Scholarly Works - Plant Sciences
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Item Open Access Published version Peer-reviewed Macrophotography of Fern Gametophytes Using a Focus Stacking System(British Pteridological Society) Deegan, Jennifer I; Deegan, TimItem Open Access Published version Peer-reviewed Sex: Not all that it's cracked up to be?(Public Library of Science (PLoS), 2018-02-22) Eves-van den Akker, Sebastian; Jones, John T; Eves-Van Den Akker, Sebastian [0000-0002-8833-9679]While sexual reproduction is generally thought to be, evolutionarily speaking, a good idea, there are a small number of organisms that are testament to the contrary. The root-knot nematodes Meloidogyne incognita, M. javanica, and M. arenaria reproduce clonally using mitotic parthenogenesis but have a broader host range, a wider geographical distribution, and a greater agricultural impact than their sexual relatives (Fig 1) [1]. Remarkably, some of these species even have the ability to overcome host resistance [2], suggesting a mechanism for adaptation in the absence of sex. The genetic basis of this plasticity, both in terms of host range and adaptability, is not fully understood. Previous genome sequencing of Meloidogyne has shown that the genome of one of these species, M. incognita, is polyploid [3], most likely as a result of hybridisation (allopolyploid), with a further study suggesting that M. incognita may be the result of multiple additive hybridisation events: a hybrid of a hybrid [4].Item Open Access Published version Peer-reviewed Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background.(Oxford University Press (OUP), 2018-03-02) Mróz, Tomasz L; Eves-van den Akker, Sebastian; Bernat, Agata; Skarzyńska, Agnieszka; Pryszcz, Leszek; Olberg, Madeline; Havey, Michael J; Bartoszewski, Grzegorz; Eves-Van Den Akker, Sebastian [0000-0002-8833-9679]Cucumber (Cucumis sativus L.) has a large, paternally transmitted mitochondrial genome. Cucumber plants regenerated from cell cultures occasionally show paternally transmitted mosaic (MSC) phenotypes, characterized by slower growth, chlorotic patterns on the leaves and fruit, lower fertility, and rearrangements in their mitochondrial DNAs (mtDNAs). MSC lines 3, 12, and 16 originated from different cell cultures all established using the highly inbred, wild-type line B. These MSC lines possess different rearrangements and under-represented regions in their mtDNAs. We completed RNA-seq on normalized and non-normalized cDNA libraries from MSC3, MSC12, and MSC16 to study their nuclear gene-expression profiles relative to inbred B. Results from both libraries indicated that gene expression in MSC12 and MSC16 were more similar to each other than MSC3. Forty-one differentially expressed genes (DEGs) were upregulated and one downregulated in the MSC lines relative to B. Gene functional classifications revealed that more than half of these DEGs are associated with stress-response pathways. Consistent with this observation, we detected elevated levels of hydrogen peroxide throughout leaf tissue in all MSC lines compared to wild-type line B. These results demonstrate that independently produced MSC lines with different mitochondrial polymorphisms show unique and shared nuclear responses. This study revealed genes associated with stress response that could become selection targets to develop cucumber cultivars with increased stress tolerance, and further support of cucumber as a model plant to study nuclear-mitochondrial interactions.Item Open Access Accepted version Peer-reviewed Arabidopsis DORN1 extracellular ATP receptor; activation of plasma membrane K+-and Ca2+-permeable conductances(Wiley-Blackwell, 2018-06) Wang, Limin; Wikins, Katie; Davies, JuliaThe first reports in the 1970s of extracellular ATP (eATP) effects on algal cytoplasmic streaming and Venus fly trap closure received little attention (Jaffe, 1973; Williamson, 1975). By the time interest in plant eATP revived, work on animals had revealed the existence of plasma membrane (PM) receptors for eATP that function in such processes as pain perception and vasodilation (Burnstock, 2016). Plant research is now catching up. eATP effects on roots (gravitropism, growth and development), hypocotyl (elongation), pollen (germination and tube growth), stomatal aperture, and cell viability are now documented (reviewed by Clark et al., 2014, Cho et al., 2017).Item Open Access Accepted version Peer-reviewed The Evolution of Diverse Floral Morphologies.