Heidrun Huber

The adaptive evolution of plasticity: Phytochrome-mediated shade avoidance responses

Abstract Many plants display a characteristic suite of developmental “shade avoidance” responses, such as stem elongation and accelerated reproduction, to the low ratio of red to far-red wavelengths (R:FR) reflected or transmitted from green vegetation. This R:FR cue of crowding and vegetation shade is perceived by the phytochrome family of photoreceptors. Phytochrome-mediated responses provide an ideal system for investigating the adaptive evolution of phenotypic plasticity in natural environments. The molecular and developmental mechanisms underlying shade avoidance responses are well studied, and testable ecological hypotheses exist for their adaptive significance. Experimental manipulation of phenotypes demonstrates that shade avoidance responses may be adaptive, resulting in phenotypes with high relative fitness in the environments that induce those phenotypes. The adaptive value of shade avoidance depends upon the competitive environment, resource availability, and the reliability of the R:FR cue for predicting the selective environment experienced by an induced phenotype. Comparative studies and a reciprocal transplant experiment with Impatiens capensis provide evidence of adaptive divergence in shade avoidance responses between woodland and clearing habitats, which may result from population differences in the frequency of selection on shade avoidance traits, as well as differences in the reliability of the R:FR cue. Recent rapid progress in elucidating phytochrome signaling pathways in the genetic model Arabidopsis thaliana and other species now provides the opportunity for studying how selection on shade avoidance traits in natural environments acts upon the molecular mechanisms underlying natural phenotypic variation.

The evolution of the worldwide leaf economics spectrum

The worldwide leaf economic spectrum (WLES) is a strikingly consistent pattern of correlations among leaf traits. Although the WLES effectively summarizes variation in plant ecological strategies, little is known about its evolution. We reviewed estimates of natural selection and genetic variation for leaf traits to test whether the evolution of the WLES was limited by selection against unfit trait combinations or by genetic constraints. There was significant selection for leaf traits on both ends of the WLES spectrum, as well as significant genetic variation for these traits. In addition, genetic correlations between WLES traits were variable in strength and direction. These data suggest that genetic constraints have had a smaller role than selection in the evolution of the WLES.

Differential effects of light quantity and spectral light quality on growth, morphology and development of two stoloniferous Potentilla species

Abstract Plant species from open habitats often show pronounced responses to shading. Apart from a reduction in growth, shading can lead to marked changes in morphology and architecture, and it may affect the rate of plant development. Natural shade comprises two basically different features, a reduction in light quantity (amount of radiation) and changes in the spectral light quality. The first aspect represents changes in resource availability, while the latter acts as a source of information for plants and can prompt morphogenetic responses. A greenhouse experiment was carried out to study the effects of changes in light quality and quantity on the growth, morphology and development of two stoloniferous Potentilla species. Individual plants were subjected to three light treatments: (1) full daylight (control); and two shade treatments, in which (2) light quantity (photon flux density) and (3) light spectral quality (red/far-red ratio) were changed independently. Plant development was followed throughout the study. Morphological parameters, biomass and clonal offspring production were measured at the end of the experiment. Morphological traits such as petiole length, leaf blade characteristics and investment patterns into spacers showed high degrees of shade-induced plasticity in both species. With a few exceptions, light quality mainly affected morphological variables, while production parameters were most responsive to changes in light quantity. Potentilla anserina allocated resources preferentially to established rosettes at the cost of stolon growth and branching, while in P. reptans, all parameters related to development and allocation were slowed down to the same extent by light limitation. Light quality changes also positively affected biomass production via changes in leaf allocation. Changes in the spectral light quality had major effects on the size of modular structures (leaves, ramets), whereas changes in light quantity mainly affected their numbers.

A modular concept of plant foraging behaviour: the interplay between local responses and systemic control

In this paper we examined the notion that plant foraging for resources in heterogeneous environments must involve: (1) plasticity at the level of individual modules in reaction to localized environmental signals; and (2) the potential for modification of these responses either by the signals received from connected modules that may be exposed to different conditions, or by the signals reflecting the overall resource status of the plant. A conceptual model is presented to illustrate how plant foraging behaviour is achieved through these processes acting in concert, from the signal reception through signal transduction to morphological or physiological response. Evidence to support the concept is reviewed, using selective root placement under nutritionally heterogeneous conditions and elongation responses of stems and petioles to shade as examples. We discussed how the adoption of this model can promote understanding of the ecological significance of foraging behaviour. We also identified a need to widen the experimental repertoires of both molecular physiology and ecology in order to increase our insight into both the regulation and functioning of foraging responses, and their relationship with the patterns of environmental heterogeneity under which plants have evolved.

