Delphine Luquet

EcoMeristem, a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis

Because of rapid advances in functional genomics there is an increasing demand for models simulating complex traits, such as the physiological and environmental controls of plant morphology. This paper describes, validates and explores the behaviour of the structural-functional model EcoMeristem, developed for cereals in the context of the Generation Challenge Program (GCP; CGIAR). EcoMeristem constructs the plant on the basis of an organogenetic body plan, driven by intrinsic (genetic) behavioural norms of meristems. These norms consist of phenological-topological rules for organ initiation and pre-dimensioning (sink creation) and rules enabling feedbacks of the plants resource status on the organogenetic processes. Plant resource status is expressed by a state variable called Internal Competition Index (Ic) calculated daily as the ratio of assimilate source (supply) over the sum of active sinks (demand). Ic constitutes an internal signal analogous to sugar signalling. Ic affects potential phytomer size, tiller initiation, leaf senescence, and carbohydrate storage and mobilisation. The model was calibrated and tested on IR64 rice grown in controlled environments, and validated with field observations for the same cultivar (Philippines). Observed distributions and dynamics of soluble sugars and starch in plant organs supported the model concepts of internal competition and the role of reserves as a buffer for Ic fluctuations. Model sensitivity analyses suggested that plant growth and development depend not only on assimilate supply, but also on organogenesis-based demand. If true, this conclusion has important consequences for crop improvement strategies.

Environmental and genetic control of morphogenesis in crops: towards models simulating phenotypic plasticity

As molecular biologists are realising the importance of physiology in understanding functional genomics of quantitative traits, and as physiologists are realising the formidable prospects for improving their phenotypic models with information on the underlying gene networks, researchers worldwide are working on linked physiological-genetic models. These efforts are in their early methodological stage despite, or because of, the availability of many different types of models, the problem being to bring together the different ways that scientists see the plant. This paper describes some current efforts to adapt phenotype models to the objective of simulating gene-phene processes at the plant or crop scale. Particular emphasis is given to the models capacity to simulate genotype x environment interaction and the resulting phenotypic plasticity, assuming that this permits the defining of model parameters that are closer to specific gene action. Three different types of approaches are presented: (1) a generic, mathematical-architectural model called GREENLAB that simulates resource-modulated morphogenesis; (2) an ecophysiological model of peach tree fruit development and filling, parameterised for a mapping population to evaluate the potential of plugging quantitative trait locus (QTL) effects into the model; and (3) the new model Ecomeristem that constructs plant architecture and its phenotypic plasticity from meristem behaviour, the principal hypothesis being that resource limitations and stresses feed back on the meristems. This latter choice is based on the fact that gene expression happens to a large extent in the meristems. The model is evaluated on the basis of preliminary studies on vegetative-stage rice. The different modelling concepts are critically discussed with respect to their ability to simulate phenotypic plasticity and to operate with parameters that approximate specific gene action, particularly in the area of morphogenesis.

Characterization of drought stress environments for upland rice and maize in central Brazil.

Drought stresses arise when the combination of rainfall and soil water supply are insufficient to meet the transpiration needs of the crop. In the Cerrado region of Goiás state, Brazil, summer rainfall is typically greater than 1000xa0mm. However, drought stress can occur during rain-free periods of only 1–3xa0weeks, since roots are frequently restricted to shallow depths due to Al-induced acidity in deeper soil layers. If these droughts are frequent, then plant breeding programs need to consider how to develop suitable germplasm for the target population of environments (TPE). A crop simulation model was used to determine patterns of drought stress for 12 locations and >30 environments (6xa0yearsxa0×xa05–6 planting dates) for short and medium duration rice crops (planted in early summer), and for maize grown either as a 1st or 2nd crop in the summer cycle. Regression analysis of the simulations confirmed the greater yield impact in both crops of drought stress (quantified as the ratio of water-limited to potential transpiration) when it occurred around the time of flowering and early grain-filling. For rice, mild mid-season droughts occurred 40–60% of the time in virgin (0.4xa0m deep for rice or 0.5xa0m for maize) soils and improved (0.8xa0m for rice or 1.0xa0m for maize) soils, with a yield reduction of <30%. More severe reproductive and grain-filling stress (yield reductions of 50% for rice to 90% for maize) occurred less frequently in rice (<30% of time) and 1st maize crop (< 10% of time). The 2nd maize crop experienced the greatest proportion (75–90%) of drought stresses that reduced yield to <50% of potential, with most of these occasions associated with later planting. The rice breeding station (CNPAF) experiences the same pattern of different drought types as for the TPE, and is largely suitable for early-stage selection of adapted germplasm based on yield potential. However, selection for virgin soil types could be augmented by evaluation on some less-improved soils in the slightly drier parts of the TPE region. Similarly, the drought patterns at the maize research station (CNPMS) and the other maize screening locations are better suited to selection of lines for the improved soil types. Development of lines for the 2nd crop and on more virgin (acidic) soils would require more targeted selection at late planting dates in drier sites.

