Between Two Fern Genomes

Ferns are the only major lineage of vascular plants not represented by a sequenced nuclear genome. This lack of genome sequence information significantly impedes our ability to understand and reconstruct genome evolution not only in ferns, but across all land plants. Azolla and Ceratopteris are ideal and complementary candidates to be the first ferns to have their nuclear genomes sequenced. They differ dramatically in genome size, life history, and habit, and thus represent the immense diversity of extant ferns. Together, this pair of genomes will facilitate myriad large-scale comparative analyses across ferns and all land plants. Here we review the unique biological characteristics of ferns and describe a number of outstanding questions in plant biology that will benefit from the addition of ferns to the set of taxa with sequenced nuclear genomes. We explain why the fern clade is pivotal for understanding genome evolution across land plants, and we provide a rationale for how knowledge of fern genomes will enable progress in research beyond the ferns themselves.

[1]  A. Lotter,et al.  The Eocene Arctic Azolla bloom: environmental conditions, productivity and carbon drawdown , 2009, Geobiology.

[2]  Michael S. Barker,et al.  Evolution of the nuclear genome of ferns and lycophytes , 2008 .

[3]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[4]  D. Britton CHROMOSOME STUDIES ON FERNS , 1953 .

[5]  Michael S. Barker,et al.  Unfurling Fern Biology in the Genomics Age , 2010 .

[6]  Jeffrey P. Mower,et al.  Complete plastid genomes from Ophioglossum californicum, Psilotum nudum, and Equisetum hyemale reveal an ancestral land plant genome structure and resolve the position of Equisetales among monilophytes , 2013, BMC Evolutionary Biology.

[7]  A. Weber,et al.  Azolla domestication towards a biobased economy? , 2014, The New phytologist.

[8]  R. Pemberton,et al.  Old World Climbing Fern (Lygodium microphyllum), a Dangerous Invasive Weed in Florida , 1998 .

[9]  M. Hasebe,et al.  Ceratopteris: A Model System for Studying Sex-Determining Mechanisms in Plants , 1995, International Journal of Plant Sciences.

[10]  J. Langdale,et al.  High-Efficiency Stable Transformation of the Model Fern Species Ceratopteris richardii via Microparticle Bombardment1[W][OPEN] , 2014, Plant Physiology.

[11]  Michael S. Barker,et al.  Paleopolyploidy in the Brassicales: Analyses of the Cleome Transcriptome Elucidate the History of Genome Duplications in Arabidopsis and Other Brassicales , 2009, Genome biology and evolution.

[12]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[13]  P. Vitousek,et al.  Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i , 2004, Oecologia.

[14]  C. Haufler,et al.  Biology and Evolution of Ferns and Lycophytes: Preface , 2008 .

[15]  K. Pryer,et al.  Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy , 2009, Proceedings of the National Academy of Sciences.

[16]  I. Leitch,et al.  Nuclear DNA Amounts in Pteridophytes , 2001 .

[17]  J. McGrath,et al.  Assessment of gene copy number in the homosporous fernsCeratopteris thalictroides andC. richardii (Parkeriaceae) by restriction fragment length polymorphisms , 1994, Plant Systematics and Evolution.

[18]  T. Warne,et al.  The Biology of the Fern Ceratopteris and Its Use as a Model System , 1995, International Journal of Plant Sciences.

[19]  L. Rieseberg,et al.  Genetic Map-Based Analysis of Genome Structure in the Homosporous Fern Ceratopteris richardii , 2006, Genetics.

[20]  D. Britton The Significance of Chromosome Numbers in Ferns , 1974 .

[21]  I. Leitch,et al.  DNA amounts for five pteridophyte species fill phylogenetic gaps in C‐value data , 2002 .

[22]  I. Leitch,et al.  Nuclear DNA C-values in 30 species double the familial representation in pteridophytes. , 2002, Annals of botany.

[23]  J. Banks GAMETOPHYTE DEVELOPMENT IN FERNS. , 1999, Annual review of plant physiology and plant molecular biology.

[24]  Alla Lapidus,et al.  Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium , 2010, PloS one.

[25]  L. G. Hickok,et al.  The Programming of Sexual Phenotype in the Homosporous Fern Ceratopteris richardii , 1993, International Journal of Plant Sciences.

