GARNet Research Roundup: March 7th 2019

This edition of the GARNet research roundup begins with a study into the genetic basis of fertility in barley led by Sarah McKim from Dundee. Second is a study from Oxford and Leicester that characterizes the proteolytic control of chloroplast import. The third paper from Levi Yant’s group at JIC and Nottingham that attempts to discover the influence of polyploidism on population genomic effects whilst the fourth paper from Juliet Coates’ lab in Birmingham uses the growth of Arabidopsis to assess the potential of algal biomass as a biofertiliser. The next two papers include co-authors from Oxford and Warwick respectively and investigate different factors that control seed viability in Arabidopsis and Brassica oleracea. The final paper includes Seth Davies from York as a co-author on a study that looks at control of the circadian clock in field-grown Arabidopsis.

Zwirek M, Waugh R, McKim SM (2019) Interaction between row-type genes in barley controls meristem determinacy and reveals novel routes to improved grain. New Phytol. doi: 10.1111/nph.15548

Open Access

Current GARNet committee members Sarah McKim is the leader of this study in which first author is Monica Zwirek. They investigate the mechanism through which the barley VRS genes contribute to spikelet fertility. They undercover the epistatic relationship between five VRS genes that explains how they contribute to controlling fertility of lateral spikelets. Importantly they demonstrate that various vrs mutant combinations improve fertility in a variety of ways, information that will be useful during the generation of new varieties of barley.

Ling Q, Broad W, Trösch R, Töpel M, Demiral Sert T, Lymperopoulos P, Baldwin A, Jarvis RP (2019) Ubiquitin-dependent chloroplast-associated protein degradation in plants. Science. doi: 10.1126/science.aav4467

Qihua Ling and William Broad are the first authors on this study from the Universities of Oxford and Leicester. They investigate the role of proteolysis in the functional control of chloroplast-envelope translocases, which are required for the transport of proteins from nucleus-encoded genes into the chloroplast. They identify two newly characterised proteins that function in the same pathway as the known ubiquitin E3 ligase SP1. These novel proteins, SP2 and CDC48, are both required for the movement of ubiquitinated proteins from the chloroplast outer envelope membrane (OEM) into the cytosol, where they are degraded by the proteolytic machinery. This process of chloroplast-associated protein degradation (CHLORAD) maintains tight control of the activity of OEM proteins and is essential for organelle function.

Monnahan P, Kolář F, Baduel P, Sailer C, Koch J, Horvath R, Laenen B, Schmickl R, Paajanen P, Šrámková G, Bohutínská M, Arnold B, Weisman CM, Marhold K, Slotte T, Bomblies K, Yant L (2019) Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nat Ecol Evol. doi: 10.1038/s41559-019-0807-4.

Patrick Monnahan at the John Innes Centre is first author on this study from the Yant lab that has recently moved to the University of Nottingham. In this collaboration with colleagues in the US, Austria, Sweden, the Czech Republic and Slovakia, they have performed large scale sequencing on 39 populations of Arabidopsis arenosa. These plants have differing levels of ploidy and they are attempting to understand how ploidy effects population genomics. They demonstrate that the ploidy effects are subtle but significant and that masking of deleterious mutations, faster substitution rates and interploidy introgression will likely impact the evolution of populations where polyploidy is common.

Ghaderiardakani F, Collas E, Damiano DK, Tagg K, Graham NS, Coates J (2019) Effects of green seaweed extract on Arabidopsis early development suggest roles for hormone signalling in plant responses to algal fertilisers. Sci Rep. doi: 10.1038/s41598-018-38093-2

Open Access

This work from the Coates lab at the University of Birmingham is led by Fatemeh Ghaderiardakani and looked into the potential of algal extracts as biofertiliser. They showed that at >0.1%, extracts taken from the common green seaweed Ulva intestinalis inhibit Arabidopsis seed germination and root elongation. At lower concentrations primary root elongation was promoted albeit with a complete loss of lateral root formation. Elemental analysis allows the authors to suggest that this effect was mediated via a novel mechanism involving aluminium. Overall the authors caution against the use of algal biofertilisers due to potential unforeseen negative effects on plant growth.

Viñegra de la Torre N, Kaschani F, Kaiser M, van der Hoorn RAL, Soppe WJJ, Misas Villamil JC (2019) Dynamic hydrolase labelling as a marker for seed quality in Arabidopsis seeds. Biochem J. doi: 10.1042/BCJ20180911.

GARNet Committee member Renier van der Hoorn is a co-author on this German-led study that investigates how the activity of seed-localised proteases can affect Arabidopsis seed germination. This study has clear real-world application regarding the storage of economically important seed stocks. They show that vacuolar processing enzymes (VPEs) become more active during aging whilst the activity of serine hydrolases declines alongside seed quality. This information has allowed the authors to develop protease-activity-based markers that will provide information about seed quality.

Schausberger C, Roach T, Stöggl WM, Arc E, Finch-Savage WE, Kranner I (2019) Abscisic acid-determined seed vigour differences do not influence redox regulation during ageing. Biochem J. doi: 10.1042/BCJ20180903

William Finch-Savage from the University of Warwick is a co-author on this Austrian-led study that looks at the effect of aging on the quality of Brassica oleracea seeds stored at two oxygen concentrations. Higher O2 causes a more rapid decrease in seed quality through aging yet in contrast aging did not alter the impact of the hormone ABA on seed viability. This study enables the authors to uncover two mechanisms that control seed quality that appear to act through different mechanisms.

Rubin MJ, Brock MT, Davis SJ, Weinig C (2019) QTL Underlying Circadian Clock Parameters Under Seasonally Variable Field Settings in Arabidopsis thaliana G3 (Bethesda). doi: 10.1534/g3.118.200770

Open Access

Seth Davies from the University of York is a co-author on this study led by Matthew Rubin from the University of Wyoming. They looked at the growth of Arabidopsis thaliana recombinant inbred lines grown in field conditions and found an extremely nuanced relationship regarding how QTLs that influence the circadian clock respond to environmental conditions. For example the authors showed that plant growth in June, July and September is controlled by different QTL architecture, demonstrating the complex regulation of the circadian clock in these field growth plants.

