Patterns of thermal adaptation in a globally distributed plant pathogen: Local diversity and plasticity reveal two-tier dynamics.

Plant pathogen populations inhabit patchy environments with contrasting, variable thermal conditions. We investigated the diversity of thermal responses in populations sampled over contrasting spatiotemporal scales, to improve our understanding of their dynamics of adaptation to local conditions. Samples of natural populations of the wheat pathogen Zymoseptoria tritici were collected from sites within the Euro-Mediterranean region subject to a broad range of climatic conditions. We tested for local adaptation, by accounting for the diversity of responses at the individual and population levels on the basis of key thermal performance curve parameters and "thermotype" (groups of individuals with similar thermal responses) composition. The characterization of phenotypic responses and genotypic structure revealed the following: (i) a high degree of individual plasticity and variation in sensitivity to temperature conditions across spatiotemporal scales and populations; and (ii) geographic variation in thermal response among populations, with major alterations due to seasonal patterns over the wheat-growing season. The seasonal shifts in functional composition suggest that populations are locally structured by selection, contributing to adaptation patterns. Further studies combining selection experiments and modeling are required to determine how functional group selection drives population dynamics and adaptive potential in response to thermal heterogeneity.

Nitrogen Uptake Efficiency, Mediated by Fine Root Growth, Early Determines Temporal and Genotypic Variations in Nitrogen Use Efficiency of Winter Oilseed Rape.

Maintaining seed yield under low N inputs is a major issue for breeding, which requires thoroughly exploiting the genetic diversity of processes related to Nitrogen Use Efficiency (NUE). However, dynamic analysis of processes underlying genotypic variations in NUE in response to N availability from sowing to harvest are scarce, particularly at the whole-plant scale. This study aimed to dynamically decipher the contributions of Nitrogen Uptake Efficiency (NUpE) and Nitrogen Utilization Efficiency (NUtE) to NUE and to identify traits underlying NUpE genetic variability throughout the growth cycle of rapeseed. Three experiments were conducted under field-like conditions to evaluate seven genotypes under two N conditions. We developed NUE_DM (ratio of total plant biomass to the amount of N available) as a new proxy of NUE at harvest, valid to discriminate genotypes from the end of inflorescence emergence, and N conditions as early as the beginning of stem elongation. During autumn growth, NUpE explained up to 100% of variations in NUE_DM, validating the major role of NUpE in NUE shaping. During this period, under low N conditions, up to 53% of the plant nitrogen was absorbed and NUpE genetic variability resulted not from differences in Specific N Uptake but in fine-root growth. NUtE mainly contributed to NUE_DM genotypic variation during the reproductive phase under high-N conditions, but NUpE contribution still accounted for 50-75% after flowering. Our study highlights for the first time NUpE and fine-root growth as important processes to optimize NUE, which opens new prospects for breeding.

Phenotyping Thermal Responses of Yeasts and Yeast-like Microorganisms at the Individual and Population Levels: Proof-of-Concept, Development and Application of an Experimental Framework to a Plant Pathogen.

Deciphering the responses of microbial populations to spatiotemporal changes in their thermal environment is instrumental in improving our understanding of their eco-evolutionary dynamics. Recent studies have shown that current phenotyping protocols do not adequately address all dimensions of phenotype expression. Therefore, these methods can give biased assessments of sensitivity to temperature, leading to misunderstandings concerning the ecological processes underlying thermal plasticity. We describe here a new robust and versatile experimental framework for the accurate investigation of thermal performance and phenotypic diversity in yeasts and yeast-like microorganisms, at the individual and population levels. In addition to proof-of-concept, the application of this framework to the fungal wheat pathogen Zymoseptoria tritici resulted in detailed characterisations for this yeast-like microorganism of (i) the patterns of temperature-dependent changes in performance for four fitness traits; (ii) the consistency in thermal sensitivity rankings of strains between in planta and in vitro growth assessments; (iii) significant interindividual variation in thermal responses, with four principal thermotypes detected in a sample of 66 strains; and (iv) the ecological consequences of this diversity for population-level processes through pairwise competition experiments highlighting temperature-dependent outcomes. These findings extend our knowledge and ability to quantify and categorise the phenotypic heterogeneity of thermal responses. As such, they lay the foundations for further studies elucidating local adaptation patterns and the effects of temperature variations on eco-evolutionary and epidemiological processes.

