An allometry perspective on crops.

Understanding trait-trait coordination is essential for successful plant breeding and crop modeling. Notably, plant size drives variation in morphological, physiological, and performance-related traits, as described by allometric laws in ecology. Yet, as allometric relationships have been limitedly studied in crops, how they influence and possibly limit crop performance remains unknown. Here, we review how an allometry perspective on crops gains insights into the phenotypic evolution during crop domestication, the breeding of varieties adapted to novel conditions, and the prediction of crop yields. As allometry is an active field of research, modeling and manipulating crop allometric relationships can help to develop more resilient and productive agricultural systems to face future challenges.

Can plants build their niche through modulation of soil microbial activities linked with nitrogen cycling? A test with Arabidopsis thaliana.

In natural systems, different plant species have been shown to modulate specific nitrogen (N) cycling processes so as to meet their N demand, thereby potentially influencing their own niche. This phenomenon might go beyond plant interactions with symbiotic microorganisms and affect the much less explored plant interactions with free-living microorganisms involved in soil N cycling, such as nitrifiers and denitrifiers. Here, we investigated variability in the modulation of soil nitrifying and denitrifying enzyme activities (NEA and DEA, respectively), and their ratio (NEA : DEA), across 193 Arabidopsis thaliana accessions. We studied the genetic and environmental determinants of such plant-soil interactions, and effects on plant biomass production in the next generation. We found that NEA, DEA, and NEA : DEA varied c. 30-, 15- and 60-fold, respectively, among A. thaliana genotypes and were related to genes linked with stress response, flowering, and nitrate nutrition, as well as to soil parameters at the geographic origin of the analysed genotypes. Moreover, plant-mediated N cycling activities correlated with the aboveground biomass of next-generation plants in home vs away nonautoclaved soil, suggesting a transgenerational impact of soil biotic conditioning on plant performance. Altogether, these findings suggest that nutrient-based plant niche construction may be much more widespread than previously thought.

Phenotypic limits of crop diversity: a data exploration of functional trait space.

Relationships between crop genetic and functional diversity are key to addressing contemporary agricultural challenges. Yet, there are few approaches for quantifying the relationship between genetic diversity and crop functional trait expression. Here, we introduce 'functional space accumulation curves' to analyze how trait space increases with the number of crop genotypes within a species. We explore the potential for functional space accumulating curves to quantify genotype-trait space relationships in four common annual crop species: barley (Hordeum vulgare), rice (Oryza sativa), soybean (Glycine max), and durum wheat (Triticum durum). We also employ these curves to describe genotype-trait space relationships in the wild annual Arabidopsis thaliana, which has not been subjected to artificial selection. All five species exhibited asymptotic functional space accumulation curves, suggesting a limit to intraspecific functional crop diversity, likely due to: dominant phenotypes represented by several genotypes; or functional redundancy that might exist among genotypes. Our findings indicate that there is a diminishing return of functional diversity with increasing number of genotypes. Our analysis demonstrates the efficacy of functional space accumulation curves in quantifying trait space occupancy of crops, with implications for managing crop diversity in agroecosystems, and genetic diversity in crop breeding programs.

Reduction in PLANT DEFENSIN 1 expression in Arabidopsis thaliana results in increased resistance to pathogens and zinc toxicity.

Ectopic expression of defensins in plants correlates with their increased capacity to withstand abiotic and biotic stresses. This applies to Arabidopsis thaliana, where some of the seven members of the PLANT DEFENSIN 1 family (AtPDF1) are recognised to improve plant responses to necrotrophic pathogens and increase seedling tolerance to excess zinc (Zn). However, few studies have explored the effects of decreased endogenous defensin expression on these stress responses. Here, we carried out an extensive physiological and biochemical comparative characterization of (i) novel artificial microRNA (amiRNA) lines silenced for the five most similar AtPDF1s, and (ii) a double null mutant for the two most distant AtPDF1s. Silencing of five AtPDF1 genes was specifically associated with increased aboveground dry mass production in mature plants under excess Zn conditions, and with increased plant tolerance to different pathogens - a fungus, an oomycete and a bacterium, while the double mutant behaved similarly to the wild type. These unexpected results challenge the current paradigm describing the role of PDFs in plant stress responses. Additional roles of endogenous plant defensins are discussed, opening new perspectives for their functions.

