Arabidopsis phenotyping through geometric morphometrics

Abstract Background Recently, great technical progress has been achieved in the field of plant phenotyping. High-throughput platforms and the development of improved algorithms for rosette image segmentation make it possible to extract shape and size parameters for genetic, physiological, and environmental studies on a large scale. The development of low-cost phenotyping platforms and freeware resources make it possible to widely expand phenotypic analysis tools for Arabidopsis. However, objective descriptors of shape parameters that could be used independently of the platform and segmentation software used are still lacking, and shape descriptions still rely on ad hoc or even contradictory descriptors, which could make comparisons difficult and perhaps inaccurate. Modern geometric morphometrics is a family of methods in quantitative biology proposed to be the main source of data and analytical tools in the emerging field of phenomics studies. Based on the location of landmarks (corresponding points) over imaged specimens and by combining geometry, multivariate analysis, and powerful statistical techniques, these tools offer the possibility to reproducibly and accurately account for shape variations among groups and measure them in shape distance units. Results Here, a particular scheme of landmark placement on Arabidopsis rosette images is proposed to study shape variation in viral infection processes. Shape differences between controls and infected plants are quantified throughout the infectious process and visualized. Quantitative comparisons between two unrelated ssRNA+ viruses are shown, and reproducibility issues are assessed. Conclusions Combined with the newest automated platforms and plant segmentation procedures, geometric morphometric tools could boost phenotypic features extraction and processing in an objective, reproducible manner.

[1]  D. Chitwood,et al.  Climate and Developmental Plasticity: Interannual Variability in Grapevine Leaf Morphology1[OPEN] , 2016, Plant Physiology.

[2]  A. Meyer,et al.  SHAPE ANALYSIS OF SYMMETRIC STRUCTURES: QUANTIFYING VARIATION AMONG INDIVIDUALS AND ASYMMETRY , 2002, Evolution; international journal of organic evolution.

[3]  D. Inzé,et al.  Cell to whole-plant phenotyping: the best is yet to come. , 2013, Trends in plant science.

[4]  Christian Peter Klingenberg,et al.  Visualizations in geometric morphometrics: How to read and how to make graphs showing shape changes , 2013 .

[5]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[6]  Ø. Hammer,et al.  PAST: PALEONTOLOGICAL STATISTICAL SOFTWARE PACKAGE FOR EDUCATION AND DATA ANALYSIS , 2001 .

[7]  Fred L Bookstein,et al.  A method of factor analysis for shape coordinates. , 2017, American journal of physical anthropology.

[8]  R. Froissart,et al.  Reduction of leaf area and symptom severity as proxies of disease-induced plant mortality: the example of the Cauliflower mosaic virus infecting two Brassicaceae hosts. , 2013, Virus research.

[9]  APPLICATION OF GEOMETRIC MORPHOMETRTCS TO THE STUDY OF POSTNATAL SIZE AND SHAPE CHANGES IN THE SKULL OF Calomys expdsus , 2004 .

[10]  Dean C. Adams,et al.  A General Framework for the Analysis of Phenotypic Trajectories in Evolutionary Studies , 2009, Evolution; international journal of organic evolution.

[11]  Alan P. Gay,et al.  Objective Definition of Rosette Shape Variation Using a Combined Computer Vision and Data Mining Approach , 2014, PloS one.

[12]  Jennifer L. Nemhauser,et al.  In: The Arabidopsis Book , 2002 .

[13]  T. Garland,et al.  Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus , 2003, Journal of evolutionary biology.

[14]  C. Manacorda,et al.  Differential mRNA Accumulation upon Early Arabidopsis thaliana Infection with ORMV and TMV-Cg Is Associated with Distinct Endogenous Small RNAs Level , 2015, PloS one.

[15]  L. F. Marcus,et al.  Advances in Morphometrics , 1996, NATO ASI Series.

[16]  P. Laufs,et al.  The Balance between the MIR164A and CUC2 Genes Controls Leaf Margin Serration in Arabidopsis[W] , 2006, The Plant Cell Online.

[17]  Guillaume Lobet,et al.  Image Analysis in Plant Sciences: Publish Then Perish. , 2017, Trends in plant science.

[18]  Cris Kuhlemeier,et al.  Leaf Asymmetry as a Developmental Constraint Imposed by Auxin-Dependent Phyllotactic Patterning[OA] , 2012, Plant Cell.

[19]  No functional sexual dimorphism in Minorcan horse assessed by geometric morphometric methods , 2015 .

[20]  C. Klingenberg Size, shape, and form: concepts of allometry in geometric morphometrics , 2016, Development Genes and Evolution.

