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Weedy rice, a pervasive and troublesome weed found across the globe, has often evolved through fertilization of rice cultivars with little importance of crop-weed gene flow. In Argentina, weedy rice has been reported as an important constraint since the early 1970s, and, in the last few years, strains with herbicide-resistance are suspected to evolve. Despite their importance, the origin and genetic composition of Argentinian weedy rice as well its adaptation to agricultural environments has not been explored so far. To study this, we conducted genotyping-by-sequencing on samples of Argentinian weedy and cultivated rice and compared them with published data from weedy, cultivated and wild rice accessions distributed worldwide. In addition, we conducted a phenotypic characterization for weedy-related traits, a herbicide resistance screening and genotyped accessions for known mutations in the acetolactate synthase (ALS) gene, which confers herbicide resistance. Our results revealed large phenotypic variability in Argentinian weedy rice. Most strains were resistant to ALS-inhibiting herbicides with a high frequency of the ALS mutation (A122T) present in Argentinian rice cultivars. Argentinian cultivars belonged to the three major genetic groups of rice: japonica, indica and aus while weeds were mostly aus or aus-indica admixed, resembling weedy rice strains from the Southern Cone region. Phylogenetic analysis supports a single origin for aus-like South American weeds, likely as seed contaminants from the United States, and then admixture with local indica cultivars. Our findings demonstrate that crop to weed introgression can facilitate rapid adaptation to agriculture environments.
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Acetolactato Sintase , Resistência a Herbicidas , Herbicidas , Oryza , Oryza/genética , Resistência a Herbicidas/genética , Argentina , Acetolactato Sintase/genética , Plantas Daninhas/genética , Fenótipo , Genótipo , Adaptação Fisiológica/genética , Produtos Agrícolas/genética , Fluxo Gênico , Agricultura , MutaçãoRESUMO
Plants synchronize their growth and development with environmental changes, which is critical for their survival. Among their life cycle transitions, seed germination is key for ensuring the survival and optimal growth of the next generation. However, even under favorable conditions, oftentimes germination can be blocked by seed dormancy, a regulatory multilayered checkpoint integrating internal and external signals. Intricate genetic and epigenetic mechanisms underlie seed dormancy establishment, maintenance, and release. In this review, we focus on recent advances that shed light on the complex mechanisms associated with physiological dormancy, prevalent in seed plants, with Arabidopsis thaliana serving as a model. Here, we summarize the role of multiple epigenetic regulators, but with a focus on histone modifications like acetylation and methylation, that finely tune dormancy responses and influence dormancy-associated gene expression. Understanding these mechanisms can lead to a better understanding of seed biology in general, as well as result in the identification of possible targets for breeding climate-resilient plants.
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BACKGROUND AND AIMS: Plants respond in a plastic manner to seasonal changes, often resulting in adaptation to environmental variation. Although much is known about how seasonality regulates developmental transitions within generations, transgenerational effects of non-stressful environmental changes are only beginning to be unveiled. This study aimed to evaluate the effects of ambient temperature changes on the expression of transgenerational plasticity in key developmental traits of Arabidopsis thaliana plants. METHODS: We grew Columbia-0 plants in two contrasting temperature environments (18 and 24 °C) during their whole life cycles, or the combination of those temperatures before and after bolting (18-24 and 24-18 °C) across two generations. We recorded seed germination, flowering time and reproductive biomass production for the second generation, and seed size of the third generation. KEY RESULTS: The environment during the whole life cycle of the first generation of plants, even that experienced before flowering, influenced the germination response and flowering time of the second generation. These effects showed opposing directions in a pattern dependent on the life stage experiencing the cue in the first generation. In contrast, the production of reproductive biomass depended on the immediate environment of the progeny generation. Finally, the seed area of the third generation was influenced positively by correlated environments across generations. CONCLUSIONS: Our results suggest that non-stressful environmental changes affect the expression of key developmental traits across generations, although those changes can have contrasting effects depending on the parental and grandparental life stage that perceives the cue. Thus, transgenerational effects in response to non-stressful cues might influence the expression of life-history traits and potential adaptation of future generations.