Natural variation of Arabidopsis thaliana responses to Cauliflower mosaic virus infection upon water deficit.

Plant virus pathogenicity is expected to vary with changes in the abiotic environment that affect plant physiology. Conversely, viruses can alter the host plant response to additional stimuli from antagonism to mutualism depending on the virus, the host plant and the environment. Ecological theory, specifically the CSR framework of plant strategies developed by Grime and collaborators, states that plants cannot simultaneously optimize resistance to both water deficit and pathogens. Here, we investigated the vegetative and reproductive performance of 44 natural accessions of A. thaliana originating from the Iberian Peninsula upon simultaneous exposure to soil water deficit and viral infection by the Cauliflower mosaic virus (CaMV). Following the predictions of Grime's CSR theory, we tested the hypothesis that the ruderal character of a plant genotype is positively related to its tolerance to virus infection regardless of soil water availability. Our results showed that CaMV infection decreased plant vegetative performance and annihilated reproductive success of all accessions. In general, water deficit decreased plant performance, but, despite differences in behavior, ranking of accessions tolerance to CaMV was conserved under water deficit. Ruderality, quantified from leaf traits following a previously published procedure, varied significantly among accessions, and was positively correlated with tolerance to viral infection under both well-watered and water deficit conditions, although the latter to a lesser extent. Also, in accordance with the ruderal character of the accession and previous findings, our results suggest that accession tolerance to CaMV infection is positively correlated with early flowering. Finally, plant survival to CaMV infection increased under water deficit. The complex interactions between plant, virus and abiotic environment are discussed in terms of the variation in plant ecological strategies at the intraspecific level.

Solving the grand challenge of phenotypic integration: allometry across scales.

Phenotypic integration is a concept related to the cascade of trait relationships from the lowest organizational levels, i.e. genes, to the highest, i.e. whole-organism traits. However, the cause-and-effect linkages between traits are notoriously difficult to determine. In particular, we still lack a mathematical framework to model the relationships involved in the integration of phenotypic traits. Here, we argue that allometric models developed in ecology offer testable mathematical equations of trait relationships across scales. We first show that allometric relationships are pervasive in biology at different organizational scales and in different taxa. We then present mechanistic models that explain the origin of allometric relationships. In addition, we emphasized that recent studies showed that natural variation does exist for allometric parameters, suggesting a role for genetic variability, selection and evolution. Consequently, we advocate that it is time to examine the genetic determinism of allometries, as well as to question in more detail the role of genome size in subsequent scaling relationships. More broadly, a possible-but so far neglected-solution to understand phenotypic integration is to examine allometric relationships at different organizational levels (cell, tissue, organ, organism) and in contrasted species.

Into the range: a latitudinal gradient or a center-margins differentiation of ecological strategies in Arabidopsis thaliana?

BACKGROUND AND AIMS: Determining within-species large-scale variation in phenotypic traits is central to elucidate the drivers of species' ranges. Intraspecific comparisons offer the opportunity to understand how trade-offs and biogeographical history constrain adaptation to contrasted environmental conditions. Here we test whether functional traits, ecological strategies from the CSR scheme and phenotypic plasticity in response to abiotic stress vary along a latitudinal or a center- margins gradient within the native range of Arabidopsis thaliana. METHODS: We experimentally examined the phenotypic outcomes of plant adaptation at the center and margins of its geographic range using 30 accessions from southern, central and northern Europe. We characterized the variation of traits related to stress tolerance, resource use, colonization ability, CSR strategy scores, survival and fecundity in response to high temperature (34 °C) or frost (- 6 °C), combined with a water deficit treatment. KEY RESULTS: We found evidence for both a latitudinal and a center-margins differentiation for the traits under scrutiny. Age at maturity, leaf dry matter content, specific leaf area and leaf nitrogen content varied along a latitudinal gradient. Northern accessions presented a greater survival to stress than central and southern accessions. Leaf area, C-scores, R-scores and fruit number followed a center-margins differentiation. Central accessions displayed a higher phenotypic plasticity than northern and southern accessions for most studied traits. CONCLUSIONS: Traits related to an acquisitive/conservative resource-use trade-off followed a latitudinal gradient. Traits associated with a competition/colonization trade-off differentiated along the historic colonization of the distribution range and then followed a center-margins differentiation. Our findings pinpoint the need to consider the joint effect of evolutionary history and environmental factors when examining phenotypic variation across the distribution range of a species.

