Glutaredoxin regulation of primary root growth is associated with early drought stress tolerance in pearl millet.

Seedling root traits impact plant establishment under challenging environments. Pearl millet is one of the most heat and drought tolerant cereal crops that provides a vital food source across the sub-Saharan Sahel region. Pearl millet's early root system features a single fast-growing primary root which we hypothesize is an adaptation to the Sahelian climate. Using crop modeling, we demonstrate that early drought stress is an important constraint in agrosystems in the Sahel where pearl millet was domesticated. Furthermore, we show that increased pearl millet primary root growth is correlated with increased early water stress tolerance in field conditions. Genetics including genome-wide association study and quantitative trait loci (QTL) approaches identify genomic regions controlling this key root trait. Combining gene expression data, re-sequencing and re-annotation of one of these genomic regions identified a glutaredoxin-encoding gene PgGRXC9 as the candidate stress resilience root growth regulator. Functional characterization of its closest Arabidopsis homolog AtROXY19 revealed a novel role for this glutaredoxin (GRX) gene clade in regulating cell elongation. In summary, our study suggests a conserved function for GRX genes in conferring root cell elongation and enhancing resilience of pearl millet to its Sahelian environment.

Pearl millet is a staple food for over 90 million people living in regions of Africa and India that typically experience high temperatures and little rainfall. It was domesticated about 4,500 years ago in the Sahel region of West Africa and is one of the most heat and drought tolerant cereal crops worldwide. In most plants, organs known as roots absorb water and essential nutrients from the soil. Young pearl millet plants develop a fast-growing primary root, but it is unclear how this unique feature helps the crop to grow in hot and dry conditions. Using weather data collected from the Sahel over a 20-year period, Fuente, Grondin et al. predicted by modelling that early drought stress is the major factor limiting pearl millet growth and yield in this region. Field experiments found that plants with primary roots that grow faster within soil were better at tolerating early drought than those with slower growing roots. Further work using genetic approaches revealed that a gene known as PgGRXC9 promotes the growth of the primary root. To better understand how this gene works, the team examined a very similar gene in a well-studied model plant known as Arabidopsis. This suggested that PgGRXC9 helps the primary root to grow by stimulating cell elongation within the root. Since it is well adapted to dry conditions, pearl millet is expected to play an important role in helping agriculture adjust to climate change. The findings of Fuente, Grondin et al. may be used by plant breeders to create more resilient and productive varieties of pearl millet.

Spatio-temporal analysis of strawberry architecture: insights into the control of branching and inflorescence complexity.

Plant architecture plays a major role in flowering and therefore in crop yield. Attempts to visualize and analyse strawberry plant architecture have been few to date. Here, we developed open-source software combining two- and three-dimensional representations of plant development over time along with statistical methods to explore the variability in spatio-temporal development of plant architecture in cultivated strawberry. We applied this software to six seasonal strawberry varieties whose plants were exhaustively described monthly at the node scale. Results showed that the architectural pattern of the strawberry plant is characterized by a decrease of the module complexity between the zeroth-order module (primary crown) and higher-order modules (lateral branch crowns and extension crowns). Furthermore, for each variety, we could identify traits with a central role in determining yield, such as date of appearance and number of branches. By modeling the spatial organization of axillary meristem fate on the zeroth-order module using a hidden hybrid Markov/semi-Markov mathematical model, we further identified three zones with different probabilities of production of branch crowns, dormant buds, or stolons. This open-source software will be of value to the scientific community and breeders in studying the influence of environmental and genetic cues on strawberry architecture and yield.

Identifying Developmental Patterns in Structured Plant Phenotyping Data.

Technological breakthroughs concerning both sensors and robotized plant phenotyping platforms have totally renewed the plant phenotyping paradigm in the last two decades. This has impacted both the nature and the throughput of data with the availability of data at high-throughput from the tissular to the whole plant scale. Sensor outputs often take the form of 2D or 3D images or time series of such images from which traits are extracted while organ shapes, shoot or root system architectures can be deduced. Despite this change of paradigm, many phenotyping studies often ignore the structure of the plant and therefore loose the information conveyed by the temporal and spatial patterns emerging from this structure. The developmental patterns of plants often take the form of succession of well-differentiated phases, stages or zones depending on the temporal, spatial or topological indexing of data. This entails the use of hierarchical statistical models for their identification.The objective here is to show potential approaches for analyzing structured plant phenotyping data using state-of-the-art methods combining probabilistic modeling, statistical inference and pattern recognition. This approach is illustrated using five different examples at various scales that combine temporal and topological index parameters, and development and growth variables obtained using prospective or retrospective measurements.

