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Desiccation Tolerance as the Basis of Long-Term Seed Viability.

ABSTRACT: Desiccation tolerance appeared as the key adaptation feature of photoautotrophic organisms for survival in terrestrial habitats. During the further evolution, vascular plants developed complex anatomy structures and molecular mechanisms to maintain the hydrated state of cell environment and sustain dehydration. However, the role of the genes encoding the mechanisms behind this adaptive feature of terrestrial plants changed with their evolution. Thus, in higher vascular plants it is restricted to protection of spores, seeds and pollen from dehydration, whereas the mature vegetative stages became sensitive to desiccation. During maturation, orthodox seeds lose up to 95% of water and successfully enter dormancy. This feature allows seeds maintaining their viability even under strongly fluctuating environmental conditions. The mechanisms behind the desiccation tolerance are activated at the late seed maturation stage and are associated with the accumulation of late embryogenesis abundant (LEA) proteins, small heat shock proteins (sHSP), non-reducing oligosaccharides, and antioxidants of different chemical nature. The main regulators of maturation and desiccation tolerance are abscisic acid and protein DOG1, which control the network of transcription factors, represented by LEC1, LEC2, FUS3, ABI3, ABI5, AGL67, PLATZ1, PLATZ2. This network is complemented by epigenetic regulation of gene expression via methylation of DNA, post-translational modifications of histones and chromatin remodeling. These fine regulatory mechanisms allow orthodox seeds maintaining desiccation tolerance during the whole period of germination up to the stage of radicle protrusion. This time point, in which seeds lose desiccation tolerance, is critical for the whole process of seed development.

SUBMITTER: Smolikova G

PROVIDER: S-EPMC7795748 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Desiccation Tolerance as the Basis of Long-Term Seed Viability.

Smolikova Galina G Leonova Tatiana T Vashurina Natalia N Frolov Andrej A Medvedev Sergei S

International journal of molecular sciences 20201224 1

Desiccation tolerance appeared as the key adaptation feature of photoautotrophic organisms for survival in terrestrial habitats. During the further evolution, vascular plants developed complex anatomy structures and molecular mechanisms to maintain the hydrated state of cell environment and sustain dehydration. However, the role of the genes encoding the mechanisms behind this adaptive feature of terrestrial plants changed with their evolution. Thus, in higher vascular plants it is restricted to ...[more]

PMID: 33374189

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Project description:Drought is one of the harshest abiotic stresses hindering seed germination, plant growth, and crop productivity. A high rate and uniformity of germination under stressful conditions are vital for crop establishment and growth; thus, for productivity. A better understanding of the genetic architecture of seed germination under drought stress is a prerequisite for further increasing yield potential. Barley is considered one of the most abiotic stresses-tolerant cereals. Elucidating the drought tolerance of barley during seed germination would indeed pave the way towards improving the performance of all cereals. However, we still know relatively little about the genetic control of drought tolerance during the seed germination phase. In our study, 218 worldwide spring barley accessions were subjected to PEG-induced drought during seed germination. Induced drought stress "20% PEG" significantly reduced the seed germination parameters and seedling related traits. A genome-wide association scan (GWAS) was used to identify genomic regions associated with our trait of interest. In total, 338 single nucleotide polymorphisms (SNPs) were found to be associated with several traits distributed across seven barley chromosomes, of which 26 genomic regions were associated with candidate genes. The current study found some of the quantitative trait loci (QTL) that have previously been reported to be linked to seed germination-related traits under drought conditions, as well as some new associations. Noteworthy, the identified QTL colocalized with a number of genes (within interval ±0.5 Mbp) that are exclusively distributed on chromosomes 1H, 2H, and 5H. The annotation of these genes in barley shows their roles in drought tolerance through encoding different transcription factors. The function of the identified genes during seed germination was also confirmed by the annotation of their counterparts in Arabidopsis. The current analyses show the power of the GWAS both for identifying putative candidate genes and for improving plant adaptive traits in barley.

Project description:Desiccation tolerance (DT) has contributed greatly to the adaptation of land plants to severe water-deficient conditions. DT is mostly observed in reproductive parts in flowering plants such as seeds. The seed DT is lost at early post germination stage but is temporally re-inducible in 1 mm radicles during the so-called DT window following a PEG treatment before being permanently silenced in 5 mm radicles of germinating seeds. The molecular mechanisms that activate/reactivate/silence DT in developing and germinating seeds have not yet been elucidated. Here, we analyzed chromatin dynamics related to re-inducibility of DT before and after the DT window at early germination in Medicago truncatula radicles to determine if DT-associated genes were transcriptionally regulated at the chromatin levels. Comparative transcriptome analysis of these radicles identified 948 genes as DT re-induction-related genes, positively correlated with DT re-induction. ATAC-Seq analyses revealed that the chromatin state of genomic regions containing these genes was clearly modulated by PEG treatment and affected by growth stages with opened chromatin in 1 mm radicles with PEG (R1P); intermediate openness in 1 mm radicles without PEG (R1); and condensed chromatin in 5 mm radicles without PEG (R5). In contrast, we also showed that the 103 genes negatively correlated with the re-induction of DT did not show any transcriptional regulation at the chromatin level. Additionally, ChIP-Seq analyses for repressive marks H2AK119ub and H3K27me3 detected a prominent signal of H3K27me3 on the DT re-induction-related gene sequences at R5 but not in R1 and R1P. Moreover, no clear H2AK119ub marks was observed on the DT re-induction-related gene sequences at both developmental radicle stages, suggesting that silencing of DT process after germination will be mainly due to H3K27me3 marks by the action of the PRC2 complex, without involvement of PRC1 complex. The dynamic of chromatin changes associated with H3K27me3 were also confirmed on seed-specific genes encoding potential DT-related proteins such as LEAs, oleosins and transcriptional factors. However, several transcriptional factors did not show a clear link between their decrease of chromatin openness and H3K27me3 levels, suggesting that their accessibility may also be regulated by additional factors, such as other histone modifications. Finally, in order to make these comprehensive genome-wide analyses of transcript and chromatin dynamics useful to the scientific community working on early germination and DT, we generated a dedicated genome browser containing all these data and publicly available at https://iris.angers.inrae.fr/mtseedepiatlas/jbrowse/?data=Mtruncatula.

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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.

Dataset Information

Desiccation Tolerance as the Basis of Long-Term Seed Viability.

Publications

Desiccation Tolerance as the Basis of Long-Term Seed Viability.

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