advance in our capacity to forecast the resilience of individual tree species, providing an evidence base for decision-making around the resilience of restoration plantings or net-zero emission strategies.

Embedding biodiversity research into climate adaptation policy and practice.

Addressing climate change risks requires collaboration and engagement across all sectors of society. In particular, effective partnerships are needed between research scientists producing new knowledge, policy-makers and practitioners who apply conservation actions on the ground. We describe the implementation of a model for increasing the application and useability of biodiversity research in climate adaptation policy and practice. The focus of the program was to increase the ability of a state government agency and natural resource practitioners in Australia to manage and protect biodiversity in a changing climate. The model comprised a five-stage process for enhancing impact (i) initiation of research projects that addressed priority conservation policy and management issues; (ii) co-design of the research using a collaborative approach involving multiple stakeholders; (iii) implementation of the research and design of decision tools and web-based resources; (iv) collaborative dissemination of the tools and resources via government and community working groups; and (v) evaluation of research impact. We report on the model development and implementation, and critically reflect on the model's impact. We share the lessons learnt from the challenges of operating within a stakeholder group with diverse objectives and criteria for success, and provide a template for creating an environmental research program with real world impact.

Leaf size estimation based on leaf length, width and shape.

BACKGROUND AND AIMS: Leaf size has considerable ecological relevance, making it desirable to obtain leaf size estimations for as many species worldwide as possible. Current global databases, such as TRY, contain leaf size data for ~30 000 species, which is only ~8% of known species worldwide. Yet, taxonomic descriptions exist for the large majority of the remainder. Here we propose a simple method to exploit information on leaf length, width and shape from species descriptions to robustly estimate leaf areas, thus closing this considerable knowledge gap for this important plant functional trait. METHODS: Using a global dataset of all major leaf shapes measured on 3125 leaves from 780 taxa, we quantified scaling functions that estimate leaf size as a product of leaf length, width and a leaf shape-specific correction factor. We validated our method by comparing leaf size estimates with those obtained from image recognition software and compared our approach with the widely used correction factor of 2/3. KEY RESULTS: Correction factors ranged from 0.39 for highly dissected, lobed leaves to 0.79 for oblate leaves. Leaf size estimation using leaf shape-specific correction factors was more accurate and precise than estimates obtained from the correction factor of 2/3. CONCLUSION: Our method presents a tractable solution to accurately estimate leaf size when only information on leaf length, width and shape is available or when labour and time constraints prevent usage of image recognition software. We see promise in applying our method to data from species descriptions (including from fossils), databases, field work and on herbarium vouchers, especially when non-destructive in situ measurements are needed.

Importance of species translocations under rapid climate change.

Species that cannot adapt or keep pace with a changing climate are likely to need human intervention to shift to more suitable climates. While hundreds of articles mention using translocation as a climate-change adaptation tool, in practice, assisted migration as a conservation action remains rare, especially for animals. This is likely due to concern over introducing species to places where they may become invasive. However, there are other barriers to consider, such as time-frame mismatch, sociopolitical, knowledge and uncertainty barriers to conservationists adopting assisted migration as a go-to strategy. We recommend the following to advance assisted migration as a conservation tool: attempt assisted migrations at small scales, translocate species with little invasion risk, adopt robust monitoring protocols that trigger an active response, and promote political and public support.

Importancia de las Reubicaciones de Especies bajo el Cambio Climático Acelerado Resumen Las especies que no pueden adaptarse o mantener el ritmo del cambio climático probablemente requieran de la intervención humana para mudarse a climas más adecuados. Mientras que cientos de artículos mencionan el uso de las reubicaciones como una herramienta de adaptación al cambio climático, en la práctica, la migración asistida todavía es rara como una acción de conservación, especialmente para animales. Lo anterior probablemente se debe a la preocupación que existe por la introducción de especies a sitios en los que podrían volverse invasoras. Sin embargo, existen otras barreras que deberían considerarse, como aquellas ocasionadas por el desfase en el marco temporal, cuestiones sociopolíticas, de conocimiento o de incertidumbre para los conservacionistas que adoptan a la migración asistida como la estrategia de cajón. Recomendamos lo siguiente para que la migración asistida avance como herramienta de conservación: intentar realizar migraciones asistidas a pequeñas escalas, reubicar especies con poco riesgo de invasión, adoptar protocolos de monitoreo robustos que generen una respuesta activa y promover el apoyo público y político.

