turning a new leaf with persistent homology: old and new ways of analyzing leaf shape and the...

Quantifying Phenotypic Variation in Tomato Introgression Lines through Local Persistent Homology

Turning a new leaf with persistent homology:old and new waysof analyzing leaf shape and the topology of plantsDan ChitwoodDonald Danforth Plant Science CenterNovember 4, 2016

Does leaf shape contain information?

If so, what do leaves tell us and how do we measure leaf shape?

A primer on leaf shape and past morphometric methods







Chitwood & Sinha, 2016Leaf shape varies byevolution, genetics, development andby present climates & ancient climates

Leaf shape varies byevolution, genetics, development andby present climates & ancient climatesChitwood & Sinha, 2016

Paleomap, scotese.com

Leaf shape varies byevolution, genetics, development andby present climates & ancient climatesChitwood & Sinha, 2016

There are many ways to measure shape:Pseudo-landmarks

Chitwood & Sinha, 2016

There are many ways to measure shape:Elliptical Fourier Descriptors


There are many ways to measure shape:Homologous landmarks


There are many ways to measure shape:All methods are comprehensive,but theyre not equivalent

LandmarksElliptical Fourier DescriptorsChitwood & Sinha, 2016

Grapevine: discriminatinggenetic, developmental, and environmental shapesExamples of old and new morphometric methods for plants

Persistent homology: a topology based morphometric methodLeaf morphospaces & a universal theory of plant morphology

Landmark-based Procrustes analysis:Superimposed homologous coordinates


Kerschbaumer and Sturmbauer (2011)International Journal of Evol. Biol.



Translate



TranslateScale



TranslateScaleRotate

Homologous landmarks:On every grape leaf






Homologous landmarks:Species differences

ShootbaseShoottipLeaf numberDevelopmental stageUnequal expansionDifferent leaf typesHomologous landmarks:Species differences manifest in adevelopmental context

ShootbaseShoottipLeaf numberDevelopmental stageUnequal expansionDifferent leaf types

Homologous landmarks:Species differences manifest in adevelopmental context

ShootbaseShoottipLeaf numberDevelopmental stageUnequal expansionDifferent leaf typesHomologous landmarks:Species differences manifest in adevelopmental context

Evolutionary vs. developmental pathsin the leaf morphospace

Species effectsChitwood et al., New Phytol, 2016

Evolutionary vs. developmental pathsin the leaf morphospace

Developmental effectsChitwood et al., New Phytol, 2016

Species can be predictedindependently from development

Chitwood et al., New Phytol, 2016

Development can be predictedindependently from species

Chitwood et al., New Phytol, 2016

Vein landmarks more sensitive to development

Chitwood et al., Plant Physiol, 2016

Vein landmarks more sensitive to development


Discriminating leaves from different years:Same vines, same developmental stagesChitwood et al., Plant Physiol, 2016

Discriminating leaves from different years:Same vines, same developmental stagesChitwood et al., Plant Physiol, 2016

Climate interannual variability:2014/15 was colder & drier than 2012/13


Climate interannual variability:2014/15 was colder & drier than 2012/13Chitwood et al., Plant Physiol, 2016

Climate interannual variability:Plasticity and evolutionary changes in leaf shape go in the same direction?


Measuring future climates:To California, wine grapes, and rootstocks!

The Vitis Underground:Adapting perennial crops for climate change:Graft transmissible effects of rootstocks on grapevine shoots

Allison Miller, Saint Louis UniversityJason Londo, USDA-ARS, Geneva, NYAnne Fennel, South Dakota State UniversityMisha Kwasinewski, MizzouLaszlo Kovacs, Missouri State UniversityPeter Cousins, E&J Gallo Winery



These slides made by:Mao LiDonald Danforth Plant Science CenterChitwood Lab & Topp LabPersistent homology: a tool to universally measureplant morphologies across organs and scales

These slides made by:Mao LiDonald Danforth Plant Science CenterChitwood Lab & Topp Lab

Persistent homology: a tool to universally measureplant morphologies across organs and scales





Verri et al. Biological Cybernetics, 1993Carlsson, Bulletin AMS, 2009Edelsbrunner et al., AMS, 2010Persistent Homology, WHY? WHAT?How many groups are there? 3? 10? 1?

rVerri et al. Biological Cybernetics, 1993Carlsson, Bulletin AMS, 2009Edelsbrunner et al., AMS, 2010Persistent Homology, WHY? WHAT?

How many groups are there? 3? 10? 1?

r

Verri et al. Biological Cybernetics, 1993Carlsson, Bulletin AMS, 2009Edelsbrunner et al., AMS, 2010Persistent Homology, WHY? WHAT?


r




How many groups are there? 3? 10? 1?It depends on scale!


Another example

Sublevel Set Filtration:

Blue RedA Persistent Homology Primer How to get a nest sequence of shapes













Superlevel Set Filtration:

Red BlueA Persistent Homology Primer How to get a nest sequence of shapes











rPersistent Homology, HOW?

