Inflorescence photosynthetic contribution to fitness releases Arabidopsis thaliana plants from trade-off constraints on early flowering.
ABSTRACT: Leaves are thought to be the primary carbon source for reproduction in plants, so a positive relationship between vegetative size and reproductive output is expected, establishing a trade-off between time to reproduction and reproductive output. A common response to higher temperatures due to climate changes is the induction of earlier transition into reproduction. Thus, in annual plants, earlier transition into flowering can potentially constrain plant size and reduce seed production. However, trade-offs between early reproduction and fitness are not always observed, suggesting mechanisms to escape the constraints of early flowering do exist. Here, we test whether inflorescence photosynthesis contribution to the reproductive output of Arabidopsis thaliana can offset the cost of early reproduction. We followed the development, growth rate and fitness of 15 accessions, and removed all rosette leaves at flowering (prior to the completion of inflorescence development or any fruit production) in half of the plants to determine the ability of inflorescences to maintain fitness in the absence of leaves. Although leaf removal significantly reduced fruit number, seed weight and plant height, even the most severely impacted accessions maintained 35% of their fitness with the inflorescence as the sole photosynthetic organ; and some accessions experienced no reduction in fitness. Differences between accessions in their ability to maintain fitness after leaf removal is best explained by earlier flowering time and the ability to maintain as many or more branches after leaf removal as in the control treatment. Although earlier flowering does constrain plant vegetative size, we found that inflorescence photosynthesis can significantly contribute to seed production, explaining why early flowering plants can maintain high fitness despite a reduction in vegetative size. Thus, plants can be released from the usually assumed trade-offs associated with earlier reproduction, and selection on inflorescence traits can mediate the impact of climate change on phenology.
Project description:The life cycles of plants are characterized by two major life history transitions-germination and the initiation of flowering-the timing of which are important determinants of fitness. Unlike annuals, which make the transition from the vegetative to reproductive phase only once, perennials iterate reproduction in successive years. The floral repressor PERPETUAL FLOWERING 1 (PEP1), an ortholog of FLOWERING LOCUS C, in the alpine perennial Arabis alpina ensures the continuation of vegetative growth after flowering and thereby restricts the duration of the flowering episode. We performed greenhouse and garden experiments to compare flowering phenology, fecundity and seed traits between A. alpina accessions that have a functional PEP1 allele and flower seasonally and pep1 mutants and accessions that carry lesions in PEP1 and flower perpetually. In the garden, perpetual genotypes flower asynchronously and show higher winter mortality than seasonal ones. PEP1 also pleiotropically regulates seed dormancy and longevity in a way that is functionally divergent from FLC. Seeds from perpetual genotypes have shallow dormancy and reduced longevity regardless of whether they after-ripened in plants grown in the greenhouse or in the experimental garden. These results suggest that perpetual genotypes have higher mortality during winter but compensate by showing higher seedling establishment. Differences in seed traits between seasonal and perpetual genotypes are also coupled with differences in hormone sensitivity and expression of genes involved in hormonal pathways. Our study highlights the existence of pleiotropic regulation of seed traits by hub developmental regulators such as PEP1, suggesting that seed and flowering traits in perennial plants might be optimized in a coordinated fashion.
Project description:Although the occurrence of epistasis and pleiotropy is widely accepted at the molecular level, its effect on the adaptive value of fitness-related genes is rarely investigated in plants. Knowledge of these features of a gene is critical to understand the molecular basis of adaptive evolution. Here we investigate the importance of pleiotropy and epistasis in determining the adaptive value of a candidate gene using the gene FRI (FRIGIDA), which is thought to be the major gene controlling flowering time variation in Arabidopsis thaliana. The effect of FRI on flowering time was analyzed in an outbred population created by randomly mating 19 natural accessions of A. thaliana. This unique population allows the estimation of FRI effects independent of any linkage association with other loci due to demographic processes or to coadapted genes. It also allows for the estimation of pleiotropic effects of FRI on fitness and inflorescence architecture. We found that FRI explains less variation in flowering time than previously observed among natural accessions, and interacts epistatically with the FLC locus. Although early flowering plants produce more fruits under spring conditions, and nonfunctional alleles of FRI were associated with early flowering, variation at FRI was not associated with fitness. We show that nonfunctional FRI alleles have negative pleiotropic effects on fitness by reducing the numbers of nodes and branches on the inflorescence. We propose that these antagonistic pleiotropic effects reduce the adaptive value of FRI, and helps explain the maintenance of alternative life history strategies across natural populations of A. thaliana.
