Dynamic growth QTL action in diverse light environments - characterization of light regime-specific and stable QTL in Arabidopsis.

Plant growth is a complex process affected by a multitude of genetic and environmental factors and their interactions. To identify genetic factors influencing plant performance under different environmental conditions, vegetative growth was assessed in Arabidopsis thaliana cultivated under constant or fluctuating light intensities, using high-throughput phenotyping and genome-wide association studies. Daily automated non-invasive phenotyping of a collection of 382 Arabidopsis accessions provided growth data during developmental progression under different light regimes at high temporal resolution. QTL for projected leaf area, relative growth rate and photosystem II operating efficiency detected under the two light regimes were predominantly condition-specific and displayed distinct temporal activity patterns, with active phases ranging from two to nine days. Eighteen protein coding genes and one miRNA gene were identified as potential candidate genes at ten QTL regions consistently found under both light regimes. Expression patterns of three candidate genes affecting projected leaf area were analysed in time-series experiments in accessions with contrasting vegetative leaf growth. These observations highlight the importance of considering both environmental and temporal patterns of QTL/allele actions and emphasize the need for detailed time-resolved analyses under diverse well-defined environmental conditions to effectively unravel the complex and stage-specific contributions of genes affecting plant growth processes.

[1]  P. Klein,et al.  Ethylene Response Factor109 Attunes Immunity, Photosynthesis, and Iron Homeostasis in Arabidopsis Leaves , 2022, Frontiers in Plant Science.

[2]  A. Fernie,et al.  Bringing more players into play: Leveraging stress in genome wide association studies. , 2022, Journal of plant physiology.

[3]  Jun Lim,et al.  SHORT-ROOT Controls Cell Elongation in the Etiolated Arabidopsis Hypocotyl , 2022, Molecules and cells.

[4]  Xin‐Jian He,et al.  Chromatin-remodeling complexes: conserved and plant-specific subunits in Arabidopsis. , 2021, Journal of integrative plant biology.

[5]  V. Sukhov,et al.  Analysis of chlorophyll fluorescence parameters as predictors of biomass accumulation and tolerance to heat and drought stress of wheat (Triticum aestivum) plants. , 2021, Functional plant biology : FPB.

[6]  A. Junker,et al.  Opportunities and limits of controlled-environment plant phenotyping for climate response traits , 2021, TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik.

[7]  R. L. Baker,et al.  Working with longitudinal data: quantifying developmental processes using function-valued trait modeling. , 2021, American journal of botany.

[8]  Hongliang Zhu,et al.  Roles of Plant Glycine-Rich RNA-Binding Proteins in Development and Stress Responses , 2021, International journal of molecular sciences.

[9]  S. Popescu,et al.  Unoccupied aerial systems discovered overlooked loci capturing the variation of entire growing period in maize , 2021, The plant genome.

[10]  G. Piro,et al.  Ride to cell wall: Arabidopsis XTH11, XTH29 and XTH33 exhibit different secretion pathways and responses to heat and drought stress , 2021, The Plant journal : for cell and molecular biology.

[11]  Rebecca A. Slattery,et al.  Perspectives on improving light distribution and light use efficiency in crop canopies. , 2021, Plant physiology.

[12]  Yusheng Zhao,et al.  Temporal dynamics of QTL effects on vegetative growth in Arabidopsis thaliana. , 2020, Journal of experimental botany.

[13]  S. Guerrier,et al.  Granger-causal testing for irregularly sampled time series with application to nitrogen signalling in Arabidopsis , 2020, bioRxiv.

[14]  W. Brüggemann,et al.  Special issue in honour of Prof. Reto J. Strasser - Comparative analysis of drought stress response of maize genotypes using chlorophyll fluorescence measurements and leaf relative water content , 2020, Photosynthetica.

[15]  Lijie Sun,et al.  Dissecting the genetic mechanisms of waterlogging tolerance in Brassica napus through linkage mapping and a genome-wide association study , 2020 .

[16]  D. Walther,et al.  Growth under Fluctuating Light Reveals Large Trait Variation in a Panel of Arabidopsis Accessions , 2020, Plants.

[17]  Ulrich Schurr,et al.  Phenotyping: New Windows into the Plant for Breeders. , 2020, Annual review of plant biology.

[18]  K. Neumann,et al.  Non-Invasive Phenotyping Reveals Genomic Regions Involved in Pre-Anthesis Drought Tolerance and Recovery in Spring Barley , 2019, Front. Plant Sci..