Persistence Barcode

65


Persistence Barcode

66


Persistence Barcode

67


Persistence Barcode

68


Persistence Barcode

69


Persistence Barcode

# connected componentsr

70


Persistence Barcode

# connected componentsrNow, apply!

71

tomato introgression linesEshed et al. , Genetic, 1999Chitwood et al., The Plant Cell 2013

(domesticated, cv. M82)(wild)

IL4_3Significant difference is caused by the gene in the small regionThe difference is usually subtle

MeasureLeaf Shape

16 annulus (rings)density estimatorA tool: Local and smoothside view

Blind to size, position, and orientation

A robust metric between barcodes: bottleneck distanceplane height(level value)

connected component


connected component


connected component


connected component


connected component


connected component


connected component


connected component


connected component


connected component


connected component

CV1 Our approach integrates very different morphological characteristics into a single descriptor.Leaf Shape QTLStatistical techniques: Multidimensional scaling (MDS, reduce dimension) Canonical variate analysis (CVA, feature that most distinguish groups)

ResultLeaf Shape QTL

Measure Serrations

Coarse approximationElliptical Fourier Transformhttp://haitham.ece.illinois.edu

First harmonics5 harmonics10 harmonics20 harmonics

Euler characteristics = # connected component - # loopslevel

90

Euler characteristics = # connected component - # loopslevel

91

Leaf Serrations QTL

level

ResultLeaf Serrations QTL

MeasureRoot Architecture

Root Architecture QTL

ResultRoot Architecture QTL

Persistent homology detects concerted changes in shoot and root architecture

Leaf Shape Root Architecture Serrations

Persistent homology detects concerted changes in shoot and root architecturemedian values plots

Persistent Homologyrobust to noise invariant with respect to orientation capable of application across diverse scales compatible with diverse functions to quantify disparate plant morphologies, architectures, and textures



2,3929,6194,76534,6372,88517,8598655,7333,30186684,8595,8142,422

176,017 leaves!Demarcating aleaf morphospace

2,3929,6194,76534,6372,88517,8598655,7333,30186684,8595,8142,422

176,017 leaves!Demarcating aleaf morphospace

Discriminating leaves:Across flowering plant families

Discriminating leaves:Across sites around the world

Transect and Leafsnap dataTransect dataDana Royer, Wesleyan UniversityDaniel Peppe, Baylor UniversityPeter Wilf, Penn StateHuff PM, Wilf P, Azumah EJ. 2003. Digital future for paleoclimate estimation from fossil leaves? Preliminary results. Palaios 18: 266-274.

Royer DL, Wilf P, Janesko DA, Kowalski EA, Dilcher DL. 2005. Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. American Journal of Botany 92: 1141-1151.

Peppe DJ, Royer DL, Cariglino B, Oliver SY, Newman S, Leight E, Enikolopov G, Fernandez-Burgos M, Herrera F, Adams JM, Correa E, Currano ED, Erickson JM, Hinojosa LF, Iglesias A, Jaramillo CA, Johnson KR, Jordan GJ, Kraft N, Lovelock EC, Lusk CH, Niinemets U, Penuelas J, Rapson G, Wing SL, Wright IJ. 2011. Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytologist, 190: 724-739. Leafsnap: A Computer Vision System for Automatic Plant Species Identification

Neeraj Kumar, Peter N. Belhumeur, Arijit Biswas, David W. Jacobs, W. John Kress, Ida C. Lopez, Joo V. B. Soares

Proceedings of the 12th European Conference on Computer Vision (ECCV), October 2012

The leaf morphospace groupAnalysisMao Li, Danforth Center

IsolationRebekah Mohn, Miami University

PotatoShelley Jansky, USDA, Wisconsin-MadisonDiego Fajardo, National Center to Genome Resources

PepperAllen van Deynze, UC DavisTheresa Hill, UC Davis

TomatoViktoriya Coneva, Danforth CenterMargaret Frank, Danforth CenterChris Topp, Danforth Center

GrapeAllison Miller, Saint Louis UniversityJason Londo, USDA/ARS, Geneva, NYLaura Klein, Saint Louis University

PassifloraWagner Otoni, Universidade Federal de VicosaArabidopsisRuthie Angelovici, University of Missouri, ColumbiaBatushansky Albert, University of Missouri, ColumbiaClement Bagaza, University of Missouri, ColumbiaEdmond Riffer, University of Missouri, ColumbiaBraden Zink, University of Missouri, Columbia

BrassicaJ. Chris Pires, University of Missouri, ColumbiaHong An, University of Missouri, ColumbiaSarah Gebken, University of Missouri, Columbia

CottonVasu Kuraparthy, North Carolina State University

ViburnumErika Edwards, Brown UniversityElizabeth Spriggs, Yale UniversityMichael Donoghue, Yale UniversitySam Schmerler, American Museum of Natural History

GrassesLynn Clark, Iowa StateTimothy Gallaher, Iowa StatePhillip Klahs, Iowa State

A universal theory of plant morphology:Persistent homology and plant topology

Chris Topp, Keith Duncan, Ni Jiang, Mao Li

A universal theory of plant morphology:Persistent homology and plant topologyChris Topp, Keith Duncan, Ni Jiang, Mao Li

Chris Topp, Keith Duncan, Ni Jiang, Mao LiA universal theory of plant morphology:Persistent homology and plant topology

Chris Topp, Keith Duncan, Ni Jiang, Mao LiA universal theory of plant morphology:Persistent homology and plant topology

Acknowledgments

FSUMio LabDonald Danforth Plant Science CenterTopp LabDonald Danforth Plant Science CenterChitwood Lab