Nearly 100 genes and functional polymorphisms underlying natural variation in plant development and physiology have been identified. In crop plants, these include genes involved in domestication ...traits, such as those related to plant architecture, fruit and seed structure and morphology, as well as yield and quality traits improved by subsequent crop breeding. In wild plants, comparable traits have been dissected mainly in Arabidopsis thaliana. In this review, we discuss the major contributions of the analysis of natural variation to our understanding of plant development and physiology, focusing in particular on the timing of germination and flowering, plant growth and morphology, primary metabolism, and mineral accumulation. Overall, functional polymorphisms appear in all types of genes and gene regions, and they may have multiple mutational causes. However, understanding this diversity in relation to adaptation and environmental variation is a challenge for which tools are now available.
Seeds are unique time capsules that can switch between 2 complex and highly interlinked stages: seed dormancy and germination. Dormancy contributes to the survival of plants because it allows to ...delay germination to optimal conditions. The switch between dormancy and germination occurs in response to developmental and environmental cues. In this review we provide a comprehensive overview of studies that have helped to unravel the molecular mechanisms underlying dormancy and germination over the last decades. Genetic and physiological studies provided a strong foundation for this field of research and revealed the critical role of the plant hormones abscisic acid and gibberellins in the regulation of dormancy and germination, and later natural variation studies together with quantitative genetics identified previously unknown genetic components that control these processes. Omics technologies like transcriptome, proteome, and translatomics analysis allowed us to mechanistically dissect these processes and identify new components in the regulation of seed dormancy and germination.
Sugar-induced anthocyanin accumulation has been observed in many plant species. We observed that sucrose (Suc) is the most effective inducer of anthocyanin biosynthesis in Arabidopsis (Arabidopsis ...thaliana) seedlings. Other sugars and osmotic controls are either less effective or ineffective. Analysis of Suc-induced anthocyanin accumulation in 43 Arabidopsis accessions shows that considerable natural variation exists for this trait. The Cape Verde Islands (Cvi) accession essentially does not respond to Suc, whereas Landsberg erecta is an intermediate responder. The existing Landsberg erecta/Cvi recombinant inbred line population was used in a quantitative trait loci analysis for Suc-induced anthocyanin accumulation (SIAA). A total of four quantitative trait loci for SIAA were identified in this way. The locus with the largest contribution to the trait, SIAA1, was fine mapped and using a candidate gene approach, it was shown that the MYB75/PAP1 gene encodes SIAA1. Genetic complementation studies and analysis of a laboratory-generated knockout mutation in this gene confirmed this conclusion. Suc, in a concentration-dependent way, induces MYB75/PAP1 mRNA accumulation. Moreover, MYB75/PAP1 is essential for the Suc-mediated expression of the dihydroflavonol reductase gene. The SIAA1 locus in Cvi probably is a weak or loss-of-function MYB75/PAP1 allele. The C24 accession similarly shows a very weak response to Suc-induced anthocyanin accumulation encoded by the same locus. Sequence analysis showed that the Cvi and C24 accessions harbor mutations both inside and downstream of the DNA-binding domain of the MYB75/PAP1 protein, which most likely result in loss of activity.
Summary
Primary seed dormancy is a mechanism that orchestrates the timing of seed germination in order to prevent out‐of‐season germination. Secondary dormancy can be induced in imbibed seeds when ...they encounter prolonged unfavourable conditions. Secondary dormancy is not induced during dry storage, and therefore the mechanisms underlying this process have remained largely unexplored. Here, a 2‐year seed burial experiment in which dormancy cycling was studied at the physiological and transcriptional level is presented. For these analyses six different Arabidopsis thaliana genotypes were used: Landsberg erecta (Ler) and the dormancy associated DELAY OF GERMINATION (DOG) near‐isogenic lines 1, 2, 3, 6 and 22 (NILDOG1, 2, 3, 6 and 22). The germination potential of seeds exhumed from the field showed that these seeds go through dormancy cycling and that the dynamics of this cycling is genotype dependent. RNA‐seq analysis revealed large transcriptional changes during dormancy cycling, especially at the time points preceding shifts in dormancy status. Dormancy cycling is driven by soil temperature and the endosperm is important in the perception of the environment. Genes that are upregulated in the low‐ to non‐dormant stages are enriched for genes involved in translation, indicating that the non‐dormant seeds are prepared for rapid seed germination.
Significance Statement
Little is known about seed dormancy under natural conditions. This field study provides an in‐depth insight, at the physiological and transcriptional level, of how Arabidopsis seeds cycle through dormancy. We show that dormancy is strongly regulated by the environment, both by seasonal changes as well as by sudden changes. We identified large transcriptional changes and show that in particular the translational machinery is upregulated when seeds are non‐dormant.
