Research on agroforestry systems and biodiversity conservation: what can we conclude so far and what should we improve?

Through a meta-analysis, Mupepele et al. (BMC Ecol Evol 21:1-193, 2021) assessed the effects of European agroforestry systems on biodiversity, estimated by species richness or species diversity. They showed that the effects of silvoarable and silvopastoral systems depend on the systems they are compared to and the taxa studied. Further, they found that only silvoarable systems increased species richness or diversity, compared to cropland. The authors conclude that agroforestry systems have weak effects on biodiversity and that landscape context or land-use history are probably more important than the practice of agroforestry in itself. However, we draw attention to important shortcomings in this meta-analysis, which downplay the potential of agroforestry for biodiversity conservation in agricultural landscapes. We hope that the meta-analysis by Mupepele et al. (BMC Ecol Evol 21:1-193, 2021), and our comments, will contribute to improving the quality of research on agroforestry systems and biodiversity conservation.

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.

Hormones and carbohydrates are both involved in the negative effects of reproduction on vegetative bud outgrowth in the mango tree: consequences for irregular bearing.

The negative effects of fruit production during one cycle on reproduction during the following cycle are generally explained by two complementary processes: hormone synthesis and carbohydrate mobilization. Our study focused on mango (Mangifera indica L.) for which it has been shown that reproduction decreases and delays vegetative bud outgrowth. This, in turn, affects flowering and fruiting in the following cycle. Vegetative growth therefore plays a pivotal role in irregular fruit production patterns across consecutive years. Our aim was to decipher the respective roles of hormones and carbohydrates on the negative effects of reproduction on vegetative growth. We analyzed the changes in various hormone (auxin, cytokinin, abscisic acid) and carbohydrate (glucose, sucrose, starch) concentrations in terminal axes with vegetative and reproductive fates of two mango cultivars, Cogshall and José, characterized by different bearing patterns, across consecutive phenological periods during a growing cycle. Auxin concentrations were high in inflorescences, fruit peduncles and axes bearing inflorescences or fruit, suggesting auxin-induced inhibition of vegetative bud outgrowth in the flowering and fruiting axes. Moreover, growing fruits, which are strong sink organs, depleted carbohydrates from non-fruiting axes. During vegetative growth, this starch depletion probably contributed to decreasing the probability of and to delaying vegetative bud outgrowth of reproductive axes for Cogshall, and of reproductive and nonreproductive axes for José. Starch dynamics in quiescent and flowering growth units during early fruit growth and their starch concentrations at fruit maturity differed between the two cultivars, presumably in relation to the observed contrasted crop loads and/or to differences in photosynthetic capacity or carbohydrate allocation. These differences between the two cultivars in terms of starch concentration in terminal axes during vegetative growth could partly explain their different bearing patterns.

Apple tree adaptation to shade in agroforestry: an architectural approach.

PREMISE: The expression of shade adaptation traits is expected to be stronger in low light and can be detrimental to flowering and yield. Our study focused on the expression of shade adaptation traits of apple trees (Malus domestica Borkh. 'Dalinette') in an agroforestry system. METHODS: The architecture of 45 apple trees in their third and fourth year was extensively described and analyzed at the tree scale and compared depending on the light quantity received during the growing season. Flower cluster phenology and the relation between leaf area and floral initiation were also investigated. RESULTS: The number of growing shoots and the leaf area were reduced by shade even if specific leaf area increased with increasing shade. Shade did not modify primary growth but did decrease secondary growth, so that apple tree shoots in shade were slender, with a lower taper and reduced number and proportion of flower clusters. The correlation between floral initiation and leaf area was high both in full and moderate light but not for apple trees in low light. Shade did not impact the date of bud burst and the early phenological stages of flower clusters, but it reduced the number of days at full bloom. CONCLUSIONS: Our results suggest that while the architecture of apple trees is modified by a reduction in light intensity, it is not until a reduction of 65% that the capability to produce fruit is impeded. These results could help optimize the design of apple-tree-based agroforestry systems.

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.

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.

Deciphering the Costs of Reproduction in Mango - Vegetative Growth Matters.