GARNet Research Roundup: January 31st 2019

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Published on: January 31, 2019

This edition of the GARNet research roundup has an initial focus on the shoot apical meristem. Firstly a study from the University of Birmingham performs network analysis to define the connections that control the global organisation of this tissue.

Second is the first of a group of papers involving authors from the Sainsbury Lab, Cambridge University and the University of Cambridge. Henrik Jönsson and Henrik Ahl contribute to a study that refines our understanding about the role of auxin in leaf dorsoventral patterning. Next from SLCU are two papers published in collaboration with the University of Helsinki that identify a set of novel regulators of cambial development.

The final SLCU paper from James Locke’s group attempts to tackle the challenging topic of ‘noise’ in biological systems. The final paper from the University of Cambridge investigate factors involved in karrikin signaling.

The penultimate paper characterises the LINC complex in monocots and includes authors from Oxford Brookes University whilst the final paper is from the University of York and performs a structural analysis of a key enzyme involved in the potential phytoremediation of TNT.

Jackson MDB, Duran-Nebreda S, Kierzkowski D, Strauss S, Xu H, Landrein B, Hamant O, Smith RS, Johnston IG, Bassel GW (2019) Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem. Cell Syst. doi: 10.1016/j.cels.2018.12.009

Open Access

George Bassel is corresponding author of this paper led by Matthew Jackson at the University of Birmingham. They use live 3D imaging and computational analysis to identify a network of cellular connections in the shoot apical meristem. They show that locally generated cell division rules lead to emergence of global tissue organisation, which facilitates cellular communication. In addition they show that global cellular organization requires the activity of the KATANIN protein.

Bhatia N, Åhl H, Jönsson H, Heisler MG (2019) Quantitative analysis of auxin sensing in leaf primordia argues against proposed role in regulating leaf dorsoventrality. Elife. doi: 10.7554/eLife.39298

Open Access

Henrik Jönsson and Henrik Ahl at SLCU are co-authors on this study led by Neha Bhatia at the University of Sydney. They use data gained from analysis of the R2D2 auxin sensor to argue against the current hypothesis stating that asymmetric auxin distribution is necessary to define the dorso-ventral polarity of the Arabidopsis leaf. They repeat previous experiments using the DII auxin sensor and through additional analysis using an auxin insensitive version of the sensor (mDII), provide results that contrast to previously published data.

Miyashima S, Roszak P, Sevilem I, Toyokura K, Blob B, Heo JO, Mellor N, Help-Rinta-Rahko H, Otero S, Smet W, Boekschoten M, Hooiveld G, Hashimoto K, Smetana O, Siligato R, Wallner ES, Mähönen AP, Kondo Y, Melnyk CW, Greb T, Nakajima K, Sozzani R, Bishopp A, De Rybel B, Helariutta Y (2019). Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature doi: 10.1038/s41586-018-0839-y

Smetana O, Mäkilä R, Lyu M, Amiryousefi A, Sánchez Rodríguez F, Wu MF, Solé-Gil A, Leal Gavarrón M, Siligato R, Miyashima S, Roszak P, Blomster T, Reed JW, Broholm S, Mähönen AP (2019). High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature. doi: 10.1038/s41586-018-0837-0

These back-to-back manuscripts include Pawel Roszak from the SLCU as an author in both papers. The corresponding author for the first paper, which is a true global collaboration, is Yrjo Helariutta who holds research positions at both SLCU and the University of Helsinki. These papers introduce a new signalling module of transcriptional factors that control radial growth initiated in procambial cells. In root protophloem cells cytokinin induces the expression of a newly characterised set of PEAR transcription factors, which form a short-range concentration gradient and initiate radial growth. To maintain tight developmental control of this program PEAR protein activity is antagonised by HD-ZIP III proteins, whose expression domain is controlled by the activity of auxin and a set of mobile miRNAs. The identification of this signalling module increases our understanding about the factors that control the growth of woody tissues and therefore has enormous translational significance.

Cortijo S, Aydin Z, Ahnert S, Locke JC (2019) Widespread inter-individual gene expression variability in Arabidopsis thaliana Mol Syst Biol. doi: 10.15252/msb.20188591

Open Access

Sandra Cortijo is the lead author of this paper and works with James Locke at SLCU. They have attempted to address the fundamental question of noise within biological outputs through analysis of gene expression from a set of identical Arabidopsis plants grown in identical conditions. They identify hundreds of genes that show variable expression between these plants, with different gene sets changing throughout the diurnal cycle. They further define this variability by identifying gene length, the number of transcription factors regulating the genes and the chromatin environment as contributory factors to explain why this variation occurs.

Swarbreck SM, Guerringue Y, Matthus E, Jamieson FJC, Davies JM (2019) Impairment in karrikin but not strigolactone sensing enhances root skewing in Arabidopsis thaliana. Plant J. doi: 10.1111/tpj.14233

Stéphanie Swarbreck is the first author of this work from Julia Davies’ lab at the University of Cambridge. They show that perception of karrikins (smoke-derived butenolides) through the interaction of the KAI2 hydrolase and MAX2 F-box protein occurs independent of strigolactone-sensing mechanism of the MAX2-D14 hydrolase interaction. Karrikins cause a root skewing phenotype so the authors use this output to identify that previously characterised SMAX1 (SUPPRESSOR OF MAX2-1)/SMXL2 and SMXL6,7,8 (SUPPRESSOR OF MAX2-1-LIKE) proteins are targets of degradation by the KAI2/MAX2 complex. Overall they show that KAI2/MAX2 limits root skewing but is not involved in the role KAI2 plays in gravi- or mechano-sensing. These results are indicative of a set of KAI2 specific ligands that control root skewing yet candidate proteins for these roles remain to be identified.

Gumber HK, McKenna JF, Estrada AL, Tolmie AF, Graumann K, Bass HW (2019) Identification and characterization of genes encoding the nuclear envelope LINC complex in the monocot species Zea mays. J Cell Sci. doi: 10.1242/jcs.221390

This paper is led by Hank Bass and Hardeep Gumber from Florida State University and includes Joe McKenna, Andrea Tolmie and Katja Graumann at Oxford Brookes as co-authors. They use phylogenetic and microscopic analysis to identify and characterise components of the nuclear-envelope spanning LINC (Linker of Nucleoskeleton to Cytoskeleton) complex in Zea mays. They identify a set of monocot-specific members of the LINC complex, which will allow an increased understanding about the functional linkages between the cytoplasm, nuclear envelope, nucleoplasm and chromatin.