(Elsevier BV, 2017-09-11) Moyroud, Edwige; Glover, Beverley J; Moyroud, Edwige [0000-0001-7908-3205]; Glover, Beverley [0000-0002-6393-819X]The angiosperm flower develops through a modular programme which, although ancient and conserved, provides the flexibility that has allowed an almost infinite variety of floral forms to emerge. In this review, we explore the evolution of floral diversity, focusing on our recent understanding of the mechanistic basis of evolutionary change. We discuss the various ways in which flower size and floral organ size can be modified, the means by which flower shape and symmetry can change, and the ways in which floral organ position can be varied. We conclude that many challenges remain before we fully understand the ecological and molecular processes that facilitate the diversification of flower structure.Item Open Access Accepted version Peer-reviewed Joining the dots.(Springer Science and Business Media LLC, 2018-01) Fattorini, Róisín; Glover, Beverley J; Glover, Beverley [0000-0002-6393-819X]It is hypothesised that morphological evolution occurs through a variety of molecular mechanisms. Position and patterning of petal spots in Clarkia evolved through changes to the regulatory region of a gene encoding the transcriptional activator of pigment synthesis, prompting its regulation by novel positional cues.Item Open Access Published version Peer-reviewed Evolution of nectar spur length in a clade of Linaria reflects changes in cell division rather than in cell expansion.(Oxford University Press (OUP), 2018-11-03) Cullen, E; Fernández-Mazuecos, M; Glover, BJ; Glover, Beverley [0000-0002-6393-819X]BACKGROUND AND AIMS: Nectar spurs (tubular outgrowths of a floral organ which contain, or give the appearance of containing, nectar) are hypothesized to be a 'key innovation' which can lead to rapid speciation within a lineage, because they are involved in pollinator specificity. Despite the ecological importance of nectar spurs, relatively little is known about their development. We used a comparative approach to investigate variation in nectar spur length in a clade of eight Iberian toadflaxes. METHODS: Spur growth was measured at the macroscopic level over time in all eight species, and growth rate and growth duration compared. Evolution of growth rate was reconstructed across the phylogeny. Within the clade we then focused on Linaria becerrae and Linaria clementei, a pair of sister species which have extremely long and short spurs, respectively. Characterization at a micromorphological level was performed across a range of key developmental stages to determine whether the difference in spur length is due to differential cell expansion or cell division. KEY RESULTS: We detected a significant difference in the evolved growth rates, while developmental timing of both the initiation and the end of spur growth remained similar. Cell number is three times higher in the long spurred L. becerrae compared with L. clementei, whereas cell length is only 1.3 times greater. In addition, overall anisotropy of mature cells is not significantly different between the two species. CONCLUSIONS: We found that changes in cell number and therefore in cell division largely explain evolution of spur length. This contrasts with previous studies in Aquilegia which have found that variation in nectar spur length is due to directed cell expansion (anisotropy) over variable time frames. Our study adds to knowledge about nectar spur development in a comparative context and indicates that different systems may have evolved nectar spurs using disparate mechanisms.Item Open Access Published version Peer-reviewed The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana.(Springer Science and Business Media LLC, 2015-07-06) Voß, Ute; Wilson, Michael H; Kenobi, Kim; Gould, Peter D; Robertson, Fiona C; Peer, Wendy A; Lucas, Mikaël; Swarup, Kamal; Casimiro, Ilda; Holman, Tara J; Wells, Darren M; Péret, Benjamin; Goh, Tatsuaki; Fukaki, Hidehiro; Hodgman, T Charlie; Laplaze, Laurent; Halliday, Karen J; Ljung, Karin; Murphy, Angus S; Hall, Anthony J; Webb, Alex AR; Bennett, Malcolm J; Webb, Alex [0000-0003-0261-4375]The endogenous circadian clock enables organisms to adapt their growth and development to environmental changes. Here we describe how the circadian clock is employed to coordinate responses to the key signal auxin during lateral root (LR) emergence. In the model plant, Arabidopsis thaliana, LRs originate from a group of stem cells deep within the root, necessitating that new organs emerge through overlying root tissues. We report that the circadian clock is rephased during LR development. Metabolite and transcript profiling revealed that the circadian clock controls the levels of auxin and auxin-related genes including the auxin response repressor IAA14 and auxin oxidase AtDAO2. Plants lacking or overexpressing core clock components exhibit LR emergence defects. We conclude that the circadian clock acts to gate auxin signalling during LR development to facilitate organ emergence.Item Open Access Published version Peer-reviewed Droplet-based microfluidic analysis and screening of single plant cells.