Project description:Flowering plants possess an unrivaled diversity of mechanisms for achieving sexual and asexual reproduction, often simultaneously. The commonest type of asexual reproduction is clonal growth (vegetative propagation) in which parental genotypes (genets) produce vegetative modules (ramets) that are capable of independent growth, reproduction, and often dispersal. Clonal growth leads to an expansion in the size of genets and increased fitness because large floral displays increase fertility and opportunities for outcrossing. Moreover, the clonal dispersal of vegetative propagules can assist "mate finding," particularly in aquatic plants. However, there are ecological circumstances in which functional antagonism between sexual and asexual reproductive modes can negatively affect the fitness of clonal plants. Populations of heterostylous and dioecious species have a small number of mating groups (two or three), which should occur at equal frequency in equilibrium populations. Extensive clonal growth and vegetative dispersal can disrupt the functioning of these sexual polymorphisms, resulting in biased morph ratios and populations with a single mating group, with consequences for fertility and mating. In populations in which clonal propagation predominates, mutations reducing fertility may lead to sexual dysfunction and even the loss of sex. Recent evidence suggests that somatic mutations can play a significant role in influencing fitness in clonal plants and may also help explain the occurrence of genetic diversity in sterile clonal populations. Highly polymorphic genetic markers offer outstanding opportunities for gaining novel insights into functional interactions between sexual and clonal reproduction in flowering plants.
Project description:Plants show ontogenetic variation in growth-defence strategies to maximize reproductive output within a community context. Most work on plant ontogenetic variation in growth-defence trade-offs has focussed on interactions with antagonistic insect herbivores. Plants respond to herbivore attack with phenotypic changes. Despite the knowledge that plant responses to herbivory affect plant mutualistic interactions with pollinators required for reproduction, indirect interactions between herbivores and pollinators have not been included in the evaluation of how ontogenetic growth-defence trajectories affect plant fitness.In a common garden experiment with the annual Brassica nigra, we investigated whether exposure to various herbivore species on different plant ontogenetic stages (vegetative, bud or flowering stage) affects plant flowering traits, interactions with flower visitors and results in fitness consequences for the plant.Effects of herbivory on flowering plant traits and interactions with flower visitors depended on plant ontogeny. Plant exposure in the vegetative stage to the caterpillar Pieris brassicae and aphid Brevicoryne brassicae led to reduced flowering time and flower production, and resulted in reduced pollinator attraction, pollen beetle colonization, total seed production and seed weight. When plants had buds, infestation by most herbivore species tested reduced flower production and pollen beetle colonization. Pollinator attraction was either increased or reduced. Plants infested in the flowering stage with P. brassicae or Lipaphis erysimi flowered longer, while infestation by any of the herbivore species tested increased the number of flower visits by pollinators.Our results show that the outcome of herbivore-flower visitor interactions in B. nigra is specific for the combination of herbivore species and plant ontogenetic stage. Consequences of herbivory for flowering traits and reproductive output were strongest when plants were attacked early in life. Such differences in selection pressures imposed by herbivores to specific plant ontogenetic stages may drive the evolution of distinct ontogenetic trajectories in growth-defence-reproduction strategies and include indirect interactions between herbivores and flower visitors. Synthesis. Plant ontogeny can define the direct and indirect consequences of herbivory. Our study shows that the ontogenetic stage of plant individuals determined the effects of herbivory on plant flowering traits, interactions with flower visitors and plant fitness.
Project description:The timing of reproduction is a critical determinant of fitness, especially in organisms inhabiting seasonal environments. Increasing evidence suggests that inter-plant communication plays important roles in plant functioning. Here, we tested the hypothesis that flowering coordination can involve communication between neighboring plants. We show that soil leachates from Brassica rapa plants growing under long-day conditions accelerated flowering and decreased allocation to vegetative organs in target plants growing under non-inductive short-day conditions. The results suggest that besides endogenous signaling and external abiotic cues, flowering timing may involve inter-plant communication, mediated by root exudates. The study of flowering communication is expected to illuminate neglected aspects of plant reproductive interactions and to provide novel opportunities for controlling the timing of plant reproduction in agricultural settings.
Project description:Herbicide resistance is an example of plant evolution caused by an increased reliance on herbicides with few sites of action to manage weed populations. This micro-evolutionary process depends on fitness, therefore the assessment of fitness differences between susceptible and resistant populations are pivotal to establish management strategies. Loose silky bentgrass (Apera spica-venti) is a serious weed in Eastern, Northern, and Central Europe with an increasing number of herbicide resistant populations. This study examined the fitness and growth characteristics of an ALS resistant biotype. Fitness and growth characteristics were estimated by comparing seed germination, biomass, seed yield and time to key growth stages at four crop densities of winter wheat (0, 48, 96, and 192 plants m-2) in a target-neighborhood design. The resistant population germinated 9-20 growing degree days (GDD) earlier than the susceptible population at 10, 16, and 22°C. No differences were observed between resistant and susceptible populations in tiller number, biomass, time to stem elongation, time to first visible inflorescence and seed production. The resistant population reached the inflorescence emergence and flowering stages in less time by 383 and 196 GDD, respectively, at a crop density of 96 winter wheat plants m-2 with no differences registered at other densities. This study did not observe a fitness cost to herbicide resistance, as often hypothesized. Inversely, a correlation between non-target site resistance (NTSR), earlier germination and earlier flowering time which could be interpreted as fitness benefits as these plant characteristics could be exploited by modifying the timing and site of action of herbicide application to better control ALS NTSR populations of A. spica-venti.