Hank Bass discusses this paper on the GARNet YouTube channel. Hank and Katja are members of the EU COST action entitled ‘Impact of Nuclear Domains On Gene Expression and Plant Traits (INDEPTH).

Tzafestas K, Ahmad L, Dani MP, Grogan G, Rylott EL, Bruce NC (2018) Structure-Guided Mechanisms Behind the Metabolism of 2,4,6-Trinitrotoluene by Glutathione Transferases U25 and U24 That Lead to Alternate Product Distribution Front Plant Sci. doi: 10.3389/fpls.2018.01846

Open Access

Kyriakos Tzafestas is the first author on this paper from the University of York led by Neil Bruce. They perform a structural analysis of the Arabidopsis tau class glutathione transferase, GSTU25, which is involved in the phytoremediation of 2,4,6-trinitrotoluene (TNT). This analysis identified of a key set of amino acids involved in a precise part of its enzymatic activity, which can in turn be transferred to the related, but enzymatically-inert GSTU24. These findings will aid in the development of increasingly efficient strategies for plant-based remediation of environmental TNT.

GARNet Research Roundup: Jan 11th 2019

The inaugural GARNet Research Roundup of 2019 firstly includes a paper from the University of Sheffield that has identified new pericentromeric epigenetic loci that affect the pathogen response. Secondly is a collaboration between researchers in Birmingham, Nottingham and Oxford that has identified a new mode of regulation of the VRN2 protein. Next are two papers from Jonathan Jones’ lab at The Sainsbury Laboratory in Norwich that firstly provides a toolkit for gene editing in Arabidopsis and secondly characterise the role of the NRG1 gene in the defense response. The penultimate paper is from Paul Devlin’s lab at RHUL and investigates the role of the circadian clock in the control of leaf overtopping whilst the final paper is a meeting report from a recent GARNet workshop on gene editing.

Furci L, Jain R, Stassen J, Berkowitz O, Whelan J, Roquis D, Baillet V, Colot V, Johannes F, Ton J (2019) Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. Elife. doi: 10.7554/eLife.40655.

Open Access

Leonardo Furci and Ritushree Jain are the lead authors on this study conducted at the University of Sheffield. The authors used a population of epigenetic recombinant inbred lines (epiRILs) to screen for resistance to the oomycete pathogen Hyaloperonospora arabidopsidis. These lines each share genetic information but have varied epigenetic changes. This analysis enabled the identification of plants with hypomethylated pericentromeric regions that were primed to better respond to the presence of this pathogen. The authors discuss the mechanism through which this might affect the defence response albeit without altering other aspects of plant growth.

Gibbs DJ, Tedds HM, Labandera AM, Bailey M, White MD, Hartman S, Sprigg C, Mogg SL, Osborne R, Dambire C, Boeckx T, Paling Z, Voesenek LACJ, Flashman E, Holdsworth MJ (2018) Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2. Nat Commun. doi: 10.1038/s41467-018-07875-7

Open Access

This collaboration between the Universities of Birmingham, Nottingham, Oxford and colleagues in Utrecht is led by Daniel Gibbs. They demonstrate that the amount of VRN2 protein, which is a member of the Polycomb Repressive Complex2, is controlled by the N-end rule pathway and that this regulation responses to both cold and hypoxia stress. Whilst the VRN2 gene is expressed throughout the plant, the N-end rule degradation pathway ensures that the protein is restricted to meristematic regions until the plant senses the appropriate abiotic stress. Classically VRN2 has been linked to the regulation of flowering time by altering gene expression at the FLC locus so this study introduces new complexity into this process through the involvement of the N-end rule pathway. More information on this linkage will undoubtedly follow over the coming years.

Daniel kindly discusses this paper on the GARNet YouTube channel.

Castel B, Tomlinson L, Locci F, Yang Y, Jones JDG (2019) Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis. PLoS One. doi: 10.1371/journal.pone.0204778

Open Access

Baptiste Castel is lead author of this work conducted at the Sainsbury Laboratory, Norwich in Jonathan Jones’ group. They have conducted a detailed analysis of the factors that contribute to successful gene editing by CRISPR-Cas9, specifically in Arabidopsis. This includes assessing the efficacy of different promotor sequences, guideRNAs, versions of Cas9 enzyme and associated regulatory sequences in the editing of a specific locus. Given that researchers are finding that different plants have different requirements when it comes to successful gene editing, this type of analysis will be invaluable for anyone who plans to conduct a gene editing experiment in Arabidopsis.

Castel B, Ngou PM, Cevik V, Redkar A, Kim DS, Yang Y, Ding P, Jones JDG (2018) Diverse NLR immune receptors activate defence via the RPW8-NLR NRG1. New Phytol. doi: 10.1111/nph.15659

In this second paper led by Baptiste Castel, they used the techniques outlined in the paper above to generate a set of CRISPR mutants deficient in NRG1, which is a RPW8-NLR resistance (R) gene. These nrg1 mutants have compromised signalling in all tested downstream TIR-NLR resistance genes. In addition the authors demonstrate that this signalling is needed for resistance to oomycete but not bacterial infection. Therefore this study reveals some significant details regarding the components of the disease response that are influenced by the activity of NRG1.

Woodley Of Menie MA, Pawlik P, Webb MT, Bruce KD, Devlin PF (2018) Circadian leaf movements facilitate overtopping of neighbors. Prog Biophys Mol Biol. doi: 10.1016/j.pbiomolbio.2018.12.012

This work is led by Michael Woodley Of Menie from Paul Devlin’s lab at Royal Holloway College and investigates the role of circadian leaf movements during shade avoidance and overtopping. Arabidopsis plants were grow in a grid system that meant leaves would interact with their neighbours and the authors show that plants with a normal circadian rhythm gained an advantage over those adapted to a longer period in which they were grown. This overtopping was additive to the advantage gained through shade avoidance and overall this paper shows that maintainance of clock-aligned leaf movements are beneficial to growth.