Modelling the bearing and branching behaviors of 1-year-old shoots in apricot genotypes.

In most temperate fruit trees, fruits are located on one-year old shoots. In Prunus species, flowers and fruits are born in axillary position along those shoots. The axillary bud fate and branching patterns are thus key components of the cultivar potential fruit production. The objective of this study was to analyze the branching and bearing behaviors of 1-year-old shoots of apricot cultivars and clones genetically closely related. Shoot structures were analyzed in terms of axillary bud fates using hidden semi-Markov chains and compared depending on the genotype, year and shoot length. The shoots were composed of three successive zones containing latent buds (basal zone), central flower buds (median zone) and vegetative buds (distal zone), respectively. The last two zones contained few associated flower buds. The zones length (in number of metamers) and occurrence strongly depended on shoot development in the two successive years. With decrease in the number of metamers per shoot, the last two zones become shorter or may not develop. While the number of metamers of the basal and distal zones and the number of associated flower buds correlated to the number of metamers of the shoot, the number of metamers of the median zone and the transition probability from the median to the distal zone were cultivar specific.

V-Mango: a functional-structural model of mango tree growth, development and fruit production.

BACKGROUND AND AIMS: Mango (Mangifera indica L.) is the fifth most widely produced fruit in the world. Its cultivation, mainly in tropical and sub-tropical regions, raises a number of issues such as the irregular fruit production across years, phenological asynchronisms that lead to long periods of pest and disease susceptibility, and the heterogeneity of fruit quality and maturity at harvest. To address these issues, we developed an integrative functional-structural plant model that synthesizes knowledge about the vegetative and reproductive development of the mango tree and opens up the possible simulation of cultivation practices. METHODS: We designed a model of architectural development in order to precisely characterize the intricate developmental processes of the mango tree. The appearance of botanical entities was decomposed into elementary stochastic events describing occurrence, intensity and timing of development. These events were determined by structural (position and fate of botanical entities) and temporal (appearance dates) factors. Daily growth and development of growth units and inflorescences were modelled using empirical distributions and thermal time. Fruit growth was determined using an ecophysiological model that simulated carbon- and water-related processes at the fruiting branch scale. KEY RESULTS: The model simulates the dynamics of the population of growth units, inflorescences and fruits at the tree scale during a growing cycle. Modelling the effects of structural and temporal factors makes it possible to simulate satisfactorily the complex interplays between vegetative and reproductive development. The model allowed the characterization of the susceptibility of mango tree to pests and the investigatation of the influence of tree architecture on fruit growth. CONCLUSIONS: This integrative functional-structural model simulates mango tree vegetative and reproductive development over successive growing cycles, allowing a precise characterization of tree phenology and fruit growth and production. The next step is to integrate the effects of cultivation practices, such as pruning, into the model.

Leaf Production and Expansion: A Generalized Response to Drought Stresses from Cells to Whole Leaf Biomass-A Case Study in the Tomato Compound Leaf.

It is clearly established that there is not a unique response to soil water deficit but that there are as many responses as soil water deficit characteristics: Drought intensity, drought duration, and drought position during plant cycle. For a same soil water deficit, responses can also differ on plant genotype within a same species. In spite of this variability, at least for leaf production and expansion processes, robust tendencies can be extracted from the literature when similar watering regimes are compared. Here, we present response curves and multi-scale dynamics analyses established on tomato plants exposed to different soil water deficit treatments. Results reinforce the trends already observed for other species: Reduction in plant leaf biomass under water stress was due to reduction in individual leaf biomass and areas whereas leaf production and specific leaf area were not affected. The dynamics of leaf expansion was modified both at the leaf and cell scales. Cell division and expansion were reduced by drought treatments as well as the endoreduplication process. Combining response curves analyses together with dynamic analyses of tomato compound leaf growth at different scales not only corroborate results on simple leaf responses to drought but also increases our knowledge on the cellular mechanisms behind leaf growth plasticity.