[19]  Ari Pekka Mähönen,et al.  Transcriptional regulatory framework for vascular cambium development in Arabidopsis roots , 2019, Nature Plants.

[20]  A. Millar,et al.  Biology and Function of miR159 in Plants , 2019, Plants.

[21]  A. Junker,et al.  Image-Derived Traits Related to Mid-Season Growth Performance of Maize Under Nitrogen and Water Stress , 2019, Front. Plant Sci..

[22]  R. Snowdon,et al.  Strong temporal dynamics of QTL action on plant growth progression revealed through high‐throughput phenotyping in canola , 2019, Plant biotechnology journal.

[23]  E. Filiz,et al.  FIT (Fer-like iron deficiency-induced transcription factor) in plant iron homeostasis: genome-wide identification and bioinformatics analyses , 2019, Journal of Plant Biochemistry and Biotechnology.

[24]  Simon C. Potter,et al.  The EMBL-EBI search and sequence analysis tools APIs in 2019 , 2019, Nucleic Acids Res..

[25]  T. Ravasi,et al.  Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change , 2019, Philosophical Transactions of the Royal Society B.

[26]  Jarno Vanhatalo,et al.  A Gaussian process model and Bayesian variable selection for mapping function-valued quantitative traits with incomplete phenotypic data , 2019, Bioinform..

[27]  Anthony M. Bolger,et al.  Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression1 , 2019, Plant Physiology.

[28]  X. Hou,et al.  Genome-wide analysis of heptahelical protein (HHP) gene family and expression of BcHHP1 in response to stresses in Brassica rapa , 2019, Biologia plantarum.

[29]  Z. Nikoloski,et al.  Genetic basis of plasticity in plants. , 2018, Journal of experimental botany.

[30]  George Wang,et al.  Image-based methods for phenotyping growth dynamics and fitness components in Arabidopsis thaliana , 2018, Plant Methods.

[31]  Z. Ren,et al.  Utilization of a Wheat55K SNP Array for Mapping of Major QTL for Temporal Expression of the Tiller Number , 2018, Front. Plant Sci..

[32]  Rea L. Antoniou-Kourounioti,et al.  Absence of warmth permits epigenetic memory of winter in Arabidopsis , 2018, Nature Communications.

[33]  Manisha Sharma,et al.  MITOGEN ACTIVATED PROTEIN KINASE: A VERSATILE SIGNALING CASCADE IN PLANTS , 2018 .

[34]  Xiangzong Meng,et al.  Plant cell surface receptor-mediated signaling – a common theme amid diversity , 2018, Journal of Cell Science.

[35]  J. Harbinson,et al.  Fluctuating Light Takes Crop Photosynthesis on a Rollercoaster Ride1[OPEN] , 2017, Plant Physiology.

[36]  J. Keilwagen,et al.  Genetic architecture and temporal patterns of biomass accumulation in spring barley revealed by image analysis , 2017, BMC Plant Biology.

[37]  A. Junker,et al.  Establishment of integrated protocols for automated high throughput kinetic chlorophyll fluorescence analyses , 2017, Plant Methods.

[38]  P. Hooykaas,et al.  An Arabidopsis mutant with high operating efficiency of Photosystem II and low chlorophyll fluorescence , 2017, Scientific Reports.

[39]  C. Gillmor,et al.  Convergent repression of miR156 by sugar and the CDK8 module of Arabidopsis Mediator. , 2017, Developmental biology.

[40]  Tracy Lawson,et al.  Importance of Fluctuations in Light on Plant Photosynthetic Acclimation1[CC-BY] , 2017, Plant Physiology.

[41]  T. Sun,et al.  Gibberellin Signaling Requires Chromatin Remodeler PICKLE to Promote Vegetative Growth and Phase Transitions1[OPEN] , 2017, Plant Physiology.

[42]  M. Logacheva,et al.  A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. , 2016, The Plant journal : for cell and molecular biology.

[43]  L. Willmitzer,et al.  A naturally occurring promoter polymorphism of the Arabidopsis FUM2 gene causes expression variation, and is associated with metabolic and growth traits. , 2016, The Plant journal : for cell and molecular biology.

[44]  Stephen P. Long,et al.  Improving photosynthesis and crop productivity by accelerating recovery from photoprotection , 2016, Science.

