Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So... Show moreAngiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So far, the angiosperm tree of life has been determined primarily by means of analyses of the plastid genome. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins. However, the limited and biased sampling of both taxa and genomes undermines confidence in the tree and its implications. Here, we build the tree of life for almost 8,000 (about 60%) angiosperm genera using a standardized set of 353 nuclear genes. This 15-fold increase in genus-level sampling relative to comparable nuclear studies provides a critical test of earlier results and brings notable change to key groups, especially in rosids, while substantiating many previously predicted relationships. Scaling this tree to time using 200 fossils, we discovered that early angiosperm evolution was characterized by high gene tree conflict and explosive diversification, giving rise to more than 80% of extant angiosperm orders. Steady diversification ensued through the remaining Mesozoic Era until rates resurged in the Cenozoic Era, concurrent with decreasing global temperatures and tightly linked with gene tree conflict. Taken together, our extensive sampling combined with advanced phylogenomic methods shows the deep history and full complexity in the evolution of a megadiverse clade. Show less
Computer vision-based wood identification has been successfully applied to recognize tree species using digital images of wood sections or surfaces. However, this image-to- species approach can... Show moreComputer vision-based wood identification has been successfully applied to recognize tree species using digital images of wood sections or surfaces. However, this image-to- species approach can only recognize a limited number of species due to two main reasons: 1) the lack of a good reference database requiring high-quality standardized images from multiple individuals of hundreds or even thousands of traded timber species, and 2) species not included in the reference database cannot be identified without expert knowledge. Another bottleneck is that the feature extraction process used by these species recognition approaches is a black box, thereby creating a discrepancy between machine learning features and wood anatomical features. This discrepancy prevents wood anatomists from understanding how these machine learning algorithms work. Here, we survey currently existing methods used in feature extraction, classification, and deep learning methods applied in wood identification along with their pitfalls and opportunities. As an example of how the field could move forward, we launch the idea of building an image-to-features-to-species identification approach based on microscopic wood images as well as text files comprising wood anatomical descriptions. This would boost wood identification in two ways: (1) extensive reference databases for each species would become less crucial as the databases are ordered at the trait level, (2) timber identification would become more feasible for species that have not yet been included in the reference database as long as wood anatomical descriptions are available. Show less
Evolutionary radiations of woody taxa within arid environments were made possible by multiple trait innovations including deep roots and embolism-resistant xylem, but little is known about how... Show moreEvolutionary radiations of woody taxa within arid environments were made possible by multiple trait innovations including deep roots and embolism-resistant xylem, but little is known about how these traits have coevolved across the phylogeny of woody plants or how they jointly influence the distribution of species. We synthesized global trait and vegetation plot datasets to examine how rooting depth and xylem vulnerability across 188 woody plant species interact with aridity, precipitation seasonality, and water table depth to influence species occurrence probabilities across all biomes. Xylem resistance to embolism and rooting depth are independent woody plant traits that do not exhibit an interspecific trade-off. Resistant xylem and deep roots increase occurrence probabilities in arid, seasonal climates over deep water tables. Resistant xylem and shallow roots increase occurrence probabilities in arid, nonseasonal climates over deep water tables. Vulnerable xylem and deep roots increase occurrence probabilities in arid, nonseasonal climates over shallow water tables. Lastly, vulnerable xylem and shallow roots increase occurrence probabilities in humid climates. Each combination of trait values optimizes occurrence probabilities in unique environmental conditions. Responses of deeply rooted vegetation may be buffered if evaporative demand changes faster than water table depth under climate change. Show less