Irregular fruit production across successive years is a major issue that limits the profitability of most temperate and tropical fruit crops. It is particularly affected by the reciprocal relationships between vegetative and reproductive growth. The concept of the costs of reproduction is defined in terms of losses in the potential future reproductive success caused by current investment in reproduction. This concept, developed in ecology and evolutionary biology, could provide a methodological framework to analyze irregular bearing in fruit crops, especially in relation to the spatial scale at which studies are done. The objective of this study was to investigate the direct effects of reproduction during a growing cycle on reproduction during the following growing cycle and the indirect effects through vegetative growth between these two reproductive events, for four mango cultivars and during two growing cycles. Two spatial scales were considered: the growth unit (GU) and the scaffold branch. Costs of reproduction were detected between two successive reproductive events and between reproduction and vegetative growth. These costs were scale-dependent, generally detected at the GU scale and infrequently at the scaffold branch scale, suggesting partial branch autonomy with respect to processes underlying the effects of reproduction on vegetative growth. In contrast, the relationships between vegetative growth and reproduction were positive at the GU scale and at the scaffold branch scale in most cases, suggesting branch autonomy for the processes, mainly local, underlying flowering and fruiting. The negative effect of reproduction on vegetative growth prevailed over the positive effect of vegetative growth on the subsequent reproduction. The costs of reproduction were also cultivar-dependent. Those revealed at the GU scale were related to the bearing behavior of each cultivar. Our results put forward the crucial role of vegetative growth occurring between two reproductive events. They are discussed in the context of irregular bearing considering both the spatial scale and the various bearing habits of the mango cultivars, in order to formulate new hypotheses about this issue.

Simulation of carbon allocation and organ growth variability in apple tree by connecting architectural and source-sink models.

BACKGROUND AND AIMS: Plant growth depends on carbon availability and allocation among organs. QualiTree has been designed to simulate carbon allocation and partitioning in the peach tree (Prunus persica), whereas MappleT is dedicated to the simulation of apple tree (Malus × domestica) architecture. The objective of this study was to couple both models and adapt QualiTree to apple trees to simulate organ growth traits and their within-tree variability. METHODS: MappleT was used to generate architectures corresponding to the 'Fuji' cultivar, accounting for the variability within and among individuals. These architectures were input into QualiTree to simulate shoot and fruit growth during a growth cycle. We modified QualiTree to account for the observed shoot polymorphism in apple trees, i.e. different classes (long, medium and short) that were characterized by different growth function parameters. Model outputs were compared with observed 3D tree geometries, considering shoot and final fruit size and growth dynamics. KEY RESULTS: The modelling approach connecting MappleT and QualiTree was appropriate to the simulation of growth and architectural characteristics at the tree scale (plant leaf area, shoot number and types, fruit weight at harvest). At the shoot scale, mean fruit weight and its variability within trees was accurately simulated, whereas the model tended to overestimate individual shoot leaf area and underestimate its variability for each shoot type. Varying the parameter related to the intensity of carbon exchange between shoots revealed that behaviour intermediate between shoot autonomy and a common assimilate pool was required to properly simulate within-tree fruit growth variability. Moreover, the model correctly dealt with the crop load effect on organ growth. CONCLUSIONS: This study provides understanding of the integration of shoot ontogenetic properties, carbon supply and transport between entities for simulating organ growth in trees. Further improvements regarding the integration of retroaction loops between carbon allocation and the resulting plant architecture are expected to allow multi-year simulations.

Genetic Variation of Morphological Traits and Transpiration in an Apple Core Collection under Well-Watered Conditions: Towards the Identification of Morphotypes with High Water Use Efficiency.

Water use efficiency (WUE) is a quantitative measurement which improvement is a major issue in the context of global warming and restrictions in water availability for agriculture. In this study, we aimed at studying the variation and genetic control of WUE and the respective role of its components (plant biomass and transpiration) in a perennial fruit crop. We explored an INRA apple core collection grown in a phenotyping platform to screen one-year-old scions for their accumulated biomass, transpiration and WUE under optimal growing conditions. Plant biomass was decompose into morphological components related to either growth or organ expansion. For each trait, nine mixed models were evaluated to account for the genetic effect and spatial heterogeneity inside the platform. The Best Linear Unbiased Predictors of genetic values were estimated after model selection. Mean broad-sense heritabilities were calculated from variance estimates. Heritability values indicated that biomass (0.76) and WUE (0.73) were under genetic control. This genetic control was lower in plant transpiration with an heritability of 0.54. Across the collection, biomass accounted for 70% of the WUE variability. A Hierarchical Ascendant Classification of the core collection indicated the existence of six groups of genotypes with contrasting morphology and WUE. Differences between morphotypes were interpreted as resulting from differences in the main processes responsible for plant growth: cell division leading to the generation of new organs and cell elongation leading to organ dimension. Although further studies will be necessary on mature trees with more complex architecture and multiple sinks such as fruits, this study is a first step for improving apple plant material for the use of water.

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.

Bud structure, position and fate generate various branching patterns along shoots of closely related Rosaceae species: a review.