Identifying phenological phases in strawberry using multiple change-point models.

Plant development studies often generate data in the form of multivariate time series, each variable corresponding to a count of newly emerged organs for a given development process. These phenological data often exhibit highly structured patterns, and the aim of this study was to identify such patterns in cultivated strawberry. Six strawberry genotypes were observed weekly for their course of emergence of flowers, leaves, and stolons during 7 months. We assumed that these phenological series take the form of successive phases, synchronous between individuals. We applied univariate multiple change-point models for the identification of flowering, vegetative development, and runnering phases, and multivariate multiple change-point models for the identification of consensus phases for these three development processes. We showed that the flowering and the runnering processes are the main determinants of the phenological pattern. On this basis, we propose a typology of the six genotypes in the form of a hierarchical classification. This study introduces a new longitudinal data modeling approach for the identification of phenological phases in plant development. The focus was on development variables but the approach can be directly extended to growth variables and to multivariate series combining growth and development variables.

Lateral Roots: Random Diversity in Adversity.

Lateral roots are essential for soil foraging and uptake of minerals and water. They feature a large morphological diversity that results from divergent primordia or root growth and development patterns. Besides a structured diversity, resulting from the hierarchical and developmental organization of root systems, there exists a random diversity, occurring between roots of similar age, of the same hierarchical order, and exposed to uniform conditions. The physiological bases and functional consequences of this random diversity are largely ignored. Here we review the evidence for such random diversity throughout the plant kingdom, present innovative approaches based on statistical modeling to account for such diversity, and set the list of its potential benefits in front of a variable and unpredictable soil environment.

Long proleptic and sylleptic shoots in peach (Prunus persica L. Batsch) trees have similar, predetermined, maximum numbers of nodes and bud fate patterns.

BACKGROUND AND AIMS: In peach (Prunus persica) trees, three types of shoots can be distinguished depending on the time of their appearance: sylleptic, proleptic and epicormic. On proleptic shoots, an average of ten phytomers are preformed in dormant buds prior to shoot growth after bud-break, whereas all phytomers are considered neoformed in sylleptic and epicormic shoots. However, casual observations indicated that proleptic and sylleptic shoots appear quite similar in number of phytomers and structure in spite of their different origins. The goal of this research was to test the hypothesis that both proleptic and sylleptic shoots exhibit similar growth characteristics by analysing their node numbers and bud fate patterns. If their growth characteristics are similar, it would indicate that the structure of both types of shoots is primarily under genetic rather than environmental control. METHODS: The number of phytomers and bud fate patterns of proleptic and sylleptic shoots of four peach cultivars grown in the same location (Winters, California) were analysed and characterized using hidden semi-Markov models. Field data were collected during winter 2016, just prior to floral bud-break. KEY RESULTS: Sylleptic shoots tended to have slightly fewer phytomers than proleptic shoots of the same cultivars. The bud fate patterns along proleptic and sylleptic shoots were remarkably similar for all the cultivars, although proleptic shoots started growing earlier (at least 1 month) in the spring than sylleptic shoots. CONCLUSIONS: This study provides strong evidence for the semi-deterministic nature of both proleptic and sylleptic shoots across four peach cultivars in terms of number of phytomers and bud fate patterns along shoots. It is apparent that the overall structure of shoots with similar numbers of phytomers was under similar genetic control for the two shoot types. Understanding shoot structural characteristics can aid in phenotypic characterization of vegetative growth of trees and in providing a foundation for vegetative management of fruit trees in horticultural settings.

Are compound leaves more complex than simple ones? A multi-scale analysis.