Regulation of tillering in sorghum: Environmental effects

BACKGROUND AND AIMSnTillering has a significant effect on canopy development and, hence, on resource capture, crop growth and grain yield in sorghum. However, the physiological basis of tillering and its regulation by environmental effects are not fully understood. The objective of this study was to understand and quantify the environmental effects on tillering in sorghum using a carbohydrate supply-demand framework.nnnMETHODSnA series of five experiments with a wide range of radiation and temperature conditions was conducted and details of the tillering responses of a single representative hybrid were monitored. The concept of internal plant competition for carbohydrate was developed for analysis of these responses.nnnKEY RESULTSnTiller appearance was highly synchronized with main shoot leaf appearance, with a consistent hierarchy for tillering across environments. The main environmental effect was on the frequency of tiller appearance, in particular of the lower-rank tillers. This explained some of the observed environmental differences in the onset of tillering. A generalized index of internal plant competition, which took account of plant assimilate supply and demand (S/D(index)) during the critical period for tillering, explained most of the variation in maximum tiller number observed across the five experiments.nnnCONCLUSIONSnThis result was consistent with the hypothesis that internal plant competition for assimilates regulates tillering in sorghum. Hence, the framework outlined has a predictive value that could provide the basis for dynamic simulation of tillering in crop growth models.

EcoMeristem, a model of morphogenesis and competition among sinks in rice. 2. Simulating genotype responses to phosphorus deficiency

Phenotypic plasticity enables plants to adjust their morphology and phenology to variable environments. Although potentially important for crop breeding and management, the physiology and genetics of plasticity traits are poorly understood, and few models exist for their study. In the previous paper of this series, the structural-functional model EcoMeristem was described and field validated for vegetative-stage rice. This study applies the model to an experimental study on phosphorus deficiency effects on two morphologically contrasting rice cultivars, IR64 and Azucena, grown in controlled environments under hydroponics culture. Phosphorus deficiency caused severe biomass growth reductions in the shoot but not in the root, thus increasing the rootu2009/u2009shoot weight ratio. It also inhibited tiller formation and leaf elongation, prolonged the phyllochron, and increased carbohydrate reserve pools in the plant. Analysis aided by the model identified inhibition of leaf extension and tillering as primary effects of the stress. Physiological feedback probably led to longer phyllochron, greater reserve accumulation and root growth stimulation. The main effect of P deficiency appeared to be a reduction in demand for assimilates in the shoot while photosynthetic radiation use efficiency remained nearly constant, resulting in spill-over of excess assimilates into reserve compartments and root growth. The results are discussed in the light of future applications of EcoMeristem for phenotyping and genetic analyses of phenotypic plasticity.