Genome-wide and comparative phylogenetic analysis of senescence-associated NAC transcription factors in sunflower (Helianthus annuus).

BACKGROUND: Leaf senescence delay impacts positively in grain yield by maintaining the photosynthetic area during the reproductive stage and during grain filling. Therefore a comprehensive understanding of the gene families associated with leaf senescence is essential. NAC transcription factors (TF) form a large plant-specific gene family involved in regulating development, senescence, and responses to biotic and abiotic stresses. The main goal of this work was to identify sunflower NAC TF (HaNAC) and their association with senescence, studying their orthologous to understand possible functional relationships between genes of different species. RESULTS: To clarify the orthologous relationships, we used an in-depth comparative study of four divergent taxa, in dicots and monocots, with completely sequenced genomes (Arabidopsis thaliana, Vitis vinifera, Musa acuminata and Oryza sativa). These orthologous groups provide a curated resource for large scale protein sequence annotation of NAC TF. From the 151 HaNAC genes detected in the latest version of the sunflower genome, 50 genes were associated with senescence traits. These genes showed significant differential expression in two contrasting lines according to an RNAseq assay. An assessment of overexpressing the Arabidopsis line for HaNAC001 (a gene of the same orthologous group of Arabidopsis thaliana ORE1) revealed that this line displayed a significantly higher number of senescent leaves and a pronounced change in development rate. CONCLUSIONS: This finding suggests HaNAC001 as an interesting candidate to explore the molecular regulation of senescence in sunflower.

An exploration of the variability of physiological responses to soil drying in relation with C/N balance across three species of the under-utilized genus Vigna.

The genus Vigna (Fabaceae) is an agriculturally important taxon, which includes several crop species such as cowpea (Vigna unguiculata L.), mung bean (Vigna radiata) and azuki bean (Vigna angularis). Most studies have focused on cowpea (V. unguiculata (L.) as a drought-resistant crop, although insights on the mechanisms that confer this species the ability to grow in dry environment are still not fully resolved. The diversity of this rich genus has been overlooked in many physiological studies. This study explores the physiological mechanisms of response to soil drying (N2 fixation, transpiration rate and changes in C and N allocation) across three species of the Vigna genus: V. radiata, V. unguiculata, V. vexillata (tuber cowpea). A significant variability among the studied Vigna accessions was found for the threshold in decline of N2 fixation with soil drying. Less variability was observed in the transpiration threshold. Through the analysis of leaf traits variation under well-watered and water-deficit conditions, we were able to relate the variability in N2 fixation and transpiration response to C/N metabolism modifications resulting in different allocation of carbon and nitrogen to leaves under water deficit.

Adaptive diversification of growth allometry in the plant Arabidopsis thaliana.

Seed plants vary tremendously in size and morphology; however, variation and covariation in plant traits may be governed, at least in part, by universal biophysical laws and biological constants. Metabolic scaling theory (MST) posits that whole-organismal metabolism and growth rate are under stabilizing selection that minimizes the scaling of hydrodynamic resistance and maximizes the scaling of resource uptake. This constrains variation in physiological traits and in the rate of biomass accumulation, so that they can be expressed as mathematical functions of plant size with near-constant allometric scaling exponents across species. However, the observed variation in scaling exponents calls into question the evolutionary drivers and the universality of allometric equations. We have measured growth scaling and fitness traits of 451 Arabidopsis thaliana accessions with sequenced genomes. Variation among accessions around the scaling exponent predicted by MST was correlated with relative growth rate, seed production, and stress resistance. Genomic analyses indicate that growth allometry is affected by many genes associated with local climate and abiotic stress response. The gene with the strongest effect, PUB4, has molecular signatures of balancing selection, suggesting that intraspecific variation in growth scaling is maintained by opposing selection on the trade-off between seed production and abiotic stress resistance. Our findings suggest that variation in allometry contributes to local adaptation to contrasting environments. Our results help reconcile past debates on the origin of allometric scaling in biology and begin to link adaptive variation in allometric scaling to specific genes.

