The seed morphospace, a new contribution towards the multidimensional study of angiosperm sexual reproductive biology.

BACKGROUND: The evolutionary success of flowering plants is associated with the vast diversity of their reproductive structures. Despite recent progress in understanding angiosperm-wide trends of floral structure and evolution, a synthetic view of the diversity in seed form and function across angiosperms is lacking. SCOPE: Here we present a roadmap to synthesise the diversity of seed forms in extant angiosperms, relying on the morphospace concept, i.e. a mathematical representation which relates multiple traits and describes the realised morphologies. We provide recommendations on how to broaden the range of measurable traits beyond mass, by using key morphological traits representative of the embryo, endosperm, and seed coat but also fruit attributes (e.g., dehiscence, fleshiness). These key traits were used to construct and analyse a morphospace to detect evolutionary trends and gain insight into how morphological traits relate to seed functions. Finally, we outline challenges and future research directions, combining the morphospace with macroevolutionary comparative methods to underline the drivers that gave rise to the diversity of observed seed forms. CONCLUSIONS: We conclude that this multidimensional approach has the potential, although still untapped, to improve our understanding of covariation among reproductive traits, and further elucidate angiosperm reproductive biology as a whole.

The global spectrum of plant form and function.

Earth is home to a remarkable diversity of plant forms and life histories, yet comparatively few essential trait combinations have proved evolutionarily viable in today's terrestrial biosphere. By analysing worldwide variation in six major traits critical to growth, survival and reproduction within the largest sample of vascular plant species ever compiled, we found that occupancy of six-dimensional trait space is strongly concentrated, indicating coordination and trade-offs. Three-quarters of trait variation is captured in a two-dimensional global spectrum of plant form and function. One major dimension within this plane reflects the size of whole plants and their parts; the other represents the leaf economics spectrum, which balances leaf construction costs against growth potential. The global plant trait spectrum provides a backdrop for elucidating constraints on evolution, for functionally qualifying species and ecosystems, and for improving models that predict future vegetation based on continuous variation in plant form and function.

Trade-off between seed dispersal in space and time.

Seed movement and delayed germination have long been thought to represent alternative risk-spreading strategies, but current evidence covers limited scales and yields mixed results. Here we present the first global-scale test of a negative correlation between dispersal and dormancy. The result demonstrates a strong and consistent pattern that species with dormant seeds have reduced spatial dispersal, also in the context of life-history traits such as seed mass and plant lifespan. Long-lived species are more likely to have large, non-dormant seeds that are dispersed far. Our findings provide robust support for the theoretical prediction of a dispersal trade-off between space and time, implying that a joint consideration of risk-spreading strategies is imperative in studying plant life-history evolution. The bet-hedging patterns in the dispersal-dormancy correlation and the associated reproductive traits have implications for biodiversity conservation, via prediction of which plant groups would be most impacted in the changing era.

Macroevolutionary patterns in seed component mass and different evolutionary trajectories across seed desiccation responses.

Seed coat and seed reserve show substantial mass variation, play different roles in plant life strategies and are shaped by different selective forces. However, remarkably little is known about the macroevolution of the relative allocation in seed components and its influence on important ecophysiological processes. Using phylogenetic comparative methods and evolutionary modelling approaches, we modelled mass changes in seed components along individual lineages for 940 species and compared the patterns across seed desiccation responses. Seed component allocation was driven primarily by changes in reserve mass rather than coat mass, as evolutionary rates in reserve mass significantly outpaced those in coat mass. Although the scaling patterns between reserve mass and coat mass were similar across desiccation responses, desiccation-sensitive seeds allocated more and evolved faster in reserve compared to desiccation-tolerant seeds. The findings emphasize the relative importance of reserve to coat in the evolution of plant reproductive strategies, revealing potential ecological advantages gained by enlarged reserve. As the first quantification of the evolutionary tempo and mode of seed component mass, our study allows a detailed interpretation of evolutionary pathways underlying seed storage behaviours and advances the understanding of the evolution of desiccation sensitivity in seeds.

A research agenda for seed-trait functional ecology.