Premise: Although Boechera (Boechereae, Brassicaceae) has become a plant model system for both ecological genomics and evolutionary biology, all previous phylogenetic studies have had limited... Show morePremise: Although Boechera (Boechereae, Brassicaceae) has become a plant model system for both ecological genomics and evolutionary biology, all previous phylogenetic studies have had limited success in resolving species relationships within the genus. The recent effective application of sequence data from target enrichment approaches to resolve the evolutionary relationships of several other challenging plant groups prompted us to investigate their usefulness in Boechera and Boechereae.Methods: To resolve the phylogeny of Boechera and closely related genera, we utilized the Hybpiper pipeline to analyze two combined bait sets: Angiosperms353, with broad applicability across flowering plants; and a Brassicaceae‐specific bait set designed for use in the mustard family. Relationships for 101 samples representing 81 currently recognized species were inferred from a total of 1114 low‐copy nuclear genes using both supermatrix and species coalescence methods.Results: Our analyses resulted in a well‐resolved and highly supported phylogeny of the tribe Boechereae. Boechereae is divided into two major clades, one comprising all western North American species of Boechera, the other encompassing the eight other genera of the tribe. Our understanding of relationships within Boechera is enhanced by the recognition of three core clades that are further subdivided into robust regional species complexes.Conclusions: This study presents the first broadly sampled, well‐resolved phylogeny for most known sexual diploid Boechera. This effort provides the foundation for a new phylogenetically informed taxonomy of Boechera that is crucial for its continued use as a model system. Show less
The mustard family (Brassicaceae) is a scientifically and economically important family, containing the model plant Arabidopsis thaliana and numerous crop species that feed billions worldwide.... Show moreThe mustard family (Brassicaceae) is a scientifically and economically important family, containing the model plant Arabidopsis thaliana and numerous crop species that feed billions worldwide. Despite its relevance, most phylogenetic trees of the family are incompletely sampled and often contain poorly supported branches. Here, we present the most complete Brassicaceae genus-level family phylogenies to date (Brassicaceae Tree of Life or BrassiToL) based on nuclear (1,081 genes, 319 of the 349 genera; 57 of the 58 tribes) and plastome (60 genes, 265 genera; all tribes) data. We found cytonuclear discordance between the two, which is likely a result of rampant hybridization among closely and more distantly related lineages. To eval- uate the impact of such hybridization on the nuclear phylogeny reconstruction, we performed five different gene sampling routines, which increasingly removed putatively paralog genes. Our cleaned subset of 297 genes revealed high support for the tribes, whereas support for the main lineages (supertribes) was moderate. Calibration based on the 20 most clock-like nuclear genes suggests a late Eocene to late Oligocene origin of the family. Finally, our results strongly support a recently published new family classification, dividing the family into two subfamilies (one with five supertribes), together representing 58 tribes. This includes five recently described or re-established tribes, including Arabidopsideae, a monogeneric tribe accommodating Arabidopsis without any close relatives. With a worldwide community of thousands of researchers working on Brassicaceae and its diverse members, our new genus-level family phylogeny will be an indispensable tool for studies on biodiversity and plant biology. Show less
Results from comparative and ecological wood anatomy combined with a number of experimental studies on plant hydraulics have led to a pervasive and longstanding assumption that wider-diameter... Show moreResults from comparative and ecological wood anatomy combined with a number of experimental studies on plant hydraulics have led to a pervasive and longstanding assumption that wider-diameter vessels are more vulnerable to drought- induced embolism than narrower vessels. Although we agree that wider vessels tend to be more vulnerable than narrower vessels within stems and within roots across most species, our current understanding of the diameter-vulnerability link does not offer a mechanistic explanation for why increased vessel diameter should consistently lead to greater vulnerability or vice versa. Causes of drought-induced embolism formation and spread likely operate at the nano-level, especially at gas-liquid-surfactant interfaces inside intervessel pit membranes. We evaluate here new perspectives on drought-induced embolism and its key anatomical and physico-chemical drivers, of which vessel diameter is one of the parameters involved, although its linkage to embolism vulnerability is likely indirect. As such, the diameter-vulnerability link does not imply that species with on average wider vessels are consistently more susceptible to drought-induced embolism compared to species with narrower vessels. Scientific priorities for future progress should focus on more accurate predictions of how water transport in plants is affected by drought, which requires a better mechanistic understanding of xylem network topology and biophysical processes at the nano-scale level in individual vessels that determine embolism formation and spread. Show less
