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bioRxiv2018

A Comprehensive Tool Set for Inducible, Cell Type-Specific Gene Expression in Arabidopsis

Understanding the context-specific role of gene function is a key objective of modern biology. To this end, we generated a resource for inducible cell-type specific trans-activation based on the well-established combination of the chimeric GR-LhG4 transcription factor and the synthetic pOp promoter. Harnessing the flexibility of the GreenGate cloning system, we produced a comprehensive set of GR-LhG4 driver lines targeting most tissues in the Arabidopsis shoot and root with a strong focus on the indeterminate meristems. We show that, when combined with effectors under control of the pOp promoter, tight temporal and spatial control of gene expression is achieved. In particular, inducible expression in F1 plants obtained from crosses of driver and effector lines allows rapid assessment of the cell type-specific impact of an effector with high temporal resolution. Thus, our comprehensive and flexible toolbox is suited to overcome the limitations of ubiquitous genetic approaches, the outputs of which are often difficult to interpret due to widespread existence of compensatory mechanisms and the integration of diverging effects in different cell types.\n\nOne sentence summary: A set of lines enabling spatio-temporal control of gene expression in Arabidopsis.

plant biology↗

bioRxiv2017

Effects Of Small-Scale Clustering Of Flowers On Pollinator Foraging Behaviour And Flower Visitation Rate

Plants often grow in clusters of various sizes and have a variable number of flowers per inflorescence. This small-scale spatial clustering affects insect foraging strategies and plant reproductive success. In our study, we aimed to determine how visitation rate and foraging behaviour of pollinators depend on the number of flowers per plant and on the size of clusters of multiple plants using Dracocephalum moldavica (Lamiaceae) as a target species. We measured flower visitation rate by observations of insects visiting single plants and clusters of plants with different numbers of flowers. Detailed data on foraging behaviour within clusters of different sizes were gathered for honeybees, Apis mellifera, the most abundant visitor of Dracocephalum in the experiments. We found that the total number of flower visitors increased with the increasing number of flowers on individual plants and in larger clusters, but less then proportionally. Although individual honeybees visited more flowers in larger clusters, they visited a smaller proportion of flowers, as has been previously observed. Consequently, visitation rate per flower and unit time peaked in clusters with an intermediate number of flowers. These patterns do not conform to expectations based on optimal foraging theory and the ideal free distribution model. We attribute this discrepancy to incomplete information about the distribution of resources. Detailed observations and video recordings of individual honeybees also showed that the number of flowers had no effect on handling time of flowers by honeybees. We evaluated the implications of these patterns for insect foraging biology and plant reproduction.

ecology↗

bioRxiv2017

Regulation of intercellular TARGET OF MONOPTEROS 7 protein transport in the Arabidopsis root

Intercellular communication coordinates hypophysis establishment in the Arabidopsis embryo. Previously, TARGET OF MONOPTEROS 7 (TMO7) was reported to be transported to the hypophysis, the founder cell of the root cap, and RNA suppression experiment implicated its function in embryonic root development. However, it remained unclear what protein properties and mechanisms mediate TMO7 protein transport, and what role the movement plays in development. Here, we report that in the post-embryonic root, TMO7 and its close relatives are transported into the root cap through plasmodesmata in a sequence, but not size dependent manner. We also show that nuclear residence is critical for TMO7 transport, and postulate that modification, potentially phosphorylation, labels TMO7 for transport. Additionally, three novel CRISPR/Cas9-induced tmo7 alleles confirmed a role in hypophysis division, but suggest complex redundancies with close relatives in root formation. Finally, we demonstrate that TMO7 transport is biologically meaningful, as local expression partially restores hypophysis division in a plasmodesmatal protein transport mutant. Our study identifies motifs and amino acids critical for TMO7 protein transport and establishes the importance of TMO7 in hypophysis and root development.\n\nSummary StatementUnique protein motifs, subcellular localization and post-translational modification, rather than protein size regulate plasmodesmatal transport of TMO7 family proteins during Arabidopsis root development.