Trait-based approaches have improved our understanding of plant evolution, community assembly and ecosystem functioning. A major challenge for the upcoming decades is to understand the functions and evolution of early life-history traits, across levels of organization and ecological strategies. Although a variety of seed traits are critical for dispersal, persistence, germination timing and seedling establishment, only seed mass has been considered systematically. Here we suggest broadening the range of morphological, physiological and biochemical seed traits to add new understanding on plant niches, population dynamics and community assembly. The diversity of seed traits and functions provides an important challenge that will require international collaboration in three areas of research. First, we present a conceptual framework for a seed ecological spectrum that builds upon current understanding of plant niches. We then lay the foundation for a seed-trait functional network, the establishment of which will underpin and facilitate trait-based inferences. Finally, we anticipate novel insights and challenges associated with incorporating diverse seed traits into predictive evolutionary ecology, community ecology and applied ecology. If the community invests in standardized seed-trait collection and the implementation of rigorous databases, major strides can be made at this exciting frontier of functional ecology.

Taxonomic affinity, habitat and seed mass strongly predict seed desiccation response: a boosted regression trees analysis based on 17 539 species.

Background and Aims: Seed desiccation response plays an important role in plant regeneration ecology, and has significant implications for species conservation. The majority of seed plants produce desiccation-tolerant (orthodox) seeds, whilst comparatively few produce desiccation-sensitive (recalcitrant) seeds that are unable to survive dehydration, and which cannot be conserved in traditional seed banks. This study develops a set of models to predict seed desiccation response in unstudied species. Methods: Taxonomy, trait, location and climate data were compiled to form a global data set of 17 539 species. Three boosted regression trees models were then developed to predict species' seed desiccation responses based on habitat and trait information for the species, and the seed desiccation responses of close relatives (either members of the same genus, family or order, depending on the model). Ten-fold cross-validation was used to test model predictive success. The utility of the models was then demonstrated by predicting seed desiccation response for two floras: Ecuador, and Britain and Ireland. Key Results: The three models had varying success rates for identifying the desiccation-sensitive species: 89 % for the genus-level model, 79 % for the family-level model and 60 % for the order-level model. The most important predictor variables were the seed desiccation responses of a species' relatives, seed mass and annual precipitation. It is predicted that 10 % of seed plants from Ecuador and 1.2 % of those from Britain and Ireland produce desiccation-sensitive seeds. Due to data availability, prediction accuracy is likely to be higher for the British and Irish flora, where it is estimated that a desiccation-sensitive species had a 96.7 % chance of being correctly identified, compared with 80.8 % in the Ecuador flora. Conclusions: These models can utilize existing data to predict species' likely seed desiccation responses, providing a gap-filling tool for global studies of plant traits, as well as critical decision-making support for plant conservation activities.

Maximizing the phylogenetic diversity of seed banks.

Ex situ conservation efforts such as those of zoos, botanical gardens, and seed banks will form a vital complement to in situ conservation actions over the coming decades. It is therefore necessary to pay the same attention to the biological diversity represented in ex situ conservation facilities as is often paid to protected-area networks. Building the phylogenetic diversity of ex situ collections will strengthen our capacity to respond to biodiversity loss. Since 2000, the Millennium Seed Bank Partnership has banked seed from 14% of the world's plant species. We assessed the taxonomic, geographic, and phylogenetic diversity of the Millennium Seed Bank collection of legumes (Leguminosae). We compared the collection with all known legume genera, their known geographic range (at country and regional levels), and a genus-level phylogeny of the legume family constructed for this study. Over half the phylogenetic diversity of legumes at the genus level was represented in the Millennium Seed Bank. However, pragmatic prioritization of species of economic importance and endangerment has led to the banking of a less-than-optimal phylogenetic diversity and prioritization of range-restricted species risks an underdispersed collection. The current state of the phylogenetic diversity of legumes in the Millennium Seed Bank could be substantially improved through the strategic banking of relatively few additional taxa. Our method draws on tools that are widely applied to in situ conservation planning, and it can be used to evaluate and improve the phylogenetic diversity of ex situ collections.

Banana seed genetic resources for food security: Status, constraints, and future priorities.