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Arabidopsis , Animais , Arabidopsis/fisiologia , Temperatura , Germinação/fisiologia , Estágios do Ciclo de Vida , Sementes/fisiologia , Adaptação FisiológicaRESUMO
Plant hybridization is a pathway for the evolution of adaptive traits. However, hybridization between adapted and nonadapted populations may affect the persistence of combinations of adaptive alleles evolved through natural selection. Seed dormancy is an adaptive trait for weedy rice because it regulates the timing of seed germination and the persistence of the soil seed bank. Hybridization between weedy and cultivated rice has been confirmed with an adaptive introgression of deep seed dormancy alleles from cultivated rice. Here, we explored the influence of hybridization on the conservation of adaptive allele combinations by evaluating natural variation and genetic structure in seed dormancy-associated genomic regions. Based on sequence variation in the genomic regions associated with seed dormancy, hybrid-derived weedy rice strains maintained most of the adaptive combinations for this trait observed in the parental weedy rice, despite equal representation of the parental weedy and cultivated rice in the whole genome sequence. Moreover, hybrid-derived weedy rice strains were more dormant than their parental weedy rice strains, and this trait was strongly influenced by the environment. This study suggests that hybridization between weedy rice (adaptive allelic combinations for seed dormancy) and cultivated rice (nonadaptive combinations) generates weedy rice strains expressing deep seed dormancy caused by genome stabilization through the removal of alleles derived from cultivated rice, in addition to the adaptive introgression of deep seed dormancy alleles derived from cultivated rice. Thus, hybridization between adapted and nonadapted populations appears to be reinforcing the trajectory towards the evolution of adaptive traits.
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Oryza , Oryza/genética , Alelos , Dormência de Plantas/genética , Variação Genética/genética , Evolução Molecular , Plantas Daninhas/genéticaRESUMO
Pleiotropy occurs when one gene influences more than one trait, contributing to genetic correlations among traits. Consequently, it is considered a constraint on the evolution of adaptive phenotypes because of potential antagonistic selection on correlated traits, or, alternatively, preservation of functional trait combinations. Such evolutionary constraints may be mitigated by the evolution of different functions of pleiotropic genes in their regulation of different traits. Arabidopsis thaliana flowering-time genes, and the pathways in which they operate, are among the most thoroughly studied regarding molecular functions, phenotypic effects, and adaptive significance. Many of them show strong pleiotropic effects. Here, we review examples of pleiotropy of flowering-time genes and highlight those that also influence seed germination. Some genes appear to operate in the same genetic pathways when regulating both traits, whereas others show diversity of function in their regulation, either interacting with the same genetic partners but in different ways or potentially interacting with different partners. We discuss how functional diversification of pleiotropic genes in the regulation of different traits across the life cycle may mitigate evolutionary constraints of pleiotropy, permitting traits to respond more independently to environmental cues, and how it may even contribute to the evolutionary divergence of gene function across taxa.
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Evolução Biológica , Flores/crescimento & desenvolvimento , Flores/genética , Regulação da Expressão Gênica de Plantas , Pleiotropia Genética , Arabidopsis/genética , Arabidopsis/crescimento & desenvolvimento , Variação GenéticaRESUMO
Background and Aims: Two critical developmental transitions in plants are seed germination and flowering, and the timing of these transitions has strong fitness consequences. How genetically independent the regulation of these transitions is can influence the expression of life cycles. Method: This study tested whether genes in the autonomous flowering-time pathway pleiotropically regulate flowering time and seed germination in the genetic model Arabidopsis thaliana, and tested whether the interactions among those genes are concordant between flowering and germination stages. Key Results: Several autonomous-pathway genes promote flowering and impede germination. Moreover, the interactions among those genes were highly concordant between the regulation of flowering and germination. Conclusions: Despite some degree of functional divergence between the regulation of flowering and germination by autonomous-pathway genes, the autonomous pathway is highly functionally conserved across life stages. Therefore, genes in the autonomous flowering-time pathway are likely to contribute to genetic correlations between flowering and seed germination, possibly contributing to the winter-annual life history.
