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Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis.

ABSTRACT: After-ripening (AR) is a time and environment regulated process occurring in the dry seed, which determines the germination potential of seeds. Both metabolism and perception of the phytohormone abscisic acid (ABA) are important in the initiation and maintenance of dormancy. However, molecular mechanisms that regulate the capacity for dormancy or germination through AR are unknown. To understand the relationship between ABA and AR, we analysed genome expression in Arabidopsis thaliana mutants defective in seed ABA synthesis (aba1-1) or perception (abi1-1). Even though imbibed mutant seeds showed no dormancy, they exhibited changes in global gene expression resulting from dry AR that were comparable with changes occurring in wild-type (WT) seeds. Core gene sets were identified that were positively or negatively regulated by dry seed storage. Each set included a gene encoding repression or activation of ABA function (LPP2 and ABA1, respectively), thereby suggesting a mechanism through which dry AR may modulate subsequent germination potential in WT seeds. Application of exogenous ABA to after-ripened WT seeds did not reimpose characteristics of freshly harvested seeds on imbibed seed gene expression patterns. It was shown that secondary dormancy states reinstate AR status-specific gene expression patterns. A model is presented that separates the action of ABA in seed dormancy from AR and dry storage regulated gene expression. These results have major implications for the study of genetic mechanisms altered in seeds as a result of crop domestication into agriculture, and for seed behaviour during dormancy cycling in natural ecosystems.

SUBMITTER: Carrera E

PROVIDER: S-EPMC2254144 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Seed metabolism is dynamically adjusted to oxygen availability. Processes underlying this auto-regulatory mechanism control the metabolic efficiency under changing environmental conditions/stress and thus, are of relevance for biotechnology. Non-symbiotic hemoglobins have been shown to be involved in scavenging of nitric oxide (NO) molecules, which play a key role in oxygen sensing/balancing in plants and animals. Steady state levels of NO are suggested to act as an integrator of energy and carbon metabolism and subsequently, influence energy-demanding growth processes in plants. RESULTS: We aimed to manipulate oxygen stress perception in Arabidopsis seeds by overexpression of the non-symbiotic hemoglobin AtHb1 under the control of the seed-specific LeB4 promoter. Seeds of transgenic AtHb1 plants did not accumulate NO under transient hypoxic stress treatment, showed higher respiratory activity and energy status compared to the wild type. Global transcript profiling of seeds/siliques from wild type and transgenic plants under transient hypoxic and standard conditions using Affymetrix ATH1 chips revealed a rearrangement of transcriptional networks by AtHb1 overexpression under non-stress conditions, which included the induction of transcripts related to ABA synthesis and signaling, receptor-like kinase- and MAP kinase-mediated signaling pathways, WRKY transcription factors and ROS metabolism. Overexpression of AtHb1 shifted seed metabolism to an energy-saving mode with the most prominent alterations occurring in cell wall metabolism. In combination with metabolite and physiological measurements, these data demonstrate that AtHb1 overexpression improves oxidative stress tolerance compared to the wild type where a strong transcriptional and metabolic reconfiguration was observed in the hypoxic response. CONCLUSIONS: AtHb1 overexpression mediates a pre-adaptation to hypoxic stress. Under transient stress conditions transgenic seeds were able to keep low levels of endogenous NO and to maintain a high energy status, in contrast to wild type. Higher weight of mature transgenic seeds demonstrated the beneficial effects of seed-specific overexpression of AtHb1.

Project description:BackgroundDuring maturation seeds acquire several physiological traits to enable them to survive drying and disseminate the species. Few studies have addressed the regulatory networks controlling acquisition of these traits at the tissue level particularly in endospermic seeds such as tomato, which matures in a fully hydrated environment and does not undergo maturation drying. Using temporal RNA-seq analyses of the different seed tissues during maturation, gene network and trait-based correlations were used to explore the transcriptome signatures associated with desiccation tolerance, longevity, germination under water stress and dormancy.ResultsDuring maturation, 15,173 differentially expressed genes were detected, forming a gene network representing 21 expression modules, with 3 being specific to seed coat and embryo and 5 to the endosperm. A gene-trait significance measure identified a common gene module between endosperm and embryo associated with desiccation tolerance and conserved with non-endospermic seeds. In addition to genes involved in protection such LEA and HSP and ABA response, the module included antioxidant and repair genes. Dormancy was released concomitantly with the increase in longevity throughout fruit ripening until 14?days after the red fruit stage. This was paralleled by an increase in SlDOG1-2 and PROCERA transcripts. The progressive increase in seed vigour was captured by three gene modules, one in common between embryo and endosperm and two tissue-specific. The common module was enriched with genes associated with mRNA processing in chloroplast and mitochondria (including penta- and tetratricopeptide repeat-containing proteins) and post-transcriptional regulation, as well several flowering genes. The embryo-specific module contained homologues of ABI4 and CHOTTO1 as hub genes associated with seed vigour, whereas the endosperm-specific module revealed a diverse set of processes that were related to genome stability, defence against pathogens and ABA/GA response genes.ConclusionThe spatio-temporal co-expression atlas of tomato seed maturation will serve as a valuable resource for the in-depth understanding of the dynamics of gene expression associated with the acquisition of seed vigour at the tissue level.

Project description:BACKGROUND:Next-generation sequencing and 'omics' platforms are used extensively in plant biology research to unravel new genomes and study their interactions with abiotic and biotic agents in the growth environment. Despite the availability of a large and growing number of genomic data sets, there are only limited resources providing highly-curated and up-to-date metabolic and regulatory networks for plant pathways. RESULTS:Using PathVisio, a pathway editor tool associated with WikiPathways, we created a gene interaction network of 430 rice (Oryza sativa) genes involved in the seed development process by curating interactions reported in the published literature. We then applied an InParanoid-based homology search to these genes and used the resulting gene clusters to identify 351 Arabidopsis thaliana genes. Using this list of homologous genes, we constructed a seed development network in Arabidopsis by processing the gene list and the rice network through a Perl utility software called Pathway GeneSWAPPER developed by us. In order to demonstrate the utility of these networks in generating testable hypotheses and preliminary analysis prior to more in-depth downstream analysis, we used the expression viewer and statistical analysis features of PathVisio to analyze publicly-available and published microarray gene expression data sets on diurnal photoperiod response and the seed development time course to discover patterns of coexpressed genes found in the rice and Arabidopsis seed development networks. These seed development networks described herein, along with other plant pathways and networks, are freely available on the plant pathways portal at WikiPathways (http://plants.wikipathways.org). CONCLUSION:In collaboration with the WikiPathways project we present a community curation and analysis platform for plant biologists where registered users can freely create, edit, share and monitor pathways supported by published literature. We describe the curation and annotation of a seed development network in rice, and the projection of a similar, gene homology-based network in Arabidopsis. We also demonstrate the utility of the Pathway GeneSWAPPER (PGS) application in saving valuable time and labor when a reference network in one species compiled in GPML format is used to project a similar network in another species based on gene homology.

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Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis.

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