Branching in temperate plants is closely linked to bud fates, either floral or vegetative. Here, we review how the fate of meristematic tissues contained in buds and their position along a shoot imprint specific branching patterns which differ among species. Through examples chosen in closely related species in different genera of the Rosaceae family, a panorama of patterns is apparent. Patterns depend on whether vegetative and floral buds are borne individually or together in mixed buds, develop as the shoot grows or after a rest period, and are located in axillary or terminal positions along the parent shoot. The resulting branching patterns are conserved among varieties in a given species but progressively change with the parent shoot length during plant ontogeny. They can also be modulated by agronomic and environmental conditions. The existence of various organizations in the topology and fate of meristematic tissues and their appendages in closely related species questions the between-species conservation of physiological and molecular mechanisms leading to bud outgrowth vs. quiescence and to floral induction vs. vegetative development.

Exploring bud dormancy completion with a combined architectural and phenological analysis: the case of apple trees in contrasting winter temperature conditions.

PREMISE OF THE STUDY: The branching pattern and phenology of trees result from interactions between the tree's genetic constitution and environmental conditions. Temperature strongly affects the duration of bud dormancy and further shoot growth. Our hypothesis was that shoot architecture is strongly affected by winter temperatures determining both the position and budburst of vegetative laterals with a lower effect on their outgrowth. METHODS: The study was conducted on four apple cultivars characterized by various chilling requirements and grown in two contrasting winter temperature conditions. A two-step approach was designed to quantify at the shoot scale first the branching pattern and second two phenological stages of vegetative laterals, budburst and outgrowth. A categorical variable, the branching zone, was built to summarize the lateral position along the shoot. It was integrated into the phenological analysis as a factor together with the cultivar and the winter temperature. KEY RESULTS: Temperature had a main effect on the distribution of vegetative laterals along the shoot. It also strongly affected budburst, which was also affected by the cultivar and the branching zone. The outgrowth of the lateral was not significantly affected by temperature but was significantly affected by the cultivar and the branching zone. Furthermore, the delayed senescence and subsequent leaf persistence during winter, characterizing the apple tree in the mild winter temperature condition, had only a weak effect on the distribution of vegetative laterals and on budburst and lateral outgrowth. CONCLUSIONS: The actual shoot architecture and budburst result from an ordered sequence of events with a pivotal role of winter temperatures on the dormancy completion of individual lateral buds. Endogenous factors related to the cultivar branching pattern overtake the temperature effect on the lateral outgrowth.

Deciphering structural and temporal interplays during the architectural development of mango trees.

Plant architecture is commonly defined by the adjacency of organs within the structure and their properties. Few studies consider the effect of endogenous temporal factors, namely phenological factors, on the establishment of plant architecture. This study hypothesized that, in addition to the effect of environmental factors, the observed plant architecture results from both endogenous structural and temporal components, and their interplays. Mango tree, which is characterized by strong phenological asynchronisms within and between trees and by repeated vegetative and reproductive flushes during a growing cycle, was chosen as a plant model. During two consecutive growing cycles, this study described vegetative and reproductive development of 20 trees submitted to the same environmental conditions. Four mango cultivars were considered to assess possible cultivar-specific patterns. Integrative vegetative and reproductive development models incorporating generalized linear models as components were built. These models described the occurrence, intensity, and timing of vegetative and reproductive development at the growth unit scale. This study showed significant interplays between structural and temporal components of plant architectural development at two temporal scales. Within a growing cycle, earliness of bud burst was highly and positively related to earliness of vegetative development and flowering. Between growing cycles, flowering growth units delayed vegetative development compared to growth units that did not flower. These interplays explained how vegetative and reproductive phenological asynchronisms within and between trees were generated and maintained. It is suggested that causation networks involving structural and temporal components may give rise to contrasted tree architectures.

Assessing allometric models to predict vegetative growth of mango (Mangifera indica; Anacardiaceae) at the current-year branch scale.

PREMISE OF THE STUDY: Accurate and reliable predictive models are necessary to estimate nondestructively key variables for plant growth studies such as leaf area and leaf, stem, and total biomass. Predictive models are lacking at the current-year branch scale despite the importance of this scale in plant science. METHODS: We calibrated allometric models to estimate leaf area and stem and branch (leaves + stem) mass of current-year branches, i.e., branches several months old studied at the end of the vegetative growth season, of four mango cultivars on the basis of their basal cross-sectional area. The effects of year, site, and cultivar were tested. Models were validated with independent data and prediction accuracy was evaluated with the appropriate statistics. KEY RESULTS: Models revealed a positive allometry between dependent and independent variables, whose y-intercept but not the slope, was affected by the cultivar. The effects of year and site were negligible. For each branch characteristic, cultivar-specific models were more accurate than common models built with pooled data from the four cultivars. Prediction quality was satisfactory but with data dispersion around the models, particularly for large values. CONCLUSIONS: Leaf area and stem and branch mass of mango current-year branches could be satisfactorily estimated on the basis of branch basal cross-sectional area with cultivar-specific allometric models. The results suggested that, in addition to the heteroscedastic behavior of the variables studied, model accuracy was probably related to the functional plasticity of branches in relation to the light environment and/or to the number of growth units composing the branches.

