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Between Two Fern Genomes Sessa, Emily B; Banks, Jo A; Barker, Michael S; Der, Joshua P; Duffy, Aaron M; Graham, Sean W; Hasebe, Mitsuyasu; Langdale, Jane; Li, Fay-Wei; Marchant, D B; Pryer, Kathleen M; Rothfels, Carl J; Roux, Stanley J; Salmi, Mari L; Sigel, Erin M; Soltis, Douglas E; Soltis, Pamela S; Stevenson, Dennis W; Wolf, Paul G Sep 25, 2014

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REVIEWBetween Two Fern GenomEmily B Sessa1,2*, Jo Ann Banks3, Michael S Barker4, JoshuaeSesilrisr dheweye fwlclade (Spermatophyta) that includes the ecologically dom-date to ca. 350 mya [17]), and the most recent commonancestor (MRCA) of the leptosporangiate ferns arose ca.Sessa et al. GigaScience 2014, 3:15http://www.gigasciencejournal.com/content/3/1/15acute in light of recent efforts to sequence the transcrip-tomes of all major lineages of green plants [23,24]. TheUSAFull list of author information is available at the end of the articleinant flowering plants. Thus, the phylogenetic position offerns makes them pivotal in the evolutionary history ofland plants (Embryophyta), and essential for a comprehen-sive understanding of the origin and diversification of280 mya [17,18]. Several fern lineages diverged from oneanother prior to the divergence of the angiosperm andgymnosperm sister clades (Figure 1).Despite the ubiquity of ferns and their ecological andevolutionary importance, genomic resources for thegroup remain sparse. Ferns are the only major clade ofvascular land plants for which a complete nuclear gen-ome has not yet been sequenced. This gap is particularly* Correspondence: emilysessa@ufl.edu1Department of Biology, Box 118525, University of Florida, Gainesville, FL32611, USA2Genetics Institute, University of Florida, Box 103610, Gainesville, FL 32611,[10-12]. Phylogenetically, ferns are sister to the seed plantKeywords: Azolla, Ceratopteris, Comparative analyses, Ferns, Genomics, Land plants, MonilophytesIntroductionFerns (Monilophyta) are an ancient lineage of land plantsthat comprise a significant component of the Earth’s terres-trial flora. They are the second largest group of vascularplants, with more than 10,000 species [1], and play a majorrole in shaping community assembly and ecological pro-cesses in many biomes. For example, ferns shape ecosys-tem regeneration, persistence, and biomass production ineastern North American temperate forests [2-4]; play key-stone roles in tropical rainforest canopies [5,6], heathlands[7], after landslides [8], and on islands [9]; and include sev-eral invasive species with significant economic impactnumerous traits found in seed plant crops and model spe-cies, such as rice and Arabidopsis [13,14].ReviewIn a broad sense, ferns include four main clades: psilotoids(whisk ferns) + ophioglossoids, equisetoids (horsetails),marattioids, and leptosporangiates (Figure 1). The leptos-porangiate ferns are the most species-rich clade by far,with over 9,000 species [15,16] that include the majorityof fern species found in temperate and tropical regions.Ferns and seed plants diverged from a common ancestoraround 380 million years ago (mya) (the oldest fern fossilsMitsuyasu Hasebe8, Jane Langdale9, Fay-Wei Li10, D BlainStanley J Roux13, Mari L Salmi13, Erin M Sigel10, Douglas Eand Paul G Wolf6AbstractFerns are the only major lineage of vascular plants not reprgenome sequence information significantly impedes our abonly in ferns, but across all land plants. Azolla and Ceratopteferns to have their nuclear genomes sequenced. They diffethus represent the immense diversity of extant ferns. Togetcomparative analyses across ferns and all land plants. Heredescribe a number of outstanding questions in plant biologtaxa with sequenced nuclear genomes. We explain why thacross land plants, and we provide a rationale for how knobeyond the ferns themselves.