[26]  L. Walker,et al.  Effects of fern thickets on woodland development on landslides in Puerto Rico , 1994 .

[27]  H. Schneider,et al.  Ferns diversified in the shadow of angiosperms , 2004, Nature.

[28]  Matthew W. Hahn,et al.  Sequencing, Assembling, and Correcting Draft Genomes Using Recombinant Populations , 2014, G3: Genes, Genomes, Genetics.

[29]  C. Haufler ELECTROPHORESIS IS MODIFYING OUR CONCEPTS OF EVOLUTION IN HOMOSPOROUS PTERIDOPHYTES , 1987 .

[30]  Saravanaraj N. Ayyampalayam,et al.  Phylotranscriptomic analysis of the origin and early diversification of land plants , 2014, Proceedings of the National Academy of Sciences.

[31]  R. Marrs,et al.  The Ecology of Bracken: Its Role in Succession and Implications for Control , 2000 .

[32]  S. Wessler,et al.  The Amborella Genome and the Evolution of Flowering Plants , 2013 .

[33]  Martin D. F. Ellwood,et al.  Doubling the estimate of invertebrate biomass in a rainforest canopy , 2004, Nature.

[34]  F. Bazzaz,et al.  THE FERN UNDERSTORY AS AN ECOLOGICAL FILTER: EMERGENCE AND ESTABLISHMENT OF CANOPY‐TREE SEEDLINGS , 1999 .

[35]  U. Mittwoch Chromosomes and Sex Differentiation , 1975 .

[36]  J. Banks The TRANSFORMER genes of the fern Ceratopteris simultaneously promote meristem and archegonia development and repress antheridia development in the developing gametophyte. , 1997, Genetics.

[37]  P. Wolf,et al.  Electrophoretic Evidence for Genetic Diploidy in the Bracken Fern (Pteridium aquilinum) , 1987, Science.

[38]  D. Soltis,et al.  Estimated rates of intragametophytic selfing in lycopods , 1988 .

[39]  T. J. Cooke,et al.  The Fern Ceratopteris richardii as a Lower Plant Model System for Studying the Genetic Regulation of Plant Photomorphogenesis , 1995, International Journal of Plant Sciences.

[40]  J. Banks,et al.  Generating autotetraploid sporophytes and their use in analyzing mutations affecting gametophyte development in the fern Ceratopteris. , 1997, Genetics.

[41]  L. Gottlieb,et al.  Genetic variation in the homosporous fern Pellaea andromedifolia , 1985 .

[42]  T. Warne,et al.  CERATOPTERIS RICHARDII: APPLICATIONS FOR EXPERIMENTAL PLANT BIOLOGY' , 1987 .

[43]  D. Soltis,et al.  The role of genetic and genomic attributes in the success of polyploids. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  F. Bazzaz,et al.  The fern understory as an ecological filter : Growth and survival of canopy-tree seedlings , 1999 .

[45]  Mari L. Salmi,et al.  Profile and Analysis of Gene Expression Changes during Early Development in Germinating Spores of Ceratopteris richardii1[w] , 2005, Plant Physiology.

[46]  J. E. Watkins,et al.  Ferns in an Angiosperm World: Cretaceous Radiation into the Epiphytic Niche and Diversification on the Forest Floor , 2012, International Journal of Plant Sciences.

[47]  S. Salzberg,et al.  Sequencing and Assembly of the 22-Gb Loblolly Pine Genome , 2014, Genetics.

[48]  Paul G. Wolf,et al.  Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants , 2001, Nature.

[49]  J. Banks,et al.  Characterization of mutations that feminize gametophytes of the fern Ceratopteris. , 2001, Genetics.

[50]  F. Fabbri Secondo Supplemento Alle Tavole Cromosomiche Delle Pteridophyta di Alberto Chiarugi , 1965 .

[51]  J. Bennetzen,et al.  The Physcomitrella Genome Reveals Evolutionary Insights into the Conquest of Land by Plants , 2008, Science.

[52]  Douglas G. Scofield,et al.  The Norway spruce genome sequence and conifer genome evolution , 2013, Nature.