How young trees cope with removal of whole or parts of shoots: an analysis of local and distant responses to pruning in 1-year-old apple (Malus xdomestica; Rosaceae) trees.

PREMISE OF STUDY: Manipulation of tree architecture by pruning provides an experimental context to analyze architectural plasticity resulting from competition between developing organs. The objective of this study was to quantify the effects of the removal of all or part of shoots through pruning on the redistribution of growth and flowering at spatial and temporal levels. METHODS: Two types of pruning cuts were applied: (1) heading cuts of either the main stem or laterals and (2) thinning cuts (i.e., complete removal) of laterals. These two types of cuts were applied in summer and winter on 1-yr-old cultivars of Fuji and Braeburn apple trees. Tree topology and geometry were described over 3 years, and responses were analyzed for both local and distant scales. RESULTS: Heading cuts induced quasi-deterministic local responses on pruned axes, whereas responses to thinning cuts were more variable. For the main stem and laterals, responses over greater spatial and temporal scales were highlighted with (1) stronger growth the year after summer pruning and (2) modification of branching and flowering along the unpruned parts after winter pruning. CONCLUSIONS: Pruning typically induced growth redistribution toward traumatic reiterations and enhanced growth of the remaining unpruned axes with a concomitant decrease of flowering and cambial growth. Although results could be interpreted in relation to the root-shoot balance, tree responses appeared highly cultivar-specific.

Genetic determinism of anatomical and hydraulic traits within an apple progeny.

The apple tree is known to have an isohydric behaviour, maintaining rather constant leaf water potential in soil with low water status and/or under high evaporative demand. However, little is known on the xylem water transport from roots to leaves from the two perspectives of efficiency and safety, and on its genetic variability. We analysed 16 traits related to hydraulic efficiency and safety, and anatomical traits in apple stems, and the relationships between them. Most variables were found heritable, and we investigated the determinism underlying their genetic control through a quantitative trait loci (QTL) analysis on 90 genotypes from the same progeny. Principal component analysis (PCA) revealed that all traits related to efficiency, whether hydraulic conductivity, vessel number and area or wood area, were included in the first PC, whereas the second PC included the safety variables, thus confirming the absence of trade-off between these two sets of traits. Our results demonstrated that clustered variables were characterized by common genomic regions. Together with previous results on the same progeny, our study substantiated that hydraulic efficiency traits co-localized with traits identified for tree growth and fruit production.

Is axis position within tree architecture a determinant of axis morphology, branching, flowering and fruiting? An essay in mango.

BACKGROUND AND AIMS: Growth and reproductive strategies of plants are often related to particular, although usually poorly characterized, spatial distributions of shoots within the plant's architecture. In this study it is therefore hypothesized that a close relationship exists between architectural position, axis morphology (length, diameter, leaf area), and functional behaviour (branching, flowering and fruiting). The study focused on the architectural position of mango growth units, defined here as being the relative position, apical or lateral, on the parent growth unit, i.e. growing from the apical or a lateral meristem, respectively. METHODS: Stem length and leaf characteristics (area, dry weight) were measured on apical and lateral growth units of four mango cultivars over two years. Branching, flowering and fruiting were assessed for both growth unit types using an exhaustive description of tree vegetative and reproductive growth over two years. The relationships between growth unit diameter and flowering and fruiting were assessed for one of the four cultivars. KEY RESULTS: A pronounced morphological dimorphism was observed for the four cultivars. Across cultivars, stem length was significantly 1.31-1.34 times longer and total leaf area was 2.54-3.47 times larger in apical compared to lateral growth units. Apical growth units tended to branch, flower and fruit more than lateral growth units. The relationship between growth unit diameter and flowering rate was quadratic and dependent on growth unit position. The relationship between growth unit diameter and fruiting rate was linear and independent of growth unit position. CONCLUSIONS: Morphological traits of mango growth units were clearly involved in the determinism of flowering and fruiting, although in different ways. The results, however, showed that current hypotheses of flowering, such as carbohydrate availability and florigenic promoters, are not sufficient in themselves if they neglect the hierarchical relationships between axes, i.e. their relative position, apical or lateral.