Adaptive potential of Coffea canephora from Uganda in response to climate change.

Understanding vulnerabilities of plant populations to climate change could help preserve their biodiversity and reveal new elite parents for future breeding programmes. To this end, landscape genomics is a useful approach for assessing putative adaptations to future climatic conditions, especially in long-lived species such as trees. We conducted a population genomics study of 207 Coffea canephora trees from seven forests along different climate gradients in Uganda. For this, we sequenced 323 candidate genes involved in key metabolic and defence pathways in coffee. Seventy-one single nucleotide polymorphisms (SNPs) were found to be significantly associated with bioclimatic variables, and were thereby considered as putatively adaptive loci. These SNPs were linked to key candidate genes, including transcription factors, like DREB-like and MYB family genes controlling plant responses to abiotic stresses, as well as other genes of organoleptic interest, such as the DXMT gene involved in caffeine biosynthesis and a putative pest repellent. These climate-associated genetic markers were used to compute genetic offsets, predicting population responses to future climatic conditions based on local climate change forecasts. Using these measures of maladaptation to future conditions, substantial levels of genetic differentiation between present and future diversity were estimated for all populations and scenarios considered. The populations from the forests Zoka and Budongo, in the northernmost zone of Uganda, appeared to have the lowest genetic offsets under all predicted climate change patterns, while populations from Kalangala and Mabira, in the Lake Victoria region, exhibited the highest genetic offsets. The potential of these findings in terms of ex situ conservation strategies are discussed.

Tallo: A global tree allometry and crown architecture database.

Data capturing multiple axes of tree size and shape, such as a tree's stem diameter, height and crown size, underpin a wide range of ecological research-from developing and testing theory on forest structure and dynamics, to estimating forest carbon stocks and their uncertainties, and integrating remote sensing imagery into forest monitoring programmes. However, these data can be surprisingly hard to come by, particularly for certain regions of the world and for specific taxonomic groups, posing a real barrier to progress in these fields. To overcome this challenge, we developed the Tallo database, a collection of 498,838 georeferenced and taxonomically standardized records of individual trees for which stem diameter, height and/or crown radius have been measured. These data were collected at 61,856 globally distributed sites, spanning all major forested and non-forested biomes. The majority of trees in the database are identified to species (88%), and collectively Tallo includes data for 5163 species distributed across 1453 genera and 187 plant families. The database is publicly archived under a CC-BY 4.0 licence and can be access from: https://doi.org/10.5281/zenodo.6637599. To demonstrate its value, here we present three case studies that highlight how the Tallo database can be used to address a range of theoretical and applied questions in ecology-from testing the predictions of metabolic scaling theory, to exploring the limits of tree allometric plasticity along environmental gradients and modelling global variation in maximum attainable tree height. In doing so, we provide a key resource for field ecologists, remote sensing researchers and the modelling community working together to better understand the role that trees play in regulating the terrestrial carbon cycle.

Detect thy family: Mechanisms, ecology and agricultural aspects of kin recognition in plants.

The phenomenon that organisms can distinguish genetically related individuals from strangers (i.e., kin recognition) and exhibit more cooperative behaviours towards their relatives (i.e., positive kin discrimination) has been documented in a wide variety of organisms. However, its occurrence in plants has been considered only recently. Despite the concerns about some methodologies used to document kin recognition, there is sufficient evidence to state that it exists in plants. Effects of kin recognition go well beyond reducing resource competition between related plants and involve interactions with symbionts (e.g., mycorrhizal networks). Kin recognition thus likely has important implications for evolution of plant traits, diversity of plant populations, ecological networks and community structures. Moreover, as kin selection may result in less competitive traits and thus greater population performance, it holds potential promise for crop breeding. Exploration of these evo-ecological and agricultural implications requires adequate control and measurements of relatedness, sufficient replication at genotypic level and comprehensive measurements of performance/fitness effects of kin discrimination. The primary questions that need to be answered are: when, where and by how much positive kin discrimination improves population performance.

Light from below matters: Quantifying the consequences of responses to far-red light reflected upwards for plant performance in heterogeneous canopies.