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Arabidopsis/fisiologia , Flores/crescimento & desenvolvimento , Germinação , Sementes/fisiologia , Arabidopsis/crescimento & desenvolvimento , Germinação/fisiologia , Fatores de TempoRESUMO
Different life stages frequently respond to the same environmental cue to regulate development so that each life stage is matched to its appropriate season. We investigated how independently each life stage can respond to shared environmental cues, focusing on vernalization, in Arabidopsis thaliana plants. We first tested whether effects of rosette vernalization persisted to influence seed germination. To test whether genes in the vernalization flowering pathway also influence germination, we assessed germination of functional and nonfunctional alleles of these genes and measured their level of expression at different life stages in response to rosette vernalization. Rosette vernalization increased seed germination in diverse ecotypes. Genes in the vernalization flowering pathway also influenced seed germination. In the Columbia accession, functional alleles of most of these genes opposed the germination response observed in the ecotypes. Some genes influenced germination in a manner consistent with their known effects on FLOWERING LOCUS C gene regulation during the transition to flowering. Others did not, suggesting functional divergence across life stages. Despite persistent effects of environmental conditions across life stages, and despite pleiotropy of genes that affect both flowering and germination, the function of these genes can differ across life stages, potentially mitigating pleiotropic constraints and enabling independent environmental regulation of different life stages.
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Arabidopsis/embriologia , Arabidopsis/genética , Temperatura Baixa , Genes de Plantas , Germinação/genética , Sementes/embriologia , Sementes/genética , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , DNA Bacteriano/genética , Ecótipo , Flores/genética , Flores/fisiologia , Regulação da Expressão Gênica de Plantas , Genótipo , Modelos Biológicos , Mutação/genéticaRESUMO
Contents 343 I. 343 II. 343 III. 347 IV. 348 348 References 348 SUMMARY: There is renewed interest in how transgenerational environmental effects, including epigenetic inheritance, contribute to adaptive evolution. The contribution of across-generation plasticity to adaptation, however, needs to be evaluated within the context of within-generation plasticity, which is often proposed to contribute more efficiently to adaptation because of the potentially greater accuracy of progeny than parental cues to predict progeny selective environments. We highlight recent empirical studies of transgenerational plasticity, and find that they do not consistently support predictions based on the higher predictive ability of progeny environmental cues. We discuss these findings within the context of the relative predictive ability of maternal and progeny cues, costs and constraints of plasticity in parental and progeny generations, and the dynamic nature of the adaptive value of within- and across-generation plasticity that varies with the process of adaptation itself. Such contingent and dynamically variable selection could account for the diversity of patterns of within- and across-generation plasticity observed in nature, and can influence the adaptive value of the persistence of environmental effects across generations.
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Adaptação Fisiológica , Meio Ambiente , FenótipoRESUMO
PREMISE OF THE STUDY: Plants adjust their phenology in response to seasonal cues experienced both by their parents and by themselves, and coordinating responses to these cues is necessary for expressing adaptive phenology. We investigated how cues are integrated across time to influence an important progeny phenotype, i.e., seed germination. METHODS: We used Arabidopsis thaliana to investigate how the photoperiod experienced by maternal parents and by progeny influences seed germination. We examined when maternal photoperiod effects on germination are imposed and how long they persist in progeny. KEY RESULTS: The photoperiod experienced by maternal plants more strongly influenced germination than the photoperiod experienced during seed imbibition. In addition, the photoperiod experienced at the prereproductive stage frequently influenced germination as strongly as that experienced during reproduction. In general, seeds from plants grown under short days had higher seed germination percentages than seeds from plants grown in longer days. These maternal effects diminished with after-ripening, but reappeared in seeds induced into secondary dormancy. CONCLUSIONS: We found no evidence that the effect of photoperiod systematically attenuates in proportion to the time that elapsed between the cue and the timing of seed germination. Moreover, more recently experienced cues did not override the effects of cues experienced previously. Instead, specific sequences of photoperiods experienced at the prereproductive and reproductive stages appear to influence germination behavior.