Parry G, Harrison CJ (2019) GARNet gene editing workshop. New Phytol. doi: 10.1111/nph.15573

Open Access

GARNet advisory committee member Jill Harrison and GARNet coordinator Geraint Parry are authors on this meeting report resulting from a GARNet organised workshop on gene editing that took place in March 2018 at the University of Bristol. Coincidentally part of the paper discusses the work that was presented at the meeting by Baptiste Castel, which is published in the paper described above.

GARNet Research Roundup: December 7th 2018

The first four papers in this GARNet Research Roundup includes research from Norwich Research Park. Firstly members of Jonathan Jones’ lab have identified a new Avr gene from Hyaloperonospora arabidopsidis. Secondly Anne Osbourn’s lab characterises two novel arabinosyltransferases that are involved in the plant defence response. Thirdly Cathie Martin’s group is involved in a study that investigates the biosynthesis of the metabolite ubiquinone. Finally in research from NRP is from Silke Robatzek’s lab, where they use a novel quantitative imaging system to characterise stomatal mutants.

The next two papers arise from work at SLCU, firstly looking at the possible role of a novel transposon family during gene-shuffling and secondly a paper that investigates the structure of an important component of the strigolactone signaling pathway.

The seventh paper from Peter Eastmond’s lab at Rothamsted Research identifies a novel gene involved in seed oil composition. The penultimate paper is from Peter Unwin at the University of Leeds and assesses the cell wall composition of ‘giant’ root cells induced by nematode Meloidogyne spp. Finally is a methods paper that describes how microCT imaging can be used to measure different leaf parameters.

Asai S, Furzer O, Cavik V, Kim DS, Ishaque N, Goritschnig S, Staskawicz B, Shirasu K, Jones JDG (2018) A downy mildew effector evades recognition by polymorphism of expression and subcellular localization. Nature Communications doi: 10.1038/s41467-018-07469-3

Open Access

Shuta Asai from Jonathan Jones’ lab at The Sainsbury Lab, Norwich is the lead-author on this study that looks at co-evolution of host and pathogen resistance genes. The relationship between Hyaloperonospora arabidopsidis (Hpa) and Arabidopsis is defined by the gene-for-gene model of host Resistance (R) genes and pathogen Avirulence (AVR) genes. In this study the authors identify the HaRxL103Emoy2 AVR gene that is recognised by the R gene RPP4 and how this resistance is broken by altered expression or cellular localization.

Louveau T, Orme A, Pfalzgraf H, Stephenson M, Melton RE, Saalbach G, Hemmings  AM, Leveau A, Rejzek M, Vickerstaff RJ, Langdon T, Field R, Osbourn AE (2018) Analysis of two new arabinosyltransferases belonging to the carbohydrate-active enzyme (CAZY) glycosyl transferase family 1 provides insights into disease resistance and sugar donor specificity. Plant Cell. doi: 10.1105/tpc.18.00641

Open Access

This research from the John Innes Centre, East Maling and Aberystwyth University is led by Thomas Louveau and Anne Osbourn and characterises two new arabinosyltransferases from oat and soybean. These enzymes are involved in the production of saponins that are involved in defence responses. These enzymes normally transfer arabinose to their substrates but through targeted mutations the authors modified one of them to instead transfer glucose. This study provides insights into the specifics of ‘sugar-donation’ and has identified potential novel targets for manipulating defence responses in two crop species.

Soubeyrand E, Johnson TS, Latimer S, Block A, Kim J, Colquhoun TA, Butelli E,  Martin C, Wilson MA, Basset G (2018) The Peroxidative Cleavage of Kaempferol Contributes to the Biosynthesis of the Benzenoid Moiety of Ubiquinone in Plants. Plant Cell. 2018 Nov 14. pii: tpc.00688.2018. doi: 10.1105/tpc.18.00688

Open Access

This US-led study includes members of Cathie Martin’s lab at the John Innes Centre as co-authors in which they investigate the flavonoid-biosynthesis pathway, in particular the land-plant-specific synthesis of ubiquinone. They used Arabidopsis and tomato mutants to dissect the ubiquinone biosynthesis pathway, revealing that the B-ring of the specalised metabolite kaempferol is incorporated into the primary metabolite ubiquinone.

Bourdais G, McLachlan DH, Rickett LM, Zhou J, Siwoszek A, Häweker H, Hartley M, Kuhn H, Morris RJ, MacLean D, Robatzek S (2018) The use of quantitative imaging to investigate regulators of membrane trafficking in Arabidopsis stomatal closure. Traffic. doi: 10.1111/tra.12625

This work from both Norwich Research Park and the University of Bristol is led by Gildas Bourdais and describes a high-throughput quantitative imaging, reverse genetic screen to characterize known stomatal mutants on the basis of their effect on the endomembrane system. This screen allowed them to precisely define the point in the signaling pathway at which each mutant was affected, providing a genetic framework for the control of stomatal closure. This image-based tool should be a valuable addition to future studies that aim to use quantitative image analysis.

Catoni M, Jonesman T, Cerruti E, Paszkowski J (2018) Mobilization of Pack-CACTA transposons in Arabidopsis suggests the mechanism of gene shuffling (2018) Nucleic Acids Res. doi: 10.1093/nar/gky1196

Open Access

This work was performed at SLCU in Jerzy Paszkowski’s lab by current University of Birmingham lecturer Marco Catoni and analyses the genomic impact of the mobilisation of Pack-TYPE transposons. They track the movement of these transposons over multiple generations, showing that they can insert into genic regions and that their subsequent incomplete excisions can cause deleterious effect on gene function. Over evolutionary time the action of this type of mobile element might therefore importantly influence gene shuffling.

Shabek N, Ticchiarelli F, Mao H, Hinds TR, Leyser O, Zheng N (2018) Structural plasticity of D3-D14 ubiquitin ligase in strigolactone signalling. Nature. doi: 10.1038/s41586-018-0743-5

Nitzan Shabek is the lead author on his US-led paper that includes Fabrizio Ticchiarelli and Ottoline Leyser from SLCU as co-authors. This paper reveals the structure of the interaction between the Arabidopsis α/β hydrolase D14 and the D3 F-box protein, which is important for multiple aspects of strigolactone signaling. They show that structural plasticity of the D3 C-terminal α-helix, which can switch between two different forms, enables the interaction between D14 and the D53 repressor protein. Providing insight into these specific interactions is key to increasing understanding of how the D14-D3 complex influences strigolactone signaling.

