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Land (Embryophyta)

Susana Magallóna,* and Khidir W. Hilub ) include whisk , horsetails, and eusporang- aDepartamento de Botánica, Instituto de Biología, Universidad iate and leptosporangiate ferns. include Nacional Autónoma de México, 3er Circuito de Ciudad Universitaria, (105 species), (one species), (540 b Del. Coyoacán, México D.F. 04510, Mexico; Department of Biological species), gnetophytes (96 species), which are the gymno- Sciences, Virginia Tech, Blacksburg, VA, 24061, USA , and angiosperms (Magnoliophyta, or P owering *To whom correspondence should be addressed (s.magallon@ plants, 270,000 species). Angiosperms represent the vast ibiologia.unam.mx) majority of the living diversity of . Here, we review the relationships and divergence times of the Abstract major lineages of embryophytes. We follow a classiA cation of embryophytes based on The four major lineages of plants are liver- phylogenetic relationships among monophyletic groups worts, , , and tracheophytes, with the lat- (2, 3). Whereas much of the basis of the classiA cation is ter comprising , ferns, and spermatophytes. Their robust, emerging results suggest some reA nements of high- relationships have yet to be determined. Different stud- er-level relationships among the four major groups. 7 is ies have yielded widely contrasting views about the time includes the inversion of the position of Bryophyta and of embryophyte origin and diversifi cation. Some propose Anthocerophyta, diB erent internal group relationships an origin of embryophytes, tracheophytes, and euphyllo- within ferns, and diB erent relationships among spermato- phytes (ferns + spermatophytes) in the , ~700– phytes. 7 e phylogenetic classiA cation provides charac- 600 million years ago (Ma), whereas others have estimated ters that are useful for establishing taxonomic deA nitions younger dates, ~440–350 Ma. In spite of large differences based on shared-derived characters. 7 e living liverworts in absolute timing, there is agreement that the major lin- are characterized by the presence of oil bodies, a distinctive eages of embryophytes and their key vegetative, physio- spermatozoid ultrastructure, and possibly lunularic acid. logical, and reproductive innovations evolved shortly after embryophyte origin.

Land plants (embryophytes) constitute a monophy- letic group that is well supported by morphological and molecular characters. Numerous vegetative and repro- ductive traits directly associated with life on land char- acterize the group (1) (Fig. 1). Embryophytes are mainly diagnosed by the presence of multicellular , cuticule, archegonia, antheridia, and sporangia, as well as by details of spermatozoid ultrastructure and cell division, and the presence of sporopollenin in walls (2). All living land plants are placed in four major taxa: (liverworts; 5000–8000 species), Bryo- phyta (mosses; ca. 13,000 species), Anthocerophyta (hornworts; 100 species), and Tracheophyta (vascular plants; 285,000 species) (3). 7 e living tracheophytes, in turn, are distributed in four groups. 7 e earliest diver- ging lineage constitutes the Lycopsida (lycophytes, or club mosses; 1230 species), which is the closest relative Fig. 1 A (Braunia squarrulosa) from Mexico displaying the to a that includes ferns and spermatophytes ( () and (red) phases. Credit: plants). Ferns (sometimes called monilophytes; ca. 10,000 C. Delgadillo Moya.

S. Magallón and K. W. Hilu. Land plants (Embryophyta). Pp. 133–137 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009).

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Angiosperms 4 3 2 Ferns Spermatophyta

Lycopsida Tracheophyta 1 Anthocerophyta Bryophyta Marchantiophyta

Np Cm O S D C P Tr J K Pg PR MESOZOIC CZ 600 500 400 300 200 100 0 Million years ago Fig. 2 A timetree of Embryophyta. Divergence times are from (), J (), K (), Np (Neoproterozoic), Table 1. Phylogenetic relationships among the major land O (), P (), Pg (Paleogene), PR (Proterozoic), lineages are not resolved; therefore, the deepest node in the S (), and Tr (). The divergence times for Nodes embryophyte is depicted as a polytomy. Abbreviations: 1 and 2 are similar but their branching is shown as C (), Cm (), CZ (), D resolved.