[21]  W. Barker Ontogeny and phylogeny. , 1980, Archives of surgery.

[22]  M. Pigliucci Phenotypic integration: studying the ecology and evolution of complex phenotypes , 2003 .

[23]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[24]  H. David Sheets,et al.  Geometric morphometrics for biologists : a primer , 2004 .

[25]  V. Viscosi Geometric morphometrics and leaf phenotypic plasticity: assessing fluctuating asymmetry and allometry in European white oaks (Quercus) , 2015 .

[26]  F. Bookstein Combining the Tools of Geometric Morphometrics , 1996 .

[27]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[28]  Malia A. Gehan,et al.  Lights, camera, action: high-throughput plant phenotyping is ready for a close-up. , 2015, Current opinion in plant biology.

[29]  S. Gould ALLOMETRY AND SIZE IN ONTOGENY AND PHYLOGENY , 1966, Biological reviews of the Cambridge Philosophical Society.

[30]  Christian Peter Klingenberg,et al.  Phenotypic plasticity in response to environmental heterogeneity contributes to fluctuating asymmetry in plants: first empirical evidence , 2018, Journal of evolutionary biology.

[31]  F. Ponz,et al.  Infectivity of turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopsis thaliana and local lesion hosts. , 1998, Virus research.

[32]  Chi-Ren Shyu,et al.  PhenoPhyte: a flexible affordable method to quantify 2D phenotypes from imagery , 2012, Plant Methods.

[33]  S. Vadlamani On the Diffusion of Shape , 2007 .

[34]  Kate E. Jones,et al.  Geometric Morphometric Approaches to Acoustic Signal Analysis in Mammalian Biology , 2013 .

[35]  Yuhua Jiao,et al.  Functional approach to high-throughput plant growth analysis , 2013, BMC Systems Biology.

[36]  Brad M. Binder,et al.  Reshaping Plant Biology: Qualitative and Quantitative Descriptors for Plant Morphology , 2017, Front. Plant Sci..

[37]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[38]  M. Stitt,et al.  Phytotyping(4D) : a light-field imaging system for non-invasive and accurate monitoring of spatio-temporal plant growth. , 2015, The Plant journal : for cell and molecular biology.

[39]  F. Bookstein,et al.  Morphometric Tools for Landmark Data: Geometry and Biology , 1999 .

[40]  C. Klingenberg MorphoJ: an integrated software package for geometric morphometrics , 2011, Molecular ecology resources.

[41]  C. Goodall Procrustes methods in the statistical analysis of shape , 1991 .

[42]  Vincent A. Ricigliano,et al.  Geometric morphometrics reveals shifts in flower shape symmetry and size following gene knockdown of CYCLOIDEA and ANTHOCYANIDIN SYNTHASE , 2017, BMC Plant Biology.

[43]  S. Punyasena,et al.  Bioinformatic and biometric methods in plant morphology1 , 2014, Applications in Plant Sciences.

[44]  F. Rohlf,et al.  A revolution morphometrics. , 1993, Trends in ecology & evolution.

[45]  M. Pigliucci Studying the plasticity of phenotypic integration in a model organism , 2004 .

[46]  Dirk Inzé,et al.  A Journey Through a Leaf: Phenomics Analysis of Leaf Growth in Arabidopsis thaliana , 2015, The arabidopsis book.

[47]  Ruth G. Shaw,et al.  Anova for Unbalanced Data: An Overview , 1993 .

[48]  Christian Peter Klingenberg,et al.  Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications , 2015, Symmetry.

[49]  Andrea Cardini,et al.  Leaf Morphology, Taxonomy and Geometric Morphometrics: A Simplified Protocol for Beginners , 2011, PloS one.

[50]  How many specimens do I need? Sampling error in geometric morphometrics: testing the sensitivity of means and variances in simple randomized selection experiments , 2015, Zoomorphology.

[51]  J. Mensch,et al.  Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation , 2011, BMC Developmental Biology.

[52]  F. Ponz,et al.  Nucleotide sequence of Chinese rape mosaic virus (oilseed rape mosaic virus), a crucifer tobamovirus infectious on Arabidopsis thaliana , 2004, Plant Molecular Biology.

[53]  SPATIOTEMPORAL REORGANIZATION OF GROWTH RATES IN THE EVOLUTION OF ONTOGENY , 2000, Evolution; international journal of organic evolution.

[54]  C. Klingenberg,et al.  Geometric morphometrics of corolla shape: dissecting components of symmetric and asymmetric variation in Erysimum mediohispanicum (Brassicaceae). , 2012, The New phytologist.