Menard GN, Bryant FM, Kelly AA, Craddock CP, Lavagi I, Hassani-Pak K, Kurup S, Eastmond PJ (2018) Natural variation in acyl editing is a determinant of seed storage oil composition. Sci Rep. doi: 10.1038/s41598-018-35136-6

Open Access

This work is led from Rothamsted Research with Guillaume Menard as first author and uses the Arabidopsis MAGIC population to identify novel genetic loci involved in seed oil composition. They identified multiple QTLs associated with the quantity of the major very long chain fatty acid species 11-eicosenoic acid (20:1), showing that the enzyme LYSOPHOSPHATIDYLCHOLINE ACYLTRANSFERASE 2 (LPCAT2), which is involved in the acyl-editing pathway, was the primary QTL. Subsequently they show LPCAT2 expression was key for varying seed 20:1 content and that natural variation in the capacity for acyl editing is an important determinant of oil content.

Bozbuga R, Lilley CJ, Knox JP, Urwin PE (2018) Host-specific signatures of the cell  wall changes induced by the plant parasitic nematode, Meloidogyne incognita (2018). Sci  Rep. doi: 10.1038/s41598-018-35529-7

Open Access

Refik Bozbuga at the University of Leeds is first author on this study that investigates the cell wall composition of nutrient-supplying ‘giant cells’ that are induced in roots following infection with Meloidogyne spp nematodes. They analysed the cell walls of giant cells from three species (Arabidopsis, maize and aduki bean) as well as using a set of Arabidopsis mutants to characterise the possible cell wall components that might influence infection rates.

Mathers AW, Hepworth C, Baillie AL, Sloan J, Jones H, Lundgren M, Fleming AJ,  Mooney SJ, Sturrock CJ (2018) Investigating the microstructure of plant leaves in 3D with lab-based X-ray computed tomography. Plant Methods. doi:  10.1186/s13007-018-0367-7

Open Access
This paper from the Universities of Nottingham, Sheffield and Lancaster provides a methodology that uses a microCT image pipeline to measure leaf intercellular airspace and to provide quantitative data on descriptors of leaf cellular architecture. They measured 6 different plant species, showing that this 3D method generates an improved dataset when compared to traditional 2D methods of measurement.

GARNet Research Roundup: October 19th 2018

This edition of the GARNet research roundup includes six papers that look at different areas of plant biology. Firstly is a Belgian-led study with co-authors from Nottingham that introduces adaptive Xerobranching, a cereal-root response that can be mimicked in Arabidopsis by modulating ABA signaling. Second is study from Juriaan Ton’s lab in Sheffield that investigates the extent of DNA methylation during transgenerational acquired disease resistance. Third is paper from the John Innes Centre that places the DET1/COP1-PIF4 signaling module as a key determinant of the plants decision to allocate resources toward growth or defence.

The fourth paper is from Siobhan Braybrook’s (now ex-) lab at SLCU and provides an extensive dataset of the shape of leaf pavement cells across plant lineages. The penultimate paper is from a group at the University of Birmingham investigating the role of TOPII in the removal of damaging chromosome interlocks that occur during meiosis. The final paper returns to the ABA signalling with a study from Rothamsted Research that looks at the impact of the N-end rule on the different growth responses that occur during seed germination.

Orman-Ligeza B, Morris EC, Parizot B, Lavigne T, Babé A, Ligeza A, Klein S, Sturrock C, Xuan W, Novák O, Ljung K, Fernandez MA, Rodriguez PL, Dodd IC, De Smet I, Chaumont F, Batoko H, Périlleux C, Lynch JP, Bennett MJ, Beeckman T, Draye X (2018) The Xerobranching Response Represses Lateral Root Formation When Roots Are Not in Contact with Water. Current Biology. doi: 10.1016/j.cub.2018.07.074

Open Access

Emily Morris and Beata Orman-Ligeza are co-authors on this Belgian-led study that includes authors from the Universities of Nottingham and Lancaster. They introduce a new adaptive response termed xerobranching that defines the repression of root branching when a root tip is not in contact with wet soil. This response occurs in cereal roots but can be mimicked in Arabidopsis by treatment with ABA as the authors show that the response is dependent on the PYR/PYL/RCAR-dependent signaling pathway. This response allows roots to respond to the realistically varied microclimate encountered through the soil and offers another excellent example of how using both cereals and Arabidopsis can provide answers that would not be possible from a single experimental system.

Stassen JHM, López A, Jain R, Pascual-Pardo D, Luna E, Smith LM, Ton J (2018) The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis. Sci Rep. doi: 10.1038/s41598-018-32448-5

Open Access

Joost Stassen and Ana Lopez are the lead authors of this study from Juriaan Ton’s lab in Sheffield that continues their work on mechanisms that explain transgenerational acquired resistance (TAR). TAR occurs in the progeny of heavily diseased plants and in this study they investigate the extent of DNA methylation in generations following exposure to pathogens. They find that the extent of TAR-induced methylation was in direct proportion to the number of previous generations that had been exposed to disease. The majority of this methylation was in the CG context in gene bodies and clearly shows that methylation is an important component of molecular changes that occur during TAR.

Gangappa SN, Kumar SV (2018) DET1 and COP1 Modulate the Coordination of Growth and Immunity in Response to Key Seasonal Signals in Arabidopsis. Cell Rep. doi: 10.1016/j.celrep.2018.08.096

Open Access

Sreeramaiah Gangappa performed this work with Vinod Kumar at the John Innes Centre in which they investigate the molecular pathways that regulate the environmental signals that feed into the balance decision between growth and defense responses. They show that De-Etiolated 1 (DET1) and Constitutive Photomorphogenic 1 (COP1) negatively regulate immunity during favourable growth conditions and that this response is coordinated through the PIF4 transcription factor. These findings lead the authors to conclude that the DET1/COP1-PIF4 module is a key determinant of the different growth requirements that are necessary to response to either environment and disease.