Secondary metabolites have more influence than morphophysiological traits on litter decomposability across genotypes of Arabidopsis thaliana.

Although interspecific variation in plant phenotype is recognised to impact afterlife processes such as litter decomposability, it is still unclear which traits and selection pressures explain these relationships. Examining intraspecific variation is crucial to identify and compare trait effects on decomposability, and investigate the potential role of natural selection. We studied the genetic variability and relationships between decomposability, plant traits typically related to decomposability at species level (morphophysiological traits), and leaf metabolites among a set of genotypes of Arabidopsis thaliana grown under controlled conditions. We also investigated correlations between decomposability and environmental variables at genotypes collection site. We investigated the genetic architecture of decomposability with genome-wide association studies (GWAS). There was large genetic variability in decomposability that was correlated with precipitation. Morphophysiological traits had a minor effect, while secondary metabolites, especially glucosinolates, were correlated with decomposability. Consistently, GWAS suggested that genes and metabolites related to the composition of cell membranes and envelopes control the variation of decomposability across genotypes. Our study suggests that decomposability varies within species as a result of metabolic adaptation to climate. Our findings highlight that subtle variations of defence-related metabolites like glucosinolates may strongly influence after-life processes such as decomposability.

Stress-Related Gene Expression Reflects Morphophysiological Responses to Water Deficit.

Acclimation to water deficit (WD) enables plants to maintain growth under unfavorable environmental conditions, although the mechanisms are not completely understood. In this study, the natural variation of long-term acclimation to moderate and severe soil WD was investigated in 18 Arabidopsis (Arabidopsis thaliana) accessions using PHENOPSIS, an automated phenotyping platform. Soil water content was adjusted at an early stage of plant development and maintained at a constant level until reproductive age was achieved. The accessions were selected based on the expression levels of ANNEXIN1, a drought-related marker. Severe WD conditions had a greater effect on most of the measured morphophysiological traits than moderate WD conditions. Multivariate analyses indicated that trait responses associated with plant size and water management drove most of the variation. Accessions with similar responses at these two levels were grouped in clusters that displayed different response strategies to WD The expression levels of selected stress-response genes revealed large natural variation under WD conditions. Responses of morphophysiological traits, such as projected rosette area, transpiration rate, and rosette water content, were correlated with changes in the expression of stress-related genes, such as NINE-CIS-EPOXYCAROTENOID DIOXYGENASE3 and N-MYC DOWNREGULATED-LIKE1 (NDL1), in response to WD Interestingly, the morphophysiological acclimation response to WD also was reflected in the gene expression levels (most notably those of NDL1, CHALCONE SYNTHASE, and MYB DOMAIN PROTEIN44) in plants cultivated under well-watered conditions. Our results may lead to the development of biomarkers and predictors of plant morphophysiological responses based on gene expression patterns.

Climate as a driver of adaptive variations in ecological strategies in Arabidopsis thaliana.

