Temporal tissue‐specific regulation of transcriptomes during barley (<i>Hordeum vulgare</i>) seed germination

Liew, Lim Chee; Narsai, Reena; Wang, Yan; Berkowitz, Oliver; Whelan, James; Lewsey, Mathew G.

doi:10.1111/tpj.14574

Cited by 26 publications

(17 citation statements)

References 72 publications

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“…To understand the role and function of protein mobilization of early germinated barley during the salt stress response, insights into the proteome remodelling process of germination will help us to understand the germination process under altered environmental conditions. Proteome and metabolome changes of the barley grain, the embryo, the endosperm, as well as changes in the redox state and in the expression of defence-related proteins have been identified using germinated grains, the aleurone layer treated with GA 3 , and germinated embryos on agar plates in normal and salt-stressed conditions [19][20][21][22][23].…”

Section: Introductionmentioning

confidence: 99%

Tissue-Specific Proteome and Subcellular Microscopic Analyses Reveal the Effect of High Salt Concentration on Actin Cytoskeleton and Vacuolization in Aleurone Cells during Early Germination of Barley

Dermendjiev

Schnurer

Weiszmann

et al. 2021

IJMS

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Cereal grain germination provides the basis for crop production and requires a tissue-specific interplay between the embryo and endosperm during heterotrophic germination involving signalling, protein secretion, and nutrient uptake until autotrophic growth is possible. High salt concentrations in soil are one of the most severe constraints limiting the germination of crop plants, affecting the metabolism and redox status within the tissues of germinating seed. However, little is known about the effect of salt on seed storage protein mobilization, the endomembrane system, and protein trafficking within and between these tissues. Here, we used mass spectrometry analyses to investigate the protein dynamics of the embryo and endosperm of barley (Hordeum vulgare, L.) at five different early points during germination (0, 12, 24, 48, and 72 h after imbibition) in germinated grains subjected to salt stress. The expression of proteins in the embryo as well as in the endosperm was temporally regulated. Seed storage proteins (SSPs), peptidases, and starch-digesting enzymes were affected by salt. Additionally, microscopic analyses revealed an altered assembly of actin bundles and morphology of protein storage vacuoles (PSVs) in the aleurone layer. Our results suggest that besides the salt-induced protein expression, intracellular trafficking and actin cytoskeleton assembly are responsible for germination delay under salt stress conditions.

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Section: Introductionmentioning

confidence: 99%

Tissue-Specific Proteome and Subcellular Microscopic Analyses Reveal the Effect of High Salt Concentration on Actin Cytoskeleton and Vacuolization in Aleurone Cells during Early Germination of Barley

Dermendjiev

Schnurer

Weiszmann

et al. 2021

IJMS

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“…In this study, we analyzed a transcriptomic dataset from 8 seed tissues (embryo proper, endosperm, suspensor, endothelium, epidermis, hilum, inner integument and outer integument) at 3 developmental stages (globular stage, heart stage and cotyledon stage) during soybean seed morphogenesis ( Figure 1 ). Our analyses determined that tissue specificity of gene expression was stronger than developmental stage specificity, as reported in other plant species [ 19 , 21 ]. Nearly half of the DEGs detected were specific to an individual seed tissue.…”

Section: Discussionmentioning

confidence: 62%

“…In addition to seed development, the germinating seed is also an excellent model to study genome regulation between cell-types. Recently laser-capture microdissection RNA-seq was applied to plumule, radicle tip and scutellum of germinating barley from which tissue-specific gene expression and storage of transcripts was characterized [ 21 ]. In maize, transcriptome analysis of embryo/endosperm interfaces revealed how the embryo and endosperm communicate in order to regulate the production the impermeable cuticle.…”

Section: Introductionmentioning

confidence: 99%

Analysis of Spatio-Temporal Transcriptome Profiles of Soybean (Glycine max) Tissues during Early Seed Development