Background and Aims: The question of which cellular mechanisms determine the variation in leaf size has been addressed mainly in plants with simple leaves. It is addressed here in tomato taking into consideration the expected complexity added by the several lateral appendages making up the compound leaf, the leaflets. Methods: Leaf and leaflet areas, epidermal cell number and areas, and endoreduplication (co-) variations were analysed in Solanum lycopersicum considering heteroblastic series in a wild type (Wva106) and an antisense mutant, the Pro35S:Slccs52AAS line, and upon drought treatments. All plants were grown in an automated phenotyping platform, PHENOPSIS, adapted to host plants grown in 7 L pots. Key Results: Leaf area, leaflet area and cell number increased with leaf rank until reaching a plateau. In contrast, cell area slightly decreased and endoreduplication did not follow any trend. In the transgenic line, leaf area, leaflet areas and cell number of basal leaves were lower than in the wild type, but higher in upper leaves. Reciprocally, cell area was higher in basal leaves and lower in upper leaves. When scaled up at the whole sympodial unit, all these traits did not differ significantly between the transgenic line and the wild type. In response to drought, leaf area was reduced, with a clear dose effect that was also reported for all size-related traits, including endoreduplication. Conclusions: These results provide evidence that all leaflets have the same cellular phenotypes as the leaf they belong to. Consistent with results reported for simple leaves, they show that cell number rather than cell size determines the final leaf areas and that endoreduplication can be uncoupled from leaf and cell sizes. Finally, they re-question a whole-plant control of cell division and expansion in leaves when the Wva106 and the Pro35S:Slccs52AAS lines are compared.

A New Phenotyping Pipeline Reveals Three Types of Lateral Roots and a Random Branching Pattern in Two Cereals.

Recent progress in root phenotyping has focused mainly on increasing throughput for genetic studies, while identifying root developmental patterns has been comparatively underexplored. We introduce a new phenotyping pipeline for producing high-quality spatiotemporal root system development data and identifying developmental patterns within these data. The SmartRoot image-analysis system and temporal and spatial statistical models were applied to two cereals, pearl millet (Pennisetum glaucum) and maize (Zea mays). Semi-Markov switching linear models were used to cluster lateral roots based on their growth rate profiles. These models revealed three types of lateral roots with similar characteristics in both species. The first type corresponds to fast and accelerating roots, the second to rapidly arrested roots, and the third to an intermediate type where roots cease elongation after a few days. These types of lateral roots were retrieved in different proportions in a maize mutant affected in auxin signaling, while the first most vigorous type was absent in maize plants exposed to severe shading. Moreover, the classification of growth rate profiles was mirrored by a ranking of anatomical traits in pearl millet. Potential dependencies in the succession of lateral root types along the primary root were then analyzed using variable-order Markov chains. The lateral root type was not influenced by the shootward neighbor root type or by the distance from this root. This random branching pattern of primary roots was remarkably conserved, despite the high variability of root systems in both species. Our phenotyping pipeline opens the door to exploring the genetic variability of lateral root developmental patterns.

Identifying Developmental Zones in Maize Lateral Root Cell Length Profiles using Multiple Change-Point Models.

The identification of the limits between the cell division, elongation and mature zones in the root apex is still a matter of controversy when methods based on cellular features, molecular markers or kinematics are compared while methods based on cell length profiles have been comparatively underexplored. Segmentation models were developed to identify developmental zones within a root apex on the basis of epidermal cell length profiles. Heteroscedastic piecewise linear models were estimated for maize lateral roots of various lengths of both wild type and two mutants affected in auxin signaling (rtcs and rum-1). The outputs of these individual root analyses combined with morphological features (first root hair position and root diameter) were then globally analyzed using principal component analysis. Three zones corresponding to the division zone, the elongation zone and the mature zone were identified in most lateral roots while division zone and sometimes elongation zone were missing in arrested roots. Our results are consistent with an auxin-dependent coordination between cell flux, cell elongation and cell differentiation. The proposed segmentation models could extend our knowledge of developmental regulations in longitudinally organized plant organs such as roots, monocot leaves or internodes.

Integrative models for joint analysis of shoot growth and branching patterns.

Plants exhibit dependences between shoot growth and branching that generate highly structured patterns. The characterization of the patterning mechanism is still an open issue because of the developmental processes involved with both succession of events (e.g. internode elongation, axillary shoot initiation and elongation) and complex dependences among neighbouring positions along the parent shoot. Statistical models called semi-Markov switching partitioned conditional generalized linear models were built on the basis of apple and pear tree datasets. In these models, the semi-Markov chain represents both the succession and lengths of branching zones, whereas the partitioned conditional generalized linear models represent the influence of parent shoot growth variables on axillary productions within each branching zone. Parent shoot growth variables were shown to influence specific developmental events. On this basis, the growth and branching patterns of two apple tree (Malus domestica) cultivars, as well as of pear trees (Pyrus spinosa) between two successive growing cycles, were compared. The proposed integrative statistical models were able to decipher the roles of successive developmental events in the growth and branching patterning mechanisms. These models could incorporate other parent shoot explanatory variables, such as the local curvature or the maximum growth rate of the leaf.