Vőfély RV, Gallagher J, Pisano GD, Bartlett M, Braybrook SA (2018) Of puzzles and pavements: a quantitative exploration of leaf epidermal cell shape. New Phytol. doi: 10.1111/nph.15461

Open Access

Work from Siobhan Braybrook’s lab features in the Research Roundup for the second consecutive edition, this time led by Roza Vofely at the Sainsbury Lab Cambridge University (SLCU). In this study they have investigated the shape of leaf epidermal pavement cells from a remarkable 278 plant taxa in order to ascertain whether certain lineages are characterized by different cell shapes and whether the presence of an undulating cell wall is common, as in both maize and Arabidopsis. Interestingly they found that these primary examples were the exception as strongly undulating cell walls were unusual. They found that different lineages were characterised by similar levels of undulation and the authors conclude that this study sets a quantitative benchmark on which future experiments can be based that aim to understand the underlying factors that control pavement cell shape.

Martinez-Garcia M, Schubert V, Osman K, Darbyshire A, Sanchez-Moran E, Franklin FCH (2018) TOPII and chromosome movement help remove interlocks between entangled chromosomes during meiosis. J Cell Biol. doi: 10.1083/jcb.201803019

Open Access
Marina Martinez‐Garcia is the lead author on this work conducted during her time working with Eugenio Sanchez-Moran and Chris Franklin at the University of Birmingham. Normal meiosis requires a lack of structural interlocks between entangled chromosomes that can result from inevitable collisions in an area so packed with nucleic acid. In this paper the authors confirm a previously developed hypothesis that topoisomerase II (TOPII) is needed to remove interlocks. However it is not the only determinant of the number of interlocks as in Arabidopsis mutants in which chromosome movement is reduced, interlocks occur irrespective of the presence of TOPII.

Zhang H, Gannon L, Jones PD, Rundle CA, Hassall KL, Gibbs DJ, Holdsworth MJ, Theodoulou FL (2018) Genetic interactions between ABA signalling and the Arg/N-end rule pathway during Arabidopsis seedling establishment. Sci Rep. doi: 10.1038/s41598-018-33630-5

Open Access

Hongtao Zhang is the lead author of this work from the lab of Freddie Theodoulou at Rothamsted Research that investigates the role of the PROTEOLYSIS6 (PRT6) N-recognin E3 ligase in the ABA response. PRT6 regulated degradation of Group VII of the Ethylene Response Factor superfamily (ERFVIIs) controls both sugar sensitivity and oil body breakdown in germinating Arabidopsis seedlings. They found that the former but not the latter response was enhanced by ABA signaling components when the ERFVIIs were stabilised. The authors conclude that during seed germination the N-end rule controls multiple layers of regulation, both in an ABA dependent and independent manner

GARNet Research Roundup: July 27th

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Published on: July 26, 2018

This GARNet research roundup includes papers that feature a number of different research areas. Firstly is work from Glasgow that investigates the photoactivation of the UVR8 light receptor. Second is work from the University of Cambridge that links the activity of the BIG protein to the circadian oscillator. The next paper has co-authors from Cambridge and looks at promotor sequences needed for expression in bundle sheath cells. The fourth paper from the University of Leeds documents an important role for peroxisomes in the drought response whilst the final manuscript includes co-authors from the University of Birmingham and looks at the role of the ASYNAPTIC4 protein during meiosis.!divAbstract

Díaz-Ramos LA, O’Hara A, Kanagarajan S, Farkas D, Strid Å, Jenkins GI. Difference in the action spectra for UVR8 monomerisation and HY5 transcript accumulation in Arabidopsis (2018) Photochem Photobiol Sci. doi: 10.1039/c8pp00138c

Open Access

Aranzazu Díaz-Ramos and Andrew O’Hara are co-first authors on this research from the University of Glasgow that investigates the activation of photomorphogenic responses by the UVR8 photoreceptor. They show that two distinct UVR8 responses, either the monomerisation of UVR homodimers or accumulation of HY5 responsive transcripts, occurs at different wavelengths.

Hearn TJ, Marti MC, Abdul-Awal SM, Wimalasekera R, Stanton CR, Haydon MJ, Theodoulou FL, Hannah MA, Webb AA (2018) BIG regulates dynamic adjustment of circadian period in Arabidopsis thaliana. Plant Physiology pp.00571.2018. doi: 10.1104/pp.18.00571

Open Access

Timothy Hearn works with Alex Webb at the University of Cambridge and in this paper characterises how the multi-functional BIG protein impacts the circadian clock. This gene was isolated in a forward genetics screen to identify signaling components that alter the response to nicotinamide, which acts as a brake on the circadian oscillator. This finding allows the authors to better understand how altering the circadian oscillator can affect appropriate phasing during different environmental conditions.

Kirschner S, Woodfield H, Prusko K, Koczor M, Gowik U, Hibberd JM, Westhoff P. Expression of SULTR2;2 in the Arabidopsis bundle sheath and vein cells is mediated by a positive regulator. J Exp Bot. 2018 Jul 19. doi: 10.1093/jxb/ery263

Open Access

Sandra Kirschner is first author on this German-led study that includes Helen Woodfield (now Cardiff University) and Julian Hibberd (University of Cambridge). They are interested in the mechanisms that restrict gene expression to bundle sheath cells in C3 plants with a longer view of understanding the biology of these cells in C4 plants. They analyse the vascular-restricted SULTR2;2 promotor and identified a short region that is necessary for its expression pattern. Importantly they show that this sequence is evolutionarily conserved across Brassicaceae and a distantly related C4 plant.

Ebeed HT, Stevenson S, Cuming AC, Baker A. Conserved and differential transcriptional responses of peroxisome associated pathways to drought, dehydration and ABA. J Exp Bot. 2018 Jul 19. doi: 10.1093/jxb/ery266

Open Access

Heba Ebeed is the lead author of this work conducted in Alison Baker’s lab at the University of Leeds. They take a comparative genomics approach to investigate the expression of peroxisome-localised genes in a moss (physcomitrella), monocot (wheat) and a dicot (arabidopsis). They show that members of three gene families are upregulated in each of these organisms following drought stress, demonstrating the importance of peroxisomes in this environmental response throughout plant evolution.

