Leaf Venation Network

Rules of Life: Design principles of evolved transportation networks in leaf veins

Venation network of  a Jojoba leaf (Simmondsia chinensis

MOTIVATION

Spatial transportation networks are critical to multicellular terrestrial organisms, including animal circulatory systems, fungal mycelial networks, and plant vasculature. These networks represent evolved solutions to maximize functional benefits relative to some set of construction costs. Although the functions vary across these domains, all these networks can share similar features, e.g. the presence of hierarchical structure, fractal-like branching, and/or nested loops. There may be general principles that unify relationships between architecture and function in these networks. Extant theory has only been able to predict primarily branching networks, suggesting that more accurate rules remain discoverable. The goal of our research is to understand the rules that link network architecture to network function using leaf venation networks as a model system. Discovering these principles could advance fundamental theory for networks and physical transport, as well as provide insight into the selective forces and biophysical constraints that have led to the evolution of organisms with diverse network architectures.

The six leaf functional axes. Image credit: I. S. Matos.

6 Leaf functional axes

Leaf venation networks may contribute to at least six different functional axes:

(1) Resistance to drought: leaf capacity to avoid water flow interruption during drought caused either by xylem embolisms (formation and expansion of air bubbles inside the xylem conduits) or xylem implosion (inwards collapse of xylem conduits cell walls).

(2) Resistance to herbivory: leaf capacity to avoid water flow disruption caused by herbivores cutting through the leaf.

(3) Resilience to damages: leaf capacity to maintain water flow after damages caused either by drought or herbivory.

(4) Flow efficiency: how much water flows across the leaf.

(5) Mechanical support: leaf capacity to remain uprigth in space against gravity and other bending forces.

(6) Construction cost: the amount of resources invested in the leaf construction.

The three key leaf architectural traits. Image credit: I. S. Matos.

3 Key leaf architectural traits

Previous studies (Blonder et al 2020, New Phytol) have identified three key traits to describe leaf venation architecture features:

(1) Venation density (VD, mm mm-2): it is a measure of how many veins there are per unit of leaf area. Higher VD values mean more veins. 

(2) Minimum spanning tree ratio (MST, dimensionless): describe the degree of branching or loopiness in the network. Higher MST values indicate networks with more loops, while lower MST values indicate more branching (i.e. tree-like) networks.

(3) Loop elongation ratio (ER, dimensionless): describe the shape of the loops. Higher ER values indicate more circular loops, while low ER values indicate more elongated loops.

CHAPTER 1

Leaf architecture and functional traits for 122 species at the University of California at Berkeley botanical garden

We collected leaf venation architecture and functional traits for a phylogenetically diverse set of 122 plant species (including ferns, basal angiosperms, monocots, basal eudicots, asterids, and rosids) sampled from the living collections of the University of California Botanical Garden at Berkeley. The sampled species originated from all continents, except Antarctica, and are distributed in different growth forms (aquatic, herb, climbing, tree, shrub). Our functional dataset comprises 32 (mechanical, hydraulic, anatomical, physiological, economical, and chemical) traits and provides a complete description of the six main leaf functional axes (flow efficiency, damage resistance to drought, resistance to herbivory, resilience, mechanical support, and construction cost). The leaf venation architecture trait dataset comprises over 5 million vein segments extracted from high-resolution whole-leaf images and contains 58 single- and 22 multiscale-statistics describing how network architecture features vary across the entire venation network. Our high-dimensional architecture-functional paired trait dataset is suitable for (1) functional and architectural characterization of plant species; (2) identification of venation architecture-function trade-offs; (3) investigation of evolutionary trends in leaf venation networks, and (4) mechanistic modeling of leaf function.

[Data available at - COMING SOON!]

Phylogenetic tree for the 122 plant species collected from the living collections of the University of California Botanical Garden at Berkeley. Image credit - I.S. Matos.

CHAPTER 2

Leaf venation network architecture coordinates functional trade-offs across vein spatial scales: evidence for multiple alternative designs

We measured architecture and functional traits on 122 ferns and angiosperms species to: describe how trade-offs vary across phylogenetic groups and vein spatial scales (small, medium, large veins) and determine whether architecture traits at each scale have independent or integrated effects on each function. 