plant biology↗

bioRxiv2015

RUST FUNGAL EFFECTORS MIMIC HOST TRANSIT PEPTIDES TO TRANSLOCATE INTO CHLOROPLASTS

Parasite effector proteins target various host cell compartments to alter host processes and promote infection. How effectors cross membrane-rich interfaces to reach these compartments is a major question in effector biology. Growing evidence suggests that effectors use molecular mimicry to subvert host cell machinery for protein sorting. We recently identified CTP1 (chloroplast-targeted protein 1), a candidate effector from the poplar leaf rust fungus Melampsora larici-populina that carries a predicted transit peptide and accumulates in chloroplasts. Here, we show that the CTP1 transit peptide is necessary and sufficient for accumulation in the stroma of chloroplasts, and is cleaved after translocation. CTP1 is part of a Melampsora-specific family of polymorphic secreted proteins whose members translocate and are processed in chloroplasts in a N-terminal signal-dependent manner. Our findings reveal that fungi have evolved effector proteins that mimic plant-specific sorting signals to traffic within plant cells.

Plant Biology↗

bioRxiv2018

A systems biology approach to explore the impact of maple tree dormancy release on sap variation and maple syrup quality

Maple sap is a complex nutrient matrix collected during Spring to produce maple syrup. The characteristics of sap change over the production period and its composition directly impacts syrup quality. This variability could in part be attributed to changes in tree metabolism following dormancy release, but little is known about these changes in deciduous trees. Therefore, understanding the variation in sap composition associated with dormancy release could help pinpoint the causes of some defects in maple syrup. In particular, a defect known as \"buddy\", is an increasing concern for the industry. This off-flavor appears around the time of bud burst, hence its name. To investigate sap variation related to bud burst and the buddy defect, we monitored sap variation with respect to a dormancy release index (Sbb) and syrup quality. First, we looked at variation in amino acid content during this period. We observed a shift in amino acid relative proportions associated with dormancy release and found that most of them increase rapidly near the point of bud burst, correlating with changes in syrup quality. Second, we identified biological processes that respond to variation in maple sap by performing a competition assay using the barcoded Saccharomyces cerevisiae prototroph deletion collection. This untargeted approach revealed that the organic sulfur content may be responsible for the development of the buddy off-flavor, and that dormancy release is necessary for the appearance of the defect, but other factors such as microbial activity may also be contributing.

plant biology↗

bioRxiv2018

A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses

SUMMARYO_LISome Aeschynomene legume species have the property of being nodulated by photosynthetic Bradyrhizobium lacking the nodABC genes. Knowledge of this unique Nod (factor)-independent symbiosis has been gained from the model A. evenia but our understanding remains limited due to the lack of comparative genetics with related taxa using a Nod-dependent process.\nC_LIO_LITo fill this gap, this study significantly broadened previous taxon sampling, including in allied genera, to construct a comprehensive phylogeny. This backbone tree was matched with data on chromosome number, genome size, low-copy nuclear genes and strengthened by nodulation tests and a comparison of the diploid species.\nC_LIO_LIThe phylogeny delineated five main lineages that all contained diploid species while polyploid groups were clustered in a polytomy and were found to originate from a single paleo-allopolyploid event. In addition, new nodulation behaviours were revealed and Nod-dependent diploid species were shown to be tractable.\nC_LIO_LIThe extended knowledge of the genetics and biology of the different lineages in the legume genus Aeschynomene provides a solid research framework. Notably, it enabled the identification of A. americana and A. patula as the most suitable species to undertake a comparative genetic study of the Nod-independent and Nod-dependent symbioses.\nC_LI