© 2014 Sessa et al.; licensee BioMed Central LCommons Attribution License (http://creativecreproduction in any medium, provided the orDedication waiver (http://creativecommons.orunless otherwise stated.edge of fern genomes will enable progress in researchOpen AccessesP Der5,15, Aaron M Duffy6, Sean W Graham7,Marchant1,11, Kathleen M Pryer10, Carl J Rothfels12,16,oltis1,2,11, Pamela S Soltis2,11, Dennis W Stevenson14ented by a sequenced nuclear genome. This lack ofity to understand and reconstruct genome evolution notare ideal and complementary candidates to be the firstramatically in genome size, life history, and habit, andr, this pair of genomes will facilitate myriad large-scalereview the unique biological characteristics of ferns andthat will benefit from the addition of ferns to the set ofern clade is pivotal for understanding genome evolutiontd. This is an Open Access article distributed under the terms of the Creativeommons.org/licenses/by/4.0), which permits unrestricted use, distribution, andiginal work is properly credited. The Creative Commons Public Domaing/publicdomain/zero/1.0/) applies to the data made available in this article,Sessa et al. GigaScience 2014, 3:15 Page 2 of 7http://www.gigasciencejournal.com/content/3/1/15assembly, analysis, and interpretation of these transcrip-tomes would benefit enormously from the availability ofwell-annotated fern genomes. Recent innovations in se-quencing technologies and the resulting torrent of whole-200300400500600Precambrian Paleozoic MJTriPerCarDevSilOrdCamPro70.0200296380323602365420LeptosporangiatAngiosperms(Flowering plantsSpermatophyta(Seed plants)Monilophyta (Ferns)EuphyllophytaTracheophyta (Vascular plants)280Figure 1 Phylogeny of major groups of land plants. Based on [13,15,19,2given, and approximate times of major divergences are indicated. Ferns as a wdivergence of the major seed plant clades. The most recent common ancestoancestors of Ceratopteris and Azolla diverged from each other ca. 200 mya, weTimeTree [21,22].genome sequencing projects have fueled a renaissancein comparative genetic and genomic analyses, and eachgenome sequenced yields new insights into plant evolu-tion. For example, the recently-sequenced genome ofEudicotsGymnospermsLycopodiophytaAmborellaMarattioidsEquisetoids(Horsetails)BryophytaCeratopterisAzollaPsilotoids(Whisk ferns)OphioglossoidsMonocots0100CenozoicesozoicPal Neour Cre1,100 spp.2 genomes10,000 spp.0 genomes1,200 spp.1 genome25,000 spp.1 genome300,000 spp.75+ genomes144147e ferns)Osmunda0]. Approximate numbers of species and available genome sequences arehole include lineages that diverged from one another prior to ther of all leptosporangiates arose approximately 280 mya [17,18]. Thell before the divergence of monocots and eudicots. Dates obtained fromSessa et al. GigaScience 2014, 3:15 Page 3 of 7http://www.gigasciencejournal.com/content/3/1/15Amborella trichopoda [25]—the sister taxon to all otherangiosperms—has revealed much about the conserva-tion of synteny across flowering plants and about gen-ome organization, as well as gene content in the ancestralangiosperm. It has also facilitated inference of ancientgenome doubling events in angiosperms. Ferns, with theirlarge genomes, high chromosome numbers, independentgametophyte phase, and mix of heterosporous and homo-sporous taxa, offer unparalleled opportunities for ground-breaking comparative genetic and genomic analyses acrossland plants as a whole.Ferns provide a stark contrast to other lineages of landplants in several key biological features. For example, an-giosperms and gymnosperms are both dominated by adiploid, spore-bearing (sporophyte) stage of the life cycle.Their haploid sexual stage, the gametophyte, is extremelyreduced (microscopic in angiosperms) and completelydependent on the sporophyte for nutrition. On the otherhand, in bryophytes (mosses, liverworts and hornworts), itis the sporophyte that is dependent at maturity on thedominant, macroscopic and photosynthetic gametophyte.Ferns and lycophytes are the only land plants where, formost taxa, both gametophytes and sporophytes are inde-pendent, free-living organisms that can each be long-lived.Unlike seed plants, which are exclusively heterosporous,ferns include both heterosporous and homosporous spe-cies. The latter group includes the majority of extant ferndiversity, in which only one spore type is produced thatdevelops into a gametophyte that is either bisexual, orwhose sex is determined by non-genetic aspects of develop-ment (e.g., pheromones from surrounding gametophytes).The evolution from homospory to heterospory—in which amegaspore develops into a female gametophyte that in-cludes one or more egg cells, and a microspore developsinto a male gametophyte