Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions

Bassel, George W.; Lan, Hui Y.; Glaab, Enrico; Gibbs, Daniel J.; Gerjets, Tanja; Krasnogor, Natalio; Bonner, Anthony J.; Holdsworth, Michael J.; Provart, Nicholas J.

doi:10.1073/pnas.1100958108

Cited by 220 publications

(255 citation statements)

References 43 publications

(42 reference statements)

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“…S1C). This region of the network contains coexpressed genes that are up-regulated by the germination-stimulating hormone GA and includes an abundance of growth-promoting cell wall remodeling genes (19,25). The spatiotemporal induction of multiple cell expansion-promoting genes from SeedNet was examined, including the xyloglucan endotransglucosylases/hydrolase (XTH) genes XTH9 and XTH19 (26) and the expansins EXPA1, EXPA8, and EXPA15.…”

Section: Resultsmentioning

confidence: 99%

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Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Bassel

Stamm

Mosca

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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177

202

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Morphogenesis occurs in 3D space over time and is guided by coordinated gene expression programs. Here we use postembryonic development in Arabidopsis plants to investigate the genetic control of growth. We demonstrate that gene expression driving the production of the growth-stimulating hormone gibberellic acid and downstream growth factors is first induced within the radicle tip of the embryo. The center of cell expansion is, however, spatially displaced from the center of gene expression. Because the rapidly growing cells have very different geometry from that of those at the tip, we hypothesized that mechanical factors may contribute to this growth displacement. To this end we developed 3D finiteelement method models of growing custom-designed digital embryos at cellular resolution. We used this framework to conceptualize how cell size, shape, and topology influence tissue growth and to explore the interplay of geometrical and genetic inputs into growth distribution. Our simulations showed that mechanical constraints are sufficient to explain the disconnect between the experimentally observed spatiotemporal patterns of gene expression and early postembryonic growth. The center of cell expansion is the position where genetic and mechanical facilitators of growth converge. We have thus uncovered a mechanism whereby 3D cellular geometry helps direct where genetically specified growth takes place.computational modeling | quantification | biomechanics | plant development | seed germination C entral to developmental biology is the question of how gene expression leads to morphogenesis and the creation of form (1, 2). However, there are few studies that link genes directly with shape change in a mechanistic way (3-5). In plants, where cells do not move, nearly all shape change and morphogenesis occur through the tightly regulated control over the mechanical properties of the cell wall. Mathematical models of plant cell growth are based on the turgor-driven Lockhart model and its derivatives (6, 7) that link the rate of cell wall expansion to the stress experienced by the wall. This model fits well with the biochemistry of the cell wall, which is composed of a strong cellulose microfibril network embedded in a pectin matrix with cross-links of hemicellulose, structural proteins, and other polysaccharides (8). Stress on the cell wall from turgor pressure causes elastic expansion, which becomes plastic as remodeling enzymes rearrange the network and incorporate new material (8). Thus, the physical manifestation of growth, cell expansion, results from a balance between genetically controlled enzymatic activity and the mechanical forces experienced by the cell wall.A common simplifying assumption is that gene expression associated with cell wall modification directly specifies the rate of growth of cells. This assumption is, however, limited as growthpromoting gene expression rarely correlates well with gradients of active cell expansion (9, 10). This suggests that gene expression patterns alone are not sufficient to pr...

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Section: Resultsmentioning

confidence: 99%

“…To identify genes driving cell expansion in the growing embryo, we examined the germination subnetwork of the condition-dependent gene-correlation network SeedNet (25) (Fig. S1C).…”

Section: Resultsmentioning

confidence: 99%

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Bassel

Stamm

Mosca

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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177

202

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“…In addition, previous studies have shown that genes related to flowering are expressed in association with seed development and germination. For example, a genome-wide expression correlation network in Arabidopsis showed that maturity-phase transition regulators such as SE, EMBRYONIC FLOWER1, and EARLY BOLTING IN SHORT DAYS are coexpressed with germination-associated genes and affect seed germination (14). Arabidopsis HISTONE MONOUBIQUITINATION1 and 2 (HUB1 and HUB2) genes regulate flowering and seed germination; seeds of hub1 and hub2 mutants displayed reduced seed dormancy (51), and hub1 seeds also exhibit strong thermotolerance to high temperature at germination (52).…”

Section: Discussionmentioning

confidence: 99%

“…Seed dormancy and germination are regulated primarily by the antagonistic actions of the plant hormones gibberellin (GA; promotive) and abscisic acid (ABA; inhibitory), whose synthesis and action vary in response to environmental signals (12). Recent studies indicate that canonical genes regulating flowering, such as FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC), are also involved in the transition from seed dormancy to germination (13)(14)(15)(16), suggesting that seed dormancy and flowering may be coordinately regulated through overlapping molecular pathways.…”

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confidence: 99%

DELAY OF GERMINATION1 ( DOG1 ) regulates both seed dormancy and flowering time through microRNA pathways

Huo

Wei

Bradford

2016

Proc. Natl. Acad. Sci. U.S.A.