Background and aims: The CSR classification categorizes plants as stress tolerators (S), ruderals (R) and competitors (C). Initially proposed as a general framework to describe ecological strategies across species, this scheme has recently been used to investigate the variation of strategies within species. For instance, ample variation along the S-R axis was found in Arabidopsis thaliana, with stress-tolerator accessions predominating in hot and dry regions, which was interpreted as a sign of functional adaptation to climate within the species. Methods: In this study the range of CSR strategies within A. thaliana was evaluated across 426 accessions originating from North Africa to Scandinavia. A position in the CSR strategy space was allocated for every accession based on three functional traits: leaf area, leaf dry matter content (LDMC) and specific leaf area (SLA). Results were related to climate at origin and compared with a previous study performed on the same species. Furthermore, the role of natural selection in phenotypic differentiation between lineages was investigated with QST-FST comparisons, using the large amount of genetic information available for this species. Key Results: Substantial variation in ecological strategies along the S-R axis was found in A. thaliana. By contrast with previous findings, stress-tolerator accessions predominated in cold climates, notably Scandinavia, where late flowering was associated with traits related to resource conservation, such as high LDMC and low SLA. Because of trait plasticity, variations in CSR classification in relation to growth conditions were also observed for the same genotypes. Conclusions: There is a latitudinal gradient of ecological strategies in A. thaliana as a result of within-species adaptation to climate. Our study also underlines the importance of growth conditions and of the methodology used for trait measurement, notably age versus stage measurement, to infer the strength and direction of trait-environment relationships. This highlights the potential and limitations of the CSR classification in explaining functional adaptation to the environment.

Occupancy and overlap in trait space along a successional gradient in Mediterranean old fields.

PREMISE OF THE STUDY: Secondary succession is a worldwide phenomenon affecting plant communities. Studying functional variation during succession aids in understanding the mechanisms through which environmental shifts drive succession. We investigated changes in the functional space occupied by herbaceous communities during succession. Furthermore, since different traits are differently affected by environmental conditions, we asked how considering different sets of plant traits impacts those changes. METHODS: Using a chronosequence of Mediterranean old fields (2-42 yr after abandonment), we analyzed shifts of the occupied functional space during succession, how the volume of occupied functional space varies compared with null expectations, and the functional overlap between communities of different successional status. We repeated these analyses considering (1) the leaf-height-seed functional dimensions separately and together and (2) different sets of traits representing those dimensions. KEY RESULTS: From early to late succession, a shift toward nutrient conservative-light competitive species occurred. Functional strategies of mid-successional communities appeared more diverse than expected by chance and less diverse than expected for early and late communities. Early and middle stages overlapped the most. These patterns were generally robust to the choice of functional axes, though important trait-specific exceptions occurred. CONCLUSIONS: We showed evidence for a well-defined history of successive dominance of different assembly mechanisms along succession, resulting in a generally stronger functional diversification in mid-succession. We also demonstrated that different traits typically grouped under one functional dimension can substantially affect the results, discouraging the use of surrogate traits from the same dimension.

The Arabidopsis cer26 mutant, like the cer2 mutant, is specifically affected in the very long chain fatty acid elongation process.

Plant aerial organs are covered by cuticular waxes, which form a hydrophobic crystal layer that mainly serves as a waterproof barrier. Cuticular wax is a complex mixture of very long chain lipids deriving from fatty acids, predominantly of chain lengths from 26 to 34 carbons, which result from acyl-CoA elongase activity. The biochemical mechanism of elongation is well characterized; however, little is known about the specific proteins involved in the elongation of compounds with more than 26 carbons available as precursors of wax synthesis. In this context, we characterized the three Arabidopsis genes of the CER2-like family: CER2, CER26 and CER26-like . Expression pattern analysis showed that the three genes are differentially expressed in an organ- and tissue-specific manner. Using individual T-DNA insertion mutants, together with a cer2 cer26 double mutant, we characterized the specific impact of the inactivation of the different genes on cuticular waxes. In particular, whereas the cer2 mutation impaired the production of wax components longer than 28 carbons, the cer26 mutant was found to be affected in the production of wax components longer than 30 carbons. The analysis of the acyl-CoA pool in the respective transgenic lines confirmed that inactivation of both genes specifically affects the fatty acid elongation process beyond 26 carbons. Furthermore, ectopic expression of CER26 in transgenic plants demonstrates that CER26 facilitates the elongation of the very long chain fatty acids of 30 carbons or more, with high tissular and substrate specificity.

Multivariate genetic analysis of plant responses to water deficit and high temperature revealed contrasting adaptive strategies.