Frequency and Microenvironmental Pattern of Selection on Plastic Shade‐Avoidance Traits in a Natural Population of Impatiens capensis

The frequency and predictability of different selective environments are important parameters in models for the evolution of plasticity but have rarely been measured empirically in natural populations. We used an experimental phytometer approach to examine the frequency, predictability, and environmental determinants of heterogeneous selection on phytochrome‐mediated shade‐avoidance responses in a natural population of the annual plant Impatiens capensis. The strength and direction of selection on shade‐avoidance traits varied substantially on a fine spatial scale. The shade‐avoidance phenotype had high relative fecundity in some microsites but was disadvantageous in other microsites. Local seedling density proved to be a surprisingly poor predictor of microenvironmental variation in the strength and direction of selection on stem elongation in this study population. At least some of this unpredictability resulted from microenvironmental variation in water availability; the shade‐avoidance phenotype was more costly in dry microsites. Thus, environmental heterogeneity in resource availability can affect the relative costs and benefits of expressing shade‐avoidance traits independent of local seedling density, the inductive environmental cue. Theory predicts that these conditions may promote local genetic differentiation in reaction norms in structured populations, as observed in I. capensis.

Shade-induced changes in the branching pattern of a stoloniferous herb: Functional response or allometric effect?

Abstract Shade-induced changes in the branching pattern of clonal plants can lead to conspicuous modifications of their growth form and architecture. It has been hypothesized that reduced branching in shade may be an adaptive trait, enabling clonal plants to escape from unfavourable patches in a heterogeneous environment by allocating resources preferentially to the growth of the main axis (i.e. linear expansion), rather than to local proliferation by branching. However, such an adaptionist interpretation may be unjustified if (1) branching frequency is a function of the ontogenetic stage of plants, and if (2) shading slows down the ontogenetic development of plants, thereby delaying branch formation. In this case, architectural differences between sun- and shade-grown individuals, harvested at the same chronological age, may not represent a functional response to changes in light conditions, but may be a by-product of effects of shade on the rate of plant development. To distinguish between these two alternatives, individuals of the stoloniferous herb Potentilla reptans were subjected to three experimental light conditions: a control treatment providing full daylight, and two shade treatments: neutral shade (13% of ambient PPFD; no changes in light spectral composition) and simulated canopy shade (13% PPFD and a reduced red:far-red ratio). Plant development was followed throughout the experiment by daily monitoring primary stolon growth as well as branch and leaf initiation. Biomass and clonal offspring production were measured when plants were harvested. At the end of the experiment shaded plants had produced significantly fewer branches than clones grown in full daylight. In all three treatments, however, initiation of secondary stolons occurred at the same developmental stage of individual ramets. Shading significantly slowed down the ontogenetic development of plants and this resulted in the observed differences in branching patterns between sun- and shade-grown individuals, when compared at the same chronological age. These results hence provide evidence that shade-induced changes in the branching pattern of clonal plants can be due to purely allometric effects. Implications for interpreting architectural changes in terms of functional shade-avoidance responses are discussed.

Spatial structure of stoloniferous herbs: an interplay between structural blue-print, ontogeny and phenotypic plasticity

Plant form and spatial structure reflect the basic architectural blue-print of a plant. In most plant species, the expression of the structural blue-print is systematically altered during ontogeny resulting in predictable changes in the allometry of plant structures and in the types of structures that are produced. The expression of the structural blue-print or the timing of ontogenetic changes is also frequently altered by environmental conditions. This latter source of variability, referred to as phenotypic plasticity, is manifested through changes in the timing and rates of meristem initiation and development, the likelihood that meristems will remain dormant or commit to different demographic fates (i.e., vegetative vs. reproductive structures), or the size and structure of the organs formed. Complex interactions among these components can result in considerable differences in form and spatial structure among individuals of the same species. This paper focuses on the importance of these different components in determining the architecture of clonal plants with long internode connections between ramets.A case study is presented that attempts to separate ontogenetic variation and phenotypic plasticity in two stoloniferous species with different structural blue-prints, in their responses to shading. In both species the rate of ontogenetic development responded to intermediate shading levels, but only at very low levels of light availability did plastic changes in branch formation occur. Under shaded conditions the two species achieved similar changes in their architecture in conspicuously different ways. We discuss how different mechanisms leading to a given architecture can be distinguished and what the ecological implications of this are.