Mosses are distinguished by multicellular gametophytic Although a few morphological analyses have found a , gametophytic , and a particular - clade formed by liverworts, mosses, and hornworts to the atozoid ultrastructure. Hornworts posses many unique exclusion of tracheophytes (5, 8), virtually all molecu- features, including a distinctively shaped apical cell, a pyre- lar analyses show those three lineages as a paraphyletic noid in , mucilage cells and cavities in the talus, grade of early diverging land plants. Nevertheless, their and an intercalary at the base of the . branching sequence and their relationship with tracheo- 7 e tracheophytes are characterized by the presence of phytes remain unclear. Either liverworts (2, 4, 7, 9–11) branching sporophytes with multiple sporangia and inde- or hornworts (5, 11) have been found to be the earliest pendent alternation of generations. Living tracheophytes diverging lineage of land plants. 7 e closest relative of are further characterized by annular or helical thickenings tracheophytes has been identiA ed as being the hornworts in and possibly by lignin deposition on the inner (7, 9, 11), the mosses (2, 4), a clade including mosses and surface of the wall. hornworts (12), or a clade including mosses and liver- Among liverworts, mosses, and hornworts, the gam- worts (5, 11, 12). etophyte (haploid phase) is dominant through the life Tracheophytes have been ubiquitously recognized as cycle, and the sporophyte (diploid phase) depends on it a monophyletic group in which the deepest split segre- for nutrients and support. 7 e early members of the lin- gates the lycophytes and the (ferns plus eage leading to tracheophytes, all now extinct, displayed spermatophytes) (2, 7, 11, 13). A relatively novel result is an alternation of independent and apparently equally the recognition that all euphyllophytes lacking , that dominant and sporophytes. Among tra- is, the eusporangiate ferns, leptosporangiate ferns, whisk cheophytes, the sporophyte is dominant; the gameto- ferns, and horsetails, are more closely related to each other phyte can either constitute a small independent plant than to spermatophytes (2, 13). A major departure from (among ferns) or be embedded in sporophytic tissues traditional ideas about relationships is the recognition (among spermatophytes). that the eusporangiate and Marattidae Phylogenetic analyses of morphological and molecu- ferns, and the leptosporangiate Polypodiidae ferns do not lar data have generally supported the monophyly of most constitute a monophyletic assemblage, but rather, that of the traditionally recognized major taxonomic groups Ophioglossidae (moonworts) and Psilotidae (whisk ferns) of embryophytes, but there have been unexpected associ- are closest relatives, and that horsetails are more closely ations of taxa, and some relationships still remain unre- related to Marattidae and/or Polypodiidae (5, 13). solved. With a few exceptions, the four major groups of Whereas monophyly is uncontested, embryophytes have been found to be monophyletic 2–7( ). deciphering the relationships of the gnetophytes (a group

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Table 1. Divergence times (Ma) and confi dence/credibility intervals (CI) among embryophytes.

Timetree Estimates Node Time Ref. (21, 29) Ref. (22) Ref. (23) Ref. (26, 27) Ref. (30, 31) Time CI Time CI Time CI Time CI Time CI 1 593 703 (21) 791–615 707.0 805–609 631.8 798–465 486.5 (26)493–480438.8– 2603– –––603813–393– ––– 3 466 411.8 (29) 409–415 – – 572.2 790–354 – – 415.5 414–418 4 355 346.1 (29) 339–353 – – 404.6 524–285 319.7 (27) 339–301 350.3 345–355

Note: Node times in the timetree represent the mean of time estimates using protein sequence data from 51 genes. For ref. (27), the average from different studies. In ref. (21), estimates are derived from pairwise date and confi dence interval (obtained from the averaged dates) for the distances among 50 nuclear protein sequences. For ref. (23), average age divergence of gymnosperms and angiosperms are derived from penalized and confi dence intervals (obtained from the averaged dates) are derived likelihood analyses focused on ferns and on angiosperms (constraining from maximum parsimony and maximum likelihood branch length angiosperm age) (27). In ref. (29), averaged dates and confi dence intervals optimization for the combined sequences of four and nuclear genes (obtained from the averaged dates) are obtained with penalized likelihood for a sample of land plant lineages using nonparametric rate smoothing. for four genes, using 1st + 2nd, and 3rd codon positions The age for Node 1 corresponds to the crown group of embryophytes (23). separately, for a sample across vascular plants. For refs. (30, 31), averaged For ref. (26), the average age and confi dence interval (obtained from the dates and confi dence intervals (obtained from the averaged dates) are averaged dates) of the divergence between liverworts and seed plants are derived from a combined data set of fi ve chloroplast protein-coding genes derived from applying one or two calibration points in penalized likelihood for a sample across land plants, with penalized likelihood implementing dating for a data set of 27 protein-coding genes. For ref. (22), the average branch-pruning and fossil-based rate smoothing. The age for Node 1 date and confi dence interval for the divergence of mosses and angiosperms corresponds to the average of the divergence of mosses and the divergence were derived from six different rate-constant and rate-variable methods of hornworts.