Phenotypic Plasticity of Rice Seedlings: Case of Phosphorus Deficiency

Abstract The aim of this study is to characterize the plasticity of root and shoot morphology in rice, the genomic model plant for cereals, using P deficiency as environmental factor causing variability. A phytotron study on Nipponbare (Oryza Sativa L.) seedlings was conducted to analyze the effects of P deficiency on plant organogenesis (tiller and leaf appearance, root apex number) and allometric relationships (root/shoot weight ratio, specific leaf area (SLA) and specific root length (SRL), blade/sheath weight ratio). The results confirmed that the main effect of P deficiency is a reduction of shoot growth for the benefit of the root system. Reduced shoot growth was associated with reduced tiller production, longer phyllochron and reduced leaf elongation rate while final leaf size remained unchanged. The reduced leaf elongation rate might be a primary response to P deficiency and this caused lower phyllochron and tillering by feedback. Allometric parameters such as SLA, SRL, root apex number per unit length and leaf blade/sheath weight ratio remained largely stable under P deficiency. Increased root growth relative to shoot was associated with increased sucrose concentration in roots, and thus possibly resulted from assimilates liberated by shoot growth inhibition. The simple theory of multiple morphological changes resulting from slow leaf expansion under P deficiency requires further experimental confirmation, after which it may serve as a basis for a mechanistic model of rice phenotypic plasticity and certain genotype X environment interactions on morphology.

Regulation of tillering in sorghum: genotypic effects

BACKGROUND AND AIMSnGenotypic variation in tillering can be caused by differences in the carbon supply-demand balance within a plant. The aim of this study was to understand and quantify the effects of genotype on tillering as a consequence of the underlying internal competition for carbohydrates.nnnMETHODSnFive sorghum hybrids, derived from inbred lines with a common genetic background and with similar phenology and plant height but contrasting tillering, were grown in five experiments. The experiments covered a wide range in radiation and temperature conditions, so that number of tillers produced varied significantly. Data on leaf area, tiller number, and biomass accumulation and partitioning were collected at regular intervals. To quantify internal plant competition for carbohydrates, a carbohydrate supply-demand index (S/D(index)) was developed and related to variation in tillering.nnnKEY RESULTSnThe appearance of main shoot leaves and tillers was highly co-ordinated across genotypes. High-tillering hybrids had a greater appearance frequency of early tiller ranks than low-tillering hybrids, and this was associated with narrower and hence smaller main shoot leaves. A generalized S/D(index) of internal plant competition accounted for most of the observed variation in maximum tiller number (N(tiller,max)) across genotypes. However, genotypic differences in the relationship between the S/D(index) and N(tiller,max) suggested that high-tillering hybrids also had a lower S/D threshold at which tillers appeared, possibly associated with hormonal effects.nnnCONCLUSIONSnThe results support the hypothesis that genotypic differences in tillering were associated with differences in plant carbon S/D balance, associated with differences in leaf size and in the threshold at which tillers grow out. The results provide avenues for phenotyping of mapping populations to identify genomic regions regulating tillering. Incorporating the results in crop growth simulation models could provide insight into the complex genotype-by-management-by-environment interactions associated with drought adaptation.

Orchestration of transpiration, growth and carbohydrate dynamics in rice during a dry-down cycle

The regulation of carbohydrate metabolism and source-sink relationships among organs play a key role in plant adaptation to drought. This study aimed at characterising the dynamics of transpiration, development, growth and carbon metabolism, as well as the expression of invertase genes, in response to drought during a dry-down cycle. Three 1-month experiments were conducted in controlled environment using the rice genotype IR64 (Oryza sativa L., indica). Plant leaf relative transpiration and expansion rates decreased linearly when fraction of transpirable soil water (FTSW) dropped below 0.66 and 0.58, respectively. Hexose and starch concentration responses to FTSW in a given organ were generally linear and opposite: in source leaves, hexose concentration increased and starch decreased, and vice versa in sink leaves and roots. Sucrose remained constant in source leaves and increased slightly in sink leaves. Starch reserves built up during stress in sink organs were rapidly mobilised upon rewatering, indicating its involvement in a mechanism to ensure recovery. Expression of cell-wall and vacuolar invertase genes under stress increased in sink leaves, interpreted as a mechanism to maintain sink activity (cell wall) and osmotic adjustment (vacuolar). It is concluded that carbohydrate metabolism in sink organs under drought is highly regulated, and important for stress adaptation.

