Ontogenetic phenotypic plasticity during the reproductive phase in Arabidopsis thaliana (Brassicaceae)

While phenotypic plasticity has been the focus of much research and debate in the recent ecological and evolutionary literature, the developmental nature of the phenomenon has been mostly overlooked. A developmental perspective must ultimately be an integral part of our understanding of how organisms cope with heterogeneous environments. In this paper I use the rapid cycling Arabidopsis thaliana to address the following questions concerning developmental plasticity. (1) Are there genetic and/or environmental differences in parameters describing ontogenetic trajectories? (2) Is ontogenetic variation produced by differences in genotypes and/or environments for two crucial traits of the reproductive phase of the life cycle, stem elongation and flower production? (3) Is there ontogenetic variability for the correlation between the two characters? I found genetic variation, plasticity, and variation for plasticity affecting at least some of the growth parameters, indicating potential for evolution via heterochronic shifts in ontogenetic trajectories. Within-population differences among families are determined before the onset of the reproductive phase, while among-population variation is the result of divergence during the reproductive phase of the ontogeny. Finally, the ontogenetic profiles of character correlations are very distinct between the ecologically meaningful categories of early- and late-flowering “ecotypes” in this species, and show susceptibility to environmental change.     

Heteroblasty in Arabidopsis thaliana (L.) Heynh

 Heteroblasty in Arabidopsis thaliana was analyzed in a variety of plants with mutations in leaf morphology using a tissue-specific β-glucuronidase gene marker. Some mutants exhibited their mutant phenotypes specifically in foliage leaves. The phenotypes associated with the foliage-leaf-specific mutations were also found to be induced ectopically in cotyledons in the presence of the lec1 mutation. Moreover, the features of an emf1lec1 double mutant showed that cotyledons can be partially converted into carpelloids. When heteroblastic traits were examined in foliage leaves in the presence of certain mutations or natural deviations by histochemical analysis of the expression of the tissue-specific marker gene, it was found that ectopic expression of the developmental program for the first foliage leaves in lec1 cotyledons seemed to affect the heteroblastic features of the first set of foliage leaves, while foliage leaves beyond the third position appeared normal. Similarly, in wild-type plants, discrepancies in heteroblastic features, relative to standard features, of foliage leaves at early positions seemed to be eliminated in foliage leaves at later positions. These results suggest that heteroblasty in foliage leaves might be affected in part by the heteroblastic stage of the preceding foliage leaves but is finally controlled autonomously at each leaf position. Received: 9 July 1999 / Accepted: 17 August 1999     

Correlated response in plasticity to selection for early flowering in Arabidopsis thaliana

Phenotypic plasticity is an important strategy for coping with changing environments. However, environmental change usually results in strong directional selection, and little is known empirically about how this affects plasticity. If genes affecting a trait value also affect its plasticity, selection on the trait should influence plasticity. Synthetic outbred populations of Arabidopsis thaliana were selected for earlier flowering under simulated spring- and winter-annual conditions to investigate the correlated response of flowering time plasticity and its effect on family-by-environment variance (Vg×e) within each selected line. We found that selection affected plasticity in an environmentally dependent manner: under simulated spring-annual conditions, selection increased the magnitude of plastic response but decreased Vg×e; selection under simulated winter-annual conditions reduced the magnitude of plastic response but did not alter Vg×e significantly. As selection may constrain future response to environmental change, the environment for crop breeding and ex situ conservation programmes should be carefully chosen. Models of species persistence under environmental change should also consider the interaction between selection and plasticity.     

Flowering time plasticity in Arabidopsis thaliana: a reanalysis of Westerman & Lawrence (1970)

Environmental variation in temperature can have dramatic effects on plant morphology, phenology, and fitness, and for this reason it is important to understand the evolutionary dynamics of phenotypic plasticity in response to temperature. We investigated constraints on the evolution of phenotypic plasticity in response to a temperature gradient in the model plant Arabidopsis thaliana by applying modern analytical tools to the classic data of Westerman & Lawrence (1970). We found significant evidence for two types of constraints. First, we detected numerous significant genetic correlations between plastic responses to temperature and the mean value of a trait across all environments, which differed qualitatively in pattern between the set of ecotypes and the set of mutant lines in the original sample. Secondly, we detected significant costs of flowering time plasticity in two of the three experimental environments, and a net pattern of selection against flowering time plasticity in the experiment overall. Thus, when explored with contemporary methods, the prescient work of Westerman & Lawrence (1970) provides new insights about evolutionary constraints on the evolution of plasticity.     