Hydraulic failure resulting from drought-induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult to... Show moreHydraulic failure resulting from drought-induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult to achieve at scale, leading to alternative metrics and correlations with more easily measured traits. These efforts have led to the longstanding and pervasive assumed mechanistic link between vessel diameter and vulnerability in angiosperms. However, there are at least two problems with this assumption that requires critical re-evaluation: (1) our current understanding of drought-induced embolism does not provide a mechanistic explanation why increased vessel width should lead to greater vulnerability, and (2) the most recent advancements in nanoscale embolism processes suggest that vessel diameter is not a direct driver. Here, we review data from physiological and comparative wood anatomy studies, highlighting the potential anatomical and physicochemical drivers of embolism formation and spread. We then put forward key knowledge gaps, emphasising what is known, unknown and speculation. A meaningful evaluation of the diameter–vulnerability link will require a better mechanistic understanding of the biophysical processes at the nanoscale level that determine embolism formation and spread, which will in turn lead to more accurate predictions of how water transport in plants is affected by drought. Show less
The Apocynaceae subfamilies Secamonoideae and Asclepiadoideae have undergone several transitions during their evolution with regard to growth form and degree of woodiness. In this study, we present... Show moreThe Apocynaceae subfamilies Secamonoideae and Asclepiadoideae have undergone several transitions during their evolution with regard to growth form and degree of woodiness. In this study, we present a wood anatomical overview of both subfamilies that complements previous work on the remaining Apocynaceae. Detailed microscopic wood descriptions using light and scanning electron microscopy were performed on 60 species that cover most Secamonoideae genera and all major woody Asclepiadoideae lineages. Our observations are in line with subfamilial and (sometimes sub)tribal delimitations. Furthermore, we present for the first time an overview of the estimated number of shifts from herbaceousness to (phylogenetically) derived woodiness in Asclepiadoideae, along with a derived woody species list with distribution and habitat information. In total, at least 168 derived woody species resulting from at least 28 independent woodiness transitions were found, with drought possibly being one of the main drivers of most of these transitions. Show less
Plant functional traits can predict community assembly and ecosystem functioning and are thus widely used in global models of vegetation dynamics and land–climate feedbacks. Still, we lack a global... Show morePlant functional traits can predict community assembly and ecosystem functioning and are thus widely used in global models of vegetation dynamics and land–climate feedbacks. Still, we lack a global understanding of how land and climate affect plant traits. A previous global analysis of six traits observed two main axes of variation: (1) size variation at the organ and plant level and (2) leaf economics balancing leaf persistence against plant growth potential. The orthogonality of these two axes suggests they are differently influenced by environmental drivers. We find that these axes persist in a global dataset of 17 traits across more than 20,000 species. We find a dominant joint effect of climate and soil on trait variation. Additional independent climate effects are also observed across most traits, whereas independent soil effects are almost exclusively observed for economics traits. Variation in size traits correlates well with a latitudinal gradient related to water or energy limitation. In contrast, varia- tion in economics traits is better explained by interactions of climate with soil fertility. These findings have the potential to improve our understanding of biodiversity patterns and our predictions of climate change impacts on biogeochemical cycles. Show less