that includes sperm—is amongthe most important transitions in the evolution of plants,with profound effects on plant reproduction and the lifecycle [26]. Nevertheless, the nuclear genome of a homospo-rous vascular plant has yet to be sequenced.Cytological studies throughout the twentieth century re-vealed that ferns, especially homosporous species (whichinclude up to 99% of extant ferns [1]), have significantlyhigher chromosome numbers than other plants [27-30].Homosporous ferns average n = 57.05 chromosomes, com-pared to n = 15.99 for flowering plants [31], and the highestchromosome number known for any multicellular organ-ism (2n = 1440) is that of the homosporous fern Ophioglos-sum reticulatum [32]. However, heterosporous fernspossess an average of only n = 13.62 chromosomes, veryclose to the average of flowering plants—another hetero-sporous lineage. To date, no explanatory hypothesis for thiscross-lineage discrepancy in chromosome numbers vs.spore type has survived rigorous testing [33]. Along withtheir high chromosome numbers, many homosporousferns have extremely large genomes [34-39], and homo-sporous ferns are the only land plants to show a strongpositive correlation between chromosome number andgenome size [40].Because of their high chromosome numbers [41,42],homosporous ferns were initially assumed to have expe-rienced many rounds of ancient whole-genome duplica-tion (polyploidy) [31], events that have likely influencedthe structures of all land plant genomes. In addition, twodecades of experiments have consistently shown that ho-mosporous ferns possessing the putative base chromosomenumbers of their genus—even if those numbers are highcompared to those of angiosperms—behave genetically asdiploids (e.g., [43-52]). Ferns also lack chromosome-levelevidence of extensive ancient polyploidy, such as syntenicchromosomal blocks [53,54]. This combination of highchromosome numbers and lack of evidence for extensivepolyploidy in homosporous ferns has been referred to asthe “polyploidy paradox” [55]. Whole-genome data are es-sential for resolving this paradox and also for understand-ing basic aspects of genome organization and differentpathways for genome streamlining and diploidization—acting post-polyploidization—that may operate in ferns vs.angiosperms.Paleopolyploidy events have been inferred in the his-tories of all angiosperm lineages studied to date (e.g.,[56]) and are implicated in the ancestral angiosperm andancestral seed plant genomes [25,57]. Thus, even con-temporary flowering plant taxa with relatively small ge-nomes, such as the model species Arabidopsis thaliana(n = 5, 125 Mb [58]), often belong to lineages that haveexperienced multiple rounds of polyploidy. Arabidopsisis thought to have experienced five such events, includ-ing the ancestral seed plant and angiosperm duplications[57,59]. Various groups have evidently responded tothese events in different ways, and data from ferns arethe key to understanding these differences. Using thesedata, we can ask, for example: how do the various gen-omic components (e.g., repetitive elements) differ acrossland plant lineages, and how do their fates differ follow-ing polyploidy? What mechanisms are responsible forthe universally smaller numbers of chromosomes in het-erosporous vs. homosporous lineages, and how do theserelate to the transitions among mating systems across landplants? What genomic changes underlie trends in gameto-phyte reduction and the shift from haploid-dominant todiploid-dominant life cycles across land plants? Do thefree-living, haploid gametophytes of ferns experience strongpurifying selection? Ferns are the crucial missing clade forunderstanding all of these evolutionary paradoxes. Mostimportantly, the addition of ferns to the set of sequencedland plant genomes will also facilitate reconstruction of theancestral euphyllophyte (ferns plus seed plants; Euphyllo-phyta) and vascular plant (Tracheophyta) genomes, and willSessa et al. GigaScience 2014, 3:15 Page 4 of 7http://www.gigasciencejournal.com/content/3/1/15inform efforts to reconstruct the ancestral seed plant gen-ome by providing an outgroup that is more suitable forcomparative analyses than are the currently available lyco-phyte [60] and moss [61] genomes. Improved understand-ing of genomic changes during the evolution