Storing seed collections of crop wild relatives, wild plant taxa genetically related to crops, is an essential component in global food security. Seed banking protects genetic resources from degradation and extinction and provides material for use by breeders. Despite being among the most important crops in the world, banana and plantain crop wild relatives are largely under-represented in genebanks. Nevertheless, banana crop wild relative seed collections are in fact held in different countries, but these have not previously been part of reporting or analysis. To fill this gap, we firstly collated banana seed accession data from 13 institutions in 10 countries. These included 537 accessions containing an estimated 430,000 seeds of 56 species. We reviewed their taxonomic coverage and seed storage conditions including viability estimates. We found that seed accessions have low viability (25% mean) representing problems in seed storage and processing. Secondly, we surveyed 22 institutions involved in banana genetic resource conservation regarding the key constraints and knowledge gaps that institutions face related to banana seed conservation. Major constraints were identified including finding suitable material and populations to collect seeds from, lack of knowledge regarding optimal storage conditions and germination conditions. Thirdly, we carried out a conservation prioritization and gap analysis of Musaceae taxa, using established methods, to index representativeness. Overall, our conservation assessment showed that despite this extended data set banana crop wild relatives are inadequately conserved, with 51% of taxa not represented in seed collections at all; the average conservation assessment showing high priority for conservation according to the index. Finally, we provide recommendations for future collecting, research, and management, to conserve banana and plantain crop wild relatives in seed banks for future generations.

Drying banana seeds for ex situ conservation.

The ability of seeds to withstand drying is fundamental to ex situ seed conservation but drying responses are not well known for most wild species including crop wild relatives. We look at drying responses of seeds of Musa acuminata and Musa balbisiana, the two primary wild relatives of bananas and plantains, using the following four experimental approaches: (i) We equilibrated seeds to a range of relative humidity (RH) levels using non-saturated lithium chloride solutions and subsequently measured moisture content (MC) and viability. At each humidity level we tested viability using embryo rescue (ER), tetrazolium chloride staining and germination in an incubator. We found that seed viability was not reduced when seeds were dried to 4% equilibrium relative humidity (eRH; equating to 2.5% MC). (ii) We assessed viability of mature and less mature seeds using ER and germination in the soil and tested responses to drying. Findings showed that seeds must be fully mature to germinate and immature seeds had negligible viability. (iii) We dried seeds extracted from ripe/unripe fruit to 35-40% eRH at different rates and tested viability with germination tests in the soil. Seeds from unripe fruit lost viability when dried and especially when dried faster; seeds from ripe fruit only lost viability when fast dried. (iv) Finally, we dried and re-imbibed mature and less mature seeds and measured embryo shrinkage and volume change using X-ray computer tomography. Embryos of less mature seeds shrank significantly when dried to 15% eRH from 0.468 to 0.262 mm3, but embryos of mature seeds did not. Based on our results, mature seeds from ripe fruit are desiccation tolerant to moisture levels required for seed genebanking but embryos from immature seeds are mechanistically less able to withstand desiccation, especially when water potential gradients are high.

Corrigendum to: Drying banana seeds for ex situ conservation.

[This corrects the article DOI: 10.1093/conphys/coab099.].

Selecting the best candidates for resurrecting extinct-in-the-wild plants from herbaria.

Resurrecting extinct species is a fascinating and challenging idea for scientists and the general public. Whereas some theoretical progress has been made for animals, the resurrection of extinct plants (de-extinction sensu lato) is a relatively recently discussed topic. In this context, the term 'de-extinction' is used sensu lato to refer to the resurrection of 'extinct in the wild' species from seeds or tissues preserved in herbaria, as we acknowledge the current impossibility of knowing a priori whether a herbarium seed is alive and can germinate. In plants, this could be achieved by germinating or in vitro tissue-culturing old diaspores such as seeds or spores available in herbarium specimens. This paper reports the first list of plant de-extinction candidates based on the actual availability of seeds in herbarium specimens of globally extinct plants. We reviewed globally extinct seed plants using online resources and additional literature on national red lists, resulting in a list of 361 extinct taxa. We then proposed a method of prioritizing candidates for seed-plant de-extinction from diaspores found in herbarium specimens and complemented this with a phylogenetic approach to identify species that may maximize evolutionarily distinct features. Finally, combining data on seed storage behaviour and longevity, as well as specimen age in the novel 'best de-extinction candidate' score (DEXSCO), we identified 556 herbarium specimens belonging to 161 extinct species with available seeds. We expect that this list of de-extinction candidates and the novel approach to rank them will boost research efforts towards the first-ever plant de-extinction.

The global spectrum of plant form and function: enhanced species-level trait dataset.