Insular woodiness (IW)—the evolutionary transition from herbaceousness toward wood- iness on islands—is one of the most iconic features of island floras. Since pioneering work by Darwin and Wallace... Show moreInsular woodiness (IW)—the evolutionary transition from herbaceousness toward wood- iness on islands—is one of the most iconic features of island floras. Since pioneering work by Darwin and Wallace, a number of drivers of IW have been proposed, such as 1) competition for sunlight requiring plants with taller and stronger woody stems and 2) drought favoring woodiness to safeguard root-to-shoot water transport. Alternatively, IW may be the indirect result of increased lifespan related to 3) a favorable aseasonal climate and/or 4) a lack of large native herbivores. However, information on the occurrence of IW is fragmented, hampering tests of these potential drivers. Here, we identify 1,097 insular woody species on 375 islands and infer at least 175 evolutionary transitions on 31 archipelagos, concentrated in six angiosperm families. Structural equation models reveal that the insular woody species richness on oceanic islands correlates with a favorable aseasonal climate, followed by increased drought and island isolation (approximating competition). When continental islands are also included, reduced herbivory pressure by large native mammals, increased drought, and island isolation are most relevant. Our results illustrate different trajectories leading to rampant convergent evolution toward IW and further emphasize archipelagos as natural laboratories of evolution, where similar abiotic or biotic conditions replicated evolution of similar traits. Show less
Pramanik, D.; Spaans, M.; Kranenburg, T.; Bogarin Chaves, D.G.; Heijungs, R.; Lens, F.P.; ... ; Gravendeel, B. 2022
Phalaenopsis is an important ornamental pot plant for the global horticultural market. The inflorescences of Phalaenopsis horticultural hybrids require support from a stick during plant... Show morePhalaenopsis is an important ornamental pot plant for the global horticultural market. The inflorescences of Phalaenopsis horticultural hybrids require support from a stick during plant cultivation because of the weight of multiple large flowers. Developing a horticultural hybrid with a sufficiently lignified inflorescence stem that does not require additional support could be a way to reduce the costs of production. This study aimed to (i) determine the orientation and degree of lignification in the inflorescence stem of different species and horticultural hybrids of Phalaenopsis and investigate whether these lignification patterns follow any (ii) topological or (iii) phylogenetic pattern of interest to further explore in genetic precision breeding. Inflorescences of comparable devel- opmental stages of six species and 17 horticultural hybrids of flowering Phalaenopsis orchids were sampled. The orientation of the inflorescence varied from erect, sub-erect, arching, to pendant. The degree of lignification was measured with ImageJ using stained microscopic tissue sections and statistically analyzed. A molecular phylogeny of the species of Phalaenopsis was reconstructed based on plastid and nuclear ribosomal DNA sequences to analyze phylogenetic patterns. Our results show a significant difference in the degree of lignification between the different Phalaenopsis species and hybrids, between peduncle and rachis, and among the six different inflorescence positions analyzed. We found a positive correlation between inflorescence orientation and the proportion of lignified area per total stem area and the proportional thickness of the lignified fiber walls in the peduncle. We conclude that the degree of lignification is heritable, as we observed among our sample size a higher positive correlation between stem lignification variables among closely related taxa compared to more distantly related ones. However, a larger species sampling is needed to further validate our results. Show less
Background: Bulk segregant analysis (BSA) can help identify quantitative trait loci (QTLs), but this may result in sub‐ stantial bycatch of functionally irrelevant genes.Results: Here we develop a... Show moreBackground: Bulk segregant analysis (BSA) can help identify quantitative trait loci (QTLs), but this may result in sub‐ stantial bycatch of functionally irrelevant genes.Results: Here we develop a Gene Ontology‐mediated approach to zoom in on specific genes located inside QTLs identified by BSA as implicated in a continuous trait. We apply this to a novel experimental system: flowering time in the giant woody Jersey kale, which we phenotyped in four bulks of flowering onset. Our inferred QTLs yielded tens of thousands of candidate genes. We reduced this by two orders of magnitude by focusing on genes annotated with terms contained within relevant subgraphs of the Gene Ontology. A pathway enrichment test then led to the circadian rhythm pathway. The genes that enriched this pathway are attested from previous research as regulating flowering time. Within that pathway, the genes CCA1, FT, and TSF were identified as having functionally significant variation compared to Arabidopsis. We validated and confirmed our ontology‐mediated results through genome sequencing and homology‐based SNP analysis. However, our ontology‐mediated approach produced additional genes of puta‐ tive importance, showing that the approach aids in exploration and discovery.Conclusions: Our method is potentially applicable to the study of other complex traits and we therefore make our workflows available as open‐source code and a reusable Docker container. Show less