Seeds accumulate mRNA during their development and have the ability to store these mRNAs over extended periods of time. On imbibition, seeds transform from a quiescent dry state (no translation) to a ...fully active metabolic state, and selectively translate subsets of these stored mRNA. Thus, seeds provide a unique developmentally regulated ‘on/off’ switch for translation. Additionally, there is extensive translational control during seed germination. Here we discuss new findings and hypotheses linked to mRNA fate and the role of translational regulation in seeds. Translation is an understated yet important mode of gene regulation. We propose seeds as a novel system to study developmentally and physiologically regulated translation.
Translational regulation is an underexplored but important aspect of gene regulation.
Powerful techniques like polysome profiling and Ribo-Seq have made it possible to reveal the translational status of mRNA subsets in cells.
There is extensive translational regulation during seed germination.
Subpopulations of mRNAs are predestined for distinct processes depending on the physiological state of the seed.
The transition between dormancy and germination represents a critical stage in the life cycle of higher plants and is an important ecological and commercial trait. In this review we present current ...knowledge of the molecular control of this trait in Arabidopsis thaliana, focussing on important components functioning during the developmental phases of seed maturation, after-ripening and imbibition. Establishment of dormancy during seed maturation is regulated by networks of transcription factors with overlapping and discrete functions. Following desiccation, after-ripening determines germination potential and, surprisingly, recent observations suggest that transcriptional and post-transcriptional processes occur in the dry seed. The single-cell endosperm layer that surrounds the embryo plays a crucial role in the maintenance of dormancy, and transcriptomics approaches are beginning to uncover endosperm-specific genes and processes. Molecular genetic approaches have provided many new components of hormone signalling pathways, but also indicate the importance of hormone-independent pathways and of natural variation in key regulatory loci. The influence of environmental signals (particularly light) following after-ripening, and the effect of moist chilling (stratification) are increasingly being understood at the molecular level. Combined postgenomics, physiology and molecular genetics approaches are beginning to provide an unparalleled understanding of the molecular processes underlying dormancy and germination.
Seed performance after dispersal is highly dependent on parental environmental cues, especially during seed formation and maturation. Here we examine which environmental factors are the most dominant ...in this respect and whether their effects are dependent on the genotypes under investigation. We studied the influence of light intensity, photoperiod, temperature, nitrate, and phosphate during seed development on five plant attributes and thirteen seed attributes, using 12 Arabidopsis genotypes that have been reported to be affected in seed traits. As expected, the various environments during seed development resulted in changed plant and/or seed performances. Comparative analysis clearly indicated that, overall, temperature plays the most dominant role in both plant and seed performance, whereas light has a prominent impact on plant traits. In comparison to temperature and light, nitrate mildly affected some of the plant and seed traits while phosphate had even less influence on those traits. Moreover, clear genotype-by-environment interactions were identified. This was shown by the fact that individual genotypes responded differentially to the environmental conditions. Low temperature significantly increased seed dormancy and decreased seed longevity of NILDOG1 and cyp707a1-1, whereas low light intensity increased seed dormancy and decreased seed longevity of NILDOG3 and NILDOG6. This also indicates that different genetic and molecular pathways are involved in the plant and seed responses. By identifying environmental conditions that affect the dormancy vs longevity correlation in the same way as previously identified naturally occurring loci, we have identified selective forces that probably shaped evolution for these important seed traits.
Highlight textThe genotype-by-environment interactions of five parental environments with seed and plant performance are mediated by distinct genetic and molecular pathways, and the selective pressures that have shaped their natural variation.
Genetic variation for seed dormancy in nature is a typical quantitative trait controlled by multiple loci on which environmental factors have a strong effect. Finding the genes underlying dormancy ...quantitative trait loci is a major scientific challenge, which also has relevance for agriculture and ecology. In this study we describe the identification of the DELAY OF GERMINATION 1 (DOG1) gene previously identified as a quantitative trait locus involved in the control of seed dormancy. This gene was isolated by a combination of positional cloning and mutant analysis and is absolutely required for the induction of seed dormancy. DOG1 is a member of a small gene family of unknown molecular function, with five members in Arabidopsis. The functional natural allelic variation present in Arabidopsis is caused by polymorphisms in the cis-regulatory region of the DOG1 gene and results in considerable expression differences between the DOG1 alleles of the accessions analyzed.
The importance of translational regulation during Arabidopsis seed germination has been shown previously. Here the role of transcriptional and translational regulation during seed imbibition of the ...very dormant DELAY OF GERMINATION 1 (DOG1) near-isogenic line was investigated.
Polysome profiling was performed on dormant and after-ripened seeds imbibed for 6 and 24 h in water and in the transcription inhibitor cordycepin. Transcriptome and translatome changes were investigated.
Ribosomal profiles of after-ripened seeds imbibed in cordycepin mimic those of dormant seeds. The polysome occupancy of mRNA species is not affected by germination inhibition, either as a result of seed dormancy or as a result of cordycepin treatment, indicating the importance of the regulation of transcript abundance.
The expression of auxin metabolism genes is discriminative during the imbibition of after-ripened and dormant seeds, which is confirmed by altered concentrations of indole-3-acetic acid conjugates and precursors.
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