Phenotypic plasticity to light intensity in Arabidopsis thaliana: invariance of reaction norms and phenotypic integration

Phenotypic plasticity (the pattern of response of organisms to changes in environmental conditions) and phenotypic integration (the pattern of character correlations) are important components of our understanding of the evolution of complex phenotypes. Most studies published so far in this area have been conducted within populations with the express aim of predicting future response to evolutionary forces. However, among-population differentiation for plasticity and trait correlations are important indicators of recent past events that have shaped the currently observable phenotypes. We investigated variation in the reaction norms of several traits in a large number of accessions of Arabidopsis thaliana exposed to different levels of light quantity as well as the environmental lability of the corresponding across-population character variance–covariance matrix. Our results show that there is an astounding degree of inter-population variation for character means and very little variation for plasticity, in agreement with the idea that A. thaliana is a light-specialist often occurring in open, disturbed habitats. However, this plant also shows patterns of plasticity that are predicted to be adaptive based on functional ecological considerations, such as an increase in either specific leaf area or leaf number (but not both) under low light. We also demonstrate that the set of character correlations in A. thaliana is extremely stable to changes in light availability, contrary to previous findings in the same species when different environmental factors were considered. Several processes that might have been responsible for the observed patterns are discussed as a prelude to follow-up research on these problems.     

Parental environmental effects on life history traits in Arabidopsis thaliana (Brassicaceae)

Environmentally induced maternal effects on offspring phenotype are well known in plants. When genotypes or maternal lineages are replicated and raised in different environmental conditions, the phenotype of their offspring often depends on the environment in which the parents developed. However, the degree to which such maternal effects are maintained over subsequent generations has not been documented in many taxa. Here we report the results of a study designed to assess the effects of parental environment on vegetative and reproductive traits, using glasshouse-raised maternal lines sampled from natural populations of Arabidopsis thaliana . Replicates of five highly selfed lines from each of four wild populations were cultivated in two abiotic environments in the glasshouse, and the quality and performance of seeds derived from these two environments were examined over two generations. We found that offspring phenotype was strongly influenced by parental environment, but because the parental environments differed with respect to the time of seed harvest, it was not possible to distinguish clearly between parental environmental effects and the possible (but unlikely) effects of seed age on offspring phenotype. We observed a rapid decline in the expression of ancestral environmental effects, and no main environmental effects on progeny phenotype persisted in the second generation. The mechanism of transmission of environmental effects did not appear to be associated with the quantity or quality of reserves in the seeds, suggesting that environmental effects may be transmitted across subsequent generations via some mechanism that generates environment-specific gene expression.     

Regulation of proline accumulation in Arabidopsis thaliana (L.) Heynh during development and in response to desiccation

Significant differences were observed in the amount and proportion of free amino acids in different organs of Arabidopsis thaliana (L.) Heynh, ecotype Columbia. The most notable were found for proline, which formed 17–26% of the total free amino acid concentration in reproductive tissues (floret and seed), but only 1–3% of the total free amino acid concentration in vegetative tissues (rosette leaf and root). Proline accumulation was associated with tissues that had relatively low water contents. Tissues which displayed high water contents, such as rosette leaves, contained low levels of proline. A significant increase in the levels of proline accumulation occurred in plants subjected to experimentally induced low water potentials as compared to unstressed plants. For instance, an 8–10-fold increase in proline was observed in the presence of 120 mmol kg^?1 NaCl or KCl, and a 20-fold increase was stimulated by 60 mmol kg^?1 PEG. However, in addition to the accumulation of proline, massive accumulation of Na⁺, K⁺ and Cl^? ions occurred in tissues of plants stressed with salt. No significant differences were observed in mineral ions in plants stressed with PEG. Isotope tracer experiments with ¹⁴C compounds established that glutamate, ornithine and arginine are precursors of the proline biosynthesis induced by PEG in response to low water potentials in Arabidopsis thaliana. We conclude that the accumulation of proline in response to PEG occurs through increased biosynthesis.     