The development of a foliar fungal pathogen does react to leaf temperature!

The thermal performance curve is an ecological concept relating the phenotype of organisms and temperature. It requires characterization of the leaf temperature for foliar fungal pathogens. Epidemiologists, however, use air temperature to assess the impacts of temperature on such pathogens. Leaf temperature can differ greatly from air temperature, either in controlled or field conditions. This leads to a misunderstanding of such impacts. Experiments were carried out in controlled conditions on adult wheat plants to characterize the response of Mycosphaerella graminicola to a wide range of leaf temperatures. Three fungal isolates were used. Lesion development was assessed twice a week, whereas the temperature of each leaf was monitored continuously. Leaf temperature had an impact on disease dynamics. The latent period of M. graminicola was related to leaf temperature by a quadratic relationship. The establishment of thermal performance curves demonstrated differences among isolates as well as among leaf layers. For the first time, the thermal performance curve of a foliar fungal pathogen has been established using leaf temperature. The experimental setup we propose is applicable, and efficient, for other foliar fungal pathogens. Results have shown the necessity of such an approach, when studying the acclimatization of foliar fungal pathogens.

To what extent may changes in the root system architecture of Arabidopsis thaliana grown under contrasted homogenous nitrogen regimes be explained by changes in carbon supply? A modelling approach.

Root system architecture adapts to low nitrogen (N) nutrition. Some adaptations may be mediated by modifications of carbon (C) fluxes. The objective of this study was to test the hypothesis that changes in root system architecture under different N regimes may be accounted for by using simple hypotheses of C allocation within the root system of Arabidopsis thaliana. With that purpose, a model during vegetative growth was developed that predicted the main traits of root system architecture (total root length, lateral root number, and specific root length). Different experimental data sets crossing three C levels and two N homogenous nutrition levels were generated. Parameters were estimated from an experiment carried out under medium C and high N conditions. They were then checked under other CxN conditions. It was found that the model was able to simulate correctly C effects on root architecture in both high and low N nutrition conditions, with the same parameter values. It was concluded that C flux modifications explained the major part of root system adaptation to N supply, even if they were not sufficient to simulate some changes, such as specific root length.

Evaluation of a turbid medium model to simulate light interception by walnut trees (hybrid NG38 × RA and Juglans regia) and sorghum canopies (Sorghum bicolor) at three spatial scales.

Light is one of the most important components to be included in functional-structural plant models that simulate the biophysical processes, such as photosynthesis, evapotranspiration and photomorphogenesis, involved in plant growth and development. In general, in these models, light is treated using a turbid medium approach in which radiation attenuation is described by the Beer-Lambert law. In the present study, we assessed the hypothesis of leaf random dispersion in the Beer-Lambert law at the whole-canopy, horizontal-layer and local scales. We compared two calculation methods of radiation attenuation: a 3D turbid medium model using the Beer-Lambert law and the other based on a projective method. The two models were compared by applying the calculations to two walnut trees and two sorghum canopies, which have contrasting structural characteristics. The structures of these canopies were measured in 3D to take into account the arrangement and orientation features of the plant elements. The assumptions made by the Beer-Lambert law allowed adequate simulation of light interception in a structure with little overlapping at the horizontal-layer and whole-canopy scales. At the local scale, discrepancies between the turbid medium model and the model based on a virtual plant were reduced with an adequate choice of structural parameters, such as the leaf inclination distribution function.

Simulating the effects of localized red:far-red ratio on tillering in spring wheat (Triticum aestivum) using a three-dimensional virtual plant model.

The outgrowth of tiller buds in Poaceae is influenced by the ratio of red to far-red light irradiance (R:FR). At each point in the plant canopy, R:FR is affected by light scattered by surrounding plant tissues. This paper presents a three-dimensional virtual plant modelling approach to simulate local effects of R:FR on tillering in spring wheat (Triticum aestivum). R:FR dependence of bud outgrowth was implemented in a wheat model, using three hypothetical responses of bud extension to R:FR (unit step, curvilinear and linear response). Bud break occurred when a threshold bud length was reached. Simulations were performed for three plant population densities. In accordance with experimental observations, fewer tillers per plant were simulated for higher plant population densities. The linear and curvilinear responses caused a delay in the increase in tiller number compared with experimental data. The unit step response approached experimental results best. It is suggested that a model based on relatively simple relations can be used to simulate degree of tillering. This study has shown that the virtual plant approach is a promising tool with which to address crop morphological and ecological research questions where the determining factors act at the level of the individual plant organ.