A global growth-form database for 143,616 vascular plant species.

For the majority of plant species in the world, we know little about their functional ecology, and not even one of the most basic traits-the species' growth habit. To fill the gap in availability of compiled plant growth-form data, we have assembled what is, to our knowledge, the largest global database on growth-form as a plant trait. We have, with extensive error checking and data synthesis, assembled a growth-form database from 163 data sources for 143,616 vascular plant species from 445 different plant families. This is 38.6% of the currently accepted vascular plant diversity. For our database, we have chosen seven categories to cover the majority of the diversity in plant growth forms: aquatic plants, epiphytes, hemiepiphytes, climbing plants, parasitic plants, holo-mycoheterotrophs, and freestanding plants. These categories were used because we were able to reconcile the wealth of existing definitions and types of growth-form information available globally to them clearly and unequivocally, and because they are complementary with existing databases. Plants in the database were designated into a category if their adult growth form fit the criterion. We make available two databases: first, the complete data set, including species for which there is currently conflicting information, and second, a consensus data set, where all available information supports one categorization. Of the plant species for which we found information, 103,138 (72%) are freestanding, 21,110 (15%) are epiphytes, and 4,046 (3%) are parasites. Our growth-form data can be used to produce useful summary statistics by clade. For example, current data suggests that half of pteridophytes are epiphytic, that all hemiepiphytes are eudicots, and that there are no parasitic monocots, gymnosperms, or pteridophytes. Growth form is a crucial piece of fundamental plant-trait data with implications for each species' ecology, evolution, and conservation, and thus this data set will be useful for a range of basic and applied questions across these areas of research. No copyright or proprietary restrictions are associated with the use of this data set, other than citation of the present Data Paper. A static version of this dataset is provided as Supporting Information, and a living and updating version of the dataset is available in a GitHub repository.

A tool to assess potential for alien plant establishment and expansion under climate change.

Predicting the influence of climate change on the potential distribution of naturalised alien plant species is an important and challenging task. While prioritisation of management actions for alien plants under current climatic conditions has been widely adopted, very few systems explicitly incorporate the potential of future changes in climate conditions to influence the distribution of alien plant species. Here, we develop an Australia-wide screening tool to assess the potential of naturalised alien plants to establish and spread under both current and future climatic conditions. The screening tool developed uses five spatially explicit criteria to establish the likelihood of alien plant population establishment and expansion under baseline climate conditions and future climates for the decades 2035 and 2065. Alien plants are then given a threat rating according to current and future threat to enable natural resource managers to focus on those species that pose the largest potential threat now and in the future. To demonstrate the screening tool, we present results for a representative sample of approximately 10% (n = 292) of Australia's known, naturalised alien plant species. Overall, most alien plant species showed decreases in area of habitat suitability under future conditions compared to current conditions and therefore the threat rating of most alien plant species declined between current and future conditions. Use of the screening tool is intended to assist natural resource managers in assessing the threat of alien plant establishment and spread under current and future conditions and thus prioritise detailed weed risk assessments for those species that pose the greatest threat. The screening tool is associated with a searchable database for all 292 alien plant species across a range of spatial scales, available through an interactive web-based portal at http://weedfutures.net/.

The AusTraits plant dictionary.