Identification of successive flowering phases highlights a new genetic control of the flowering pattern in strawberry.

The genetic control of the switch between seasonal and perpetual flowering has been deciphered in various perennial species. However, little is known about the genetic control of the dynamics of perpetual flowering, which changes abruptly at well-defined time instants during the growing season. Here, we characterize the perpetual flowering pattern and identify new genetic controls of this pattern in the cultivated strawberry. Twenty-one perpetual flowering strawberry genotypes were phenotyped at the macroscopic scale for their course of emergence of inflorescences and stolons during the growing season. A longitudinal analysis based on the segmentation of flowering rate profiles using multiple change-point models was conducted. The flowering pattern of perpetual flowering genotypes takes the form of three or four successive phases: an autumn-initiated flowering phase, a flowering pause, and a single stationary perpetual flowering phase or two perpetual flowering phases, the second one being more intense. The genetic control of flowering was analysed by quantitative trait locus mapping of flowering traits based on these flowering phases. We showed that the occurrence of a fourth phase of intense flowering is controlled by a newly identified locus, different from the locus FaPFRU, controlling the switch between seasonal and perpetual flowering behaviour. The role of this locus was validated by the analysis of data obtained previously during six consecutive years.

Characterization of Pearl Millet Root Architecture and Anatomy Reveals Three Types of Lateral Roots.

Pearl millet plays an important role for food security in arid regions of Africa and India. Nevertheless, it is considered an orphan crop as it lags far behind other cereals in terms of genetic improvement efforts. Breeding pearl millet varieties with improved root traits promises to deliver benefits in water and nutrient acquisition. Here, we characterize early pearl millet root system development using several different root phenotyping approaches that include rhizotrons and microCT. We report that early stage pearl millet root system development is characterized by a fast growing primary root that quickly colonizes deeper soil horizons. We also describe root anatomical studies that revealed three distinct types of lateral roots that form on both primary roots and crown roots. Finally, we detected significant variation for two root architectural traits, primary root lenght and lateral root density, in pearl millet inbred lines. This study provides the basis for subsequent genetic experiments to identify loci associated with interesting early root development traits in this important cereal.

Modelling the influence of dimerisation sequence dissimilarities on the auxin signalling network.

BACKGROUND: Auxin is a major phytohormone involved in many developmental processes by controlling gene expression through a network of transcriptional regulators. In Arabidopsis thaliana, the auxin signalling network is made of 52 potentially interacting transcriptional regulators, activating or repressing gene expression. All the possible interactions were tested in two-way yeast-2-hybrid experiments. Our objective was to characterise this auxin signalling network and to quantify the influence of the dimerisation sequence dissimilarities on the interaction between transcriptional regulators. RESULTS: We applied model-based graph clustering methods relying on connectivity profiles between transcriptional regulators. Incorporating dimerisation sequence dissimilarities as explanatory variables, we modelled their influence on the auxin network topology using mixture of linear models for random graphs. Our results provide evidence that the network can be simplified into four groups, three of them being closely related to biological groups. We found that these groups behave differently, depending on their dimerisation sequence dissimilarities, and that the two dimerisation sub-domains might play different roles. CONCLUSIONS: We propose here the first pipeline of statistical methods combining yeast-2-hybrid data and protein sequence dissimilarities for analysing protein-protein interactions. We unveil using this pipeline of analysis the transcriptional regulator interaction modes.

Identifying developmental phases in the Arabidopsis thaliana rosette using integrative segmentation models.

The change in leaf size and shape during ontogeny associated with heteroblastic development is a composite trait for which extensive spatiotemporal data can be acquired using phenotyping platforms. However, only part of the information contained in such data is exploited, and developmental phases are usually defined using a selected organ trait. We here introduce new methods for identifying developmental phases in the Arabidopsis rosette using various traits and minimum a priori assumptions. A pipeline of analysis was developed combining image analysis and statistical models to integrate morphological, shape, dimensional and expansion dynamics traits for the successive leaves of the Arabidopsis rosette. Dedicated segmentation models called semi-Markov switching models were built for selected genotypes in order to identify rosette developmental phases. Four successive developmental phases referred to as seedling, juvenile, transition and adult were identified for the different genotypes. We show that the degree of covering of the leaf abaxial surface with trichomes is insufficient to define these developmental phases. Using our pipeline of analysis, we were able to identify the supplementary seedling phase and to uncover the structuring role of various leaf traits. This enabled us to compare on a more objective basis the vegetative development of Arabidopsis mutants.