plant biology↗

bioRxiv2016

Modelling tree growth taking into account carbon source and sink limitations

Increasing CO2 concentrations are strongly controlled by the behaviour of undisturbed forests, which are believed to be a major current sink of atmospheric CO2. There are many models which predict forest responses to environmental changes but they are almost exclusively carbon source (i.e. photosynthesis) driven. Here we present a model for an individual tree that takes into account also the intrinsic limits of meristems and cellular growth rates, as well as control mechanisms within the tree that influence its diameter and height growth over time. This new framework is built on process-based understanding combined with differential equations solved by the Runge-Kutta-Fehlberg (RKF45) numerical method. It was successfully tested for stands of beech trees in two different sites representing part of a long-term forest yield experiment in Germany. This model provides new insights into tree growth and limits to tree height, and addresses limitations of previous models with respect to sink-limited growth.\n\nAuthor SummaryGreenhouse gas emissions, in particular of CO2, have emerged as one of the most important global concerns, and it is therefore important to understand the behaviour of forests as they absorb and store a very large quantity of carbon. Most models treat forests as boxes with growth only driven by photosynthesis, while their actual growth depends also on many other important processes such as the maximal rate at which individual cells can grow, the influences of temperature and soil moisture on these cells, and the control that the tree has on itself through endogenous signalling pathways. Therefore, and with inspiration from process-based understanding of the biological functioning of trees, we have developed a model which takes into account these different factors. We first use this knowledge and additional basic assumptions to derive a system of several equations which, when solved, enable us to predict the height and the radius of an individual tree at a given time, provided that we have enough information about its initial state and its surroundings. We use the Runge-Kutta-Fehlberg mathematical method to obtain a numerical solution and thus predict the development of the height and radius of an individual tree over time under specified conditions.

Plant Biology↗

bioRxiv2017

Widespread Negative Frequency-Dependent Selection Maintains Diversity in the Legume-Rhizobia Symbiosis: Balancing nodulation may explain the paradox of rhizobium diversity

The evolutionary origin and ecological maintenance of biodiversity is a central problem in biology. For diversity to be stable through time, each genotype or species must have an advantage when rare. This negative frequency-dependence prevents deterministic extinction and mitigates the stochastic loss of diversity (1-4). However, models of mutualism typically generate positive frequency-dependence that reduces diversity (5-8). Here, we report empirical evidence for negative frequency-dependence in the legume-rhizobium mutualism within a single host generation, a phenomenon that we term balancing nodulation. Balancing nodulation increases rare rhizobia across all 13 legume genera investigated to date, at high and low inoculum densities, and with minimal genetic differentiation between rhizobia strains. While the mechanism generating this phenomenon is currently unknown, balancing nodulation could actively maintain variation in the rhizobia-legume symbiosis.

plant biology↗

bioRxiv2017

The genetic architecture of recurrent segregation distortion in Arabidopsis thaliana

The equal probability of transmission of alleles from either parent during sexual reproduction is a central tenet of genetics and evolutionary biology. Yet, there are many cases where this rule is violated. Such violations limit intraspecific gene flow and can facilitate the formation of genetic barriers, a first step in speciation. Biased transmission of alleles, or segregation distortion, can result from a number of biological processes including epistatic interactions between incompatible loci, gametic selection, and meiotic drive. Examples of these phenomena have been identified in many species, implying that they are universal, but comprehensive species-wide studies of segregation distortion are lacking. We have performed a species-wide screen for distorted allele frequencies in over 500 segregating populations of Arabidopsis thaliana using reduced-representation genome sequencing. Biased transmission of alleles was evident in up to a quarter of surveyed populations. Most populations exhibited distortion at only one genomic region, with some regions being repeatedly affected in multiple populations. Our results begin to elucidate the species-level architecture of biased transmission of genetic material in A. thaliana, and serve as a springboard for future studies into the basis of intraspecific genetic barriers.

plant biology↗

bioRxiv2018

Can you make morphometrics work when you know the right answer? Pick and mix approaches for apple identification.

Morphological classification of living things has challenged science for several centuries and has led to a wide range of objective morphometric approaches in data gathering and analysis. In this paper we explore those methods using apple cultivars, a model biological system in which discrete groups are pre-defined but in which there is a high level of overall morphological similarity. The effectiveness of morphometric techniques in discovering the groups is evaluated using statistical learning tools. No one technique proved optimal in classification on every occasion, linear morphometric techniques slightly out-performing geometric (72.6% accuracy on test set versus 66.7%). The combined use of these techniques with post-hoc knowledge of their individual successes with particular cultivars achieves a notably higher classification accuracy (77.8%). From this we conclude that even with pre-determined discrete categories, a range of approaches is needed where those categories are intrinsically similar to each other, and we raise the question of whether in studies where potentially continuous natural variation is being categorised the level of match between categories is routinely set too high.

