scholarly journals Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour

2021 ◽  
Author(s):  
Elise Bizouerne ◽  
Julia Buitink ◽  
Benoît Ly-Vu ◽  
Joseph Ly-Vu ◽  
Eddi Esteban ◽  
...  

Abstract Background During 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.Results During 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. Conclusion The 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.

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Elise Bizouerne ◽  
Julia Buitink ◽  
Benoît Ly Vu ◽  
Joseph Ly Vu ◽  
Eddi Esteban ◽  
...  

Abstract Background During 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. Results During 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. Conclusion The 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.


2020 ◽  
Author(s):  
Elise Bizouerne ◽  
Julia Buitink ◽  
Benoît Ly-Vu ◽  
Joseph Ly-Vu ◽  
Eddi Esteban ◽  
...  

Abstract Background During 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. Results During 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 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. Conclusion The spatio-temporal co-expression atlas of 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.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Gareth B. Gillard ◽  
Lars Grønvold ◽  
Line L. Røsæg ◽  
Matilde Mengkrog Holen ◽  
Øystein Monsen ◽  
...  

Abstract Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80–100 million years ago. Results We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of “toxic mutations”. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. Conclusions Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.


Plant Direct ◽  
2021 ◽  
Author(s):  
Jutapak Jenkitkonchai ◽  
Poppy Marriott ◽  
Weibing Yang ◽  
Napaporn Sriden ◽  
Jae‐Hoon Jung ◽  
...  

2011 ◽  
Vol 165 (3) ◽  
pp. 469-476 ◽  
Author(s):  
Audrey Doublier ◽  
Delphine Farlay ◽  
Mohamed T Khebbab ◽  
Xavier Jaurand ◽  
Pierre J Meunier ◽  
...  

ObjectiveTo investigate interactions between strontium (Sr) and bone mineral and its effects on mineralization in osteoporotic women treated long-term with Sr ranelate (SrRan).DesignIn this study, 34 iliac bone biopsies were analyzed after 2, 12, 24, 36, 48, and 60 months of treatment with SrRan.MethodsSr global distribution was analyzed by X-ray cartography and the percentage of bone area containing Sr was calculated in the bone samples. The focal distribution of Sr in all bone samples was investigated by X-ray microanalysis. The degree of mineralization was assessed by quantitative microradiography.ResultsAbsent from old bone formed before the beginning of treatment, Sr was exclusively present in bone formed during this treatment with a much higher focal Sr content in new bone structural units than in old ones. A progressive increase in the extent of areas containing Sr was observed during treatment. The focal bone Sr content in recently formed bone was constant over treatment. Secondary mineralization was maintained at a normal level during treatment.ConclusionThus, the quality of bone mineralization (density and heterogeneity at tissue level) was preserved after a long-term treatment with SrRan.


2017 ◽  
Vol 15 (02) ◽  
pp. 1650045 ◽  
Author(s):  
Olga V. Petrovskaya ◽  
Evgeny D. Petrovskiy ◽  
Inna N. Lavrik ◽  
Vladimir A. Ivanisenko

Gene network modeling is one of the widely used approaches in systems biology. It allows for the study of complex genetic systems function, including so-called mosaic gene networks, which consist of functionally interacting subnetworks. We conducted a study of a mosaic gene networks modeling method based on integration of models of gene subnetworks by linear control functionals. An automatic modeling of 10,000 synthetic mosaic gene regulatory networks was carried out using computer experiments on gene knockdowns/knockouts. Structural analysis of graphs of generated mosaic gene regulatory networks has revealed that the most important factor for building accurate integrated mathematical models, among those analyzed in the study, is data on expression of genes corresponding to the vertices with high properties of centrality.


1987 ◽  
Vol 65 (2) ◽  
pp. 130-135 ◽  
Author(s):  
S. G. A. Power ◽  
J. R. G. Challis

Changes in estrogen production are considered important in the sequence of events leading to parturition. We sought tissue-specific changes in the concentration of unconjugated estrone (E1) and estradiol (E2) in intrauterine fetal (amnion, chorion) and maternal (endometrium, myometrium) tissues during normal pregnancy, labour, and ACTH-induced labour in sheep. The mean concentrations of E1 and E2 in the fetal membranes were higher than in endometrium and myometrium. In amnion there were no consistent changes in estrone concentrations with gestation, although estradiol concentrations increased between day 130 and term. In the endometrium there were increases in both estrone and estradiol between day 100 and term, whereas in the myometrium increases in the concentrations of E1 and E2 occurred between days 130–135 and term. Animals showing a labourlike pattern of uterine contractions after intrafetal ACTH administration did not show significant differences in estrone or estradiol concentrations in amnion, chorion, or endometrium compared with saline-infused controls. However, there was a progressive increase in the concentration of estrone and estradiol in the myometrium during ACTH-induced labour. We conclude that changes in the concentrations of estrone and estradiol in intrauterine tissues vary between the tissues studied and the two estrogens. In general, estrogen concentrations increased towards term, but this trend was more marked in the maternal than fetal tissues. The changes in estrone concentrations in myometrium, but not in the other tissues, were replicated during ACTH-induced labour. Our results would be compatible with the suggestion that tissue-specific changes in estrogen concentrations may contribute to the local intrauterine steroid milieu during pregnancy and at term.