[55]  B. Sidlauskas Continuous and Arrested Morphological Diversification in Sister Clades of Characiform Fishes: A Phylomorphospace Approach , 2008, Evolution; international journal of organic evolution.

[56]  P. Prusinkiewicz,et al.  Model for the regulation of Arabidopsis thaliana leaf margin development , 2011, Proceedings of the National Academy of Sciences.

[57]  Charles Oxnard,et al.  Biology Clearly Needs Morphometrics. Does Morphometrics Need Biology? , 2009 .

[58]  Michael S. Engel,et al.  A new interpretation of the bee fossil Melitta willardi Cockerell (Hymenoptera, Melittidae) based on geometric morphometrics of the wing , 2014, ZooKeys.

[59]  Igor Grigoriev,et al.  A segmentation procedure using colour features applied to images of Arabidopsis thaliana. , 2013, Functional plant biology : FPB.

[60]  A. Evin,et al.  Geometric morphometric analysis of grain shape and the identification of two-rowed barley (Hordeum vulgare subsp. distichum L.) in southern France , 2014 .

[61]  Wilfrid S. Kendall,et al.  Alignments in two-dimensional random sets of points , 1980, Advances in Applied Probability.

[62]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[63]  Alexander G. Fletcher,et al.  Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences , 2017, bioRxiv.

[64]  F L Bookstein,et al.  Biometrics, biomathematics and the morphometric synthesis. , 1996, Bulletin of mathematical biology.

[65]  Cédric Gaucherel,et al.  Momocs: Outline Analysis Using R , 2014 .

[66]  S. Elena,et al.  Viral Strain-Specific Differential Alterations in Arabidopsis Developmental Patterns. , 2015, Molecular plant-microbe interactions : MPMI.

[67]  R. Hull,et al.  Matthews' plant virology , 2002 .

[68]  J. Krieger,et al.  Controlling for Curvature in the Quantification of Leaf Form , 2010 .

[69]  J. T. Matus,et al.  Arabidopsis paves the way: genomic and network analyses in crops. , 2011, Current opinion in biotechnology.

[70]  F. James Rohlf,et al.  The tps series of software , 2015 .

[71]  A. Galston Plant Physiology , 1967, Nature.

[72]  Thierry Candresse,et al.  Top 10 plant viruses in molecular plant pathology. , 2011, Molecular plant pathology.

[73]  A. Cardini Missing the third dimension in geometric morphometrics: how to assess if 2D images really are a good proxy for 3D structures? , 2014 .

[74]  C. Klingenberg,et al.  PART OF A SPECIAL ISSUE ON DEVELOPMENTAL ROBUSTNESS AND SPECIES DIVERSITY The role of pollinators in the evolution of corolla shape variation, disparity and integration in a highly diversified plant family with a conserved floral bauplan , 2016 .

[75]  F. Rohlf,et al.  Geometric morphometrics: Ten years of progress following the ‘revolution’ , 2004 .

[76]  W. Philips,et al.  Rosette Tracker: An Open Source Image Analysis Tool for Automatic Quantification of Genotype Effects1[C][W] , 2012, Plant Physiology.

[77]  M. Benton,et al.  Trends in Ecology & Evolution , 2019 .

[78]  J. Claude,et al.  Log-Shape Ratios, Procrustes Superimposition, Elliptic Fourier Analysis: Three Worked Examples in R , 2013 .

[79]  C. Manacorda,et al.  Salicylic acid determines differential senescence produced by two Turnip mosaic virus strains involving reactive oxygen species and early transcriptomic changes. , 2013, Molecular plant-microbe interactions : MPMI.

[80]  Arezki Boudaoud,et al.  Multiscale quantification of morphodynamics: MorphoLeaf software for 2D shape analysis , 2016, Development.

[81]  Elizabeth A. Kellogg,et al.  High-throughput phenotyping. , 2017, American journal of botany.

[82]  C. Granier,et al.  Phenotyping and beyond: modelling the relationships between traits. , 2014, Current opinion in plant biology.

[83]  Daniel W. McShea,et al.  Detecting changes in morphospace occupation patterns in the fossil record: characterization and analysis of measures of disparity , 2001, Paleobiology.

[84]  M. Bai,et al.  Evolutionary Constraints in Hind Wing Shape in Chinese Dung Beetles (Coleoptera: Scarabaeinae) , 2011, PloS one.

[85]  Patrick Laufs,et al.  Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis , 2007, Development.

[86]  D'arcy W. Thompson,et al.  On Growth and Form , 1917, Nature.

[87]  Paolo Remagnino,et al.  Plant species identification using digital morphometrics: A review , 2012, Expert Syst. Appl..