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Arabidopsis/fisiologia , Germinação/fisiologia , Fotoperíodo , Sementes/crescimento & desenvolvimento , Arabidopsis/efeitos da radiação , Germinação/efeitos da radiação , Dormência de Plantas/fisiologia , Dormência de Plantas/efeitos da radiação , Reprodução/fisiologia , Reprodução/efeitos da radiação , Sementes/fisiologiaRESUMO
BACKGROUND: Seeds adjust their germination based on conditions experienced before and after dispersal. Post-dispersal cues are expected to be more accurate predictors of offspring environments, and thus offspring success, than pre-dispersal cues. Therefore, germination responses to conditions experienced during seed maturation may be expected to be superseded by responses to conditions experienced during seed imbibition. In taxa of disturbed habitats, neighbours frequently reduce the performance of germinants. This leads to the hypotheses that a vegetative canopy will reduce germination in such taxa, and that a vegetative canopy experienced during seed imbibition will over-ride germination responses to a canopy experienced during seed maturation, since it is a more proximal cue of immediate competition. These hypotheses were tested here in Arabidopsis thaliana METHODS: Seeds were matured under a simulated canopy (green filter) or white light. Fresh (dormant) seeds were imbibed in the dark, white light or canopy at two temperatures (10 or 22 °C), and germination proportions were recorded. Germination was also recorded in after-ripened (less dormant) seeds that were induced into secondary dormancy and imbibed in the dark at each temperature, either with or without brief exposure to red and far-red light. KEY RESULTS: Unexpectedly, a maturation canopy expanded the conditions that elicited germination, even as seeds lost and regained dormancy. In contrast, an imbibition canopy impeded or had no effect on germination. Maturation under a canopy did not modify germination responses to red and far-red light. Seed maturation under a canopy masked genetic variation in germination. CONCLUSIONS: The results challenge the hypothesis that offspring will respond more strongly to their own environment than to that of their parents. The observed relaxation of germination requirements caused by a maturation canopy could be maladaptive for offspring by disrupting germination responses to light cues after dispersal. Alternatively, reduced germination requirements could be adaptive by allowing seeds to germinate faster and reduce competition in later stages even though competition is not yet present in the seedling environment. The masking of genetic variation by maturation under a canopy, moreover, could impede evolutionary responses to selection on germination.
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Germinação/fisiologia , Arabidopsis/crescimento & desenvolvimento , Ecologia , Meio Ambiente , Germinação/efeitos da radiação , Sementes/crescimento & desenvolvimento , Sementes/efeitos da radiação , Luz Solar , TemperaturaRESUMO
Plants are extremely plastic organisms. They continuously receive and integrate environmental information and adjust their growth and development to favour fitness and survival. When this integration of information affects subsequent life stages or the development of subsequent generations, it can be considered an environmental memory. Thus, plant memory is a relevant mechanism by which plants respond adaptively to different environments. If the cost of maintaining the response is offset by its benefits, it may influence evolutionary trajectories. As such, plant memory has a sophisticated underlying molecular mechanism with multiple components and layers. Nonetheless, when mathematical modelling is combined with knowledge of ecological, physiological, and developmental effects as well as molecular mechanisms as a tool for understanding plant memory, the combined potential becomes unfathomable for the management of plant communities in natural and agricultural ecosystems. In this review, we summarize recent advances in the understanding of plant memory, discuss the ecological requirements for its evolution, outline the multilayered molecular network and mechanisms required for accurate and fail-proof plant responses to variable environments, point out the direct involvement of the plant metabolism and discuss the tremendous potential of various types of models to further our understanding of the plant's environmental memory. Throughout, we emphasize the use of plant memory as a tool to unlock the secrets of the natural world.
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Grain sorghum [Sorghum bicolor (L) moench] exhibits intraspecific variability for the rate of dormancy release and pre-harvest sprouting behavior. Two inbred lines with contrasting sprouting response were compared: IS9530 (resistant) and RedlandB2 (susceptible). Precocious dormancy release in RedlandB2 is related to an early loss of embryo sensitivity to ABA and higher levels of gibberellins in imbibed grains as compared with IS9530. With the aim of identifying potential regulatory sites for gibberellin metabolism involved in the expression of dormancy in immature grains of both lines, we carried out a time course analysis of transcript levels of putative gibberellin metabolism genes and hormone content (GA(1), GA(4), GA(8) and GA(34)). A lower embryonic GA(4) level in dormant IS9530 was related to a sharp and transient induction of two SbGA2-oxidase (inactivation) genes. In contrast, these genes were not induced in less dormant RedlandB2, while expression of two SbGA20-oxidase (synthesis) genes increased together with active GA(4) levels before radicle protrusion. Embryonic levels of GA(4) and its catabolite GA(34) correlated negatively. Thus, in addition to the process of gibberellin synthesis, inactivation is also important in regulating GA(4) levels in immature grains. A negative regulation by gibberellins was observed for SbGA20ox2, SbGA2ox1 and SbGA2ox3 and also for SbGID1 encoding a gibberellin receptor. We propose that the coordinated regulation at the transcriptional level of several gibberellin metabolism genes identified in this work affects the balance between gibberellin synthesis and inactivation processes, controlling active GA(4) levels during the expression of dormancy in maturing sorghum grains.