[45]  N. Provart,et al.  The Bio-Analytic Resource: Data visualization and analytic tools for multiple levels of plant biology , 2016 .

[46]  Hui Jiang,et al.  Time dependent genetic analysis links field and controlled environment phenotypes in the model C4 grass Setaria , 2016, bioRxiv.

[47]  Björn Usadel,et al.  Genetic architecture of plant stress resistance: multi‐trait genome‐wide association mapping , 2016, New Phytologist.

[48]  E. Kramer,et al.  Breaking the mold: understanding the evolution and development of lateral organs in diverse plant models. , 2016, Current opinion in genetics & development.

[49]  Karsten M. Borgwardt,et al.  1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana , 2016, Cell.

[50]  Mark G. M. Aarts,et al.  Phenomics for photosynthesis, growth and reflectance in Arabidopsis thaliana reveals circadian and long-term fluctuations in heritability , 2016, Plant Methods.

[51]  Zhiwu Zhang,et al.  Iterative Usage of Fixed and Random Effect Models for Powerful and Efficient Genome-Wide Association Studies , 2016, PLoS genetics.

[52]  C. Dean,et al.  RNA Binding Proteins RZ-1B and RZ-1C Play Critical Roles in Regulating Pre-mRNA Splicing and Gene Expression during Development in Arabidopsis , 2015, Plant Cell.

[53]  M. Sillanpää,et al.  Dynamic Quantitative Trait Locus Analysis of Plant Phenomic Data. , 2015, Trends in plant science.

[54]  Wen J. Li,et al.  Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation , 2015, Nucleic Acids Res..

[55]  Xavier Sirault,et al.  Improving photosynthesis and yield potential in cereal crops by targeted genetic manipulation: Prospects, progress and challenges , 2015 .

[56]  K. Broman,et al.  Mapping Quantitative Trait Loci Underlying Function-Valued Traits Using Functional Principal Component Analysis and Multi-Trait Mapping , 2015, G3: Genes, Genomes, Genetics.

[57]  Emily M. Strait,et al.  The arabidopsis information resource: Making and mining the “gold standard” annotated reference plant genome , 2015, Genesis.

[58]  Johanna A Bac-Molenaar,et al.  Genome-wide association mapping of growth dynamics detects time-specific and general quantitative trait loci , 2015, Journal of experimental botany.

[59]  Xiaodong Wang,et al.  Dynamic and comparative QTL analysis for plant height in different developmental stages of Brassica napus L. , 2015, Theoretical and Applied Genetics.

[60]  Mark G. M. Aarts,et al.  Natural Genetic Variation for Acclimation of Photosynthetic Light Use Efficiency to Growth Irradiance in Arabidopsis1[OPEN] , 2015, Plant Physiology.

[61]  Astrid Junker,et al.  Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems , 2015, Front. Plant Sci..

[62]  C. Xiang,et al.  Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation , 2014, Nature Communications.

[63]  J. Reif,et al.  Genetic dynamics underlying phenotypic development of biomass yield in triticale , 2014, BMC Genomics.

[64]  Christian Klukas,et al.  Integrated Analysis Platform: An Open-Source Information System for High-Throughput Plant Phenotyping1[C][W][OPEN] , 2014, Plant Physiology.

[65]  M. Livny,et al.  High-Throughput Computer Vision Introduces the Time Axis to a Quantitative Trait Map of a Plant Growth Response , 2013, Genetics.

[66]  Tomás C. Moyano,et al.  Integrated RNA-seq and sRNA-seq analysis identifies novel nitrate-responsive genes in Arabidopsis thaliana roots , 2013, BMC Genomics.

[67]  K. Geuten,et al.  Heterochronic genes in plant evolution and development , 2013, Front. Plant Sci..

[68]  A. Korte,et al.  The advantages and limitations of trait analysis with GWAS: a review , 2013, Plant Methods.

[69]  Lei Yang,et al.  miR172b Controls the Transition to Autotrophic Development Inhibited by ABA in Arabidopsis , 2013, PloS one.

[70]  B. Faircloth,et al.  Primer3—new capabilities and interfaces , 2012, Nucleic acids research.

[71]  Jian Ye,et al.  Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction , 2012, BMC Bioinformatics.

[72]  Dirk Inzé,et al.  Leaf size control: complex coordination of cell division and expansion. , 2012, Trends in plant science.