Here we provide the 'Global Spectrum of Plant Form and Function Dataset', containing species mean values for six vascular plant traits. Together, these traits -plant height, stem specific density, leaf area, leaf mass per area, leaf nitrogen content per dry mass, and diaspore (seed or spore) mass - define the primary axes of variation in plant form and function. The dataset is based on ca. 1 million trait records received via the TRY database (representing ca. 2,500 original publications) and additional unpublished data. It provides 92,159 species mean values for the six traits, covering 46,047 species. The data are complemented by higher-level taxonomic classification and six categorical traits (woodiness, growth form, succulence, adaptation to terrestrial or aquatic habitats, nutrition type and leaf type). Data quality management is based on a probabilistic approach combined with comprehensive validation against expert knowledge and external information. Intense data acquisition and thorough quality control produced the largest and, to our knowledge, most accurate compilation of empirically observed vascular plant species mean traits to date.

Using seminatural and simulated habitats for seed germination ecology of banana wild relatives.

Ecologically meaningful seed germination experiments are constrained by access to seeds and relevant environments for testing at the same time. This is particularly the case when research is carried out far from the native area of the studied species.Here, we demonstrate an alternative-the use of glasshouses in botanic gardens as simulated-natural habitats to extend the ecological interpretation of germination studies. Our focal taxa were banana crop wild relatives (Musa acuminata subsp. burmannica, Musa acuminata subsp. siamea, and Musa balbisiana), native to tropical and subtropical South-East Asia. Tests were carried out in Belgium, where we performed germination tests in relation to foliage-shading/exposure to solar radiation and seed burial depth, as well as seed survival and dormancy release in the soil. We calibrated the interpretation of these studies by also conducting an experiment in a seminatural habitat in a species native range (M. balbisiana-Los Baños, the Philippines), where we tested germination responses to exposure to sun/shade. Using temperature data loggers, we determined temperature dynamics suitable for germination in both these settings.In these seminatural and simulated-natural habitats, seeds germinated in response to exposure to direct solar radiation. Seed burial depth had a significant but marginal effect by comparison, even when seeds were buried to 7 cm in the soil. Temperatures at sun-exposed compared with shaded environments differed by only a few degrees Celsius. Maximum temperature of the period prior to germination was the most significant contributor to germination responses and germination increased linearly above a threshold of 23℃ to the maximum temperature in the soil (in simulated-natural habitats) of 35℃.Glasshouses can provide useful environments to aid interpretation of seed germination responses to environmental niches.

Seed Banks as Incidental Fungi Banks: Fungal Endophyte Diversity in Stored Seeds of Banana Wild Relatives.

Seed banks were first established to conserve crop genetic diversity, but seed banking has more recently been extended to wild plants, particularly crop wild relatives (CWRs) (e.g., by the Millennium Seed Bank (MSB), Royal Botanic Gardens Kew). CWRs have been recognised as potential reservoirs of beneficial traits for our domesticated crops, and with mounting evidence of the importance of the microbiome to organismal health, it follows that the microbial communities of wild relatives could also be a valuable resource for crop resilience to environmental and pathogenic threats. Endophytic fungi reside asymptomatically inside all plant tissues and have been found to confer advantages to their plant host. Preserving the natural microbial diversity of plants could therefore represent an important secondary conservation role of seed banks. At the same time, species that are reported as endophytes may also be latent pathogens. We explored the potential of the MSB as an incidental fungal endophyte bank by assessing diversity of fungi inside stored seeds. Using banana CWRs in the genus Musa as a case-study, we sequenced an extended ITS-LSU fragment in order to delimit operational taxonomic units (OTUs) and used a similarity and phylogenetics approach for classification. Fungi were successfully detected inside just under one third of the seeds, with a few genera accounting for most of the OTUs-primarily Lasiodiplodia, Fusarium, and Aspergillus-while a large variety of rare OTUs from across the Ascomycota were isolated only once. Fusarium species were notably abundant-of significance in light of Fusarium wilt, a disease threatening global banana crops-and so were targeted for additional sequencing with the marker EF1α in order to delimit species and place them in a phylogeny of the genus. Endophyte community composition, diversity and abundance was significantly different across habitats, and we explored the relationship between community differences and seed germination/viability. Our results show that there is a previously neglected invisible fungal dimension to seed banking that could well have implications for the seed collection and storage procedures, and that collections such as the MSB are indeed a novel source of potentially useful fungal strains.