2016 ◽  
Vol 113 (47) ◽  
pp. E7610-E7618 ◽  
Author(s):  
Dapeng Li ◽  
Sven Heiling ◽  
Ian T. Baldwin ◽  
Emmanuel Gaquerel

Secondary metabolite diversity is considered an important fitness determinant for plants’ biotic and abiotic interactions in nature. This diversity can be examined in two dimensions. The first one considers metabolite diversity across plant species. A second way of looking at this diversity is by considering the tissue-specific localization of pathways underlying secondary metabolism within a plant. Although these cross-tissue metabolite variations are increasingly regarded as important readouts of tissue-level gene function and regulatory processes, they have rarely been comprehensively explored by nontargeted metabolomics. As such, important questions have remained superficially addressed. For instance, which tissues exhibit prevalent signatures of metabolic specialization? Reciprocally, which metabolites contribute most to this tissue specialization in contrast to those metabolites exhibiting housekeeping characteristics? Here, we explore tissue-level metabolic specialization in Nicotiana attenuata, an ecological model with rich secondary metabolism, by combining tissue-wide nontargeted mass spectral data acquisition, information theory analysis, and tandem MS (MS/MS) molecular networks. This analysis was conducted for two different methanolic extracts of 14 tissues and deconvoluted 895 nonredundant MS/MS spectra. Using information theory analysis, anthers were found to harbor the most specialized metabolome, and most unique metabolites of anthers and other tissues were annotated through MS/MS molecular networks. Tissue–metabolite association maps were used to predict tissue-specific gene functions. Predictions for the function of two UDP-glycosyltransferases in flavonoid metabolism were confirmed by virus-induced gene silencing. The present workflow allows biologists to amortize the vast amount of data produced by modern MS instrumentation in their quest to understand gene function.


2007 ◽  
Vol 34 (7) ◽  
pp. 601 ◽  
Author(s):  
Stanislawa Pukacka ◽  
Ewelina Ratajczak

The ascorbate–glutathione system was studied during development and desiccation of seeds of two Acer species differing in desiccation tolerance: Norway maple (Acer platanoides L., orthodox) and sycamore (Acer pseudoplatanus L., recalcitrant). The results showed remarkable differences in the concentration and redox balance of ascorbate and glutathione between these two kinds of seeds during development, and a significant dependence between glutathione content and acquisition of desiccation tolerance in Norway maple seeds. There were relatively small differences between the species in the activities of enzymes of the ascorbate–glutathione cycle: ascorbate peroxidase (APX, EC 1.11.1.11), monodehydroascorbate reductase (MR, EC 1.6.5.4), dehydroascorbate reductase (DHAR, EC 1.8.5.1), and glutathione reductase (GR, EC 1.6.4.2). At the end of seed maturation, ascorbic acid content and the activities of the above enzymes was about the same in both species The electrophoretic pattern of APX isoenzymes was also similar for both species, and the intensity of the bands decreased at the end of seed maturation in both species. When sycamore seeds were desiccated to a moisture content of less than 26%, there was a marked decrease in seed viability and an increase in the production of reactive oxygen species. During desiccation, Norway maple seeds had a more active defence system, which was reflected in a higher glutathione content, a higher glutathione redox status, a higher ascorbate redox status, and higher activities of APX, MR, DHAR, GR and GPX (glutathione peroxidase). During desiccation, sulfhydryl-to-disulfide transition into proteins was more intense in Norway maple seeds than sycamore seeds. All of these results suggest that, in orthodox seeds, the ascorbate–glutathione cycle plays an important role in the acquisition of tolerance to desiccation, in protein maturation, and in protection from reactive oxygen species.


2015 ◽  
Vol 112 (15) ◽  
pp. 4707-4712 ◽  
Author(s):  
Ben-Yang Liao ◽  
Meng-Pin Weng

High-throughput gene expression profiling has revealed substantial leaky and extraneous transcription of eukaryotic genes, challenging the perceptions that transcription is strictly regulated and that changes in transcription have phenotypic consequences. To assess the functional implications of mRNA transcription directly, we analyzed mRNA expression data derived from microarrays, RNA-sequencing, and in situ hybridization, together with phenotype data of mouse mutants as a proxy of gene function at the tissue level. The results indicated that despite the presence of widespread ectopic transcription, mRNA expression and mutant phenotypes of mammalian genes or tissues remain associated. The expression-phenotype association at the gene level was particularly strong for tissue-specific genes, and the association could be underestimated due to data insufficiency and incomprehensive phenotyping of mouse mutants; the strength of expression-phenotype association at the tissue level depended on tissue functions. Mutations on genes expressed at higher levels or expressed at earlier embryonic stages more often result in abnormal phenotypes in the tissues where they are expressed. The mRNA expression profiles that have stronger associations with their phenotype profiles tend to be more evolutionarily conserved, indicating that the evolution of transcriptome and the evolution of phenome are coupled. Therefore, mutations resulting in phenotypic aberrations in expressed tissues are more likely to occur in highly transcribed genes, tissue-specific genes, genes expressed during early embryonic stages, or genes with evolutionarily conserved mRNA expression profiles.


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