[73]  Willem Kruijer,et al.  High throughput screening with chlorophyll fluorescence imaging and its use in crop improvement. , 2012, Current opinion in biotechnology.

[74]  Lindsay A. Turnbull,et al.  How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists , 2012 .

[75]  O. Loudet,et al.  Disentangling the Intertwined Genetic Bases of Root and Shoot Growth in Arabidopsis , 2012, PloS one.

[76]  W. Schröder,et al.  Arabidopsis plants grown in the field and climate chambers significantly differ in leaf morphology and photosystem components , 2012, BMC Plant Biology.

[77]  J. Borevitz,et al.  Natural Genetic Variation for Growth and Development Revealed by High-Throughput Phenotyping in Arabidopsis thaliana , 2012, G3: Genes | Genomes | Genetics.

[78]  A. Auton,et al.  Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel , 2011, Nature Genetics.

[79]  S. Sultan,et al.  The role of developmental plasticity in evolutionary innovation , 2011, Proceedings of the Royal Society B: Biological Sciences.

[80]  R. Pierik,et al.  Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. , 2011, The Plant journal : for cell and molecular biology.

[81]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[82]  R. Henry,et al.  Chloroplast genome sequences from total DNA for plant identification. , 2011, Plant biotechnology journal.

[83]  E. Finnegan,et al.  Plant phenotypic plasticity in a changing climate. , 2010, Trends in plant science.

[84]  Lonnie R. Welch,et al.  AGRIS: the Arabidopsis Gene Regulatory Information Server, an update , 2010, Nucleic Acids Res..

[85]  J. Y. Kim,et al.  Comparative analysis of Arabidopsis zinc finger-containing glycine-rich RNA-binding proteins during cold adaptation. , 2010, Plant physiology and biochemistry : PPB.

[86]  K. Nishitani,et al.  Light Quality-Mediated Petiole Elongation in Arabidopsis during Shade Avoidance Involves Cell Wall Modification by Xyloglucan Endotransglucosylase/Hydrolases1[C][W][OA] , 2010, Plant Physiology.

[87]  Matthias Meyer,et al.  Illumina sequencing library preparation for highly multiplexed target capture and sequencing. , 2010, Cold Spring Harbor protocols.

[88]  L. Janss,et al.  Bayesian multi-QTL mapping for growth curve parameters , 2010, BMC proceedings.

[89]  Lei Li,et al.  Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression , 2010, Proceedings of the National Academy of Sciences.

[90]  H. Scharr,et al.  Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. , 2009, Functional plant biology : FPB.

[91]  Detlef Weigel,et al.  The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis , 2009, Cell.

[92]  Detlef Weigel,et al.  SHOREmap: simultaneous mapping and mutation identification by deep sequencing , 2009, Nature Methods.

[93]  M. Bänziger,et al.  Drought stress and tropical maize: QTL-by-environment interactions and stability of QTLs across environments for yield components and secondary traits , 2009, Theoretical and Applied Genetics.

[94]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[95]  B. Cairns,et al.  The biology of chromatin remodeling complexes. , 2009, Annual review of biochemistry.

[96]  Hailing Jin,et al.  An Effector of RNA-Directed DNA Methylation in Arabidopsis Is an ARGONAUTE 4- and RNA-Binding Protein , 2009, Cell.

[97]  E. Blum,et al.  A Protracted and Dynamic Maturation Schedule Underlies Arabidopsis Leaf Development[W] , 2008, The Plant Cell Online.

[98]  R. Jetter,et al.  Identification of the Wax Ester Synthase/Acyl-Coenzyme A:Diacylglycerol Acyltransferase WSD1 Required for Stem Wax Ester Biosynthesis in Arabidopsis12[W][OA] , 2008, Plant Physiology.

[99]  A. Orellana,et al.  Golgi transporters: opening the gate to cell wall polysaccharide biosynthesis. , 2008, Current opinion in plant biology.

[100]  Zhang-liang Chen,et al.  A gain-of-function mutation of transcriptional factor PTL results in curly leaves, dwarfism and male sterility by affecting auxin homeostasis , 2008, Plant Molecular Biology.

[101]  O. Fiehn,et al.  Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations , 2007, The Plant journal : for cell and molecular biology.

[102]  E. F. Walton,et al.  Plant Methods Protocol: a Highly Sensitive Rt-pcr Method for Detection and Quantification of Micrornas , 2022 .