In vegetation stands, plants receive red to far-red ratio (R:FR) signals of varying strength from all directions. However, plant responses to variations in R:FR reflected from below have been largely ignored despite their potential consequences for plant performance. Using a heterogeneous rose canopy, which consists of bent shoots down in the canopy and vertically growing upright shoots, we quantified upward far-red reflection by bent shoots and its consequences for upright shoot architecture. With a three-dimensional plant model, we assessed consequences of responses to R:FR from below for plant photosynthesis. Bent shoots reflected substantially more far-red than red light, causing reduced R:FR in light reflected upwards. Leaf inclination angles increased in upright shoots which received low R:FR reflected from below. The increased leaf angle led to an increase in simulated plant photosynthesis only when this low R:FR was reflected off their own bent shoots and not when it reflected off neighbour bent shoots. We conclude that plant response to R:FR from below is an under-explored phenomenon which may have contrasting consequences for plant performance depending on the type of vegetation or crop system. The responses are beneficial for performance only when R:FR is reflected by lower foliage of the same plants.

TRY plant trait database - enhanced coverage and open access.

Plant 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.

Variation in plastic responses to light results from selection in different competitive environments-A game theoretical approach using virtual plants.

Phenotypic plasticity is a vital strategy for plants to deal with changing conditions by inducing phenotypes favourable in different environments. Understanding how natural selection acts on variation in phenotypic plasticity in plants is therefore a central question in ecology, but is often ignored in modelling studies. Here we present a new modelling approach that allows for the analysis of selection for variation in phenotypic plasticity as a response strategy. We assess selection for shade avoidance strategies of Arabidopsis thaliana in response to future neighbour shading signalled through a decrease in red:far-red (R:FR) ratio. For this, we used a spatially explicit 3D virtual plant model that simulates individual Arabidopsis plants competing for light in different planting densities. Plant structure and growth were determined by the organ-specific interactions with the light environment created by the vegetation structure itself. Shade avoidance plastic responses were defined by a plastic response curve relating petiole elongation and lamina growth to R:FR perceived locally. Different plasticity strategies were represented by different shapes of the response curve that expressed different levels of R:FR sensitivity. Our analyses show that the shape of the selected shade avoidance strategy varies with planting density. At higher planting densities, more sensitive response curves are selected for than at lower densities. In addition, the balance between lamina and petiole responses influences the sensitivity of the response curves selected for. Combining computational virtual plant modelling with a game theoretical analysis represents a new step towards analysing how natural selection could have acted upon variation in shade avoidance as a response strategy, which can be linked to genetic variation and underlying physiological processes.

Quantifying the contribution of bent shoots to plant photosynthesis and biomass production of flower shoots in rose (Rosa hybrida) using a functional-structural plant model.

BACKGROUND AND AIMS: The success of using bent shoots in cut-rose (Rosa hybrida) production to improve flower shoot quality has been attributed to bent shoots capturing more light and thus providing more assimilates for flower shoot growth. We aimed at quantifying this contribution of photosynthesis by bent shoots to flower shoot growth. METHODS: Rose plants were grown with four upright flower shoots and with no, one or three bent shoots per plant. Plant architectural traits, leaf photosynthetic parameters and organ dry weight were measured. A functional-structural plant (FSP) model of rose was used to calculate photosynthesis of upright shoots and bent shoots separately, taking into account the heterogeneous canopy structure of these plants. KEY RESULTS: Bent shoots contributed to 43-53 % of total assimilated CO2 by the plant. Plant photosynthesis increased by 73 and 117 % in plants with, respectively, one and three bent shoots compared with plants without bent shoots. Upright shoot photosynthesis was not significantly affected by the presence of bent shoots. However, upright shoot dry weight increased by 35 and 59 % in plants with, respectively, one and three bent shoots compared with plants without bent shoots. The increased upright shoot dry weight was entirely due to the contribution of extra photosynthesis by bent shoots, as this was the only source that could induce differences in upright shoot growth apart from their own photosynthesis. At least 47-51 % of the photosynthesis by bent shoots was translocated to upright shoots to support their biomass increase. CONCLUSIONS: Based on model simulations, we conclude that the positive effect of shoot bending on flower shoot growth and quality in cut-rose production system can almost entirely be attributed to assimilate supply from bent shoots. FSP modelling is a useful tool to quantify the contributions of photosynthesis by different parts of heterogeneous canopies.

Disentangling the effects of photosynthetically active radiation and red to far-red ratio on plant photosynthesis under canopy shading: a simulation study using a functional-structural plant model.