of seed plantswill provide a new perspective for examining key evolution-ary innovations in that clade, such as the seed itself.To capture and characterize the genetic, genomic, andecological diversity of ferns, we recommend two candi-dates for genome sequencing: Azolla (Azollaceae: Salvi-niales) and Ceratopteris (Pteridaceae: Polypodiales). Bothhave been promoted as model ferns for genome sequen-cing [14,40,62,63] and together, Azolla and Ceratopterisare a powerful combination. They cumulatively representmore than 400 million years of independent evolution(MRCA 200 mya [16]), and embody the key genomic andlife-history characteristics of interest for fern genomesequencing.Azolla is a heterosporous, free-floating water fern witha compact, 750 Mb (1C) genome and n = 22 chromo-somes [38,64]. It has long been valued in Southeast Asiaas a green fertilizer due to its symbiotic relationship withNostoc azollae, a cyanobacterium that lives in cavitiesenclosed by the leaf tissue of Azolla [65] and renders itcapable of nitrogen fixation [66]. Azolla also has promiseas a biofuel and bioremediator in carbon sequestrationefforts [63]. In addition, Azolla has been implicated asthe cause of a massive shift in Earth’s climate approxi-mately 50 mya [67], when atmospheric carbon dioxidelevels were apparently halved by Azolla-driven carbonsequestration [68-70]. A genome sequence for Azollawill allow us to explore its relationship with its symbi-onts and may facilitate efforts to harness its nitrogen-fixing ability on a scale large enough to provide aninexpensive source of nitrogen-rich fertilizer [71].Recently, the BGI (formerly Beijing Genomics Insti-tute) agreed to complete the first fern genome sequen-cing project, for Azolla, in collaboration with principalinvestigator K.M. Pryer and colleagues (see [72,73]). Sup-plemental funds were also raised through crowdfunding[74,75], and the PIs are currently gathering material for theproject. This planned sequencing of Azolla will provide ini-tial and much-needed genomic resources for ferns, butgiven the deep divergence times, variation in life-historycharacteristics, and diversity within this clade, one ferngenome is simply not enough to address the full range ofoutstanding genomic questions in ferns and across landplants.Ceratopteris provides an ideal contrast to Azolla. It is ho-mosporous, and its genome is 11.26Gb (1C; DB Marchant,unpublished), an order of magnitude larger than that ofAzolla. This size is more typical of genome sizes found inleptosporangiate ferns and is closer to the size scale of coni-fer genomes than to Azolla. Ceratopteris is the “Arabidopsisof the fern world”: it can be readily transformed with re-combinant DNA [76,77] and has a fast life cycle, featuresthat have made it an ideal genetic model system for study-ing sex expression and mating systems [78-81], sporeand gametophyte development [82-87], and even plantresponses to gravity during space flight [88]. In addition, arapidly developing strain of Ceratopteris has been used ex-tensively as an educational model system in undergradu-ate and K-12 biology instruction worldwide [89,90].The earliest candidates for genome sequencing in plantstended to be those with small and simple genomes thatcould be assembled with relative ease. As the trend to-wards whole-genome sequencing intensifies, an increasingnumber of taxa with large or complex genomes will be ofinterest for complete nuclear genome sequencing. It islikely that most large fern genomes will not assemble eas-ily using current techniques, making them important testcases for improved sequencing strategies, mapping, andespecially assembly approaches, such as those recently de-veloped for sequencing of the 22Gb (1C) loblolly pine[91,92] and 20Gb (1C) Norway spruce [93] genomes [94].Ceratopteris will provide such an opportunity, and geneticresources for this species already exist to facilitate the as-sembly process. These include a genetic linkage map andmapping population comprising ~500 doubled haploidlines (DHLs) [53], which will allow efficient de novo se-quencing and high-quality assembly, leveraging, for ex-ample, the recombinant population genome constructionapproach of Hahn et al. [95]. Azolla will provide a novelopportunity to sequence a plant nuclear genome that hasco-evolved for more than 