(Public Library of Science (PLoS), 2018) Yu, Ziyi; Boehm, Christian R; Hibberd, Julian M; Abell, Chris; Haseloff, Jim; Burgess, Steven J; Reyna-Llorens, Ivan; Reyna-Llorens, Ivan [0000-0001-7964-7306]Droplet-based microfluidics has been used to facilitate high-throughput analysis of individual prokaryote and mammalian cells. However, there is a scarcity of similar workflows applicable to rapid phenotyping of plant systems where phenotyping analyses typically are time-consuming and low-throughput. We report on-chip encapsulation and analysis of protoplasts isolated from the emergent plant model Marchantia polymorpha at processing rates of >100,000 cells per hour. We use our microfluidic system to quantify the stochastic properties of a heat-inducible promoter across a population of transgenic protoplasts to demonstrate its potential for assessing gene expression activity in response to environmental conditions. We further demonstrate on-chip sorting of droplets containing YFP-expressing protoplasts from wild type cells using dielectrophoresis force. This work opens the door to droplet-based microfluidic analysis of plant cells for applications ranging from high-throughput characterisation of DNA parts to single-cell genomics to selection of rare plant phenotypes.Item Open Access Published version Peer-reviewed TransRate: reference-free quality assessment of de novo transcriptome assemblies.(Cold Spring Harbor Laboratory, 2016-08) Smith-Unna, Richard; Boursnell, Chris; Patro, Rob; Hibberd, Julian M; Kelly, Steven; Hibberd, Julian [0000-0003-0662-7958]TransRate is a tool for reference-free quality assessment of de novo transcriptome assemblies. Using only the sequenced reads and the assembly as input, we show that multiple common artifacts of de novo transcriptome assembly can be readily detected. These include chimeras, structural errors, incomplete assembly, and base errors. TransRate evaluates these errors to produce a diagnostic quality score for each contig, and these contig scores are integrated to evaluate whole assemblies. Thus, TransRate can be used for de novo assembly filtering and optimization as well as comparison of assemblies generated using different methods from the same input reads. Applying the method to a data set of 155 published de novo transcriptome assemblies, we deconstruct the contribution that assembly method, read length, read quantity, and read quality make to the accuracy of de novo transcriptome assemblies and reveal that variance in the quality of the input data explains 43% of the variance in the quality of published de novo transcriptome assemblies. Because TransRate is reference-free, it is suitable for assessment of assemblies of all types of RNA, including assemblies of long noncoding RNA, rRNA, mRNA, and mixed RNA samples.Item Open Access Published version Peer-reviewed Maximizing the potential of multi-parental crop populations.(Elsevier BV, 2016-12) Ladejobi, Olufunmilayo; Elderfield, James; Gardner, Keith A; Gaynor, R Chris; Hickey, John; Hibberd, Julian M; Mackay, Ian J; Bentley, Alison R; Hibberd, Julian [0000-0003-0662-7958]Most agriculturally significant crop traits are quantitatively inherited which limits the ease and efficiency of trait dissection. Multi-parent populations overcome the limitations of traditional trait mapping and offer new potential to accurately define the genetic basis of complex crop traits. The increasing popularity and use of nested association mapping (NAM) and multi-parent advanced generation intercross (MAGIC) populations raises questions about the optimal design and allocation of resources in their creation. In this paper we review strategies for the creation of multi-parent populations and describe two complementary in silico studies addressing the design and construction of NAM and MAGIC populations. The first simulates the selection of diverse founder parents and the second the influence of multi-parent crossing schemes (and number of founders) on haplotype creation and diversity. We present and apply two open software resources to simulate alternate strategies for the development of multi-parent populations.Item Open Access Accepted version Peer-reviewed Regulatory gateways for cell-specific gene expression in C4 leaves with Kranz anatomy.