plant biology↗

bioRxiv2015

GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown roots systems

Root systems develop different root types that individually sense cues from their local environment and integrate this information with systemic signals. This complex multidimensional amalgam of inputs enables continuous adjustment of root growth rates, direction and metabolic activity that define a dynamic physical network. Current methods for analyzing root biology balance physiological relevance with imaging capability. To bridge this divide, we developed an integrated imaging system called Growth and Luminescence Observatory for Roots (GLO-Roots) that uses luminescence-based reporters to enable studies of root architecture and gene expression patterns in soil-grown, light-shielded roots. We have developed image analysis algorithms that allow the spatial integration of soil properties, gene expression and root system architecture traits. We propose GLO-Roots as a system that has great utility in presenting environmental stimuli to roots in ways that evoke natural adaptive responses and in providing tools for studying the multi-dimensional nature of such processes.

Plant Biology↗

bioRxiv2018

Chromatin immunoprecipitation-sequencing and RNA-sequencing for complex and low-abundance tree buds

Chromatin immunoprecipitation-sequencing (ChIP-seq) is a robust technique to study interactions between proteins, such as histones or transcription factors, and DNA. This technique in combination with RNA-sequencing (RNA-seq) is a powerful tool to better understand biological processes in eukaryotes. We developed a combined ChIP-seq and RNA-seq protocol for tree buds (Prunus avium L., Prunus persica L Batch, Malus x domestica Borkh.) that has also been successfully tested on Arabidopsis thaliana and Saccharomyces cerevisiae. Tree buds contain phenolic compounds that negatively interfere with ChIP and RNA extraction. In addition to solving this problem, our protocol is optimised to work on small amounts of material. Furthermore, one of the advantages of this protocol is that samples for ChIP-seq are cross-linked after flash freezing, making it possible to work on trees growing in the field and to perform ChIP-seq and RNA-seq on the same starting material. Focusing on dormant buds in sweet cherry, we explored the link between expression level and H3K4me3 enrichment for all genes, including a strong correlation between H3K4me3 enrichment at the DORMANCY-ASSOCIATED MADS-box 5 (PavDAM5) loci and its expression pattern. This protocol will allow analysis of chromatin and transcriptomic dynamics in tree buds, notably during its development and response to the environment.

plant biology↗

bioRxiv2018

Quantitative variation within a species for traits underpinning C4 photosynthesis

Engineering C4 photosynthesis into C3 crops such as rice or wheat could substantially increase their yield by alleviating photorespiratory losses1,2. This objective is challenging because the C4 pathway involves complex modifications to the biochemistry, cell biology and anatomy of leaves3. Forward genetics has provided limited insight into the mechanistic basis of these characteristics and there have been no reports of significant quantitative intra-specific variation of C4 attributes that would allow trait-mapping4,5. Here we show that accessions of C4 Gynandropsis gynandra collected from locations across Africa and Asia exhibit natural variation in key characteristics of C4 photosynthesis. Variable traits include bundle sheath size and vein density, gas exchange parameters and carbon-isotope discrimination associated with the C4 state, but also abundance of transcripts encoding core enzymes of the C4 cycle. Traits relating to water use showed more quantitative variation than those associated with carbon assimilation. We propose variation in these traits likely adapted the hydraulic system for increased water use efficiency rather than improving carbon fixation, indicating that selection pressure may drive C4 diversity in G. gynandra by acting to modify water use rather than photosynthesis. As these accessions can be easily crossed and produce fertile offspring, our findings indicate that natural variation within a C4 species is sufficiently large to allow genetic-mapping of key anatomical C4 traits and regulators.

plant biology↗

bioRxiv2018

Growth of Sphagnum riparium is strongly rhythmic: Contribution of the seasonal, circalunar and third rhythmiccomponents