162

149

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Seed germination and flowering, two critical developmental transitions in plant life cycles, are coordinately regulated by genetic and environmental factors to match plant establishment and reproduction to seasonal cues. The DELAY OF GERMINATION1 (DOG1) gene is involved in regulating seed dormancy in response to temperature and has also been associated genetically with pleiotropic flowering phenotypes across diverse Arabidopsis thaliana accessions and locations. Here we show that DOG1 can regulate seed dormancy and flowering times in lettuce (Lactuca sativa, Ls) and Arabidopsis through an influence on levels of microRNAs (miRNAs) miR156 and miR172. In lettuce, suppression of LsDOG1 expression enabled seed germination at high temperature and promoted early flowering in association with reduced miR156 and increased miR172 levels. In Arabidopsis, higher miR156 levels resulting from overexpression of the MIR156 gene enhanced seed dormancy and delayed flowering. These phenotypic effects, as well as conversion of MIR156 transcripts to miR156, were compromised in DOG1 loss-of-function mutant plants, especially in seeds. Overexpression of MIR172 reduced seed dormancy and promoted early flowering in Arabidopsis, and the effect on flowering required functional DOG1. Transcript levels of several genes associated with miRNA processing were consistently lower in dry seeds of Arabidopsis and lettuce when DOG1 was mutated or its expression was reduced; in contrast, transcript levels of these genes were elevated in a DOG1 gain-of-function mutant. Our results reveal a previously unknown linkage between two critical developmental phase transitions in the plant life cycle through a DOG1-miR156-miR172 interaction.T he life cycles of flowering plants are characterized by distinct phase transitions such as from seed to seedling (germination) or from vegetative to reproductive development (flowering) (1). The timing of germination and flowering both require precise environmental sensing and integrated responses to multiple inputs so that developmental transitions can be accurately matched to seasonal conditions (1-3). Seeds use temperature as a signal of the seasonal and current environmental conditions to determine opportune times to germinate with respect to the potential for seedling survival (2, 4, 5). Similarly, in many plants the transition from vegetative to floral development occurs in response to environmental cues, particularly temperature and day length (6, 7). Ecological and evolutionary studies have found that seed germination and flowering traits within species are coadapted across habitat ranges (8-11). Seed dormancy and germination are regulated primarily by the antagonistic actions of the plant hormones gibberellin (GA; promotive) and abscisic acid (ABA; inhibitory), whose synthesis and action vary in response to environmental signals (12). Recent studies indicate that canonical genes regulating flowering, such as FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC), are also involved in the transition from seed dormanc...

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“…However, targeted networks, focusing on a specific condition, organ, or developmental phase, allow the dissection of fine regulatory switches that will otherwise be obscured through global comparisons (Usadel et al, 2009). One example is the SeedNet, a genome-wide network model describing transcriptional interactions, representing a binary phase transition study, in nongerminating (or dormant) and germinating Arabidopsis thaliana seeds (Bassel et al, 2011). Integration of the expression data at the resolution of developmental stages and in different environmental contexts is expected to generate a high confidence dynamic gene regulatory model (Long et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways

Righetti¹,

Vu²,

Pelletier³

et al. 2015

Plant Cell

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118

191

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Seed longevity, the maintenance of viability during storage, is a crucial factor for preservation of genetic resources and ensuring proper seedling establishment and high crop yield. We used a systems biology approach to identify key genes regulating the acquisition of longevity during seed maturation of Medicago truncatula. Using 104 transcriptomes from seed developmental time courses obtained in five growth environments, we generated a robust, stable coexpression network (MatNet), thereby capturing the conserved backbone of maturation. Using a trait-based gene significance measure, a coexpression module related to the acquisition of longevity was inferred from MatNet. Comparative analysis of the maturation processes in M. truncatula and Arabidopsis thaliana seeds and mining Arabidopsis interaction databases revealed conserved connectivity for 87% of longevity module nodes between both species. Arabidopsis mutant screening for longevity and maturation phenotypes demonstrated high predictive power of the longevity cross-species network. Overrepresentation analysis of the network nodes indicated biological functions related to defense, light, and auxin. Characterization of defense-related wrky3 and nf-x1-like1 (nfxl1) transcription factor mutants demonstrated that these genes regulate some of the network nodes and exhibit impaired acquisition of longevity during maturation. These data suggest that seed longevity evolved by co-opting existing genetic pathways regulating the activation of defense against pathogens.

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Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions

Cited by 220 publications

References 43 publications

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

DELAY OF GERMINATION1 ( DOG1 ) regulates both seed dormancy and flowering time through microRNA pathways

Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways

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