(Oxford University Press (OUP), 2017-01) Reeves, Gregory; Grangé-Guermente, Mathieu J; Hibberd, Julian M; Hibberd, Julian [0000-0003-0662-7958]C4 photosynthesis is a carbon-concentrating mechanism that increases delivery of carbon dioxide to RuBisCO and as a consequence reduces photorespiration. The C4 pathway is therefore beneficial in environments that promote high photorespiration. This pathway has evolved many times, and involves restricting gene expression to either mesophyll or bundle sheath cells. Here we review the regulatory mechanisms that control cell-preferential expression of genes in the C4 cycle. From this analysis, it is clear that the C4 pathway has a complex regulatory framework, with control operating at epigenetic, transcriptional, post-transcriptional, translational, and post-translational levels. Some genes of the C4 pathway are regulated at multiple levels, and we propose that this ensures robust expression in each cell type. Accumulating evidence suggests that multiple genes of the C4 pathway may share the same regulatory mechanism. The control systems for C4 photosynthesis gene expression appear to operate in C3 plants, and so it appears that pre-existing mechanisms form the basis of C4 photosynthesis gene expression.Item Open Access Published version Peer-reviewed µCube: A Framework for 3D Printable Optomechanics(Ubiquity Press, 2018-05-16) Delmans, Mihails; Haseloff, Jim; Delmans, Mihails [0000-0001-5248-4375]; Haseloff, Jim [0000-0003-4793-8058]Scientific instruments often require the integration of mechanics, electronics and optics. While the use of 3D printing techniques and commodity electronics has lowered the cost of instrumentation, the design and prototyping of optical components and light paths can be challenging and expensive. In recent years, attempts have been made to make optical devices more affordable using 3D printing as a method for production of optomechanical components. In this paper we present an assembly standard for the production of 3D printed optical devices. We describe a framework for parametric design of modular mounts, present two modules built using the framework, and demonstrate the potential for generalised design of modular optical devices following the μCube standard.Item Open Access Published version Peer-reviewed Natural Variation within a Species for Traits Underpinning C4 Photosynthesis.(Oxford University Press (OUP), 2018-06) Reeves, Gregory; Singh, Pallavi; Rossberg, Timo A; Sogbohossou, EO Deedi; Schranz, M Eric; Hibberd, Julian M; Reeves, Gregory [0000-0002-3474-8960]; Singh, Pallavi [0000-0003-3694-6378]; Rossberg, Timo A [0000-0001-9805-4899]; Sogbohossou, EO Deedi [0000-0002-9034-0062]; Schranz, M Eric [0000-0001-6777-6565]; Hibberd, Julian M [0000-0003-0662-7958]Engineering C4 photosynthesis into C3 crops could substantially increase their yield by alleviating photorespiratory losses. This objective is challenging because the C4 pathway involves complex modifications to the biochemistry, cell biology, and anatomy of leaves. Forward genetics has provided limited insight into the mechanistic basis of these properties, and there have been no reports of significant quantitative intraspecific variation of C4 attributes that would allow trait mapping. Here, we show that accessions of the C4 species 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. The abundance of transcripts encoding core enzymes of the C4 cycle also showed significant variation. Traits relating to water use showed more quantitative variation than those associated with carbon assimilation. We propose that 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 modifying water use rather than photosynthesis. The accessions analyzed can be easily crossed and produce fertile offspring. Our findings, therefore, indicate that natural variation within this C4 species is sufficiently large to allow genetic mapping of key C4 traits and regulators.Item Open Access Published version Peer-reviewed Ultrastructure and optics of the prism-like petal epidermal cells of Eschscholzia californica (California poppy).