Traits with intuitive names, a clear scope and explicit description are essential for all trait databases. The lack of unified, comprehensive, and machine-readable plant trait definitions limits the utility of trait databases, including reanalysis of data from a single database, or analyses that integrate data across multiple databases. Both can only occur if researchers are confident the trait concepts are consistent within and across sources. Here we describe the AusTraits Plant Dictionary (APD), a new data source of terms that extends the trait definitions included in a recent trait database, AusTraits. The development process of the APD included three steps: review and formalisation of the scope of each trait and the accompanying trait description; addition of trait metadata; and publication in both human and machine-readable forms. Trait definitions include keywords, references, and links to related trait concepts in other databases, enabling integration of AusTraits with other sources. The APD will both improve the usability of AusTraits and foster the integration of trait data across global and regional plant trait databases.

Changing plant functional diversity over the last 12,000 years provides perspectives for tracking future changes in vegetation communities.

Plant communities are largely reshaped by climate and the environment over millennia, providing a powerful tool for understanding their response to future climates. Using a globally applicable functional palaeocological approach, we provide a deeper understanding of fossil pollen-inferred long-term response of vegetation to past climatic disturbances based on changes in functional trait composition. Specifically, we show how and why the ecological strategies exhibited by vegetation have changed through time by linking observations of plant traits to multiple pollen records from southeast Australia to reconstruct past functional diversity (FD, the value and the range of species traits that influence ecosystem functioning). The drivers of FD changes were assessed quantitatively by comparing FD reconstructions to independent records of past climates. During the last 12,000 years, peaks in FD were associated with both dry and wet climates in southeast Australia, with shifts in leaf traits particularly pronounced under wet conditions. Continentality determined the degree of stability maintained by high FD, with the greatest seen on the mainland. We expect projected frequent drier conditions in southeast Australia over coming decades to drive changes in vegetation community functioning and productivity mirroring the functional palaeocological record, particularly in western Tasmania and western southeast mainland.

Characterizing Effects of Microbial Biostimulants and Whole-Soil Inoculums for Native Plant Revegetation.

Soil microbes play important roles in plant health and ecosystem functioning, however, they can often be disturbed or depleted in degraded lands. During seed-based revegetation of such sites there is often very low germination and seedling establishment success, with recruitment of beneficial microbes to the rhizosphere one potential contributor to this problem. Here we investigated whether Australian native plant species may benefit from planting seed encapsulated within extruded seed pellets amended with one of two microbe-rich products: a commercial vermicast extract biostimulant or a whole-soil inoculum from a healthy reference site of native vegetation. Two manipulative glasshouse trials assessing the performance of two Australian native plant species (Acacia parramattensis and Indigofera australis) were carried out in both unmodified field-collected soil (trial 1) and in the same soil reduced in nutrients and microbes (trial 2). Seedling emergence and growth were compared between pelleted and bare-seeded controls and analyzed alongside soil nutrient concentrations and culturable microbial community assessments. The addition of microbial amendments maintained, but did not improve upon, high levels of emergence in both plant species relative to unamended pellets. In trial 1, mean time to emergence of Acacia parramattensis seedlings was slightly shorter in both amended pellet types relative to the standard pellets, and in trial 2, whole-soil inoculum pellets showed significantly improved growth metrics. This work shows that there is potential for microbial amendments to positively affect native plant emergence and growth, however exact effects are dependent on the type of amendment, the plant species, and the characteristics of the planting site soil.

Germination at Extreme Temperatures: Implications for Alpine Shrub Encroachment.

Worldwide, shrub cover is increasing across alpine and tundra landscapes in response to warming ambient temperatures and declines in snowpack. With a changing climate, shrub encroachment may rely on recruitment from seed occurring outside of the optimum temperature range. We used a temperature gradient plate in order to determine the germination niche of 14 alpine shrub species. We then related the range in laboratory germination temperatures of each species to long-term average temperature conditions at: (1) the location of the seed accession site and (2) across each species geographic distribution. Seven of the species failed to germinate sufficiently to be included in the analyses. For the other species, the germination niche was broad, spanning a range in temperatures of up to 17 °C, despite very low germination rates in some species. Temperatures associated with the highest germination percentages were all above the range of temperatures present at each specific seed accession site. Optimum germination temperatures were consistently within or higher than the range of maximum temperatures modelled across the species' geographic distribution. Our results indicate that while some shrub species germinate well at high temperatures, others are apparently constrained by an inherent seed dormancy. Shrub encroachment in alpine areas will likely depend on conditions that affect seed germination at the microsite-scale, despite overall conditions becoming more suitable for shrubs at high elevations.