Chambon A, West A, Vezon D, Horlow C, De Muyt A, Chelysheva L, Ronceret A, Darbyshire AR, Osman K, Heckmann S, Franklin FCH, Grelon M (2018) Identification of ASYNAPTIC4, a component of the meiotic chromosome axis. Plant Physiol. pii: pp.01725.2017. doi: 10.1104/pp.17.01725

Chris Franklin and Alice Darbyshire from the University of Birmingham are co-authors on this French-led study that looks into the role of the ASYNAPTIC4 (ASY4) protein in the control of synapsis formation during meiosis. Plants without ASY4 activity have defective chromosomal axis formation and cannot undergo synapsis. Although the initiation of recombination is unaffected in asy4 mutants, later processes are altered, demonstrating the key role for ASY4 during meiosis

GARNet Research Roundup: April 27th

This weeks GARNet research roundup features four papers that include Malcolm Bennett (University of Nottingham) as an author. The first three are linked manuscripts that investigate the role of auxin on root hair development that is controlled by varying phosphate levels. Ranjan Swarup provides an audio summary of two of these papers on the GARNet YouTube and podcast feeds.

The fourth paper from Nottingham is a collaboration with GARNet PI Jim Murray (Cardiff University) that characterises the STM gene network and its influence on meristem development.

The fifth paper from the lab of Paul Dupree in Cambridge characterises the stem transcriptome whilst the next paper from Iain Johnston and George Bassel (University of Birmingham) identifies a bet-hedging network that influences seed germination. The final paper features Seth Davies (University of York) as a co-author and investigates the impact of changes in circadian rhythms on short architecture.

Researchers at the University of Nottingham are involved in three back-to-back papers that add a mechanistic framework to the relationship between phosphate and auxin signaling in root hairs.

Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, Traini R, Truskina J, Leftley N, Hanlon M, Swarup K, Rashed A, Voß U, Alonso J, Stepanova A, Yun J, Ljung K, Brown KM, Lynch JP, Dolan L, Vernoux T, Bishopp A, Wells D, von Wirén N, Bennett MJ, Swarup R (2018) A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun. 9(1):1409. doi: 10.1038/s41467-018-03851-3

Open Access

The first paper is led by Ranjan Swarup and defines components of auxin biosynthetic, transport and signaling pathways that are involved in the change root hair development in response to different phosphate concentrations in Arabidopsis. Ranjan discusses this paper on YouTube.

Giri J, Bhosale R, Huang G, Pandey BK, Parker H, Zappala S, Yang J, Dievart A, Bureau C, Ljung K, Price A, Rose T, Larrieu A, Mairhofer S, Sturrock CJ, White P, Dupuy L, Hawkesford M, Perin C, Liang W, Peret B, Hodgman CT, Lynch J, Wissuwa M, Zhang D, Pridmore T, Mooney SJ, Guiderdoni E, Swarup R, Bennett MJ (2018). Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nat Commun. 9(1):1408. doi: 10.1038/s41467-018-03850-4

Open Access

This paper led by Malcolm Bennett uses a rice model to investigate the relationship between auxin and root hair elongation in response to low concentrations of phosphate. They show rice aux1 mutants have significant changes in root architecture.

Dindas J, Scherzer S, Roelfsema MRG, von Meyer K, Müller HM, Al-Rasheid KAS, Palme K, Dietrich P, Becker D, Bennett MJ, Hedrich R (2018) AUX1-mediated root hair auxin influx governs SCF(TIR1/AFB)-type Ca(2+) signaling. Nat Commun. 9(1):1174. doi: 10.1038/s41467-018-03582-5

Open Access

The third paper includes Malcolm Bennett as a co-author and investigates how the auxin transport and signaling pathways stimulate calcium signaling during root hair elongation.

Scofield S, Murison A, Jones A, Fozard J, Aida M, Band LR, Bennett M, Murray JAH (2018) Coordination of meristem and boundary functions by transcription factors in the SHOOT MERISTEMLESS regulatory network. Development pii: dev.157081. doi: 10.1242/dev.157081

Open Access
GARNet PI Jim Murray is the corresponding author on this manuscript that is led by Dr Simon Scofield and includes collaborators from the University of Nottingham. They have explored the gene regulatory network that is regulated by the key meristem identity gene SHOOT MERISTEMLESS (STM). This network includes an over-representation of transcription factor families, each of which have distinct roles in meristem development. They use in planta experimentation and in silico modeling to investigate the relationship between STM and CUC1 in more detail. Overall this study confirms that STM is a central regulator of shoot meristem function.

Faria-Blanc N, Mortimer JC, Dupree P (2018) A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis. Front Plant Sci. 9:384. doi: 10.3389/fpls.2018.00384

Open Access

Paul Dupree (University of Cambridge) is the corresponding author of this study that uses a range of Arabidopsis cell wall mutants to investigate the stem transcriptome. In plants with defects in xylan synthesis the authors found surprisingly few transcriptional changes. This indicates that once plants have committed to a terminal secondary cell wall program there is little need for transcriptional changes even after cell wall damage.

Johnston IG, Bassel GW (2018) Identification of a bet-hedging network motif generating noise in hormone concentrations and germination propensity in Arabidopsis. J R Soc Interface. 15(141). pii: 20180042. doi: 10.1098/rsif.2018.0042.

Open Access
Iain Johnston (University of Birmingham) leads this study that has identified a bet-hedging network that links hormone signaling during Arabidopsis germination. This type of network allows plants to more easily adapt to varying environmental conditions but can preclude maximum growth. In this system the network is based upon the regulation of ABA synthesis, activity and degradation, which is maintained at a constant mean level even though it exhibits significant noise. They investigate the parameters that might be tweaked to reduce variation in germination rate and therefore might be targets for modification in order to maximise responses under particular environmental conditions.

George Bassel who is a co-author on this paper will be speaking at the GARNet2018 Meeting in York in September.

Rubin MJ, Brock MT, Baker RL, Wilcox S, Anderson K, Davis SJ, Weinig C (2018) Circadian rhythms are associated with shoot architecture in natural settings. New Phytol. doi: 10.1111/nph.15162.

Seth Davies (University of York) is a co-author on this study that assesses the effect of circadian rhythms on aerial phenotypes that lead to fruit production in field grown Arabidopsis. This was assessed over two growing seasons and they show that variation in clock function significantly impacts shoot architecture.

Arabidopsis Research Roundup: December 8th.