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Agricultura , Regulação da Expressão Gênica de Plantas , Genes de Plantas/genética , Giberelinas/metabolismo , Dormência de Plantas/genética , Sorghum/crescimento & desenvolvimento , Sorghum/genética , Perfilação da Expressão Gênica , Regulação da Expressão Gênica no Desenvolvimento , Filogenia , RNA Mensageiro/genética , RNA Mensageiro/metabolismo , Sementes/genética , Sementes/crescimento & desenvolvimento , Sorghum/enzimologiaRESUMO
Stresses resulting from high transpiration demand induce adjustments in plants that lead to reductions of water loss. These adjustments, including changes in water absorption, transport and/or loss by transpiration, are crucial to normal plant development. Tomato wild type (WT) and phytochrome A (phyA)-mutant plants, fri1-1, were exposed to conditions of either low or high transpiration demand and several morphological and physiological changes were measured during stress conditions. Mutant plants rapidly wilted compared to WT plants after exposure to high evaporative demand. Root size and hydraulic conductivity did not show significant differences between genotypes, suggesting that water absorption and transport through this organ could not explain the observed phenotype. Moreover, stomatal density was similar between genotypes, whereas transpiration and stomatal conductance were both lower in mutant than in WT plants. This was accompanied by a lower stem-specific hydraulic conductivity in mutant plants, which was associated to lower xylem vessel number and transversal area in fri1-1 plants, producing a reduction in water supply to the leaves, which rapidly wilted under high evaporative demand. PhyA signaling might facilitate the adjustment to environments differing widely in water evaporative demand in part through the modulation of xylem dimensions.
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Transporte Biológico/fisiologia , Fitocromo A/metabolismo , Transpiração Vegetal/fisiologia , Solanum lycopersicum/crescimento & desenvolvimento , Solanum lycopersicum/fisiologia , Água/metabolismo , Aclimatação , Variação Genética , Genótipo , Solanum lycopersicum/genética , Folhas de Planta/fisiologia , Raízes de Plantas/fisiologia , Caules de Planta/fisiologia , Estômatos de Plantas/fisiologia , Especificidade da Espécie , Estresse Fisiológico , Luz Solar , Xilema/metabolismoRESUMO
The RNA-directed DNA Methylation pathway (RdDM) influences progeny seed responses to different maternal environments. However, its role in the regulation of early traits in response to non-stressful environmental cues across generations, which can potentially affect life cycle adjustment to seasonal changes, has not been explored in detail. Here we show that the RdDM pathway regulates overall germination but, in some instances, it does so depending on the early life maternal environment. Altogether, our results support that epigenetic memory (mediated by RdDM) is regulating intergenerational transmission of environmental information to affect the phenotypic expression of early traits.
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Tomato (Solanum lycopersicum) seed germination can be inhibited by continuous irradiation with far-red light (FRc) and re-induced by a subsequent red light pulse. In this study, we carried out a global transcript analysis of seeds subjected to FRc inhibitory treatment, with and without a subsequent red light pulse, using potato cDNA microarrays. We also identified and characterized genes involved in light-modulated germination as elements of the phytochrome signalling pathway. Microarray data showed that the inhibition of germination by FRc involves the induction of a large number of genes and the repression of a significantly smaller quantity. Multivariate analysis established an underlying pattern of expression dependent on physiological treatment and incubation time, and identified different groups of genes associated with dormancy maintenance, inhibition and promotion of germination. We showed that ELIP, CSN6, SOS2 and RBP are related to the photocontrol of germination. These genes are known to participate in other physiological processes, but their participation in germination has not been suggested previously. Light quality regulates the tomato seed transcriptome during phytochrome-modulated germination through changes in the expression of certain sets of genes. In addition, ELIP and GIGANTEA were confirmed as components of the phytochrome A signalling pathway during FRc inhibition of germination.