The typical black coloured ebony wood (Diospyros, Ebenaceae) is desired as a com- mercial timber because of its durable and aesthetic properties. Surprisingly, a comprehensive wood anatomical... Show moreThe typical black coloured ebony wood (Diospyros, Ebenaceae) is desired as a com- mercial timber because of its durable and aesthetic properties. Surprisingly, a comprehensive wood anatomical overview of the genus is lacking, making it impossible to fully grasp the diversity in microscopic anatomy and to distinguish between CITES protected species native to Madagascar and the rest. We present the largest microscopic wood anatomical reference database for ebony woods and reconstruct evolutionary patterns in the microscopic wood anatomy within the family level using an earlier generated molecular phylogeny. Wood samples from 246 Diospyros species are described based on standardised light microscope observations. For the ancestral state reconstruction, we selected eight wood anatomical characters from 88 Ebenaceae species (including 29 Malagasy Diospyros species) that were included in the most recently reconstructed family phylogeny. Within Diospyros, the localisation of prismatic crystals (either in axial parenchyma or in rays) shows the highest phylogenetic value and appears to have a biogeographical signal. The molecular defined subclade Diospyros clade IX can be clearly distinguished from other ebony woods by its storied structure. Across Ebenaceae, Lissocarpa is distinguishable from the remaining genera by the combined presence of scalariform and simple vessel perforation plates, and Royena typically has silica bodies instead of prismatic crystals. The local deposition of prismatic crystals and the presence of storied structure allow identifying ebony wood species at the subgeneric level, but species-level identification is not possible. In an attempt to improve the identification accuracy of the CITES protected Malagasy woods, we applied computer vision algorithms based on microscopic images from our reference database (microscopic slides from ca. 1000 Diospyros specimens) and performed chemical profiling based on DART TOFMS. Show less
Lens, F.P.; Liang, C.; Guo, Y.; Tang, X.; Jahanbanifard, M.; Soares Correa da Silva, F.; ... ; Verbeek, F.J. 2020
Wood anatomy is one of the most important methods for timber identification. However, training wood anatomy experts is time-consuming, while at the same time the number of senior wood anatomists... Show moreWood anatomy is one of the most important methods for timber identification. However, training wood anatomy experts is time-consuming, while at the same time the number of senior wood anatomists with broad taxonomic expertise is de- clining. Therefore, we want to explore how a more automated, computer-assisted approach can support accurate wood identification based on microscopic wood anatomy. For our exploratory research, we used an available image dataset that has been applied in several computer vision studies, consisting of 112 — mainly neotropical — tree species representing 20 images of transverse sections for each species. Our study aims to review existing computer vision methods and compare the success of species identification based on (1) several image classifiers based on manually adjusted texture features, and (2) a state-of-the-art approach for image classification based on deep learning, more specifically Convolutional Neural Networks (CNNs). In support of previous studies, a considerable increase of the correct identification is accomplished using deep learning, leading to an accuracy rate up to 95.6%. This remarkably high success rate highlights the fundamental potential of wood anatomy in species identification and motivates us to expand the existing database to an extensive, worldwide reference database with transverse and tangential microscopic images from the most traded timber species and their look-a-likes. This global reference database could serve as a valuable future tool for stakeholders involved in combatting illegal logging and would boost the societal value of wood anatomy along with its collections and experts. Show less
Plant traits—the morphological, anatomical, physiological, biochemical and phenological characteristics of plants—determine how plants respond to environmental factors, affect other trophic levels,... Show morePlant traits—the morphological, anatomical, physiological, biochemical and phenological characteristics of plants—determine how plants respond to environmental factors, affect other trophic levels, and influence ecosystem properties and their benefits and detriments to people. Plant trait data thus represent the basis for a vast area of research spanning from evolutionary biology, community and functional ecology, to biodiversity conservation, ecosystem and landscape management, restoration, biogeography and earth system modelling. Since its foundation in 2007, the TRY database of plant traits has grown continuously. It now provides unprecedented data coverage under an open access data policy and is the main plant trait database used by the research community worldwide. Increasingly, the TRY database also supports new frontiers of trait‐based plant research, including