This weeks Research Roundup begins with two papers from the University of Edinburgh on very different topics of Arabidopsis research. Firstly Alistair McCormick and Sofirtios Tsaftaris introduce a new low-cost phenotyping platform whilst Gerben Ooijen’s group has analysed the role of SUMOylation in the control of the circadian clock. The next three papers each involve wide UK collaborations and either look at plant nutrient composition (Nottingham, Dundee, York), the role of N-end rule pathway in the control of seed storage mobilisation (Rothamsted, Nottingham, Oxford, Birmingham, Cambridge) or the development of a new tool for the study of phloem sieve elements (Leeds, Rothamsted, Cambridge, Newcastle). The penultimate paper from Daniel Zilbermann (JIC) highlights the global mechanisms of methyltransferase function in Arabidopsis and mice whilst the final paper from Alexandre Ruban (QMUL) and co-authors continues his groups work to unpick the specifics of NPQ.

Dobrescu A, Scorza LCT, Tsaftaris SA, McCormick AJ (2017) A “Do-It-Yourself” phenotyping system: measuring growth and morphology throughout the diel cycle in rosette shaped plants. Plant Methods. doi: 10.1186/s13007-017-0247-6

Open Access

University of Edinburgh colleagues Alistair McCormick and Sofirtios Tsaftaris lead this work that presents a low cost phenotyping system for the analysis of the growth rate and phenotypic characteristics of Arabidopsis thaliana rosettes. The software that they have developed allows the accurate segmentation of multiple rosettes within a single image and overall offers a straightforward solution for automated phenotyping across a range of growth environments.

Hansen LL, van den Burg HA, van Ooijen G (2017) Sumoylation Contributes to Timekeeping and Temperature Compensation of the Plant Circadian Clock. J Biol Rhythms. doi: 10.1177/0748730417737633

Gerben van Ooijen (University of Edinburgh) is the corresponding author of this work that has identified SUMOylation as a novel mechanism of regulating circadian clock genes in Arabidopsis. Plants with defects in sumoylation have altered circadian periods that exhibit incorrect temperature compensation. Overall these results indicate that sumoylation importantly buffers clock function in response to changing temperatures.

Alcock TD, Havlickova L, He Z, Bancroft I, White PJ, Broadley MR, Graham NS (2017) Identification of Candidate Genes for Calcium and Magnesium Accumulation in Brassica napus L. by Association Genetics. Front Plant Sci. doi: 10.3389/fpls.2017.01968

Open Access

Neil Graham and Martin Broadley (University of Nottingham) are the corresponding authors of this study that has taken advantage of the Brassica napus Associative Transcriptomes RIPR diversity panel developed by Ian Bancroft’s lab in York. Novel loci involved with an altered response to calcium and magnesium were identified in B.napus before mineral composition was analysed in Arabidopsis mutants defective in orthologous genes. The analysed plants exhibited alteration in mineral composition, meaning that the associated Brassica loci might be targets for future breeding strategies aimed at improving plant nutrient compositions.

Zhang H, Gannon L, Hassall KL, Deery MJ, Gibbs DJ, Holdsworth MJ, van der Hoorn RAL, Lilley KS, Theodoulou FL (2017) N-terminomics reveals control of Arabidopsis seed storage proteins and proteases by the Arg/N-end rule pathway. New Phytol. doi: 10.1111/nph.14909

Freddie Theodoulou (Rothamsted Research) is the corresponding author of this research that involved a collaboration with colleagues in Cambridge, Birmingham, Nottingham and Oxford. They have performed a proteomic analysis on etiolated seedlings to identify those proteins designated for degradation by the N-end rule pathway. They analysed prt6 mutant plants that lack the function of the E3 ligase PROTEOLYSIS6 (PRT6) and discovered that N-terminal peptides from 45 protein groups were upregulated in this mutant, corresponding to the equivalent downregulation of several known N-end rule proteases. Overall the authors show that PRT6 plays an important role in the regulation of seed storage mobilisation in young seedlings and is therefore a possible future target to manipulate the plant responses to adverse environmental conditions. Dr Kirsty Hassall, a statistician at Rothamsted, is an author on this paper and in the latest edition of the GARNish newsletter explains how she interacts with plant scientists during her work.

Torode TA, O’Neill RE, Marcus SE, Cornuault V, Pose-Albacete S, Lauder RP, Kracun SK, Gro Rydahl M, Andersen MCF, Willats WGT, Braybrook SA, Townsend BJ, Clausen MH, Knox JP (2017) Branched pectic galactan in phloem-sieve-element cell walls: implications for cell mechanics. Plant Physiol. doi: 10.1104/pp.17.01568 Open Access

Paul Knox (University of Leeds) is the corresponding author of this study that includes contributions from researchers at SLCU, Newcastle and Rothamsted. This work is based around the development of a monoclonal antibody, LM26 that is able to recognize a β-1,6-galactosyl substitution of β-1,4-galactan. LM26 has allowed the identification of this unusual branched galactan that is specific to phloem elements and the authors hope that it can be a useful tool in future studies on the biology of phloem elements

Lyons DB, Zilberman D (2017) DDM1 and Lsh remodelers allow methylation of DNA wrapped in nucleosomes. Elife. doi: 10.7554/eLife.30674 Open Access

Daniel Zilberman has recently moved to the John Innes Centre and is the lead author of this work that was conducted when he was working in US. This research is a cross-kingdom analysis showing that nucleosome-free DNA is the preferred target for methyltransferases in both Arabidopsis and mice, and that nucleosomes appear to be a barrier to the function of these enzymes. Furthermore they demonstrate that linker-specific methylation that is usually absent in Arabidopsis can be introduced by removal of histone H1. This shows that flowering plants still possess this ability despite its loss, during the evolution of H1, over a billion years ago.

Tutkus M, Chmeliov J, Rutkauskas D, Ruban AV, Valkunas L (2017) Influence of the Carotenoid Composition on the Conformational Dynamics of Photosynthetic Light-Harvesting Complexes. J Phys Chem Lett. doi: 10.1021/acs.jpclett.7b02634

Alexandre Ruban (QMUL) is a co-author on this study that investigates the role that carotenoid composition plays in the control of Non-photochemical quenching (NPQ), a mechanism that protects the photosynthetic apparatus from light-damage. Arabidopsis mutants with differing carotenoid compositions were analysed for the dynamics of the conformation switches that occur during NPQ. Interestingly they show that LHCII has robust function  that is resistant to different carotenoid concentrations.

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