(Wiley, 2018-08) Wilts, Bodo D; Rudall, Paula J; Moyroud, Edwige; Gregory, Tom; Ogawa, Yu; Vignolini, Silvia; Steiner, Ullrich; Glover, Beverley J; Wilts, Bodo D [0000-0002-2727-7128]; Rudall, Paula J [0000-0002-4816-1212]; Moyroud, Edwige [0000-0001-7908-3205]; Ogawa, Yu [0000-0003-0677-7913]; Vignolini, Silvia [0000-0003-0664-1418]; Steiner, Ullrich [0000-0001-5936-339X]; Glover, Beverley J [0000-0002-6393-819X]The petals of Eschscholzia californica (California poppy) are robust, pliable and typically coloured intensely orange or yellow owing to the presence of carotenoid pigments; they are also highly reflective at certain angles, producing a silky effect. To understand the mechanisms behind colour enhancement and reflectivity in California poppy, which represents a model species among early-divergent eudicots, we explored the development, ultrastructure, pigment composition and optical properties of the petals using light microscopy and electron microscopy combined with both spectrophotometry and goniometry. The elongated petal epidermal cells each possess a densely thickened prism-like ridge that is composed primarily of cell wall. The surface ridges strongly focus incident light onto the pigments, which are located in plastids at the cell base. Our results indicate that this highly unusual, deeply ridged surface structure not only enhances the deep colour response in this desert species, but also results in strongly angle-dependent 'silky' reflectivity that is anisotropic and mostly directional.Item Open Access Accepted version Peer-reviewed Acid growth: an ongoing trip.(Oxford University Press (OUP), 2018-01-04) Arsuffi, Giulia; Braybrook, Siobhan A; Arsuffi, Giulia [0000-0003-1877-8534]Since its first formulation almost 50 years ago, acid growth has had a chequered past complicated by utilization of diverse species and organs for testing alongside necessary but coarse methodology. Within the past 25 years, we have gained new insights into the molecular mechanisms behind the transduction of the signal auxin into the reality of an apoplastic pH shift as well as the effect on cell wall mechanics and the biochemical players within the wall contributing to the resultant growth. In this review, we begin by discussing the historical work and its complications, move on to the modern work and its addition to acid growth, which we finally summarize in an updated model which includes new postulations and questions.Item Open Access Published version Peer-reviewed Massive crossover elevation via combination of HEI10 and recq4a recq4b during Arabidopsis meiosis.(National Academy of Sciences, 2018-03-06) Henderson, IR; Henderson, Ian [0000-0001-5066-1489]During meiosis, homologous chromosomes undergo reciprocal crossovers, which generate genetic diversity and underpin classical crop improvement. Meiotic recombination initiates from DNA double-strand breaks (DSBs), which are processed into singlestranded DNA that can invade a homologous chromosome. The resulting joint molecules can ultimately be resolved as crossovers. In Arabidopsis, competing pathways balance the repair of ∼100– 200 meiotic DSBs into ∼10 crossovers per meiosis, with the excess DSBs repaired as noncrossovers. To bias DSB repair toward crossovers, we simultaneously increased dosage of the procrossover E3 ligase gene HEI10 and introduced mutations in the anticrossovers helicase genes RECQ4A and RECQ4B. As HEI10 and recq4a recq4b increase interfering and noninterfering crossover pathways, respectively, they combine additively to yield a massive meiotic recombination increase. Interestingly, we also show that increased HEI10 dosage increases crossover coincidence, which indicates an effect on interference. We also show that patterns of interhomolog polymorphism and heterochromatin drive recombination increases distally towards the subtelomeres in both HEI10 and recq4a recq4b backgrounds, while the centromeres remain crossover suppressed. These results provide a genetic framework for engineering meiotic recombination landscapes in plant genomes.Item Open Access Accepted version Peer-reviewed Independent signalling cues underpin arbuscular mycorrhizal symbiosis and large lateral root induction in rice.