Sun

et al. 2020

IJMS

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Soybean (Glycine max) is an important crop providing oil and protein for both human and animal consumption. Knowing which biological processes take place in specific tissues in a temporal manner will enable directed breeding or synthetic approaches to improve seed quantity and quality. We analyzed a genome-wide transcriptome dataset from embryo, endosperm, endothelium, epidermis, hilum, outer and inner integument and suspensor at the global, heart and cotyledon stages of soybean seed development. The tissue specificity of gene expression was greater than stage specificity, and only three genes were differentially expressed in all seed tissues. Tissues had both unique and shared enriched functional categories of tissue-specifically expressed genes associated with them. Strong spatio-temporal correlation in gene expression was identified using weighted gene co-expression network analysis, with the most co-expression occurring in one seed tissue. Transcription factors with distinct spatiotemporal gene expression programs in each seed tissue were identified as candidate regulators of expression within those tissues. Gene ontology (GO) enrichment of orthogroup clusters revealed the conserved functions and unique roles of orthogroups with similar and contrasting expression patterns in transcript abundance between soybean and Arabidopsis during embryo proper and endosperm development. Key regulators in each seed tissue and hub genes connecting those networks were characterized by constructing gene regulatory networks. Our findings provide an important resource for describing the structure and function of individual soybean seed compartments during early seed development.

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“…LCM was performed as described previously (Liew et al ., 2020). Briefly, after harvesting the first true leaves were immediately fixed in Farmer’s solution (3:1 ethanol:acetic acid) by infiltration for 10 min in a vacuum and after further incubation for 4 h processed using the Leica Semi‐Enclosed Benchtop Tissue Processor TP1020 (Leica Biosystems) for an ethanol series (75%, 85%, 3× 100% [v/v] for 1 h each), followed by an ethanol:xylene series (75:25%, 50:50%, 25:75% [v/v] for 1 h each) and a final xylene series (2× 100% [v/v] for 1 h each).…”

Section: Methodsmentioning

confidence: 99%

RNA‐seq analysis of laser microdissected Arabidopsis thaliana leaf epidermis, mesophyll and vasculature defines tissue‐specific transcriptional responses to multiple stress treatments

Berkowitz

Liew

et al. 2021

The Plant Journal

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SUMMARY Acclimation of plants to adverse conditions requires the coordination of gene expression and signalling pathways between tissues and cell types. As the energy and carbon capturing organs, leaves are significantly affected by abiotic and biotic stresses. However, tissue‐ or cell type‐specific analyses of stress responses have focussed on the Arabidopsis root. Here, we comparatively explore the transcriptomes of three leaf tissues (epidermis, mesophyll, vasculature) after induction of diverse stress pathways by chemical stimuli (antimycin A, 3‐amino‐1,2,4‐triazole, methyl viologen, salicylic acid) and ultraviolet light in Arabidopsis using laser capture microdissection followed by RNA sequencing. Stimulation of stress pathways caused an overall reduction in the number of genes expressed in a tissue‐specific manner, though a small subset gained or changed their tissue specificity. We find no evidence of a common stress response, with only a few genes consistently responsive to two or more treatments in the analysed tissues. However, differentially expressed genes overlap between tissues for individual treatments. A focussed analysis provided evidence for an interaction of auxin and ethylene that mediates retrograde signalling during mitochondrial dysfunction specifically in the epidermis, and a gene regulatory network defined the hierarchy of interactions. Taken together, we have generated an extensive reference dataset that will be valuable for future experiments analysing transcriptional responses on a tissue or single‐cell level. Our results will enable the tailoring of the tissue‐specific engineering of stress‐tolerant plants.

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Temporal tissue‐specific regulation of transcriptomes during barley (Hordeum vulgare) seed germination

Cited by 26 publications

References 72 publications

Tissue-Specific Proteome and Subcellular Microscopic Analyses Reveal the Effect of High Salt Concentration on Actin Cytoskeleton and Vacuolization in Aleurone Cells during Early Germination of Barley

Tissue-Specific Proteome and Subcellular Microscopic Analyses Reveal the Effect of High Salt Concentration on Actin Cytoskeleton and Vacuolization in Aleurone Cells during Early Germination of Barley

Analysis of Spatio-Temporal Transcriptome Profiles of Soybean (Glycine max) Tissues during Early Seed Development

RNA‐seq analysis of laser microdissected Arabidopsis thaliana leaf epidermis, mesophyll and vasculature defines tissue‐specific transcriptional responses to multiple stress treatments

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