BACKGROUND AND AIMS: Shading by an overhead canopy (i.e. canopy shading) entails simultaneous changes in both photosynthetically active radiation (PAR) and red to far-red ratio (R:FR). As plant responses to PAR (e.g. changes in leaf photosynthesis) are different from responses to R:FR (e.g. changes in plant architecture), and these responses occur at both organ and plant levels, understanding plant photosynthesis responses to canopy shading needs separate analysis of responses to reductions in PAR and R:FR at different levels. METHODS: In a glasshouse experiment we subjected plants of woody perennial rose (Rosa hybrida) to different light treatments, and so separately quantified the effects of reductions in PAR and R:FR on leaf photosynthetic traits and plant architectural traits. Using a functional-structural plant model, we separately quantified the effects of responses in these traits on plant photosynthesis, and evaluated the relative importance of changes of individual traits for plant photosynthesis under mild and heavy shading caused by virtual overhead canopies. KEY RESULTS: Model simulations showed that the individual trait responses to canopy shading could have positive and negative effects on plant photosynthesis. Under mild canopy shading, trait responses to reduced R:FR on photosynthesis were generally negative and with a larger magnitude than effects of responses to reduced PAR. Conversely, under heavy canopy shading, the positive effects of trait responses to reduced PAR became dominant. The combined effects of low-R:FR responses and low-PAR responses on plant photosynthesis were not equal to the sum of the separate effects, indicating interactions between individual trait responses. CONCLUSIONS: Our simulation results indicate that under canopy shading, the relative importance of plant responses to PAR and R:FR for plant photosynthesis changes with shade levels. This suggests that the adaptive significance of plant plasticity responses to one shading factor depends on plant responses to the other.

Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics.

Vegetation stands have a heterogeneous distribution of light quality, including the red/far-red light ratio (R/FR) that informs plants about proximity of neighbors. Adequate responses to changes in R/FR are important for competitive success. How the detection and response to R/FR are spatially linked and how this spatial coordination between detection and response affects plant performance remains unresolved. We show in Arabidopsis thaliana and Brassica nigra that localized FR enrichment at the lamina tip induces upward leaf movement (hyponasty) from the petiole base. Using a combination of organ-level transcriptome analysis, molecular reporters, and physiology, we show that PIF-dependent spatial auxin dynamics are key to this remote response to localized FR enrichment. Using computational 3D modeling, we show that remote signaling of R/FR for hyponasty has an adaptive advantage over local signaling in the petiole, because it optimizes the timing of leaf movement in response to neighbors and prevents hyponasty caused by self-shading.

Ecological significance of light quality in optimizing plant defence.

Plants balance the allocation of resources between growth and defence to optimize fitness in a competitive environment. Perception of neighbour-detection cues, such as a low ratio of red to far-red (R:FR) radiation, activates a suite of shade-avoidance responses that include stem elongation and upward leaf movement, whilst simultaneously downregulating defence. This downregulation is hypothesized to benefit the plant either by mediating the growth-defence balance in favour of growth in high plant densities or, alternatively, by mediating defence of individual leaves such that those most photosynthetically productive are best protected. To test these hypotheses, we used a 3D functional-structural plant model of Brassica nigra that mechanistically simulates the interactions between plant architecture, herbivory, and the light environment. Our results show that plant-level defence expression is a strong determinant of plant fitness and that leaf-level defence mediation by R:FR can provide a fitness benefit in high densities. However, optimal plant-level defence expression does not decrease monotonically with plant density, indicating that R:FR mediation of defence alone is not enough to optimize defence between densities. Therefore, assessing the ecological significance of R:FR-mediated defence is paramount to better understand the evolution of this physiological linkage and its implications for crop breeding.

Understanding and optimizing species mixtures using functional-structural plant modelling.

Plant species mixtures improve productivity over monocultures by exploiting species complementarities for resource capture in time and space. Complementarity results in part from competition avoidance responses that maximize resource capture and growth of individual plants. Individual organs accommodate to local resource levels, e.g. with regard to nitrogen content and photosynthetic capacity or by size (e.g. shade avoidance). As a result, the resource acquisition in time and space is improved and performance of the community as a whole is increased. Modelling is needed to unravel the primary drivers and subsequent dynamics of complementary growth responses in mixtures. Here, we advocate using functional-structural plant (FSP) modelling to analyse the functioning of plant mixtures. In FSP modelling, crop performance is a result of the behaviour of the individual plants interacting through competitive and complementary resource acquisition. FSP models can integrate the interactions between structural and physiological plant responses to the local resource availability and strength of competition, which drive resource capture and growth of individuals in species mixtures. FSP models have the potential to accelerate mixed-species plant research, and thus support the development of knowledge that is needed to promote the use of mixtures towards sustainably increasing crop yields at acceptable input levels.

Elucidating the interaction between light competition and herbivore feeding patterns using functional-structural plant modelling.