(Wiley-Blackwell, 2017-12-22) Chiu, Chai Hao; Choi, Jeongmin; Paszkowski, Uta; Choi, Jeongmin [0000-0001-7753-3348]; Paszkowski, Uta [0000-0002-7279-7632]Perception of arbuscular mycorrhizal fungi (AMF) triggers distinct plant signalling responses for parallel establishment of symbiosis and induction of lateral root formation. Rice receptor kinase CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) and α/β-fold hydrolase DWARF14-LIKE (D14L) are involved in pre-symbiotic fungal perception. After 6 wk post-inoculation with Rhizophagus irregularis, root developmental responses, fungal colonization and transcriptional responses were monitored in two independent cerk1 null mutants; a deletion mutant lacking D14L, and with D14L complemented as well as their respective wild-type cultivars (cv Nipponbare and Nihonmasari). Here we show that although essential for symbiosis, D14L is dispensable for AMF-induced root architectural modulation, which conversely relies on CERK1. Our results demonstrate uncoupling of symbiosis and the symbiotic root developmental signalling during pre-symbiosis with CERK1 required for AMF-induced root architectural changes.Item Open Access Accepted version Peer-reviewed Evidence-based controls for epidemics using spatio-temporal stochastic models in a Bayesian framework.(The Royal Society, 2018-11-29) Adrakey, Hola K; Streftaris, George; Cunniffe, Nik J; Gottwald, Tim R; Gilligan, Christopher A; Gibson, Gavin J; Cunniffe, Nik [0000-0002-3533-8672]; Gilligan, Christopher [0000-0002-6845-0003]The control of highly infectious diseases of agricultural and plantation crops and livestock represents a key challenge in epidemiological and ecological modelling, with implemented control strategies often being controversial. Mathematical models, including the spatio-temporal stochastic models considered here, are playing an increasing role in the design of control as agencies seek to strengthen the evidence on which selected strategies are based. Here, we investigate a general approach to informing the choice of control strategies using spatio-temporal models within the Bayesian framework. We illustrate the approach for the case of strategies based on pre-emptive removal of individual hosts. For an exemplar model, using simulated data and historic data on an epidemic of Asiatic citrus canker in Florida, we assess a range of measures for prioritizing individuals for removal that take account of observations of an emerging epidemic. These measures are based on the potential infection hazard a host poses to susceptible individuals (hazard), the likelihood of infection of a host (risk) and a measure that combines both the hazard and risk (threat). We find that the threat measure typically leads to the most effective control strategies particularly for clustered epidemics when resources are scarce. The extension of the methods to a range of other settings is discussed. A key feature of the approach is the use of functional-model representations of the epidemic model to couple epidemic trajectories under different control strategies. This induces strong positive correlations between the epidemic outcomes under the respective controls, serving to reduce both the variance of the difference in outcomes and, consequently, the need for extensive simulation.Item Open Access Published version Peer-reviewed The major barriers to evidence-informed conservation policy and possible solutions.(Wiley, 2018) Rose, David C; Sutherland, William J; Amano, Tatsuya; González-Varo, Juan P; Robertson, Rebecca J; Simmons, Benno I; Wauchope, Hannah S; Kovacs, Eszter; Durán, América Paz; Vadrot, Alice BM; Wu, Weiling; Dias, Maria P; Di Fonzo, Martina MI; Ivory, Sarah; Norris, Lucia; Nunes, Matheus Henrique; Nyumba, Tobias Ochieng; Steiner, Noa; Vickery, Juliet; Mukherjee, Nibedita; Sutherland, William [0000-0002-6498-0437]; Amano, Tatsuya [0000-0001-6576-3410]; Simmons, Benno [0000-0002-2751-9430]; Wauchope, Hannah [0000-0001-5370-4616]; Kovacs, Eszter [0000-0003-3516-7786]; Nyumba, Tobias [0000-0002-7821-5197]; Mukherjee, Nibedita [0000-0002-2970-1498]Conservation policy decisions can suffer from a lack of evidence, hindering effective decision-making. In nature conservation, studies investigating why policy is often not evidence-informed have tended to focus on Western democracies, with relatively small samples. To understand global variation and challenges better, we established a global survey aimed at identifying top barriers and solutions to the use of conservation science in policy. This obtained the views of 758 people in policy, practice, and research positions from 68 countries across six languages. Here we show that, contrary to popular belief, there is agreement between groups about how to incorporate conservation science into policy, and there is thus room for optimism. Barriers related to the low priority of conservation were considered to be important, while mainstreaming conservation was proposed as a key solution. Therefore, priorities should focus on convincing the public of the importance of conservation as an issue, which will then influence policy-makers to adopt pro-environmental long-term policies.