Continuous high-resolution monitoring of Sphagnum growth can provide insights into the biological rhythms of moss growth. Moss Sphagnum riparium is a convenient model for growth monitoring. Application of the method of geotropic curvatures has enabled a three-year monitoring with two to five-day intervals. We measured the increment in ca. 85000 shoots and produced ca. 3500 growth rate estimates, making this study a champion in precision compared to previous efforts. The zeitgeber for seasonal growth rhythms is the temperature seasonal cycle (R2=0.21-0.52). When the temperature changes by 10{degrees}C, moss growth rate is modified by 0.10-0.17cm/day according to the linear model, and 1.47-2.06-fold in the exponential model. The zeitgeber for circalunar rhythms is the lunar synodic cycle (R2=0.14-0.26). The average amplitude of the fluctuations it induces in the growth rate is 0.0425- 0.0572cm/day, which is equivalent to the effect of a 3.43-4.53{degrees}C change in temperature. The third rhythm can be distinguished in periodograms. Its period ranges from 10 to 16 days, but we did not detect the zeitgeber.\n\nIn total, three rhythms explain 51-78% of the growth rate. We believe that the strong rhythmicity in Sphagnum growth is associated with shoot growth synchronization.

plant biology↗

bioRxiv2017

The evolutionary history of the current global Ramularia collo-cygni epidemic

Ramularia Leaf Spot (RLS) has emerged as a threat for barley production in many regions of the world. Late appearance of unspecific symptoms caused that Ramularia collo-cygni could only by molecular diagnostics be detected as the causal agent of RLS. Although recent research has shed more light on the biology and genomics of the pathogen, the cause of the recent global spread remains unclear.\n\nTo address urgent questions, especially on the emergence to a major disease, life-cycle, transmission, and quick adaptation to control measures, we de-novo sequenced the genome of R. collo-cygni (urug2 isolate). Additionally, we sequenced fungal RNA from 6 different conditions, which allowed for an improved genome annotation. This resulted in a high quality draft assembly of about 32 Mb, with only 78 scaffolds with an N50 of 2.1 Mb. The overall annotation enabled the prediction of 12.346 high confidence genes. Genomic comparison revealed that R. collo-cygni has significantly diverged from related Dothidiomycetes, including gain and loss of putative effectors, however without obtaining species-specific genome features.\n\nTo evaluate the species-wide genetic diversity, we sequenced the genomes of 19 R. collo-cygni isolates from multiple geographic locations and diverse hosts and mapped sequences to our reference genome. Admixture analyses show that R. collo-cygni is world-wide genetically uniform and that samples do not show a strong clustering on either geographical location or host species. To date, the teleomorph of R. collo-cygni has not been observed. Analysis of linkage disequilibrium shows that in the world-wide sample set there are clear signals of recombination and thus sexual reproduction, however these signals largely disappear when excluding three outliers samples, suggesting that the main global expansion of R. collo-cygni comes from mixed or clonally propagating populations. We further analysed the historic population size (Ne) of R. collo-cygni using Bayesian simulations.\n\nWe discuss how our genomic data and population genetics analysis can help understand the current R. collo-cygni epidemic and provide different hypothesis that are supported by our data. We specifically highlight how recombination, clonal spreading and lack of host-specificity could further support global epidemics of this increasingly recognized plant disease and suggest specific approaches to combat this pathogen.

plant biology↗

bioRxiv2016

Reproductive biology of three Ziziphus species (Rhamnaceae)

The reproductive biology of three Ziziphus species: Z. jujube, Z. mauritiana and Z. spina-christi, with respect to seasonal growth stages, floral biology, pollen performance, fruit set and seed viability were compared. To elucidate the reasons for variations in reproductive success we also estimated the ploidy levels among the genotypes of these tree species. Four genotypes of Z. mauritiana and Z. jujube each, and two natural selections of Z. spina-christi were grown in the Negev highlands at the Sde Boqer experimental plot. Field observations were conducted to determine seasonal growth stages and floral biology; laboratory studies included florescent microscopy, differential interference contrast microscopy, in vitro pollen germination and histological techniques. Seasonal growth stages were similar in Z. spina-christi and Z. mauritiana but distinct in Z. jujube, which was the earliest species. Flower opening stages were similar in all species and genotypes. Anthesis timing was genotype specific and did not depend on species. Anthesis types were subdivided into early and late morning as well as afternoon. We found a wide range of values for the number of flowers per inflorescence between species and genotypes, but all genotypes set one fruit per inflorescence with the exception of Z. jujube genotype Tamar, which set two fruit per inflorescence. Significant variation in fruit weight was observed between species as well as genotypes. Fruit of Z. mauritiana and Z jujube weighed between 9 to 37 g while fruit weight of Z. spina-christi was between 0.5 to 0.7 g. Flowers of all species and genotypes had two ovules but viable seed set per fruit differed dramatically between species under open pollination. Viable seed set was about 18% for Z. mauritiana and Z jujube, while Z. spina-christi, had the highest viable seed set at about 84%. Histological analysis revealed post fertilization embryo abortion which may be responsible for the relatively low reproductive success in Z. mauritiana and Z. jujube. The results obtained in this study provide an important basis for selecting elite complementary genotypes toward the optimization of Ziziphus fruit production in semi-arid regions.

