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Title: Persistent homology demarcates a leaf morphospace: towards discerning constraint from selection

Author
item LI, MAO - Danforth Plant Science Center
item AN, HONG - University Of Missouri
item ANGELOVICI, RUTHIE - University Of Missouri
item BAGAZA, CLEMENT - University Of Missouri
item BATUSHANSKY, ALBERT - University Of Missouri
item CLARK, LYNN - Iowa State University
item CONEVA, VIKTORIYA - Kenyon College
item DONOGHUE, MICHAEL - Yale University
item EDWARDS, ERIKA - Yale University
item FAJARDO, DIEGO - National Center For Genome Resources
item FANG, HUI - North Carolina State University
item FRANK, MARGARET - Cornell University
item GALLAHER, TIMOTHY - Iowa State University
item GEBKEN, SARAH - University Of Missouri
item HILL, THERESA - University Of California, Davis
item JANSKY, SHELLY - University Of Wisconsin
item KAUR, BALJINDER - North Carolina State University
item KLAHS, PHILIP - Iowa State University
item KLEIN, LAURA - St Louis University
item KURAPARTHY, VASU - North Carolina State University
item Londo, Jason
item MIGICOVSKY, ZOE - Dalhousie University
item MILLER, ALLISON - St Louis University
item MOHN, REBEKAH - Miami Dade University
item MYLES, SEAN - Dalhousie University
item OTONI, WAGNER - Universidade Federal De Vicosa
item PIRES, JC - University Of Missouri
item RIFFER, EDMOND - University Of Missouri
item SCHMERLER, SAM - Brown University
item SPRIGGS, ELIZABETH - Yale University
item TOPP, CHRISTOPHER - Danforth Plant Science Center
item VAN DEYNZE, ALLEN - University Of California, Davis
item ZHANG, KUANG - North Carolina State University
item ZHU, LINGLONG - North Carolina State University
item ZINK, BRADEN - University Of Missouri
item CHITWOOD, DANIEL - Michigan State University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/9/2018
Publication Date: 4/25/2018
Citation: Li, M., An, H., Angelovici, R., Bagaza, C., Batushansky, A., Clark, L., Coneva, V., Donoghue, M., Edwards, E., Fajardo, D., Fang, H., Frank, M., Gallaher, T., Gebken, S., Hill, T.A., Jansky, S., Kaur, B., Klahs, P., Klein, L., Kuraparthy, V., Londo, J.P., Migicovsky, Z., Miller, A., Mohn, R., Myles, S., Otoni, W., Pires, J., Riffer, E., Schmerler, S., Spriggs, E., Topp, C.N., Van Deynze, A., Zhang, K., Zhu, L., Zink, B., Chitwood, D.H. 2018. Persistent homology demarcates a leaf morphospace: towards discerning constraint from selection. Frontiers in Plant Science. 1.

Interpretive Summary: Leaf shapes across the plant kingdom are incredibly diverse, complex, and beautiful. In addition to being beautiful, leaves are essential to plant growth and development. Differences in leaf shape can contribute to survival in hot, dry, cold, and humid environments. Additionally, manipulation of leaf shapes in agriculture could increase yields and decrease farm imputs, if the genetic control of shape can be uncovered. Researchers interested in understanding how and why leaves have different shapes require a standard method for leaf shape measurements in order to be able to compare across different species. Presented here is a new method of determining the different aspects of leaf shape (length, width, lobes, simple, complex, etc.,) all in the same context. 182,707 different leaves, collected from 141 different plant families and from 75 global locations were examined with this new morphological measurement, called persistent homology. This method is capable of determining what plant family a leaf comes from, indicating that some aspects of leaf shape are genetic and are held constant based on evolutionary history. Additionally, this method can also determine geographic location of collection, demonstrating some aspects of leaf shape are driven predominantly by environment. Taken together, this data provides a new tool for agricultural researchers trying to optimize plant canopies in croplands as well as provides a tool for evolutionary biologists, botanists, and plant scientists to compare and contrast data collected worldwide.

Technical Abstract: Current morphometric methods that comprehensively measure shape cannot compare the disparate leaf shapes found in seed plants and are sensitive to processing artifacts. We explore the use of persistent homology, a topological method applied as a filtration across simplicial complexes (or more simply, a method to measure topological features of spaces across different spatial resolutions), to overcome these limitations. The described method isolates subsets of shape features and measures the spatial relationship of neighboring pixel densities in a shape. We apply the method to the analysis of 182,707 leaves, both published and unpublished, representing 141 plant families collected from 75 sites throughout the world. By measuring leaves from throughout the seed plants using persistent homology, a defined morphospace comparing all leaves is demarcated. Clear differences in shape between major phylogenetic groups are detected and estimates of leaf shape diversity within plant families are made. This approach does not only predict plant family, but also the collection site, confirming phylogenetically invariant morphological features that characterize leaves from specific locations. Defining the boundaries of an empirically measured morphospace is the first step towards addressing the hypothesis of whether developmental constraint or evolutionary selection is the driving force behind leaf shape diversity. The application of a persistent homology method, using topological features, to measure leaf shape allows for a unified morphometric framework to measure plant form, including shape and branching architectures.