Differentiated Responses of Apple Tree Floral Phenology to Global Warming in Contrasting Climatic Regions.

The responses of flowering phenology to temperature increases in temperate fruit trees have rarely been investigated in contrasting climatic regions. This is an appropriate framework for highlighting varying responses to diverse warming contexts, which would potentially combine chill accumulation (CA) declines and heat accumulation (HA) increases. To examine this issue, a data set was constituted in apple tree from flowering dates collected for two phenological stages of three cultivars in seven climate-contrasting temperate regions of Western Europe and in three mild regions, one in Northern Morocco and two in Southern Brazil. Multiple change-point models were applied to flowering date series, as well as to corresponding series of mean temperature during two successive periods, respectively determining for the fulfillment of chill and heat requirements. A new overview in space and time of flowering date changes was provided in apple tree highlighting not only flowering date advances as in previous studies but also stationary flowering date series. At global scale, differentiated flowering time patterns result from varying interactions between contrasting thermal determinisms of flowering dates and contrasting warming contexts. This may explain flowering date advances in most of European regions and in Morocco vs. stationary flowering date series in the Brazilian regions. A notable exception in Europe was found in the French Mediterranean region where the flowering date series was stationary. While the flowering duration series were stationary whatever the region, the flowering durations were far longer in mild regions compared to temperate regions. Our findings suggest a new warming vulnerability in temperate Mediterranean regions, which could shift toward responding more to chill decline and consequently experience late and extended flowering under future warming scenarios.

How different pruning severities alter shoot structure: a modelling approach in young 'Nonpareil' almond trees.

Axillary meristem fate patterns along shoots, also referred to as shoot structure, appear to be fairly consistent among trees within a genotype growing under similar conditions. Less is known about shoot structural plasticity following external manipulations, such as pruning. The aim of this study on almond (Prunus dulcis (Mill.)) shoots was to investigate how pruning severity affects the structure of 1-year-old shoots that grew after pruning (regrowth shoots), the 2-year-old portion of shoots that remained from the previous year's growth after pruning (pruned shoots), and whether regrowth shoots reiterate the structure of the original 1-year-old shoots before pruning. Three pruning severities were imposed and the structures along the different shoots were assessed by building hidden semi-Markov models of axillary meristem fates. The structures of regrowth and pruned shoots depended on pruning severity, but maintained some of the original shoot characteristics. Regrowth shoots developed more complex structures with severe pruning, but had simpler structures than original shoots indicating progressive simplification with tree age. Pruned shoot structures were affected by the severity of pruning, by the structure when the shoots were 1 year old, and probably by local competition among buds. Changes in structure due to pruning can be modelled and be predictable.

Analysing growth and development of plants jointly using developmental growth stages.

BACKGROUND AND AIMS: Plant growth, the increase of organ dimensions over time, and development, the change in plant structure, are often studied as two separate processes. However, there is structural and functional evidence that these two processes are strongly related. The aim of this study was to investigate the co-ordination between growth and development using mango trees, which have well-defined developmental stages. METHODS: Developmental stages, determined in an expert way, and organ sizes, determined from objective measurements, were collected during the vegetative growth and flowering phases of two cultivars of mango, Mangifera indica. For a given cultivar and growth unit type (either vegetative or flowering), a multistage model based on absolute growth rate sequences deduced from the measurements was first built, and then growth stages deduced from the model were compared with developmental stages. KEY RESULTS: Strong matches were obtained between growth stages and developmental stages, leading to a consistent definition of integrative developmental growth stages. The growth stages highlighted growth asynchronisms between two topologically connected organs, namely the vegetative axis and its leaves. CONCLUSIONS: Integrative developmental growth stages emphasize that developmental stages are closely related to organ growth rates. The results are discussed in terms of the possible physiological processes underlying these stages, including plant hydraulics, biomechanics and carbohydrate partitioning.