[103]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[104]  Karine Chenu,et al.  Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. , 2007, Annals of botany.

[105]  Sarah Hake,et al.  The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA , 2007, Nature Genetics.

[106]  R. Wu,et al.  Functional mapping — how to map and study the genetic architecture of dynamic complex traits , 2006, Nature Reviews Genetics.

[107]  H. Goodman,et al.  A novel gene family in Arabidopsis encoding putative heptahelical transmembrane proteins homologous to human adiponectin receptors and progestin receptors. , 2005 .

[108]  R. Deal,et al.  Nuclear Actin-Related Proteins as Epigenetic Regulators of Development1 , 2005, Plant Physiology.

[109]  M. Stitt,et al.  Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis1[w] , 2005, Plant Physiology.

[110]  Mark G. M. Aarts,et al.  Altered photosynthetic performance of a natural Arabidopsis accession is associated with atrazine resistance. , 2005, Journal of experimental botany.

[111]  Joachim Selbig,et al.  A Robot-Based Platform to Measure Multiple Enzyme Activities in Arabidopsis Using a Set of Cycling Assays: Comparison of Changes of Enzyme Activities and Transcript Levels during Diurnal Cycles and in Prolonged Darknessw⃞ , 2004, The Plant Cell Online.

[112]  M. Guerinot,et al.  The Essential Basic Helix-Loop-Helix Protein FIT1 Is Required for the Iron Deficiency Response , 2004, The Plant Cell Online.

[113]  Bernd Weisshaar,et al.  FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana , 2004, FEBS letters.

[114]  F. Cellier,et al.  Characterization of AtCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis. , 2004, The Plant journal : for cell and molecular biology.

[115]  Dick Vreugdenhil,et al.  Quantitative Trait Locus Analysis of Growth-Related Traits in a New Arabidopsis Recombinant Inbred Population1 , 2004, Plant Physiology.

[116]  Thomas Altmann,et al.  Heterosis of Biomass Production in Arabidopsis. Establishment during Early Development1 , 2004, Plant Physiology.

[117]  R. Poethig,et al.  The Arabidopsis Heterochronic Gene ZIPPY Is an ARGONAUTE Family Member , 2003, Current Biology.

[118]  E. Coen,et al.  Genetic Control of Surface Curvature , 2003, Science.

[119]  Wilhelm Gruissem,et al.  Cell Cycle-regulated Gene Expression inArabidopsis * , 2002, The Journal of Biological Chemistry.

[120]  Detlef Weigel,et al.  Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana. , 2002, Genetics.

[121]  M. Pfaffl,et al.  A new mathematical model for relative quantification in real-time RT-PCR. , 2001, Nucleic acids research.

[122]  D. Leister,et al.  Identification of Photosynthetic Mutants of Arabidopsis by Automatic Screening for Altered Effective Quantum Yield of Photosystem 2 , 2000, Photosynthetica.

[123]  S. Sultan Phenotypic plasticity for plant development, function and life history. , 2000, Trends in plant science.

[124]  Fabio Cavallini,et al.  Fitting a Logistic Curve to Data , 1993 .

[125]  R. Chazdon,et al.  The Importance of Sunflecks for Forest Understory Plants Photosynthetic machinery appears adapted to brief, unpredictable periods of radiation , 1991 .

[126]  J. Leemans,et al.  Engineering herbicide resistance in plants. , 1988, Trends in genetics : TIG.

[127]  J. Hirschberg,et al.  Molecular Basis of Herbicide Resistance in Amaranthus hybridus , 1983, Science.

[128]  J. Tukey Comparing individual means in the analysis of variance. , 1949, Biometrics.

[129]  A. Junker,et al.  Genetic variation of growth dynamics in maize (Zea mays L.) revealed through automated non‐invasive phenotyping , 2017, The Plant journal : for cell and molecular biology.

[130]  Johanna A Bac-Molenaar,et al.  Genome-wide association mapping of time-dependent growth responses to moderate drought stress in Arabidopsis. , 2016, Plant, cell & environment.

[131]  Thomas R. Gingeras,et al.  STAR: ultrafast universal RNA-seq aligner , 2013, Bioinform..

[132]  Connor W. McEntee,et al.  The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. , 2007, Cold Spring Harbor symposia on quantitative biology.

[133]  J. Leipner,et al.  The Application of Chlorophyll Fluorescence to Study Light, Temperature, and Drought Stress , 2003 .