Project description:In plants, extensive intra-specific variation exists in the allocation of resources between vegetative growth and reproduction, reflecting different functional strategies. A simple method for the classification of intra-specific variation in these strategies would enable characterization of evolutionary and ecological processes.C-S-R theory can be applied to classify functional strategies (competitive C; stress tolerant, S; ruderal, R) in different plant species. Using a diverse set of arabidopsis ( Arabidopsis thaliana ) accessions grown under common conditions, it was tested whether a simple approach designed for allocating C-S-R strategies at the species level can also be used to analyse intra-specific variation.Substantial intra-specific variation between arabidopsis accessions was found along the S-R axis. There was a positive correlation of temperature at the geographical origin with the dimension of S and a negative correlation with the dimension of R. Flowering time in a natural annual cycle and leaf dry matter content were identified as the main determinants of this adaptation, with plants originating from warmer climates having a higher leaf dry matter content and flowering earlier in a common garden.It was shown that functional strategies reflect adaptation to climate, with consequences for important traits such as fecundity and total plant dry weight. The approach could be used in genome-wide association studies to determine the genetic basis of functional strategies in wild species or crops.
Project description:Male plants of spinach (Spinacea oleracea L.) senesce following flowering. It has been suggested that nutrient drain by male flowers is insufficient to trigger senescence. The partitioning of radiolabelled photosynthate between vegetative and reproductive tissue was compared in male (staminate) versus female (pistillate) plants. After the start of flowering staminate plants senesce 3 weeks earlier than pistillate plants. Soon after the start of flowering, staminate plants allocated several times as much photosynthate to flowering structures as did pistillate plants. The buds of staminate flowers with developing pollen had the greatest draw of photosynthate. When the staminate plants begin to show senescence 68% of fixed C was allocated to the staminate reproductive structures. In the pistillate plants, export to the developing fruits and young flowers remained near 10% until mid-reproductive development, when it increased to 40%, declining to 27% as the plants started to senesce. These differences were also present on a sink-mass corrected basis. Flowers on staminate spinach plants develop faster than pistillate flowers and have a greater draw of photosynthate than do pistillate flowers and fruits, although for a shorter period. Pistillate plants also produce more leaf area within the inflorescence to sustain the developing fruits. The (14)C in the staminate flowers declined due to respiration, especially during pollen maturation; no such loss occurred in pistillate reproductive structures. The partitioning to the reproductive structures correlates with the greater production of floral versus vegetative tissue in staminate plants and their more rapid senescence. As at senescence the leaves still had adequate carbohydrate, the resources are clearly phloem-transported compounds other than carbohydrates. The extent of the resource redistribution to reproductive structures and away from the development of new vegetative sinks, starting very early in the reproductive phase, is sufficient to account for the triggering of senescence in the rest of the plant.
Project description:Plants have evolved developmental mechanisms to ensure reproduction when in sub-optimal local environments. The shade-avoidance syndrome is one such mechanism that causes plants to elongate and accelerate flowering. Plants sense shade via the decreased red:far-red (R:FR) ratio that occurs in shade. We explored natural variation in flowering behavior caused by a decrease in the R:FR ratio of Arabidopsis thaliana accessions. A survey of accessions revealed that most exhibit a vigorous rapid-flowering response in a FR-enriched environment. However, a subset of accessions appeared to be compromised in the accelerated-flowering component of the shade-avoidance response. The genetic basis of the muted response to FR enrichment was studied in three accessions (Fl-1, Hau-0, and Mir-0). For all three accessions, the reduced FR flowering-time effect mapped to the FLOWERING LOCUS T (FT) region, and the FT alleles from these accessions are expressed at a lower level in FR-enriched light compared to alleles from accessions that respond robustly to FR enrichment. In the Mir-0 accession, a second genomic region, which includes CONSTANTS (CO), also influenced flowering in FR-enriched conditions. We have demonstrated that variation in the degree of precocious flowering in shaded conditions (low R:FR ratio) results from allelic variation at FT.
Project description:FLOWERING LOCUS T (FT) encodes a systemic signal communicating the perception of long day photoperiod from leaves to the shoot apex to induce the floral transition. Transient expression of FT in the phloem companion cells of rosette leaves for one to several days was previously shown to be sufficient to commit plants to flowering. Here we show that partial commitment results in pleiotropic inflorescence meristem reversion phenotypes. FT expression is much stronger in organs formed after the floral transition such as cauline leaves, sepals, and developing siliques. We show that expression of FT and its paralog TWIN SISTER OF FT (TSF) after the floral transition plays a role in inflorescence meristem stabilization even if plants flower very late in development. CONSTANS (CO), the major activator of FT, is not required to prevent late reproductive reversion. The requirement for FT is temporal since reproductive reversion to a vegetative state occurs only in recently formed inflorescence meristems. Unlike for the expression of FT in leaves, neither the distal putative FT enhancer nor long-day photoperiod is required for FT expression in developing siliques. Expression of FT in developing siliques and their supporting stems is sufficient to stabilize flowering during the sensitive developmental window indicating that fruit generated FT participates in inflorescence stabilization.