Background and Aims: Plants usually compete with neighbouring plants for resources such as light as well as defend themselves against herbivorous insects. This requires investment of limiting resources, resulting in optimal resource distribution patterns and trade-offs between growth- and defence-related traits. A plant's competitive success is determined by the spatial distribution of its resources in the canopy. The spatial distribution of herbivory in the canopy in turn differs between herbivore species as the level of herbivore specialization determines their response to the distribution of resources and defences in the canopy. Here, we investigated to what extent competition for light affects plant susceptibility to herbivores with different feeding preferences. Methods: To quantify interactions between herbivory and competition, we developed and evaluated a 3-D spatially explicit functional-structural plant model for Brassica nigra that mechanistically simulates competition in a dynamic light environment, and also explicitly models leaf area removal by herbivores with different feeding preferences. With this novel approach, we can quantitatively explore the extent to which herbivore feeding location and light competition interact in their effect on plant performance. Key Results: Our results indicate that there is indeed a strong interaction between levels of plant-plant competition and herbivore feeding preference. When plants did not compete, herbivory had relatively small effects irrespective of feeding preference. Conversely, when plants competed, herbivores with a preference for young leaves had a strong negative effect on the competitiveness and subsequent performance of the plant, whereas herbivores with a preference for old leaves did not. Conclusions: Our study predicts how plant susceptibility to herbivory depends on the composition of the herbivore community and the level of plant competition, and highlights the importance of considering the full range of dynamics in plant-plant-herbivore interactions.

Subtle variation in shade avoidance responses may have profound consequences for plant competitiveness.

Background and Aims: Although phenotypic plasticity has been shown to be beneficial for plant competitiveness for light, there is limited knowledge on how variation in these plastic responses plays a role in determining competitiveness. Methods: A combination of detailed plant experiments and functional-structural plant (FSP) modelling was used that captures the complex dynamic feedback between the changing plant phenotype and the within-canopy light environment in time and 3-D space. Leaf angle increase (hyponasty) and changes in petiole elongation rates in response to changes in the ratio between red and far-red light, two important shade avoidance responses in Arabidopsis thaliana growing in dense population stands, were chosen as a case study for plant plasticity. Measuring and implementing these responses into an FSP model allowed simulation of plant phenotype as an emergent property of the underlying growth and response mechanisms. Key Results: Both the experimental and model results showed that substantial differences in competitiveness may arise between genotypes with only marginally different hyponasty or petiole elongation responses, due to the amplification of plant growth differences by small changes in plant phenotype. In addition, this study illustrated that strong competitive responses do not necessarily have to result in a tragedy of the commons; success in competition at the expense of community performance. Conclusions: Together, these findings indicate that selection pressure could probably have played a role in fine-tuning the sensitive shade avoidance responses found in plants. The model approach presented here provides a novel tool to analyse further how natural selection could have acted on the evolution of plastic responses.

Biomass dynamics in a logged forest: the role of wood density.

Wood density (WD) is believed to be a key trait in driving growth strategies of tropical forest species, and as it entails the amount of mass per volume of wood, it also tends to correlate with forest carbon stocks. Yet there is relatively little information on how interspecific variation in WD correlates with biomass dynamics at the species and population level. We determined changes in biomass in permanent plots in a logged forest in Vietnam from 2004 to 2012, a period representing the last 8 years of a 30 years logging cycle. We measured diameter at breast height (DBH) and estimated aboveground biomass (AGB) growth, mortality, and net AGB increment (the difference between AGB gains and losses through growth and mortality) per species at the individual and population (i.e. corrected for species abundance) level, and correlated these with WD. At the population level, mean net AGB increment rates were 6.47 Mg ha-1 year-1 resulting from a mean AGB growth of 8.30 Mg ha-1 year-1, AGB recruitment of 0.67 Mg ha-1 year-1 and AGB losses through mortality of 2.50 Mg ha-1 year-1. Across species there was a negative relationship between WD and mortality rate, WD and DBH growth rate, and a positive relationship between WD and tree standing biomass. Standing biomass in turn was positively related to AGB growth, and net AGB increment both at the individual and population level. Our findings support the view that high wood density species contribute more to total biomass and indirectly to biomass increment than low wood density species in tropical forests. Maintaining high wood density species thus has potential to increase biomass recovery and carbon sequestration after logging.

When does it pay off to prime for defense? A modeling analysis.