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Perfilação da Expressão Gênica , Regulação da Expressão Gênica de Plantas/efeitos da radiação , Germinação/genética , Germinação/efeitos da radiação , Luz , Sementes/genética , Solanum lycopersicum/genética , Genes de Plantas , Solanum lycopersicum/efeitos da radiação , Família Multigênica , Análise Multivariada , Análise de Sequência com Séries de Oligonucleotídeos , Regiões Promotoras Genéticas/genética , Reprodutibilidade dos Testes , Sementes/efeitos da radiaçãoRESUMO
Plants respond not only to the environment in which they find themselves, but also to that of their parents. The combination of within- and trans-generational phenotypic plasticity regulates plant development. Plants use light as source of energy and also as a cue of competitive conditions, since the quality of light (ratio of red to far-red light, R:FR) indicates the presence of neighbouring plants. Light regulates many aspects of plant development, including seed germination. To understand how seeds integrate environmental cues experienced at different times, we quantified germination responses to changes in light quantity (irradiance) and quality (R:FR) experienced during seed maturation and seed imbibition in Arabidopsis thaliana genotypes that differ in their innate dormancy levels and after treatments that break or reinduce dormancy. In two of the genotypes tested, reduced irradiance as well as reduced R:FR during seed maturation induced higher germination; thus, the responses to light quantity and R:FR reinforced each other. In contrast, in a third genotype, reduced irradiance during seed maturation induced progeny germination, but response to reduced R:FR was in the opposite direction, leading to a very weak or no overall effect of a simulated canopy experienced by the mother plant. During seed imbibition, reduced irradiance and reduced R:FR caused lower germination in all genotypes. Therefore, responses to light experienced at different times (maturation vs. imbibition) can have opposite effects. In summary, seeds responded both to light resources (irradiance) and to cues of competition (R:FR), and trans-generational plasticity to light frequently opposed and was stronger than within-generation plasticity.
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FLOWERING LOCUS C (FLC) has a major regulatory role in the timing of flowering in Arabidopsis thaliana (L.) Heynh. and has more recently been shown to influence germination. Here, we investigated the conditions under which FLC influences germination, and demonstrated that its effect depends on the level of primary and secondary dormancy and the temperature of seed imbibition. We tested the germination response of genotypes with different degrees of FLC activity over the course of after-ripening and after secondary dormancy induction by hot stratification. Genotypes with high FLC-activity showed higher germination; this response was greatest when seeds exhibited primary dormancy or were induced into secondary dormancy by hot stratification. In this study, which used less dormant seeds, the effect of FLC was more evident at 22°C, the less permissive germination temperature, than at 10°C, in contrast to prior published results that used more dormant seeds. Thus, because effects of FLC variation depend on dormancy, and because the range of temperature that permits germination also depends on dormancy, the temperature at which FLC affects germination can also vary with dormancy. Finally, we document that the effect of FLC can depend on FRIGIDA and that FRIGIDA itself appears to influence germination. Thus, pleiotropy between germination and flowering pathways in A. thaliana extends beyond FLC and involves other genes in the FLC genetic pathway.
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In Arabidopsis seeds, germination is promoted only by phytochromes, principally phytochrome B (phyB) and phytochrome A (phyA). Despite the abundant information concerning the molecular basis of phyB signaling downstream of PIF1/PIL5, the signaling network inducing germination by phyA is poorly known. Here, we describe the influence of phyA on the transcriptome of Arabidopsis seeds when germination is induced by a far-red (FR) pulse. The expression of 11% of the genome was significantly regulated by phyA. Most of the genes were up-regulated and the changes noted late (i.e. 5 h after a FR pulse), whereas changes in down-regulated genes were more abundant earlier (i.e. 0.5 h after a FR pulse). Auxin- and GA-associated elements were overrepresented in the genes that were modified by phyA. A significant number of genes whose expression was affected by phyA had not been previously reported to be dependent on PIL5. Among them, homozygotic mutant seeds of MYB66, a SAUR-like protein, PIN7, and GASA4 showed an impaired promotion of germination by phyA. Natural variation at the transcriptional level was found in early signaling and GA metabolic genes, but not in ABA metabolic and expansin genes between Columbia and Landsberg erecta accessions. Although phyA and phyB/PIL5 signaling pathways share some molecular components, our data suggest that phyA signaling is partially independent of PIL5 when germination is promoted by very low fluences of light.