of gymnosperms) to the angiosperms and other gymno- Family , rendering the conifers paraphy- sperms has proven di. cult. Spermatophytes are repre- letic (“gnepine” hypothesis); or with gnetophytes closest to sented in the present day by only four or 0 ve evolutionary the monophyletic conifers (“gnetifer” hypothesis). Recent lineages, which are survivors of a much larger historical results have shown that the “gnetophyte-sister” signal is diversity. Phylogenetic analyses of morphological data provided by sites with high substitution rates, and that this have yielded a variety of hypotheses regarding relation- result is not obtained if rapidly changing sites are excluded ships among living and extinct spermatophytes, but they from analysis, or if data are analyzed with optimization agree in indicating a close relationship between gneto- methods that are less prone to the long-branch attraction phytes and angiosperms (14), which together with a few problem (16, 17, 19). $ e “gnepine” and “gnetifer” rela- particular extinct lineages formed a clade named the tionships are prevalent results from analyses using sites anthophytes. Molecular analyses have only rarely sup- with intermediate to low rates, or using all types of data ported a phylogenetic closeness between gnetophytes analyzed with parametric optimization criteria (17–19). and angiosperms to the exclusion of all other living Whereas the “gnepine” result is more frequent than the seed plants (15), and, when they did, the result has been “gnetifer” one, the two topologies are very similar and shown to be highly improbable with molecular data (16). statistically indistinguishable from the point of view of the Nevertheless, other than rejecting an anthophyte asso- phylogenetic signal in the data (19). Although the position ciation, molecular data have so far failed to provide a of gnetophytes is particularly unstable, currently preva- single universally supported hypothesis of relationship lent molecular results point at the phylogenetic closeness among living spermatophytes. between gnetophytes and conifers, and suggest that all More recently, two hypotheses, which di3 er in the living gymnosperms (including gnetophytes) are more position of gnetophytes, have emerged as the main com- closely related to each other than to angiosperms. petitors (15, 17–19). In one, gnetophytes are the closest Relatively few studies have dated embryophytes or the relatives of a group containing all other living spermato- major divergences within them (20). Heckman et al. (21) phytes (“gnetophyte-sister” hypothesis). In the second one, used the sequences of 50 nuclear proteins for a taxonomic gnetophytes are closely related to conifers within a clade sample, including one moss and seven angiosperms, to that includes all living gymnosperms. $ is hypothesis is estimate the time of divergence of mosses and tracheo- obtained in two variants: with gnetophytes closest to the phytes. By estimating pairwise distances calibrated with