AusTraits, a curated plant trait database for the Australian flora.

We introduce the AusTraits database - a compilation of values of plant traits for taxa in the Australian flora (hereafter AusTraits). AusTraits synthesises data on 448 traits across 28,640 taxa from field campaigns, published literature, taxonomic monographs, and individual taxon descriptions. Traits vary in scope from physiological measures of performance (e.g. photosynthetic gas exchange, water-use efficiency) to morphological attributes (e.g. leaf area, seed mass, plant height) which link to aspects of ecological variation. AusTraits contains curated and harmonised individual- and species-level measurements coupled to, where available, contextual information on site properties and experimental conditions. This article provides information on version 3.0.2 of AusTraits which contains data for 997,808 trait-by-taxon combinations. We envision AusTraits as an ongoing collaborative initiative for easily archiving and sharing trait data, which also provides a template for other national or regional initiatives globally to fill persistent gaps in trait knowledge.

Areas of global importance for conserving terrestrial biodiversity, carbon and water.

To meet the ambitious objectives of biodiversity and climate conventions, the international community requires clarity on how these objectives can be operationalized spatially and how multiple targets can be pursued concurrently. To support goal setting and the implementation of international strategies and action plans, spatial guidance is needed to identify which land areas have the potential to generate the greatest synergies between conserving biodiversity and nature's contributions to people. Here we present results from a joint optimization that minimizes the number of threatened species, maximizes carbon retention and water quality regulation, and ranks terrestrial conservation priorities globally. We found that selecting the top-ranked 30% and 50% of terrestrial land area would conserve respectively 60.7% and 85.3% of the estimated total carbon stock and 66% and 89.8% of all clean water, in addition to meeting conservation targets for 57.9% and 79% of all species considered. Our data and prioritization further suggest that adequately conserving all species considered (vertebrates and plants) would require giving conservation attention to ~70% of the terrestrial land surface. If priority was given to biodiversity only, managing 30% of optimally located land area for conservation may be sufficient to meet conservation targets for 81.3% of the terrestrial plant and vertebrate species considered. Our results provide a global assessment of where land could be optimally managed for conservation. We discuss how such a spatial prioritization framework can support the implementation of the biodiversity and climate conventions.

Publisher Correction: Open Science principles for accelerating trait-based science across the Tree of Life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Open Science principles for accelerating trait-based science across the Tree of Life.

Synthesizing trait observations and knowledge across the Tree of Life remains a grand challenge for biodiversity science. Species traits are widely used in ecological and evolutionary science, and new data and methods have proliferated rapidly. Yet accessing and integrating disparate data sources remains a considerable challenge, slowing progress toward a global synthesis to integrate trait data across organisms. Trait science needs a vision for achieving global integration across all organisms. Here, we outline how the adoption of key Open Science principles-open data, open source and open methods-is transforming trait science, increasing transparency, democratizing access and accelerating global synthesis. To enhance widespread adoption of these principles, we introduce the Open Traits Network (OTN), a global, decentralized community welcoming all researchers and institutions pursuing the collaborative goal of standardizing and integrating trait data across organisms. We demonstrate how adherence to Open Science principles is key to the OTN community and outline five activities that can accelerate the synthesis of trait data across the Tree of Life, thereby facilitating rapid advances to address scientific inquiries and environmental issues. Lessons learned along the path to a global synthesis of trait data will provide a framework for addressing similarly complex data science and informatics challenges.