We found that generalized architecture-function trade-offs are weak. Architecture strongly predicts leaf support and damage resistance axes, but weakly predicts efficiency and resilience axes. Architecture traits at different spatial scales contribute to different functional axes, allowing plants to independently modulate different functions by varying network properties at each scale.

This independence of vein architecture traits within and across spatial scales may enable evolution of multiple alternative designs of leaf networks that achieve equivalent functions or trade-off among multiple functions. 

[Read full paper at - COMING SOON!]

Radar chart for hypothesized combinations of leaf venation architecture traits (VD, MST, ER) at three vein spatial scales (small, medium, large) that would have evolved if each of the six leaf functional axis was independently optimized.  For example, in panel (b) damage resistance to drought should be higher in networks with lower density of large veins, branching large and medium veins and more circular loops in small veins.  While in panel (c) damage resistance to herbivory should be higher in networks with higher large vein density and more circular loops at all scales; 


CHAPTER 3

Leaf conduits grow wider than thicker and are potentially vulnerable to implosion under drought

Xylem conduits have lignified walls to resist crushing pressures. The thicker the double-wall (T) relative to its maximum diameter (D), the greater the collapse/implosion resistance. Having xylem that is more resistant than necessary incurs high costs and reduced flow, while having xylem not resistant enough may lead to catastrophic collapse under drought. Despite the importance of xylem implosion safety in determining plant drought resistance, it is still unclear how leaves scale TxD to trade-off among implosion safety, flow efficiency, mechanical support, and construction cost. We measured T and D in over 7,000 leaf xylem conduits of 122 ferns and angiosperms species to investigate how the TxD scaling varies across species, clades, habitats, growth forms, and vein orders. Overall, leaf xylem conduits grow wider than thicker, potentially resulting in high flow efficiency and lower cost, but at the expense of high vulnerability to implosion. Conduits seem particularly vulnerable to implosion in monocots, aquatic species and in species from hydric habitats, as well as in major veins. The absence of strong trade-offs within the leaf functional traits examined suggests that implosion safety at the whole-leaf level cannot be easily predicted by the sum of the individual conduits’ resistance to collapse.

[Read full paper at - COMING SOON!]

Leaf cross-sectional images showing variation in the dimensions, shape, number, and arrangement of leaf xylem conduits (tracheids and vessel elements) across ferns and angiosperm species. (a) Randia laetevirens (asterid); (b) Onoclea sensibilis (fern); (c) Parajubaea torallyi (monocot); (d) Camellia sinensis (asterid); (e) Deyeuxia nutkaensis (monocot); (f) Illicium lanceolatum (basal angiosperm); (g) Asimina triloba (basal angiosperm); (h) Cyclanthus bipartitus (monocot); (i) Phillyrea latifolia (asterid); (j) Prosartes hookeri (monocot); (k) Simmondsia chinensis (rosid); (l) Romneya coulteri (basal eudicot); (m) Montinia caryophyllacea (asterid); (n) Montinia caryophyllacea (asterid): collapsed xylem conduits. x= xylem conduits; f = fibers.


CHAPTER 4

Evolutionary trends in the leaf venation network architecture


[Read full paper at - COMING SOON!]

CHAPTER 5

Simulations of leaf functioning using electronic circuits


[Read full paper at - COMING SOON!]

ACKNOWLEDGEMENT

We are grateful to all staff of the University of California Botanical Garden at Berkeley for the logistical support, especially to the horticulturists Ethan Fenner, Eric Hupperts, James Fong, Noah Gapsis, Gideon Dollarhide, Sophia Warsh, Jason Bonham, and Corina Rieder who helped us with sample collection. We thank Denise Schines for sharing histological and microscopy methods. We also thank Prof. Cynthia Looy and Prof. Todd Dawson for lending their equipment to obtain the leaf anatomical dataset. This study was supported by the NSF (grant DEB-2025282), the University of California at Berkeley, and the UK Natural Environment Research Council (NE/M019160/1).

LAND ACKNOWLEDGEMENT

We acknowledge the Ohlone people as the first nations owners of the lands where the University of California at Berkeley now stands and where this research was conducted.