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multiple external secondary calibrations, a Precambrian dated as Pennsylvanian (310 Ma) in the -based ana- (703 ± 45 Ma) divergence time was estimated. Subse- lysis and as Mississippian (329 or 333 Ma, depending on quently those data were analyzed using Bayesian and whether the angiosperm age was A xed or not at 132 Ma) in likelihood rate smoothing methods (22), and a similar the angiosperm-based analysis. 7 ese dates are relatively date was obtained (707 ± 98 Ma). close to the Mississippian (Namurian) age of Cordaitales Soltis et al. (23) evaluated the impact of diB erent genes, (28), presumably the oldest fossil member of the group calibration points, and branch lengths on ages of embry- containing the living lineages of spermatophytes. ophytes as a whole, and of tracheophyte lineages. 7 eir Magallón and Sanderson (29) conducted a study includ- study was based on three plastid protein-coding genes ing all tracheophyte lineages, one liverwort and one charo- and the nuclear 18S ribosomal DNA. Using the topology phycean outgroup, using the plastid protein-coding genes obtained by Pryer et al. (13), with the three atpB, psaA, psbB, and rbcL. Ages were estimated with lineages forming a clade, and branch lengths estimated penalized likelihood, implementing a 419 Ma calibration with maximum parsimony (MP) and with maximum to tracheophytes, derived from the age of the oldest fossil likelihood (ML), divergence times across the tree were pertaining to that divergence (2). 7 e impact of diB erent estimated with a nonparametric rate smoothing method. gene and codon position partitions, and that of includ- Estimated divergence times diB ered substantially depend- ing or excluding fossil-derived constraints on the ages of ing on the calibrations used and on estimation conditions. 20 nodes, was evaluated. Estimates were found to vary By calibrating the tree at the divergence between the two substantially depending on the data and the constraints sampled angiosperms at 125 MY, embryophytes were used. In fossil-constrained estimations, the average age of estimated to have originated in the Precambrian (546.8 or euphyllophytes was Lower Devonian (411.8 ± 3 Ma), and 716.8 Ma with MP and ML branch lengths, respectively). Mississippian (346.1 ± 7 Ma) for spermatophytes. Tracheophytes were estimated to be of Precambrian Hilu et al. (30, 31) expanded the data set of Magallón (710.1 Ma) or Upper Cambrian (495.9) age, and euphyl- and Sanderson (29) to include all major lineages of lophytes of Precambrian (683.4 Ma) or Middle–Upper embryophytes, and the sequences of matK, a plastid pro- Ordovician (460.9 Ma) age, with MP and ML branch tein-coding gene with a relatively fast substitution rate, lengths, respectively. Spermatophytes were estimated as representing so far the single dating study that encom- considerably younger, of Middle Ordovician (465.4 Ma) passes the embr yophy tes as a whole and its major lineages. or Mississippian (343.7 Ma) age, with MP and ML branch Dating was based on a Bayesian tree in which liverworts lengths, respectively. All the preceding dates are consid- are the earliest diverging land plants, and hornworts erably older than spore-containing plant fragments from are closest to tracheophytes. Dating was conducted with the Late Ordovician (24) and of microscopic dispersed penalized likelihood implementing optimal rate smooth- from the Middle Ordovician (25), which are the ing derived from branch-pruning and fossil-based cross oldest generally accepted reports of land plants (24). validations. Calibration and age constraints were very Sanderson (26) used 27 plastid protein-coding genes similar to those in Magallón and Sanderson (29), includ- for 10 land plants and an algal outgroup to estimate ing calibration at the tracheophyte node and 22 min- the age of embryophytes. By using the semiparamet- imum age constraints, but also imposing a maximal 464 ric penalized likelihood method implementing two Ma age to embryophytes, derived from Late Ordovician alternative internal calibrations points, the divergence remains of presumed crown group embryophytes (24). between liverworts and seed plants was found to be of 7 e divergence of mosses from all other embryophytes Lower Ordovician age (483 or 490 Ma, depending if one was estimated as Upper Ordovician (446 ± 1 Ma), or two calibration points were applied). Schneider et al. and the split between hornworts and tracheophytes as (27) investigated the timing of diversiA cation of poly- Silurian (Llandovery; 432 ± 1 Ma). 7 e age of the tra- pod ferns and angiosperms using two independent data cheophyte node was A xed for calibration at 421 Ma (27). sets, one with rbcL and rps4 sequences for 45 ferns and age was estimated as Lower Devonian outgroups, and another with atpB, rbcL, and nuclear (415.5 ± 2 Ma), which is close to the age of , the 18S rDNA sequences for 95 angiosperms and outgroups. oldest euphyllophyte fossil ( 2). Spermatophytes were Ages were estimated with penalized likelihood by A xing estimated to be Mississippian (350.3 ± 5 Ma), older but the age of euphyllophytes at 380 Ma, and constraining relatively close to the age of Cordaitales. several nodes with fossil-derived minimum ages. 7 e Studies about the time of origin and early diversiA - divergence between gymnosperms and angiosperms was cation of embryophytes suggest two widely contrasting