70 million years along with thegenomes of its obligate, vertically-inherited symbioticmicrobiome. The genome of one such symbiont has beensequenced [66], but additional components of the fernmicrobiome are not well characterized.ConclusionsFerns are a phylogenetically pivotal and evolutionarilycritical group of plants, yet they remain a group forwhich we lack extensive nuclear genomic resources. Thisis an astonishing reality, given the progress that has beenmade to date elsewhere across the tree of life. Transcrip-tome sequencing efforts such as the 1,000 Plants Project[23] have vastly expanded the gene sequence resourcesavailable for plants, but genes alone are insufficient toanswer the most pressing questions in fern and landplant genome evolution. Ferns are crucial for under-standing many aspects of plant development, physiology,metabolism, and evolution, and they hold the answers tokey questions that have puzzled evolutionary and com-parative biologists for more than a century. Betweenthese two ferns—Ceratopteris and Azolla—evolution hasoperated for 400 million years, providing tremendousopportunity for differences to accumulate, both betweenSessa et al. GigaScience 2014, 3:15 Page 5 of 7http://www.gigasciencejournal.com/content/3/1/15these genomes and between ferns and other extantplants. Simultaneous sequencing of Azolla and Ceratop-teris will close the phylogenetic gap in available plant ge-nomes, and more importantly, will complete the criticalframework necessary for rigorous comparative studies ofgenome structure and function across land plants.AbbreviationsGb: Gigabases; Mb: Megabases; MRCA: Most recent common ancestor;mya: Million years ago.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsEBS and PGW conceived and drafted the paper; all other authors edited,contributed comments to, and read and approved the final manuscript.AcknowledgementsThe title alludes to the popular internet comedy series “Between Two Fernswith Zach Galifianakis”: http://www.funnyordie.com/between_two_ferns.Note from the EditorsA related discussion by Fay-Wei Li and Kathleen Pryer on crowdfundingefforts to sequence the Azolla fern genome is published alongside thisarticle [75].Author details1Department of Biology, Box 118525, University of Florida, Gainesville, FL32611, USA. 2Genetics Institute, University of Florida, Box 103610, Gainesville,FL 32611, USA. 3Department of Botany and Plant Pathology, PurdueUniversity, 915 West State Street, West Lafayette, IN 47907, USA. 4Departmentof Ecology & Evolutionary Biology, University of Arizona, 1041 East LowellStreet, Tucson, AZ 85721, USA. 5Department of Biology, Penn StateUniversity, 201 Life Science Building, University Park, PA 16801, USA. 6EcologyCenter and Department of Biology, Utah State University, 5305 Old Main Hill,Logan, UT 84322, USA. 7Department of Botany, University of British Columbia,3529-6720 University Blvd., Vancouver, BC V6T 1Z4, Canada. 8NationalInstitute for Basic Biology, 38 Nishigounaka, Myo-daiji-cho, Okazaki 444-8585,Japan. 9Department of Plant Sciences, University of Oxford, South Parks Road,Oxford OX1 3RB, UK. 10Department of Biology, Duke University, Post OfficeBox 90338, Durham, NC 27708, USA. 11Florida Museum of Natural History,Dickinson Hall, University of Florida, Gainesville, FL 32611, USA. 12Departmentof Zoology, University of British Columbia, 2329 W. Mall, WAITING Vancouver,BC V6T 1Z4, Canada. 13Department of Molecular Biosciences, University ofTexas, 205 W. 24th Street, Austin, TX 78712, USA. 14New York BotanicalGarden, 2900 Southern Boulevard, Bronx, NY 10458, USA. 15Current address:Department of Biological Science, California State University, 800 N. StateCollege Blvd., Fullerton, CA 92831, USA. 16Current address: UniversityHerbarium and Department of Integrative Biology, University of California,1001 Valley Life Sciences Building, Berkeley, Berkeley, CA 94720, USA.Received: 8 August 2014 Accepted: 18 September 2014Published: 25 September 2014References1. Smith AR, Pryer K, Schuettpelz E, Korall P, Schneider H, Wolf P:A classification for extant ferns. Taxon 2006, 55:705–731.2. George LO, Bazzaz FA: The fern understory as an ecological filter:Emergence and establishment of canopy-tree seedlings. Ecology 1999,80:833–845.3. 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