What forces maintain variation within populations? Do similar forces promote divergence among populations? Research in the McDaniel lab is mainly aimed at answering these questions using classical genetic and genomic analyses of the moss model system Ceratodon purpureus. Currently we are focused on two projects: 1 – the evolutionary causes and consequences of dioecy (ie, having separate males and females); and 2 – the community genomics of moss-associated nitrogen fixation in a changing Arctic. We also maintain an interest in using Physcomitrella patens as a model for gene function analysis.
Why work with mosses?
Mosses are ubiquitous and important components of many ecosystems, and participate in fascinating interactions with other small organisms, including microarthropods, nitrogen-fixing bacteria, vascular plants and other mosses. The evolutionary processes that shape variation in other more conspicuous organism operate on mosses, too, writ small. Mosses spend much of their lives as haploids which makes both molecular and genetic analyses easier than in diploid systems. Additionally, the laboratory resources for mosses are excellent (Cove et al. 2009). We have a well-annotated genome sequence for Physcomitrella patens and a draft of the C. purpureus genome is now available. Both species undergo efficient gene targeting, both are easily cultivated in laboratory conditions, and there is an active community of moss researchers that meets annually.
Evolutionary causes and consequences of dioecy
The origin and maintenance of separate sexes (dioecy) is an enduring evolutionary puzzle – why should an organism give up the economy and reproductive assurance afforded by hermaphroditism? Curiously, about half of moss species have separate sexes. With Gordon Burleigh (UF) and John Atwood (MOBOT), we found that dioecy has evolved many times in the mosses (McDaniel et al. 2013a). Our experimental work in C. purpureus and P. patens suggests that this biased transition results from the benefits of sexual dimorphism (McDaniel 2005, McDaniel et al. 2008) rather than as a means to avoid inbreeding (McDaniel et al. 2010, Perroud et al. 2011). Regardless of the cause, this circumstance makes mosses a well-replicated natural experiment for studying the genetic, genomic, and macroevolutionary consequences of having separate sexes. As part of an NSF GoLife grant (DEB-1541506, with Gordon Burleigh, Christine Davis, and Emily Sessa) we are expanding this initiative to all of the flagellate plants (ie, excluding the non-flagellate angiosperms).
The major genomic consequence of dioecy is often non-recombining sex chromosomes. The haploid (UV) moss sex chromosomes provide an important contrast to the more widely studied XY and ZW systems and allow us to tease apart the effects of suppressed recombination and sex-limited inheritance on sex chromosome evolution (Bachtrog et al. 2011; McDaniel et al. 2013b). Dioecy also creates an arena for sexual antagonism, in which genes have different fitness consequences in males and females. With Sarah Eppley and Todd Rosenstiel (PSU) we are seeking to understand the forces generating sexual dimorphism in metabolite production in C. purpureus. With José-Miguel Ponciano and Marta Wayne (UF) and Pierre-François Perroud (Uni. Marburg) we are developing statistical and molecular tools to understand the genetics of non-Mendelian transmission (McDaniel et al. 2007, Norrell et al. 2014) and genetic conflict over offspring provisioning in natural populations of C. purpureus. This work is funded by NSF EAGER grant (DEB-1541005) to Stuart and José-Miguel.
The Ceratodon purpureus genome project
The ~360Mb genome of C. purpureus was sequenced through the DOE-JGI CSP2010 competition. C. purpureus was chosen to be the second moss sequenced (after P. patens) due to its UV sex chromosome system, its abundant natural variation in a variety of ecologically important and DOE-mission relevant traits, as well as its ease of manipulation in the lab. The female GG1 lab isolate (collected in Grosse Gerunds, Austria by David Cove) was chosen for WGS. To generate a chromosome scale assembly, a mapping population between GG1 and the male lab isolate R40 (collected by Stuart in Petersburg Pass, New York, USA) was also sequenced, along with a minimum spanning path of BACs across the GG1 non-recombining U-chromosome. To date, protonemal transcriptomes of GG1 and R40 have been generated using the 454 platform (Szövenyí et al. 2015), and mature gametophore transcriptomes for both isolates have been generated with Illumina technology. An additional 23 isolates representing the geographic diversity of the species have been resequenced with a coverage of ~30X, and protonemal transcriptomes and metabolite profiles are currently being generated for an additional 20 isolates. Some of the raw data is now available on GenBank, and we plan to have assembled data available on COSMOSS as soon as it’s complete.
Community genomics of moss-associated nitrogen fixation in a changing Arctic
Bryophytes and their associated microbes are critical components of carbon (C) and nitrogen (N) cycling in arctic tundra and boreal forest ecosystems, yet the assembly and function of these communities is poorly understood. Mosses, in particular the closely related feather mosses Hylocomium splendens and Pleurozium schreberi, account for approximately half of the net primary productivity in these biomes and are the primary drivers of soil organic layer C accumulation. Moss-associated microbes are also the major source of biologically fixed N inputs to these nitrogen-limited ecosystems, meaning that ecosystem C dynamics are highly sensitive to inputs and turnover of N from diverse assemblages of mosses and their microbes. Importantly, rates of biological N fixation depend in complex ways upon the moss host genetics and the composition of the moss microbiome. With Michelle Mack (NAU), Noah Fierer (CU), and José-Miguel Ponciano we have begun to identity the historical and contemporary drivers of variation in community assembly and function of this rapidly changing ecosystem, and how bryophyte-associated N fixation will change in a warmer climate. Our ultimate goal is to use moss-microbe interactions in high latitude systems as a model to inform our broader understanding of how biodiversity interacts with ecosystem function in the context of a changing climate.
Gene function analysis using Physcomitrella patens
P. patens is one of the few eukaryotes to undergo gene targeting via homologous recombination, making it a valuable model for gene function analysis. We are collaborating with Matias Kirst (UF) that uses gene targeting in P. patens to understand the role of Expanded Vessel Elements (EVE) in the evolution of tracheophytes. We are also collaborating with Mark Settles and Brad Barbazuk (UF) on structure-function analysis of U12 splicing factors, and the downstream consequences of mutations in these factors for global transcription and cell proliferation. This work was funded by a UF Office of Research Seed Grant in 2014.