Plant Diversity Conservation Challenges and Prospects-The Perspective of Botanic Gardens and the Millennium Seed Bank.

There is a pressing need to conserve plant diversity to prevent extinctions and to enable sustainable use of plant material by current and future generations. Here, we review the contribution that living collections and seed banks based in botanic gardens around the world make to wild plant conservation and to tackling global challenges. We focus in particular on the work of Botanic Gardens Conservation International and the Millennium Seed Bank of the Royal Botanic Gardens, Kew, with its associated global Partnership. The advantages and limitations of conservation of plant diversity as both living material and seed collections are reviewed, and the need for additional research and conservation measures, such as cryopreservation, to enable the long-term conservation of 'exceptional species' is discussed. We highlight the importance of networks and sharing access to data and plant material. The skill sets found within botanic gardens and seed banks complement each other and enable the development of integrated conservation (linking in situ and ex situ efforts). Using a number of case studies we demonstrate how botanic gardens and seed banks support integrated conservation and research for agriculture and food security, restoration and reforestation, as well as supporting local livelihoods.

Challenges for Ex Situ Conservation of Wild Bananas: Seeds Collected in Papua New Guinea Have Variable Levels of Desiccation Tolerance.

Ex situ seed conservation of banana crop wild relatives (Musa spp. L.), is constrained by critical knowledge gaps in their storage and germination behaviour. Additionally, challenges in collecting seeds from wild populations impact the quality of seed collections. It is, therefore, crucial to evaluate the viability of seeds from such collecting missions in order to improve the value of future seed collections. We evaluate the seed viability of 37 accessions of seven Musa species, collected from wild populations in Papua New Guinea, during two collecting missions. Seeds from one mission had already been stored in conventional storage (dried for four months at 15% relative humidity, 20 °C and stored for two months at 15% relative humdity, -20 °C), so a post-storage test was carried out. Seeds from the second mission were assessed freshly extracted and following desiccation. We used embryo rescue techniques to overcome the barrier of germinating in vivo Musa seeds. Seeds from the first mission had low viability (19 ± 27% mean and standard deviation) after storage for two months at 15% relative humidity and -20 °C. Musa balbisiana Colla seeds had significantly higher post-storage germination than other species (p < 0.01). Desiccation reduced germination of the seeds from the second collecting mission, from 84 ± 22% (at 16.7 ± 2.4% moisture content) to 36 ± 30% (at 2.4 ± 0.8% moisture content). There was considerable variation between and (to a lesser extent) within accessions, a proportion of individual seeds of all but one species (Musa ingens N.W.Simmonds) survived desiccation and sub-zero temperature storage. We identified that seeds from the basal end of the infructescence were less likely to be viable after storage (p < 0.001); and made morphological observations that identify seeds and infructescences with higher viability in relation to their developmental maturity. We highlight the need for research into seed eco-physiology of crop wild relatives in order to improve future collecting missions.

Quality indicators for non-small cell lung cancer operations with use of a modified Delphi consensus process.

BACKGROUND: The aim of this project was to develop a set of quality indicators to assess surgical decision making in the care of patients with non-small cell lung cancer (NSCLC). METHODS: A multidisciplinary Expert Panel of 16 physicians used a modified Delphi process to identify quality indicators that evaluated the processes of care in patients with NSCLC. A systematic review identified potential indicators, which were rated on actionability, validity, usefulness, discriminability, and feasibility in two rounds of questionnaires. The first questionnaire was completed by the Expert Panel and by the larger thoracic surgical community of practice; the second questionnaire was sent to only the Expert Panel. Expert Panel members attended an in-person meeting to review the results of the two questionnaires and to compile the final list of indicators by consensus. RESULTS: From the literature review, 41 potential indicators were identified. An additional 16 indicators were suggested by the Expert Panel: 13 indicators in the two rounds of questionnaires and three after the discussion at the in-person meeting. One further indicator was identified after the in-person meeting. In the end, 17 indicators were chosen from seven domains: preoperative assessment, staging, surgical procedures, pathology, adjuvant therapy, surgical outcomes, and miscellaneous CONCLUSIONS: By use of a modified Delphi process, 17 indicators to assess the quality of processes of surgical care for patients with NSCLC were developed.