Plant Biology↗

bioRxiv2018

TuxNet: A simple interface to process RNA sequencing data and infer gene regulatory networks

Predicting gene regulatory networks (GRNs) from gene expression profiles has become a common approach for identifying important biological regulators. Despite the increase in the use of inference methods, existing computational approaches do not integrate RNA-sequencing data analysis, are often not automated, and are restricted to users with bioinformatics and programming backgrounds. To address these limitations, we have developed TuxNet, an integrated user-friendly platform, which, with just a few selections, allows to process raw RNA-sequencing data (using the Tuxedo pipeline) and infer GRNs from these processed data. TuxNet is implemented as a graphical user interface and, using expression data from any organism with an existing reference genome, can mine the regulations among genes either by applying a dynamic Bayesian network inference algorithm, GENIST, or a regression tree-based pipeline that uses spatiotemporal data, RTP-STAR. To illustrate the use of TuxNet while getting insight into the regulatory cascade downstream of the Arabidopsis root stem cell regulator PERIANTHIA (PAN), we obtained time course gene expression data of a PAN inducible line and inferred a GRN using GENIST. Using RTP-STAR, we then inferred the network of a PAN secondary downstream gene, ATHB13, for which we obtained wildtype and mutant expression profiles. Our case studies feature the versatility of TuxNet to infer networks using different types of gene expression data (i.e time course and steady-state data) as well as how inference networks are used to identify important regulators.\n\nSUMMARYTuxNet offers a simple interface for non-computational biologists to infer GRNs from raw RNA-seq data.

plant biology↗

bioRxiv2018

Functions of farmers’ preferred tree species and their potential carbon stocks in southern Burkina Faso: implications for biocarbon initiatives

The success of terrestrial carbon sequestration projects for rural development in sub-Saharan Africa lies in the (i) involvement of local populations in the selection of woody species, which represent the biological assets they use to meet their daily needs, and (ii) information about the potential of these species to store carbon. Although the latter is a key prerequisite, there is very little information available. To help fill this gap, the present study was undertaken in four pilot villages (Kou, Dao, Vrassan and Cassou) in Ziro Province, south-central Burkina Faso. The objective was to determine carbon storage potential for top-priority woody species preferred by local smallholders. We used (i) participatory rural appraisal consisting of group discussions and key informant interviews to identify priority species and functions, and (ii) landscape assessment of carbon stocks in the preferred woody species. Results revealed over 79 priority tree and shrub species grouped into six functions, of which medicine, food and income emerge as the most important ones for the communities. For these functions, smallholders overwhelmingly listed Vitellaria paradoxa, Parkia biglobosa, Afzelia africana, Adansonia digitata, Detarium microcarpum, and Lannea microcarpa among the most important tree species. Among the preferred woody species in Cassou and Kou, the highest quantity of carbon was stored by V. paradoxa (1,460.6 {+/-}271.0 kg C ha-1 to 2,798.1{+/-}521.0 kg C ha-1) and the lowest by Grewia bicolor (1.6{+/-}1.3 kg C ha-1). The potential carbon stored by the preferred tree communities was estimated at 5,766.2 Mg C ha-1 (95% CI: 5,258.2; 6,274.2 Mg C ha-1) in Kou and 6,664.0 Mg C ha-1 (95% CI: 5,810.2; 7,517.8 Mg C ha-1) in Cassou. The findings of this study will help design data-based development of biocarbon projects, which are rare in the West African Sahel despite being considered as one of the most impactful climate change resilient strategies.

plant biology↗