Shade avoidance in the clonal herb Trifolium fragiferum : a field study with experimentally manipulated vegetation height

In herbaceous canopies light availability can show high degrees of spatial variability in a vertical and also in a horizontal direction. Stoloniferous plants are hence likely to encounter differences in light availability during their ontogenetic development. Different mechanisms, such as petiole elongation, plasticity in internode length and branching, and an enhanced allocation to sexual reproduction have been suggested to represent viable shade-avoidance mechanisms for clonal plants.In a field experiment we tested the response of the stoloniferous herb Trifolium fragiferum L. to experimentally manipulated vegetation heights. Naturally occurring clonal fragments were exposed to four different vegetation heights ranging from 0 cm (high light availability created by clipping the surrounding natural vegetation at ground level) to 20 cm (natural shading in closed canopy). The growth and development of individual clones was followed for two months. At the end of the experiment above-ground plant parts were harvested. Growth-related and morphological parameters (e.g., petiole and internode length) as well as patterns of meristem utilization (i.e., flowering, branching) were recorded.Neither primary stolon growth and biomass accumulation nor branching and flowering were significantly affected by treatments. However, increased vegetation height resulted in a reduced number of secondary ramets and also had strong positive effects on petiole length, leading to marked changes in the architecture of plants growing in canopies of different heights. In addition, the average weight of individual ramets on the primary stolon was markedly higher in plants exposed to taller vegetation as compared to shorter vegetation.The results of this study suggest the occurrence of a trade-off between clonal expansion (i.e., secondary ramet production) and the average size of clonal offspring. If grown under higher vegetation plants invested more into the size of individual ramets, especially into elongating petioles, and less into the growth and development of lateral branches. Placing leaf laminae higher up in the canopy results in an enhanced light interception which has apparently buffered negative effects of increased vegetation height on whole-clone biomass. Plants grown under shorter vegetation invested more into lateral spread by producing more, but smaller ramets.

Variation in flooding-induced morphological traits in natural populations of white clover (Trifolium repens) and their effects on plant performance during soil flooding

BACKGROUND AND AIMS Soil flooding leads to low soil oxygen concentrations and thereby negatively affects plant growth. Differences in flooding tolerance have been explained by the variation among species in the extent to which traits related to acclimation were expressed. However, our knowledge of variation within natural species (i.e. among individual genotypes) in traits related to flooding tolerance is very limited. Such data could tell us on which traits selection might have taken place, and will take place in future. The aim of the present study was to show that variation in flooding-tolerance-related traits is present among genotypes of the same species, and that both the constitutive variation and the plastic variation in flooding-induced changes in trait expression affect the performance of genotypes during soil flooding. METHODS Clones of Trifolium repens originating from a river foreland were subjected to either drained, control conditions or to soil flooding. Constitutive expression of morphological traits was recorded on control plants, and flooding-induced changes in expression were compared with these constitutive expression levels. Moreover, the effect of both constitutive and flooding-induced trait expression on plant performance was determined. KEY RESULTS Constitutive and plastic variation of several morphological traits significantly affected plant performance. Even relatively small increases in root porosity and petiole length contributed to better performance during soil flooding. High specific leaf area, by contrast, was negatively correlated with performance during flooding. CONCLUSIONS The data show that different genotypes responded differently to soil flooding, which could be linked to variation in morphological trait expression. As flooded and drained conditions exerted different selection pressures on trait expression, the optimal value for constitutive and plastic traits will depend on the frequency and duration of flooding. These data will help us understanding the mechanisms affecting short- and long-term dynamics in flooding-prone ecosystems.

Fitness consequences of natural variation in flooding‐induced shoot elongation in Rumex palustris

• Plants can respond to their environment by morphological plasticity. Generally, the potential benefits of adaptive plastic responses are beyond doubt under predictable environmental changes. However, the net benefits may be less straightforward when plants encounter temporal stresses, such as flooding in river flood plains. • Here, we tested whether the balance of costs and benefits associated with flooding-induced shoot elongation depends on the flooding regime, by subjecting Rumex palustris plants with different elongation capacity to submergence of different frequency and duration. • Our results showed that reaching the surface by shoot elongation is associated with fitness benefits, as under less frequent, but longer, flooding episodes plants emerging above the floodwater had greater biomass production than plants that were kept below the surface. As we predicted, slow-elongating plants had clear advantages over fast-elongating ones if submergence was frequent but of short duration, indicating that elongation also incurs costs. • Our data suggest that high costs select for weak plasticity under frequent environmental change. In contrast to our predictions, however, fast-elongating plants did not have an overall advantage over slow-elongating plants when floods lasted longer. This indicates that the delicate balance between benefits and costs of flooding-induced elongation depends on the specific characteristics of the flooding regime.