the identification of data gaps and the subsequent mobilization or measurement of new data. To support this development, in this article we evaluate the extent of the trait data compiled in TRY and analyse emerging patterns of data coverage and representativeness. Best species coverage is achieved for categorical traits—almost complete coverage for ‘plant growth form’. However, most traits relevant for ecology and vegetation modelling are characterized by continuous intraspecific variation and trait–environmental relationships. These traits have to be measured on individual plants in their respective environment. Despite unprecedented data coverage, we observe a humbling lack of completeness and representativeness of these continuous traits in many aspects. We, therefore, conclude that reducing data gaps and biases in the TRY database remains a key challenge and requires a coordinated approach to data mobilization and trait measurements. This can only be achieved in collaboration with other initiatives. Show less
Jahanbanifard, M.; Gravendeel, B.; Lens, F.P.; Verbeek, F.J. 2019
Shared ancestry among species and correlation between vessel diameter and plant height can obscure the mechanisms linking vessel diameter to current climate distributions of angiosperms. Because... Show moreShared ancestry among species and correlation between vessel diameter and plant height can obscure the mechanisms linking vessel diameter to current climate distributions of angiosperms. Because wood is complex, various traits may interact to influence vessel function. Specifically, pit vesturing (lignified cell wall protuberances associated with bordered pits) and perforation plate morphology could alter the relationships between vessel diameter, climate and plant height. Using phylogenetically informed analyses, we tested for associations between vessel diameter, climate and maximum plant height across angiosperm species with different pit vesturing (presence/absence) and perforation plate morphology (simple/scalariform and quantitative variation). We show significantly larger changes in vessel diameter and maximum plant height across climates for species with vestures and simple perforation plates, compared to nonvestured species and those with scalariform plates. We also found a significantly greater increase in height for a given increase in vessel diameter with lower percentage of scalariform plates. Our study provides novel insights into the evolution of angiosperm xylem by showing that vessel pit vesturing and perforation plate morphologies can modify relationships among xylem vessels, climate and height. Our findings highlight the complexity of xylem adaptations to cli- mate, substantiating an integrative view of xylem function in the study of wood evolution. Show less
Dória, L.C.; Meijs, C.; Podadera, D.S.; Del Arco, M.; Smets, E.; Delzon, S.; Lens, F.P. 2019
• Background and Aims Plant survival under extreme drought events has been associated with xylem vulnerability to embolism (the disruption of water transport due to air bubbles in conduits).... Show more• Background and Aims Plant survival under extreme drought events has been associated with xylem vulnerability to embolism (the disruption of water transport due to air bubbles in conduits). Despite the ecological and economic importance of herbaceous species, studies focusing on hydraulic failure in herbs remain scarce. Here, we assess the vulnerability to embolism and anatomical adaptations in stems of seven herbaceous Brassicaceae species occurring in different vegetation zones of the island of Tenerife, Canary Islands, and merged them with a similar hydraulic–anatomical data set for herbaceous Asteraceae from Tenerife.• Methods Measurements of vulnerability to xylem embolism using the in situ flow centrifuge technique along with light and transmission electron microscope observations were performed in stems of the herbaceous species. We also assessed the link between embolism resistance vs. mean annual precipitation and anatomical stem characters.• Key Results The herbaceous species show a 2-fold variation in stem P50 from –2.1 MPa to –4.9 MPa. Within Hirschfeldia incana and Sisymbrium orientale, there is also a significant stem P50 difference between populations growing in contrasting environments. Variation in stem P50 is mainly explained by mean annual precipitation as well as by the variation in the degree of woodiness (calculated as the proportion of lignified area per total stem area) and to a lesser extent by the thickness of intervessel pit membranes. Moreover, mean annual precipitation explains the total variance in embolism resistance and stem anatomical traits.• Conclusions The degree of woodiness and thickness of intervessel pit membranes are good predictors of embolism resistance in the herbaceous Brassicaceae and Asteraceae species studied. Differences in mean annual precipitation across the sampling sites affect embolism resistance and stem anatomical characters, both being important characters determining survival and distribution of the herbaceous eudicots. Show less