Plants can prepare for future herbivore attack through a process called priming. Primed plants respond more strongly and/or faster to insect attack succeeding the priming event than nonprimed plants, while the energetic costs of priming are relatively low. To better understand the evolution of priming, we developed a simulation model, partly parameterized for Brassica nigra plants, to explore how the fitness benefits of priming change when plants are grown in different biotic environments. Model simulations showed that herbivore dynamics (arrival probability, arrival time, and feeding rate) affect the optimal duration, the optimal investment and the fitness benefits of priming. Competition for light increases the indirect costs of priming, but may also result in a larger payoff when the nonprimed plant experiences substantial leaf losses. This modeling approach identified some important knowledge gaps: herbivore arrival rates on individual plants are rarely reported but they shape the optimal duration of priming, and it would pay off if the likelihood, severity and timing of the attack could be discerned from the priming cue, but it is unknown if plants can do so. In addition, the model generated some testable predictions, for example that the sensitivity to the priming cue decreases with plant age.

Trends in tropical tree growth: re-analyses confirm earlier findings.

In a recent Opinion article, Brienen et al. (2016) raise doubts about our finding that tropical tree growth has not increased during 150 years of CO2 rise (Groenendijk et al., 2015; van der Sleen et al., 2015). They claim that our tree-ring data contain evidence for historical growth stimulation that was concealed due to failing regeneration in several species. Here we show that (i) the correction method proposed by Brienen et al. induces a bias towards finding positive growth trends, (ii) the results of Brienen et al. rest on selective removal of species, (iii) there is a simple and effective way to accommodate effects of recruitment failure by subsetting data, and (iv) the application of this method confirms our earlier findings. Thus, our results are robust to effects of recruitment failure and our conclusions remain unchanged: we find no evidence for historical growth changes in our studied tree species.

Explaining long-term inter-individual growth variation in plant populations: persistence of abiotic factors matters.

An unanswered question in ecology is whether the environmental factors driving short-term performance also determine the often observed long-term performance differences among individuals. Here, we analyze the extent to which temporal persistence of spatial heterogeneity in environmental factors can contribute to long-term inter-individual variation in stem length growth. For a natural population of a long-lived understorey palm, we first quantified the effect of several environmental factors on stem length growth and survival. We then performed individual-based simulations of growth trajectories, in which we varied, for two environmental factors: (1) the strength of the effect on stem length growth and (2) the temporal persistence. Short-term variation in stem length growth was strongly driven by light availability. Auto-correlation in light availability and soil pH increased simulated variation in stem length growth among 20-year-old palms to levels similar to the observed variation. Analyses in which we varied both the strength of the effect on stem length growth and the temporal persistence of the environmental factors revealed that a large fraction of observed long-term growth differences can be explained, as long as one of these effects is strong. This implies that environmental factors that are relatively unimportant for short-term performance can still drive long-term performance differences when the environmental variation is sufficiently persistent over time.

Plant-plant interactions mediate the plastic and genotypic response of Plantago asiatica to CO2: an experiment with plant populations from naturally high CO2 areas.

BACKGROUND AND AIMS: The rising atmospheric CO2 concentration ([CO2]) is a ubiquitous selective force that may strongly impact species distribution and vegetation functioning. Plant-plant interactions could mediate the trajectory of vegetation responses to elevated [CO2], because some plants may benefit more from [CO2] elevation than others. The relative contribution of plastic (within the plant's lifetime) and genotypic (over several generations) responses to elevated [CO2] on plant performance was investigated and how these patterns are modified by plant-plant interactions was analysed. METHODS: Plantago asiatica seeds originating from natural CO2 springs and from ambient [CO2] sites were grown in mono stands of each one of the two origins as well as mixtures of both origins. In total, 1944 plants were grown in [CO2]-controlled walk-in climate rooms, under a [CO2] of 270, 450 and 750 ppm. A model was used for upscaling from leaf to whole-plant photosynthesis and for quantifying the influence of plastic and genotypic responses. KEY RESULTS: It was shown that changes in canopy photosynthesis, specific leaf area (SLA) and stomatal conductance in response to changes in growth [CO2] were mainly determined by plastic and not by genotypic responses. We further found that plants originating from high [CO2] habitats performed better in terms of whole-plant photosynthesis, biomass and leaf area, than those from ambient [CO2] habitats at elevated [CO2] only when both genotypes competed. Similarly, plants from ambient [CO2] habitats performed better at low [CO2], also only when both genotypes competed. No difference in performance was found in mono stands. CONCLUSION: The results indicate that natural selection under increasing [CO2] will be mainly driven by competitive interactions. This supports the notion that plant-plant interactions have an important influence on future vegetation functioning and species distribution. Furthermore, plant performance was mainly driven by plastic and not by genotypic responses to changes in atmospheric [CO2].