How genetic factors control plant performance under stressful environmental conditions is a central question in ecology and for crop breeding. A multivariate framework was developed to examine the genetic architecture of performance-related traits in response to interacting environmental stresses. Ecophysiological and life history traits were quantified in the Arabidopsis thaliana Ler × Cvi mapping population exposed to constant soil water deficit and high air temperature. The plasticity of the genetic variance-covariance matrix (G-matrix) was examined using mixed-effects models after regression into principal components. Quantitative trait locus (QTL) analysis was performed on the predictors of genotype effects and genotype by environment interactions (G × E). Three QTLs previously identified for flowering time had antagonistic G × E effects on carbon acquisition and the other traits (phenology, growth, leaf morphology, and transpiration). This resulted in a size-dependent response of water use efficiency (WUE) to high temperature but not soil water deficit, indicating that most of the plasticity of carbon acquisition and WUE to temperature is controlled by the loci that control variation of development, size, growth, and transpiration. A fourth QTL, MSAT2.22, controlled the response of carbon acquisition to specific combinations of watering and temperature irrespective of plant size and development, growth, and transpiration rate, which resulted in size-independent plasticity of WUE. These findings highlight how the strategies to optimize plant performance may differ in response to water deficit and high temperature (or their combination), and how different G × E effects could be targeted to improve plant tolerance to these stresses.

Growing on calcareous soils and facing climate change.

Soil calcium carbonate (CaCO3) impacts plant mineral nutrition far beyond Fe metabolism, imposing constraints for crop growth and quality in calcareous agrosystems. Our knowledge on plant strategies to tolerate CaCO3 effects mainly refers to Fe acquisition. This review provides an update on plant cellular and molecular mechanisms recently described to counteract the negative effects of CaCO3 in soils, as well as recent efforts to identify genetic bases involved in CaCO3 tolerance from natural populations, that could be exploited to breed CaCO3-tolerant crops. Finally, we review the impact of environmental factors (soil water content, air CO2, and temperature) affecting soil CaCO3 equilibrium and plant tolerance to calcareous soils, and we propose strategies for improvement in the context of climate change.

Ecological trade-offs drive phenotypic and genetic differentiation of Arabidopsis thaliana in Europe.

Plant diversity is shaped by trade-offs between traits related to competitive ability, propagule dispersal, and stress resistance. However, we still lack a clear understanding of how these trade-offs influence species distribution and population dynamics. In Arabidopsis thaliana, recent genetic analyses revealed a group of cosmopolitan genotypes that successfully recolonized Europe from its center after the last glaciation, excluding older (relict) lineages from the distribution except for their north and south margins. Here, we tested the hypothesis that cosmopolitans expanded due to higher colonization ability, while relicts persisted at the margins due to higher tolerance to competition and/or stress. We compared the phenotypic and genetic differentiation between 71 European genotypes originating from the center, and the south and north margins. We showed that a trade-off between plant fecundity and seed mass shapes the differentiation of A. thaliana in Europe, suggesting that the success of the cosmopolitan groups could be explained by their high dispersal ability. However, at both north and south margins, we found evidence of selection for alleles conferring low dispersal but highly competitive and stress-resistance abilities. This study sheds light on the role of ecological trade-offs as evolutionary drivers of the distribution and dynamics of plant populations.

The Arabidopsis leaf quantitative atlas: a cellular and subcellular mapping through unified data integration.

Quantitative analyses and models are required to connect a plant's cellular organisation with its metabolism. However, quantitative data are often scattered over multiple studies, and finding such data and converting them into useful information is time-consuming. Consequently, there is a need to centralise the available data and to highlight the remaining knowledge gaps. Here, we present a step-by-step approach to manually extract quantitative data from various information sources, and to unify the data format. First, data from Arabidopsis leaf were collated, checked for consistency and correctness and curated by cross-checking sources. Second, quantitative data were combined by applying calculation rules. They were then integrated into a unique comprehensive, referenced, modifiable and reusable data compendium representing an Arabidopsis reference leaf. This atlas contains the metrics of the 15 cell types found in leaves at the cellular and subcellular levels.