[53]  M. Huber,et al.  Episodic fresh surface waters in the Eocene Arctic Ocean , 2006, Nature.

[54]  M. Donoghue,et al.  An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants , 2010, Proceedings of the National Academy of Sciences.

[55]  H. G. Baker,et al.  Evolutionary Significance of Polyploidy in the Pteridophyta , 1966, Science.

[56]  S. Newmaster,et al.  DNA content variation in monilophytes and lycophytes: large genomes that are not endopolyploid , 2011, Chromosome Research.

[57]  C. N. Stewart,et al.  Stable Transformation of Ferns Using Spores as Targets: Pteris vittata and Ceratopteris thalictroides1[W][OPEN] , 2013, Plant Physiology.

[58]  R. Tryon Development and Evolution of Fern Floras of Oceanic Islands , 1970 .

[59]  L. Rieseberg,et al.  A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern, Ceratopteris richardii , 2007, Genetics.

[60]  D. Sankoff,et al.  Polyploidy and angiosperm diversification. , 2009, American journal of botany.

[61]  E. Zimmer,et al.  Deciding among green plants for whole genome studies. , 2002, Trends in plant science.

[62]  R. Chasan Ceratopteris: A Model Plant for the 90s. , 1992, The Plant cell.

[63]  F. Fabbri Ricerche al Microscopio Ottico ed Elettronico Sulla Struttura del Nucleolo di Cellule Meristematiche di Alcune Piante e Considerazioni Critiche Sulla Teoria del «Nucleolonema» , 1963 .

[64]  I. Manton Book Reviews: Problems of Cytology and Evolution in the Pteridophyta , 1951 .

[65]  Le-Shin Wu,et al.  Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies , 2014, Genome Biology.

[66]  G. Likens,et al.  The Hubbard Brook Ecosystem Study: Productivity, Nutrients, and Phytosociology of the Herbaceous Layer , 1970 .

[67]  Y. Qiu,et al.  Azolla — A Model Organism for Plant Genomic Studies , 2003, Genomics, proteomics & bioinformatics.

[68]  Claude W. dePamphilis,et al.  Ancestral polyploidy in seed plants and angiosperms , 2011, Nature.

[69]  Stanley J. Roux,et al.  Gene expression changes induced by space flight in single-cells of the fern Ceratopteris richardii , 2008, Planta.

[70]  D. Soltis,et al.  Genetic evidence suggests that homosporous ferns with high chromosome numbers are diploid. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[71]  K. Pryer,et al.  Crowdfunding the Azolla fern genome project: a grassroots approach , 2014, GigaScience.

[72]  M. Kelty,et al.  Establishment and Control of Hay-scented Fern: A Native Invasive Species , 1999, Biological Invasions.

[73]  Sònia Garcia,et al.  Recent updates and developments to plant genome size databases , 2013, Nucleic Acids Res..

[74]  R. Bateman,et al.  HETEROSPORY: THE MOST ITERATIVE KEY INNOVATION IN THE EVOLUTIONARY HISTORY OF THE PLANT KINGDOM , 1994 .

[75]  Michael S. Barker,et al.  The Selaginella Genome Identifies Genetic Changes Associated with the Evolution of Vascular Plants , 2011, Science.

[76]  Amborella Genome The Amborella Genome and the Evolution of Flowering Plants , 2013, Science.

[77]  D. Soltis,et al.  A conifer genome spruces up plant phylogenomics , 2013, Genome Biology.

[78]  S. Graham,et al.  Utility of a large, multigene plastid data set in inferring higher-order relationships in ferns and relatives (monilophytes). , 2010, American journal of botany.

[79]  H. Schneider,et al.  Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. , 2004, American journal of botany.

[80]  G. A. Peters,et al.  The Azolla–Anabaena symbiosis: endophyte continuity in the Azolla life‐cycle is facilitated by epidermal trichomes † , 2006 .

[81]  Paul G. Wolf,et al.  A classification for extant ferns , 2006 .

[82]  D. Soltis GENETIC EVIDENCE FOR DIPLOIDY IN EQUISETUM , 1986 .

[83]  D. Soltis,et al.  Evolution of DNA amounts across land plants (embryophyta). , 2005, Annals of botany.