An official website of the United States government
ABSTRACT A complete picture of how signaling pathways lead to multicellularity is largely unknown. Previously, we generated mutations in a protein prenylation enzyme, GGB, and showed that it is essential for maintaining multicellularity in the moss Physcomitrium patens. Here, we show that ROP GTPases act as downstream factors that are prenylated by GGB and themselves play an important role in the multicellularity of P. patens. We also show that the loss of multicellularity caused by the suppression of GGB or ROP GTPases is due to uncoordinated cell expansion, defects in cell wall integrity and the disturbance of the directional control of cell plate orientation. Expressing prenylatable ROP in the ggb mutant not only rescues multicellularity in protonemata but also results in development of gametophores. Although the prenylation of ROP is important for multicellularity, a higher threshold of active ROP is required for gametophore development. Thus, our results suggest that ROP activation via prenylation by GGB is a key process at both cell and tissue levels, facilitating the developmental transition from one dimension to two dimensions and to three dimensions in P. patens.
more »
« less
This content will become publicly available on April 4, 2026
Tissue-like multicellular development triggered by mechanical compression in archaea
The advent of clonal multicellularity is a critical evolutionary milestone, seen often in eukaryotes, rarely in bacteria, and only once in archaea. We show that uniaxial compression induces clonal multicellularity in haloarchaea, forming tissue-like structures. These archaeal tissues are mechanically and molecularly distinct from their unicellular lifestyle, mimicking several eukaryotic features. Archaeal tissues undergo a multinucleate stage followed by tubulin-independent cellularization, orchestrated by active membrane tension at a critical cell size. After cellularization, tissue junction elasticity becomes akin to that of animal tissues, giving rise to two cell types—peripheral (Per) and central scutoid (Scu) cells—with distinct actin and protein glycosylation polarity patterns. Our findings highlight the potential convergent evolution of a biophysical mechanism in the emergence of multicellular systems across domains of life.
more »
« less
- Award ID(s):
- 2222076
- PAR ID:
- 10610938
- Publisher / Repository:
- AAAS
- Date Published:
- Journal Name:
- Science
- Volume:
- 388
- Issue:
- 6742
- ISSN:
- 0036-8075
- Page Range / eLocation ID:
- 109 to 115
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The ability to program collective cell migration can allow us to control critical multicellular processes in development, regenerative medicine, and invasive disease. However, while various technologies exist to make individual cells migrate, translating these tools to control myriad, collectively interacting cells within a single tissue poses many challenges. For instance, do cells within the same tissue interpret a global migration ‘command’ differently based on where they are in the tissue? Similarly, since no stimulus is permanent, what are the long-term effects of transient commands on collective cell dynamics? We investigate these questions by bioelectrically programming large epithelial tissues to globally migrate ‘rightward’ via electrotaxis. Tissues clearly developed distinct rear, middle, side, and front responses to a single global migration stimulus. Furthermore, at no point poststimulation did tissues return to their prestimulation behavior, instead equilibrating to a 3rd, new migratory state. These unique dynamics suggested that programmed migration resets tissue mechanical state, which was confirmed by transient chemical disruption of cell–cell junctions, analysis of strain wave propagation patterns, and quantification of cellular crowd dynamics. Overall, this work demonstrates how externally driving the collective migration of a tissue can reprogram baseline cell–cell interactions and collective dynamics, even well beyond the end of the global migratory cue, and emphasizes the importance of considering the supracellular context of tissues and other collectives when attempting to program crowd behaviors.more » « less
-
Abstract The evolutionary transition to multicellularity requires shifting the primary unit of selection from cells to multicellular collectives. How this occurs in aggregative organisms remains poorly understood. Clonal development provides a direct path to multicellular adaptation through genetic identity between cells, but aggregative organisms face a constraint: selection on collective-level traits cannot drive adaptation without positive genetic assortment. We leveraged experimental evolution of flocculatingSaccharomyces cerevisiaeto examine the evolution and role of genetic assortment in multicellular adaptation. After 840 generations of selection for rapid settling, 13 of 19 lineages evolved increased positive assortment relative to their ancestor. However, assortment provided no competitive advantage during settling selection, suggesting it arose as an indirect effect of selection on cell-level traits rather than through direct selection on collective-level properties. Genetic reconstruction experiments and protein structure modeling revealed two distinct pathways to assortment: kin recognition mediated by mutations in theFLO1adhesion gene and generally enhanced cellular adhesion that improved flocculation efficiency independent of partner genotype. The evolution of assortment without immediate adaptive benefit suggests that key innovations enabling multicellular adaptation may arise indirectly through cell-level selection. Our results demonstrate fundamental constraints on aggregative multicellularity and help explain why aggregative lineages have remained simple.more » « less
-
Human pluripotent stem cell (hPSC)-derived neural organoids display unprecedented emergent properties. Yet in contrast to the singular neuroepithelial tube from which the entire central nervous system (CNS) develops in vivo, current organoid protocols yield tissues with multiple neuroepithelial units, a.k.a. neural rosettes, each acting as independent morphogenesis centers and thereby confounding coordinated, reproducible tissue development. Here, we discover that controlling initial tissue morphology can effectively (>80%) induce single neural rosette emergence within hPSC-derived forebrain and spinal tissues. Notably, the optimal tissue morphology for observing singular rosette emergence was distinct for forebrain versus spinal tissues due to previously unknown differences in ROCK-mediated cell contractility. Following release of geometric confinement, the tissues displayed radial outgrowth with maintenance of a singular neuroepithelium and peripheral neuronal differentiation. Thus, we have identified neural tissue morphology as a critical biophysical parameter for controlling in vitro neural tissue morphogenesis furthering advancement towards biomanufacture of CNS tissues with biomimetic anatomy and physiology.more » « less
-
null (Ed.)Background Oviposition decisions are critical to the fitness of herbivorous insects and are often impacted by the availability and condition of host plants. Monarch butterflies ( Danaus plexippus ) rely on milkweeds ( Asclepias spp.) for egg-laying and as food for larvae. Previous work has shown that monarchs prefer to oviposit on recently regrown plant tissues (after removal of above-ground biomass) while larvae grow poorly on plants previously damaged by insects. We hypothesized that these effects may depend on the life-history strategy of plants, as clonal and non-clonal milkweed species differ in resource allocation and defense strategies. Methodology/Principal Findings We first confirmed butterfly preference for regrown tissue in a field survey of paired mowed and unmowed plots of the common milkweed A. syriaca . We then experimentally studied the effects of plant damage (comparing undamaged controls to plants clipped and regrown, or damaged by insects) on oviposition choice, larval performance, and leaf quality of two closely related clonal and non-clonal species pairs: (1) A. syriaca and A. tuberosa , and (2) A. verticillata and A. incarnata . Clonal and non-clonal species displayed different responses to plant damage, impacting the proportions of eggs laid on plants. Clonal species had similar mean proportions of eggs on regrown and control plants (≈35–40% each), but fewer on insect-damaged plants (≈20%). Meanwhile non-clonal species had similar oviposition on insect-damaged and control plants (20–30% each) but more eggs on regrown plants (40–60%). Trait analyses showed reduced defenses in regrown plants and we found some evidence, although variable, for negative effects of insect damage on subsequent larval performance. Conclusions/Significance Overall, non-clonal species are more susceptible and preferred by monarch butterflies following clipping, while clonal species show tolerance to clipping and induced defense to insect herbivory. These results have implications for monarch conservation strategies that involve milkweed habitat management by mowing. More generally, plant life-history may mediate growth and defense strategies, explaining species-level variation in responses to different types of damage.more » « less