Ultrastructure of microsporogenesis and microgametogenesis inArabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae)

Summary The process of microsporogenesis and microgametogenesis was studied at the ultrastructural level in wild-typeArabidopsis thaliana ecotype Wassilewskija to provide a basis for comparison with nuclear male-sterile mutants of the same ecotype. From the earliest stage studied to mature pollen just prior to anther dehiscence, microsporocyte/microspore/pollen development follows the general pattern seen in most angiosperms. The tapetum is of the secretory type with loss of the tapetal cell walls beginning at about the time of microsporocyte meiosis. Wall loss exhibits polarity with the tapetal protoplasts becoming located at a distance from the inner tangential walls first, followed by an increase in distance from the radial walls beginning at the interior edge and progressing outward. The inner tangential and radial tapetal walls are completely degenerated by the microspore tetrad stage. Unlike other members of the Brassicaceae that have been studied, the tapetal cells ofA. thaliana Wassilewskija also lose their outer tangential walls, and secretion occurs from all sides of the cells. Exine wall precursors are secreted from the tapetal cells in a process that appears to involve dilation of individual endoplasmic reticulum cisternae that fuse with the tapetal cell membrane and release their contents into the locule. Following completion of the exine, the tapetal cell plastids develop membranebound inclusions with osmiophilic and electron-transparent regions. The plastids undergo ultrastructural changes that suggest breakdown of the inclusion membranes followed by release of their contents into the locule prior to the complete degeneration of the tapetal cells.     

pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh

A novel P-deficient mutant of Arabidopsis thaliana, pho3, was isolated by screening for root acid phosphatase (APase) activity in plants grown under low-P conditions. pho3 had 30% less APase activity in roots than the wild type and, in contrast to wild-type plants, root APase activity did not increase in response to growth in low P. However, shoot APase activity was higher in pho3 than in the wild-type plants. In addition, the pho3 mutant had a P-deficient phenotype, even when grown in P-sufficient conditions. The total P content of 11-d-old pho3 plants, grown in agar media with a plentiful supply of P, was about 25% lower than the wild-type level in the shoot, and about 65% lower in the roots. In the rosette leaves of mature soil-grown pho3 plants the total P content was again reduced, to about 50% of wild-type levels. pho3 exhibited a number of characteristics normally associated with low-P stress, including severely reduced growth, increased anthocyanin content (at least 100-fold greater than the wild type in soil-grown plants) and starch accumulation. The results suggest that the mutant is unable to respond to low internal P levels, and may lack a transporter or a signalling component involved in regulating P nutrition. Received: 21 March 2000 / Accepted: 15 August 2000     

Low air humidity increases leaf-specific hydraulic conductance of Arabidopsis thaliana (L.) Heynh (Brassicaceae)

The typical isohydric plant response to low relative humidity involves stomatal closure, followed by long-term responses like adjustment of shoot-to-root ratios. Little information is available on the early responses of the root system to exposure of shoots to low humidity, nor is it clear to what extent responses of Arabidopsis thaliana conform to the isohydric model. In this study, A. thaliana plants grown hydroponically at high humidity were exposed to two constant relative humidities, 17% and 77%, while the root system remained in aerated nutrient solution. Leaf conductance (g(s)), transpiration, water potential (Psi(l)), osmotic potential, and whole plant hydraulic conductance (K) were determined for the following time intervals: 0-10, 10-20, and 20-40 min, and 0-5, 5-10, and 24-29 h. At low relative humidity, no change in g(s) was detected. Psi(l) decreased by 0.28 MPa during the first 5 h and then remained stable. During the first hour, leaf-specific K averaged 1.6 x 10(-5) kg MPa(-1) m(-2) s(-1) at high humidity. At low humidity it increased >3-fold to 5.8 x 10(-5) kg MPa(-1) m(-2) s(-1). Similar significant differences in K were observed during all time periods. Low concentration mercury amendments in the hydroponic solution (5 microM and 10 microM HgCl(2)) had no discernible influence, but pre-exposure to 50 microM HgCl(2) reduced K differences between humidity treatments. As HgCl(2) is known to be a potent inhibitor of aquaporin function, this suggests that aquaporins may have played a role in the fast hydraulic response of plants transferred to low humidity. The rapid hydraulic response and the influence of mercury raise the possibility that an alternative response to atmospheric dryness is increased K modulated by aquaporins.     

Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh

In higher plants, stems and roots show negative and positive gravitropism, respectively. However, current knowledge on the graviresponse of leaves is lacking. In this study, we analyzed the positioning and movement of rosette leaves of Arabidopsis thaliana under light and dark conditions. We found that the radial positioning of rosette leaves was not affected by the direction of gravity under continuous white light. In contrast, when plants were shifted to darkness, the leaves moved upwards, suggesting negative gravitropism. Analysis of the phosphoglucomutase and shoot gravitropism 2-1 mutants revealed that the sedimenting amyloplasts in the leaf petiole are important for gravity perception, as is the case in stems and roots. In addition, our detailed physiological analyses revealed a unique feature of leaf movement after the shift to darkness, i.e. movement could be divided into negative gravitropism and nastic movement. The orientation of rosette leaves is ascribed to a combination of these movements.     

Ion channels in guard cells of Arabidopsis thaliana (L.) Heynh.

Despite the availability of many mutants for signal transduction, Arabidopsis thaliana guard cells have so far not been used in electrophysiological research. Problems with the isolation of epidermal strips and the small size of A. thaliana guard cells were often prohibiting. In the present study these difficulties were overcome and guard cells were impaled with double-barreled microelectrodes. Membrane-potential recordings were often stable for over half an hour and voltage-clamp measurements could be conducted. The guard cells were found to exhibit two states. The majority of the guard cells had depolarized membrane potentials, which were largely dependent on external K⁺ concentrations. Other cells displayed spontaneous transitions to a more hyperpolarized state, at which the free-running membrane potential (E_m) was not sensitive to the external K⁺ concentration. Two outward-rectifying conductances were identified in cells in the depolarized state. A slow outward-rectifying channel (s-ORC) had properties resembling the K⁺-selective ORC of Vicia faba guard cells (Blatt, 1988, J Membr Biol 102: 235–246). The activation and inactivation times and the activation potential, all depended on the reversal potential (E_rev) of the s-ORC conductance. The s-ORC was blocked by Ba²⁺ (K_1/2 = 0.3–1.3mM) and verapamil (K_1/2 = 15–20 μM). A second rapid outward-rectifying conductance (r-ORC) activated instantaneously upon stepping the voltage to positive values and was stimulated by Ba²⁺. Inward-rectifying channels (IRC) were only observed in cells in the hyperpolarized state. The activation time and activation potential of this channel were not sensitive to the external K⁺ concentration. The slow activation of the IRC (t_1/2 ≈ 0.5 s) and its negative activation potential (V_threshold = −155 mV) resemble the values found for the KAT1 channel expressed in Saccharomyces cerevisiae (Bertl et al., 1995, Proc Natl Acad Sci USA 92: 2701–2705). The results indicate that A. thaliana guard cells provide an excellent system for the study of signal transduction processes. Received: 28 March 1996 / Accepted: 11 November 1996     

磷空间有效性对拟南芥根形态构型的影响

磷空间有效性显著影响拟南芥主、侧根生长。在均一的磷处理下,极度磷胁迫或过量供磷均会导致拟南芥主根变短和侧根密度降低。在分层的磷处理下,上层高磷下层低磷能明显促进主根伸长生长,提高侧根在高磷区域的密度,说明植物根系在下层低磷区感受到磷胁迫信号后,可促进上层高磷区侧根的形成和发育。     

The pattern of secondary root formation in curving roots of Arabidopsis thaliana (L.) Heynh.

Abstract. A gravitational stimulus was used to induce the curvature of the main root of Arabidopsis thaliana. The number of secondary roots increased on the convex side and decreased on the concave side of any curved main root axes in comparison with straight roots used as the control. The same phenomenon was observed with the curved main roots of plants grown on a clinostat and of mutant plants exhibiting random root orientation. The data suggest that the pattern of lateral root formation is associated with curvature but is independent of the environmental stimuli used to induce curvature.