Temperature and Turgor "Limitation" and Environmental "Control" in Xylem Biology and Dendrochronology.

Trees and other woody plants are immensely ecologically important, making it essential to understand the causes of relationships between tree structure and function. To help these efforts, we highlight persistent traditions in plant biology of appealing to environmental factors "limiting" or "controlling" woody plant features. Examples include the idea that inevitable drops in cell turgor with plant height limit cell expansion and thus leaf size and tree height; that low temperatures prohibit lignification of cells and thus the growth of woody plants at high elevation; and notions from dendrochronology and related fields that climate factors such as rainfall and temperature "control" growth ring features. We show that notions of "control," "limitation," and the like imply that selection would favor a given trait value, but that these would-be favored values are developmentally impossible to produce. Such "limitation" scenarios predict trait frequency distributions that are very narrow and are abruptly curtailed at the upper limit of developmental possibility (the right-hand side of the distribution). Such distributions have, to our knowledge, never been observed, so we see little empirical support for "limitation" hypotheses. We suggest that, as a more productive starting point, plant biologists should examine adaptation hypotheses, in which developmental possibility is wide (congruent with the wide ranges of trait variation that really are observed), but only some of the possible variants are favored. We suggest that (1) the traditional the proximate/ultimate causation distinction, (2) purging scenarios of teleology/anthropomorphism, and (3) stating hypotheses in terms of developmental potential and natural selection are three simple ways of making "limitation" hypotheses clearer with regard to biological process and thus empirically testable.

The vessel wall thickness-vessel diameter relationship across woody angiosperms.

PREMISE: Comparative anatomy is necessary to identify the extremes of combinations of functionally relevant structural traits, to ensure that physiological data cover xylem anatomical diversity adequately, and thus achieve a global understanding of xylem structure-function relations. A key trait relationship is that between xylem vessel diameter and wall thickness of both the single vessel and the double vessel+adjacent imperforate tracheary element (ITE). METHODS: We compiled a comparative data set with 1093 samples, 858 species, 350 genera, 86 families, and 33 orders. We used broken linear regression and an algorithm to explore changes in parameter values from linear regressions using subsets of the data set to identify a threshold, at 90-µm vessel diameter, in the wall thickness-diameter relationship. RESULTS: Below 90 µm diameter for vessels, virtually any wall thickness could be associated with virtually any diameter. Below this threshold, selection is free to favor a very wide array of combinations, such as very thick walls and narrow vessels in ITE-free herbs, or very thin-walled, wide vessels in evergreen dryland pioneers. Above 90 µm, there was a moderate positive relationship. CONCLUSIONS: Our analysis shows that the space of vessel wall thickness-diameter combinations is very wide, with selection apparently eliminating individuals with vessel walls "too thin" for their diameter. Most importantly, our survey revealed poorly studied plant hydraulic syndromes (functionally significant trait combinations). These data suggest that the full span of trait combinations, and thus the minimal set of hydraulic syndromes requiring study to span woody plant functional diversity adequately, remains to be documented.

The Widened Pipe Model of plant hydraulic evolution.

Shaping global water and carbon cycles, plants lift water from roots to leaves through xylem conduits. The importance of xylem water conduction makes it crucial to understand how natural selection deploys conduit diameters within and across plants. Wider conduits transport more water but are likely more vulnerable to conduction-blocking gas embolisms and cost more for a plant to build, a tension necessarily shaping xylem conduit diameters along plant stems. We build on this expectation to present the Widened Pipe Model (WPM) of plant hydraulic evolution, testing it against a global dataset. The WPM predicts that xylem conduits should be narrowest at the stem tips, widening quickly before plateauing toward the stem base. This universal profile emerges from Pareto modeling of a trade-off between just two competing vectors of natural selection: one favoring rapid widening of conduits tip to base, minimizing hydraulic resistance, and another favoring slow widening of conduits, minimizing carbon cost and embolism risk. Our data spanning terrestrial plant orders, life forms, habitats, and sizes conform closely to WPM predictions. The WPM highlights carbon economy as a powerful vector of natural selection shaping plant function. It further implies that factors that cause resistance in plant conductive systems, such as conduit pit membrane resistance, should scale in exact harmony with tip-to-base conduit widening. Furthermore, the WPM implies that alterations in the environments of individual plants should lead to changes in plant height, for example, shedding terminal branches and resprouting at lower height under drier climates, thus achieving narrower and potentially more embolism-resistant conduits.