Computational Morphodynamics: A Modeling Framework to Understand Plant Growth

Chickarmane, Vijay; Roeder, Adrienne; Tarr, Paul T.; Cunha, Alexandre; Tobin, Cory; Meyerowitz, Elliot M.

doi:10.1146/annurev-arplant-042809-112213

Cited by 78 publications

(62 citation statements)

References 132 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Since any of these microscopic reorganizations would lead to indistinguishable macroscopic deformations, all of these possibilities must be considered in phenotypic analysis of tissue morphogenesis [16,17]. In the context of plant morphodynamics [18], our study has emphasized that in addition to differential cell division and isotropic cell expansion, differential cell anisotropy can also play a dominant role in evolutionarily significant shape change. Petal spur sculpting and spur-length diversity across the genus Aquilegia, even in its most extreme expressions, can be explained solely through variation in cell anisotropy.…”

Section: Discussionmentioning

confidence: 96%

Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy

et al. 2011

View full text Add to dashboard Cite

The role of petal spurs and specialized pollinator interactions has been studied since Darwin. Aquilegia petal spurs exhibit striking size and shape diversity, correlated with specialized pollinators ranging from bees to hawkmoths in a textbook example of adaptive radiation. Despite the evolutionary significance of spur length, remarkably little is known about Aquilegia spur morphogenesis and its evolution. Using experimental measurements, both at tissue and cellular levels, combined with numerical modelling, we have investigated the relative roles of cell divisions and cell shape in determining the morphology of the Aquilegia petal spur. Contrary to decades-old hypotheses implicating a discrete meristematic zone as the driver of spur growth, we find that Aquilegia petal spurs develop via anisotropic cell expansion. Furthermore, changes in cell anisotropy account for 99 per cent of the spur-length variation in the genus, suggesting that the true evolutionary innovation underlying the rapid radiation of Aquilegia was the mechanism of tuning cell shape.

show abstract

Section: Discussionmentioning

confidence: 96%

Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy

et al. 2011

View full text Add to dashboard Cite

show abstract

“…The mathematical model described below seeks to explore how different processes interact to produce the gibberellin distribution and how this distribution is able, through the gibberellin signaling pathway, to determine the DELLA distribution. A multiscale modeling approach is essential to understanding the complexity of such a system (12)(13)(14); for example, a genetic mutation may alter both the gibberellin pathway and the growth dynamics, and modeling can integrate these perturbations to predict the DELLA distribution. In this work, we focus on the root elongation zone.…”

mentioning

confidence: 99%

Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

Band

Úbeda-Tomás

Dyson

et al. 2012

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

103

View full text Add to dashboard Cite

In the elongation zone of the Arabidopsis thaliana plant root, cells undergo rapid elongation, increasing their length by ∼10-fold over 5 h while maintaining a constant radius. Although progress is being made in understanding how this growth is regulated, little consideration has been given as to how cell elongation affects the distribution of the key regulating hormones. Using a multiscale mathematical model and measurements of growth dynamics, we investigate the distribution of the hormone gibberellin in the root elongation zone. The model quantifies how rapid cell expansion causes gibberellin to dilute, creating a significant gradient in gibberellin levels. By incorporating the gibberellin signaling network, we simulate how gibberellin dilution affects the downstream components, including the growth-repressing DELLA proteins. We predict a gradient in DELLA that provides an explanation of the reduction in growth exhibited as cells move toward the end of the elongation zone. These results are validated at the molecular level by comparing predicted mRNA levels with transcriptomic data. To explore the dynamics further, we simulate perturbed systems in which gibberellin levels are reduced, considering both genetically modified and chemically treated roots. By modeling these cases, we predict how these perturbations affect gibberellin and DELLA levels and thereby provide insight into their altered growth dynamics.H ormone distributions within plant tissues affect plant growth and development (1). Although many studies have investigated the influence of nonuniform distributions of the hormone auxin, gradients in other hormones also govern plant growth (2, 3). In some regions of the plant, cells undergo rapid expansion that dilutes their contents, including hormones. In these regions, organ-scale hormone gradients can arise due to the interplay between dilution, diffusion, production, decay, and receptor binding. Such complex dynamics govern in particular the distribution of the plant hormone gibberellin, which is involved in a diverse range of developmental processes including germination, organ development, and growth (4).A well-studied context for gibberellin growth regulation is provided by the primary root of the model species Arabidopsis thaliana (3, 5, 6). At the organ level, the Arabidopsis primary root classically presents three distinct morphological zones (ref. 7; Fig. 1A): Cells divide in the meristem, which is located close to the root tip; after a number of divisions, cells then move through the elongation zone, where they rapidly increase in length with negligible change in radius; finally, cells stop growing on entering the mature zone. Gibberellin has been described as a key hormone in regulating both cell division in the root meristem (6) and cell elongation in the elongation zone (5).Gibberellin regulates cell elongation and division by mediating the destabilization of DELLA proteins (8, 9). Gibberellin first binds with its receptor GID1, forming gibberellin-GID1 complexes that can then interact wi...

show abstract

“…We previously found that the CgAUX1 gene that encodes an auxin influx carrier functionally equivalent to Arabidopsis AtAUX1 is expressed in the vascular tissues and in Frankia-infected cells in C. glauca nodules (Péret et al, 2007). To test whether this CgAUX1 expression might be sufficient to explain the pattern of auxin accumulation, we used a computational modeling approach similar to the ones that have been applied successfully to study developmental processes such as phyllotaxis (de Reuille et al, 2006;Chickarmane et al, 2010). Auxin fluxes and accumulation patterns in a tissue can be inferred from the cellular localization of transporters.…”

Section: Resultsmentioning

confidence: 99%

Auxin Carriers Localization Drives Auxin Accumulation in Plant Cells Infected by Frankia in Casuarina glauca Actinorhizal Nodules

et al. 2010

View full text Add to dashboard Cite

Actinorhizal symbioses are mutualistic interactions between plants and the soil bacteria Frankia that lead to the formation of nitrogen-fixing root nodules. Little is known about the signaling mechanisms controlling the different steps of the establishment of the symbiosis. The plant hormone auxin has been suggested to play a role. Here we report that auxin accumulates within Frankia-infected cells in actinorhizal nodules of Casuarina glauca. Using a combination of computational modeling and experimental approaches, we establish that this localized auxin accumulation is driven by the cell-specific expression of auxin transporters and by Frankia auxin biosynthesis in planta. Our results indicate that the plant actively restricts auxin accumulation to Frankia-infected cells during the symbiotic interaction.

show abstract

Computational Morphodynamics: A Modeling Framework to Understand Plant Growth

Cited by 78 publications

References 132 publications

Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy

Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy

Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

Auxin Carriers Localization Drives Auxin Accumulation in Plant Cells Infected by Frankia in Casuarina glauca Actinorhizal Nodules

Contact Info

Product

Resources

About