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views. One set of studies (21–23) jointly suggest embry- References ophyte origin and diB erentiation of liverworts, bryo- 1. L. E. Graham, in : Evolution and Ontogeny, phytes, hornworts, tracheophytes, and euphyllophytes S. Blackmore, R. B. Knox, Eds. (Academic Press, London, during a short time in the Precambrian. Spermatophyte 1990). diB erentiation is estimated to have occurred substantially 2. P. Kenrick, P. R. Crane, e Origin and Early DiversiA cation later, in the Ordovician. Another set of studies (26, 27, of Land Plants, A Cladistic Study. (Smithsonian Institution 29–31) suggest embryophyte origin and diversiA cation in Press, Washington and London, 1997), pp. 441. the Paleozoic, in a period of ~70 Ma spanning from the 3. P. R. Crane, P. Kenrick, Aliso 15, 87 (1997). Lower Ordovician origin of embryophytes, to the Lower 4. B. D. Mishler, S. P. Churchill, Brittonia 36, 406 (1984). Devonian origin of euphyllophytes. Spermatophyte ori- 5. K. S. Renzaglia et al., Phil. Trans. Roy. Soc. Lond. B 355, 769 (2000). gin is estimated as being somewhat younger, from the 6. J. Shaw, K. S. Renzaglia, Am. J. Bot. 91, 1557 (2004). Mississippian. 7. Y.-L. Qiu et al., Proc. Natl. Acad. Sci. U.S.A. 103, 15511 In spite of the considerable diB erences in absolute tim- (2006). ing, available evidence congruently suggests the diB er- 8. D. J. Garbary, K. S. Renzaglia, J. G. Duckett, Plant Syst. entiation of embryophyte lineages occurred shortly aJ er Evol. 188, 237 (1993). embryophyte origin. Whereas major innovations neces- 9. L. A. Lewis, B. D. Mishler, R. Vilgalys, Mol. Phylogenet. sary for survival in the terrestrial environment most Evol. 7, 377 (1997). likely evolved before the diB erentiation of embryophyte 10. Y.-L. Qiu et al., Nature 394, 671 (1998). lineages, a substantial amount of morphological and 11. D. L. Nickrent et al., Mol. Biol. Evol. 17, 1885 (2000). physiological innovation took place during the initial 12. R. J. DuB , D. L. Nickrent, Am. J. Bot. 86, 372 (1999). phase of embryophyte evolution. 7 e shiJ from a dom- 13. K. M. Pryer et al., Nature 409, 618 (2001). inant gametophytic phase to a dominant sporophytic 14. P. R. Crane, Ann. MO Bot. Gard. 72, 716 (1985). 15. C. Rydin, M. Källersjö, E. M. Friis, Int. J. Plant. Sci. 163, phase, including the evolution of branched sporophytes 197 (2002). with multiple sporangia, and the evolution of lignitized 16. M. J. Sanderson et al., Mol. Biol. Evol. 17, 782 (2000). cells, particularly of the type that characterize living 17. S. Magallón, M. J. Sanderson, Am. J. Bot. 89, 1991 (2002). tracheophytes, occurred with the diB erentiation of tra- 18. D. E. Soltis, P. S. Soltis, M. J. Zanis, Am. J. Bot. 89, 1670 cheophytes. With the diB erentiation of lycophytes and (2002). euphyllophytes, two evolutionary types of leaves evolved: 19. J. G. Burleigh, S. Mathews, Am. J. Bot. 91, 1599 (2004). simple leaves vascularized by veins that do not form a gap 20. M. J. Sanderson et al., Am. J. Bot. 91, 1656 (2004). in the main vascular strand of the stem, in the 21. D. S. Heckman et al., Science 293, 1129 (2001). lineage; and “true” leaves, derived from modiA cation of 22. S. B. Hedges, J. E. Blair, M. L. Venturi, J. L. Shoe, BMC branching axes, in the euphyllophyte lineage. 7 e origin Evol. Biol. 4, 2 (2004). of spermatophytes apparently lagged behind the initial 23. P. S. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 99, 4430 (2002). embryophyte diversiA cation. Whereas most 24. C. H. Wellman, P. L. OsterloB , U. Mohiuddin, Nature likely evolved several times among tracheophytes, the 425, 282 (2003). sequence of innovations necessary to give rise to the seed 25. P. K. Strother, S. Al-Hajri, A. Traverse, Geology 24, 55 from a heterosporous reproductive system occurred (1996). only once (32). With the origin of spermatophytes, the 26. M. J. Sanderson, Am. J. Bot. 90, 954 (2003). major vegetative and reproductive innovations of embry- 27. H. Schneider et al., Nature 428, 553 (2004). ophytes, including dominant sporophytes, vascularized 28. T. N. Taylor, E. L. Taylor, e Biology and Evolution of systems, and seeds, had evolved. 7 e substantially dif- Fossil Plants (Prentice Hall, Englewood CliB s, New ferent estimates of the timing of embryophyte origin and Jersey, 1993). early diversiA cation suggest that the investigation of this 29. S. Magallón and M. J. Sanderson, Evolution 59, 1653 question would greatly beneA t from a comprehensive (2005). integration of fossils and molecular clocks. 30. K. W. Hilu, S. Magallón, D. Quandt, XVII International Botanical Congress Abstracts, p. 200 (2005). 31. K. W. Hilu, S. Magallón, D. Quandt, Annual Meeting of the Botanical Society of America Abstracts, p. 46 (2006). Acknowledgment 32. K. M. Pryer, H. Schneider, S. Magallón, in Assembling We thank J. A. Barba for his help in preparing the initial the Tree of Life, J. CracraJ , M. J. Donoghue, Eds. (Oxford version of Fig. 2. University Press, New York, 2004), pp. 138–153.

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