Grain, sugar and biomass accumulation in tropical sorghums. I. Trade-offs and effects of phenological plasticity

Grain and sweet sorghum (Sorghum bicolor (L.) Moench) differ in their ability to produce either high grain yield or high sugar concentration in the stems. Some cultivars of sorghum may yield both grains and sugar. This paper investigates the trade-offs among biomass, grain and sugar production. Fourteen tropical sorghum genotypes with contrasted sweetness and PP sensitivity were evaluated in the field near Bamako (Mali) at three sowing dates under favourable rainfed conditions. Plant phenology, morphology, dry matter of different organs and stem sugar content were measured at anthesis and grain maturity. A panicle pruning treatment was implemented after anthesis. Late sowing (shorter days) led to a decrease in total leaf number, dry mass and sugar yield even in PP-insensitive genotypes because of an increased phyllochron. Dry matter production and soluble sugar accumulation were strongly correlated with leaf number. Sugar concentration varied little among sowing dates or between anthesis and maturity. This indicates that sugar accumulation happened mainly before anthesis, thus largely escaping from competition with grain filling. This was confirmed by the low impact of panicle pruning on sugar concentration. Changes in sugar concentration from anthesis to maturity were negatively correlated with harvest index but not with grain yield. Physiological trade-offs among sugar, biomass and grain production under favourable rainfall are small in late-maturing and PP-sensitive sweet sorghums cultivated under sudano-sahelian conditions. The results differ from earlier reports that focussed on early maturing, PP-insensitive germplasm. Further research is needed on the interactions of these traits with agricultural practices and drought.

Model-assisted physiological analysis of Phyllo, a rice architectural mutant

Studies of phenotype of knockout mutants can provide new insights into physiological, phenological and architectural feedbacks in the plant system. Phyllo, a mutant of Nippon Bare rice (Oryza sativa L.) producing small leaves in rapid succession, was isolated during multiplication of a T-DNA insertion library. Phyllo phenotype was compared with the wild type (WT) during vegetative development in hydroponics culture using a wide range of physiological and biometric measurements. These were integrated with the help of the functional-structural model EcoMeristem, explicitly designed to study interactions between morphogenesis and carbon assimilation. Although the phenotype of the mutant was caused by a single recessive gene, it differed in many ways from the WT, suggesting a pleiotropic effect of this mutation. Phyllochron was 25 (1-4 leaf stage) to 38% (>>4 leaf stage) shorter but showed normal transition from juvenile to adult phase after leaf 4. Leaf size also increased steadily with leaf position as in WT. The mutant had reduced leaf blade lengthu2009:u2009width and bladeu2009:u2009sheath length ratios, particularly during the transition from heterotrophic to autotrophic growth. During the same period, rootu2009:u2009shoot dry weight ratio was significantly diminished. Specific leaf area (SLA) was strongly increased in the mutant but showed normal descending patterns with leaf position. Probably related to high SLA, the mutant had much lower light-saturated leaf photosynthetic rates and lower radiation use efficiency (RUE) than the WT. Leaf extension rates were strongly reduced in absolute terms but were high in relative terms (normalised by final leaf length). The application of the EcoMeristem model to these data indicated that the mutant was severely deficient in assimilate, resulting from low RUE and high organ initiation rate causing high assimilate demand. This was particularly pronounced during the heterotrophic-autotrophic transition, probably causing shorter leaf blades relative to sheaths, as well as a temporary reduction of assimilate partitioning to roots. The model accurately simulated the mutants high leaf mortality and absence of tillering. The simulated assimilate shortage was supported by observed reductions in starch storage in sheaths. Soluble sugar concentrations differed between mutant and WT in roots but not in shoots. Specifically, the hexoseu2009:u2009sucrose ratio was 50% lower in the roots of the mutant, possibly indicating low invertase activity. Furthermore, two OsCIN genes coding for cell wall invertases were not expressed in roots, and others were expressed weakly. This was interpreted as natural silencing via sugar signalling. In summary, the authors attributed the majority of observed allometric and metabolic modifications in the mutant to an extreme assimilate shortage caused by hastened shoot organogenesis and inefficient leaf morphology.