- Award ID(s):
- 1755430
- NSF-PAR ID:
- 10174192
- Date Published:
- Journal Name:
- EvoDevo
- Volume:
- 11
- Issue:
- 13
- ISSN:
- 2041-9139
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
The evolutionary transition from single-celled to multicellular individuality requires organismal fitness to shift from the cell level to a cell group. This reorganization of fitness occurs by re-allocating the two components of fitness, survival and reproduction, between two specialized cell types in the multicellular group: soma and germ, respectively. How does the genetic basis for such fitness reorganization evolve? One possible mechanism is the co-option of life history genes present in the unicellular ancestors of a multicellular lineage. For instance, single-celled organisms must regulate their investment in survival and reproduction in response to environmental changes, particularly decreasing reproduction to ensure survival under stress. Such stress response life history genes can provide the genetic basis for the evolution of cellular differentiation in multicellular lineages. The regA-like gene family in the volvocine green algal lineage provides an excellent model system to study how this co-option can occur. We discuss the origin and evolution of the volvocine regA-like gene family, including regA—the gene that controls somatic cell development in the model organism Volvox carteri. We hypothesize that the co-option of life history trade-off genes is a general mechanism involved in the transition to multicellular individuality, making volvocine algae and the regA-like family a useful template for similar investigations in other lineages.more » « less
-
Volvocine green algae are a model for understanding the evolution of mating types and sexes. They are facultatively sexual, with gametic differentiation occurring in response to nitrogen starvation (-N) in most genera and to sex inducer hormone in Volvox . The conserved RWP-RK family transcription factor (TF) MID is encoded by the minus mating-type locus or male sex-determining region of heterothallic volvocine species and dominantly determines minus or male gametic differentiation. However, the factor(s) responsible for establishing the default plus or female differentiation programs have remained elusive. We performed a phylo-transcriptomic screen for autosomal RWP-RK TFs induced during gametogenesis in unicellular isogamous Chlamydomonas reinhardtii (Chlamydomonas) and in multicellular oogamous Volvox carteri (Volvox) and identified a single conserved ortho-group we named Volvocine Sex Regulator 1 (VSR1). Chlamydomonas vsr1 mutants of either mating type failed to mate and could not induce expression of key mating-type-specific genes. Similarly, Volvox vsr1 mutants in either sex could initiate sexual embryogenesis, but the presumptive eggs or androgonidia (sperm packet precursors) were infertile and unable to express key sex-specific genes. Yeast two-hybrid assays identified a conserved domain in VSR1 capable of self-interaction or interaction with the conserved N terminal domain of MID. In vivo coimmunoprecipitation experiments demonstrated association of VSR1 and MID in both Chlamydomonas and Volvox. These data support a new model for volvocine sexual differentiation where VSR1 homodimers activate expression of plus /female gamete-specific-genes, but when MID is present, MID-VSR1 heterodimers are preferentially formed and activate minus /male gamete-specific-genes.more » « less
-
The evolution of multicellularity is a major evolutionary transition that underlies the radiation of many species in all domains of life, especially in eukaryotes. The volvocine green algae are an unconventional model system that holds great promise in the field given its genetic tractability, late transition to multicellularity, and phenotypic diversity. Multiple efforts at linking multicellularity-related developmental landmarks to key molecular changes, especially at the genome level, have provided key insights into the molecular innovations or lack thereof that underlie multicellularity. Twelve developmental changes have been proposed to explain the evolution of complex differentiated multicellularity in the volvocine algae. Co-option of key genes, such as cell cycle and developmental regulators has been observed, but with few exceptions, known co-option events do not seem to coincide with most developmental features observed in multicellular volvocines. The apparent lack of “master multicellularity genes” combined with no apparent correlation between gene gains for developmental processes suggest the possibility that many multicellular traits might be the product gene-regulatory and functional innovations; in other words, multicellularity can arise from shared genomic repertoires that undergo regulatory and functional overhauls.more » « less
-
Summary Volvox carteri and other volvocine green algae comprise an excellent model for investigating developmental complexity and its origins. Here we describe a method for targeted mutagenesis inV. carteri usingCRISPR /Cas9 components expressed from transgenes. We usedV. carteri nitrate reductase gene (nitA ) regulatory sequences to conditionally expressStreptococcus pyogenes Cas9, andV. carteri U6RNA gene regulatory sequences to constitutively express single‐guideRNA (sgRNA ) transcripts.Volvox carteri was bombarded with both Cas9 vector and one of several sgRNA vectors programmed to target different test genes (glsA ,regA andinvA ), and transformants were selected for expression of a hygromycin‐resistance marker present on the sgRNA vector. Hygromycin‐resistant transformants grown with nitrate as sole nitrogen source (inducing fornitA ) were tested for Cas9 and sgRNA expression, and for the ability to generate progeny with expected mutant phenotypes. Some transformants of a somatic regenerator (Reg) mutant strain receiving sgRNA plasmid withglsA protospacer sequence yielded progeny (at a rate of ~0.01%) with a gonidialess (Gls) phenotype similar to that observed for previously describedglsA mutants, and sequencing of theglsA gene in independent mutants revealed short deletions within the targeted region ofglsA , indicative of Cas9‐directed non‐homologous end joining. Similarly, bombardment of a morphologically wild‐type strain with the Cas9 plasmid and sgRNA plasmids targetingregA orinvA yieldedregA andinvA mutant transformants/progeny, respectively (at rates of 0.1–100%). The capacity to make precisely directed frameshift mutations should greatly accelerate the molecular genetic analysis of development inV. carteri , and of developmental novelty in the volvocine algae. -
null (Ed.)The evolution of multicellularity was a major transition in evolution and set the stage for unprecedented increases in complexity, especially in land plants and animals. Here, we explore the genetics underlying a de novo origin of multicellularity in a microbial evolution experiment carried out on the green alga Chlamydomonas reinhardtii . We show that large-scale changes in gene expression underlie the transition to a multicellular life cycle. Among these, changes to genes involved in cell cycle and reproductive processes were overrepresented, as were changes to C. reinhardtii -specific and volvocine-specific genes. These results suggest that the genetic basis for the experimental evolution of multicellularity in C. reinhardtii has both lineage-specific and shared features, and that the shared features have more in common with C. reinhardtii 's relatives among the volvocine algae than with other multicellular green algae or land plants.more » « less