Simulation of the three-dimensional distribution of the red:far-red ratio within crop canopies.

It is widely recognized that the red:far-red ratio (zeta) acts as a signal that triggers plant morphogenesis. New insights into photomorphogenesis have been gained through experiments in controlled environments. Extrapolation of such results to field conditions requires characterization of the zeta signal perceived by plant organs within canopies. This paper presents a modeling approach to characterize this signal. A wheat (Triticum aestivum) architectural model was coupled with a three-dimensional light model estimating the irradiances of virtual sensors. Architectural parameters and zeta values were measured on two contrasting spring wheat canopies under outdoor conditions. Light simulations were compared with measurements, and an analysis of sensitivity to measurement conditions was carried out. The model results agreed well with measurements and previously published data. The sensitivity analysis showed that zeta strongly depends on canopy development as well as on sky conditions, sensor orientation, and sensor field of view. This paper shows that modeling enables investigation of zeta distribution in a canopy over space and time. It also shows that the characterization of light quality strongly depends on measurement conditions, and that any discrepancies in results are likely attributable to different experimental set-ups. The usefulness of this modeling approach for crop photomorphogenesis studies is discussed.

Phylloclimate or the climate perceived by individual plant organs: what is it? How to model it? What for?

This review introduces the emergence of a new research topic, phylloclimate, located at the crossroads between ecophysiology and canopy microclimate research. Phylloclimate corresponds to the physical environment actually perceived by each individual aerial organ of a plant population, and is described by physical variables such as spectral irradiance, temperature, on-leaf water and features of around-organ air (wind speed, temperature, humidity, etc.). Knowing the actual climate in which plant organs grow may enable advances in the understanding of plant-environment interactions, as knowing surface temperature instead of air temperature enabled advances in the study of canopy development. Characterizing phylloclimate variables, using experimental work or modeling, raises many questions such as the choice of suitable space- and time-scale as well as the ability to individualize plant organs within a canopy. This is of particular importance when aiming to link phylloclimate and function-structure plant models. Finally, recent trends and challenging questions in phylloclimate research are discussed, as well as the possible applications of phylloclimate results.

Towards a generic architectural model of tillering in Gramineae, as exemplified by spring wheat (Triticum aestivum).

This paper presents an architectural model of wheat (Triticum aestivum), designed to explain effects of light conditions at the individual leaf level on tillering kinetics. Various model variables, including blade length and curvature, were parameterized for spring wheat, and compared with winter wheat and other Gramineae species. The architectural model enables simulation of plant properties at the level of individual organs. Parameterization was based on data derived from an outdoor experiment with spring wheat cv. Minaret. Final organ dimensions of tillers could be modelled using the concept of relative phytomer numbers. Various variables in spring wheat showed marked similarities to winter wheat and other species, suggesting possibilities for a general Gramineae architectural model. Our descriptive model is suitable for our objective: investigating light effects on tiller behaviour. However, we plan to replace the descriptive modelling solutions by physiological, mechanistic solutions, starting with the localized production and partitioning of assimilates as affected by abiotic growth factors.

Maize leaves turn away from neighbors.

In commercial crops, maize (Zea mays) plants are typically grown at a larger distance between rows (70 cm) than within the same row (16-23 cm). This rectangular arrangement creates a heterogeneous environment in which the plants receive higher red light (R) to far-red light (FR) ratios from the interrow spaces. In field crops, the hybrid Dekalb 696 (DK696) showed an increased proportion of leaves toward interrow spaces, whereas the experimental hybrid 980 (Exp980) retained random leaf orientation. Mirrors reflecting FR were placed close to isolated plants to simulate the presence of neighbors in the field. In addition, localized FR was applied to target leaves in a growth chamber. During their expansion, the leaves of DK696 turned away from the low R to FR ratio signals, whereas Exp980 leaves remained unaffected. On the contrary, tillering was reduced and plant height was increased by low R to FR ratios in Exp980 but not in DK696. Isolated plants preconditioned with low R/FR-simulating neighbors in a North-South row showed reduced mutual shading among leaves when the plants were actually grouped in North-South rows. These observations contradict the current view that phytochrome-mediated responses to low R/FR are a relic from wild conditions, detrimental for crop yield.