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The Gnetales: Recent Insights on Their Morphology, Reproductive Biology, Chromosome Numbers, Biogeography, and Divergence Times

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The Gnetales: Recent Insights on Their Morphology, Reproductive Biology, Chromosome Numbers, Biogeography, and Divergence Times Journal of Systematics JSE and Evolution doi: 10.1111/jse.12190 Review The Gnetales: Recent insights on their morphology, reproductive biology, chromosome numbers, biogeography, and divergence times Stefanie M. Ickert-Bond1* and Susanne S. Renner2 1University of Alaska Museum of the North and Department of Biology and Wildlife, University of Alaska Fairbanks, 907 Yukon Dr., PO Box 756960, Fairbanks, Alaska 99775-6960, USA 2Institute of Systematic Botany and Mycology, University of Munich (LMU), Menzinger Str. 67, 80638 Munich, Germany *Author for correspondence. E-mail: [email protected]. Tel./Fax: 1-907-474-6277/1-907-474-5469. Received 23 November 2015; Accepted 15 December 2015; Article first published online 12 January 2016 Abstract Ephedra, Gnetum, and Welwitschia constitute the gymnosperm order Gnetales of still unclear phylogenetic relationships within seed plants. Here we review progress over the past 10 years in our understanding of their species diversity, morphology, reproductive biology, chromosome numbers, and genome sizes, highlighting the unevenness in the sampling of species even for traits that can be studied in preserved material, such as pollen morphology. We include distribution maps and original illustrations of key features, and specify which species groups or geographic areas are undersampled. Key words: biogeography, chromosome numbers, fertilization, morphology, phylogenetics, pollen, pollination, polyploidy. Mais les Gnetophytes se presentent au botaniste, depuis In terms of their morphology and even basic ecology, longtemps, comme un ensemble d’un inter et^ exceptionnel et the Gnetales remain enigmatic, with surprising discoveries comme un enigme particulierement irritante. continuing to be made (e.g., Wetschnig, 1997; Mundry Pierre Martens, 1971 &Stutzel,€ 2004; Friedman, 2015; Ickert-Bond et al., 2015; Les Gnetophytes Rydin & Bolinder, 2015). Here we review progress over the past 10 years in our understanding of the species The Gnetales are a clade of three genera that is morpho- diversity, morphology, reproductive biology, chromosome logically and genetically so disparate from the remaining numbers, and genome sizes of the Gnetales, highlighting seed plant (cycads, Ginkgo, angiosperms, and Coniferales) the unevenness in the sampling of species even for traits that its precise placement has remained unclear (Mathews, that can be studied in preserved material, such as pollen 2009; reviewed in Mathews et al., 2010; Fig. 1). The order morphology. Gnetales Luersson (or the subclass Gnetidae Pax) is characterized by compound cones with unisexual repro- ductive units borne in the axils of bracts, with the The Gnetales: Three Disparate Mono- ovules surrounded by 1-2 envelopes and the integument extending into a micropylar tube carrying the pollination generic Families droplets (Kubitzki, 1990). This combination of traits is Gnetum L. (Markgraf, 1930) and Ephedra L. (Cutler, 1939 for extremely rare in fossil forms (Krassilov, 2009). Tran- North America only) were monographed in the last century; scriptome data for 92 streptophytes, analyzed along with Welwitschia contains but a single species, endemic to the 11 complete plant genomes, support a position of Gnetales Namib Desert (Leuenberger, 2001; Figs. 2, 3). Ephedra is sister either as sister to Coniferales, represented by seven to the other two genera and comprises about 54 species genera, or as sister to one of their families, the Pinaceae, distributed evenly between the deserts of the Old and New represented by Cedrus and Pinus (Wickett et al., 2014). A World (Stapf, 1889; Ickert-Bond, 2003; Figs. 2, 3; Table 1). placement of the Gnetales near to or inside Coniferales Gnetum has ten species in South America, two to four in would be consistent with previously published analyses tropical West Africa (Biye et al., 2014; Figs. 2, 3; Table 1), and ca. of concatenated gene alignments that aimed to reduce 25 in tropical Asia (Markgraf, 1930; Price, 1996; Won & Renner, long-branch attraction artifacts by implementing various 2006; Hou et al., 2015). Multi-locus analyses of nuclear and among-site rate heterogeneity models (e.g., Bowe et al., plastid DNA sequences have shed light on species relation- 2000; Chaw et al., 2000; Burleigh & Mathews 2007a, 2007b; ships within Ephedra and Gnetum (Ickert-Bond & Wojciechow- Lee et al., 2011; Wu et al., 2011; Zhong et al., 2011; Ruhfel ski, 2004; Won & Renner, 2005a, 2005b, 2006; Ickert-Bond et al., 2014). et al., 2009; Rydin & Korall, 2009; Rydin et al., 2010; Loera et al., January 2016 | Volume 54 | Issue 1 | 1–16 © 2015 Institute of Botany, Chinese Academy of Sciences 2 Ickert-Bond & Renner The species of Ephedra occur in Old World and New World deserts, semideserts, desert steppes or in seasonally dry habitats, such as mediterranean-type evergreen or deciduous woodlands and subtropical thorn scrub (Fig. 2; Ickert-Bond, 2003; Freitag, 2010: Fig. G2-01A). The genus ranges from depressions below sea level (Death Valley of California and Dead Sea area) to about 5000 m in the Andes of Ecuador (E. rupestris, Ickert-Bond, 2005) and to 5300 m in the Himalayas (E. gerardiana, Fu et al., 1999). The desert species tend to be clonal, forming phytogenic mounds by accumulat- ing sand, particularly in dune habitats. Branching in Ephedra is often broom-like with nearly parallel and fastigiate to ascending (virgate) green stems (Fig. 3A). Wood anatomical features of Ephedra include the presence of vessels that increase conducting efficiency as compared to tracheid-only systems in non-gnetalean gymnosperms (reviewed in Carlquist, 2012). The abundance of vessels and their diameter are greatest in the lianoid and scrambling species, while the alpine species have virtually no vessels (Carlquist, 1988; Motomura et al., 2007; Carlquist, 2012). Narrow vessels are characteristic for plants of very dry or desert habitats and probably provide conductive insurance by reducing embolisms (Carlquist, 2012). Nucleated fiber-trache- ids with abundant starch storage often form tangential bands in Ephedra and also appear an adaptation to extremely arid habitats. The female cones (ovulate strobili) of Ephedra consist of bracts in decussate or ternate (as a mode of verticillate) phyllotaxy, with the distal pair/whorl enclosing one to three seeds, each surrounded by a seed envelope (Figs. 3B, 3C, 4E). An anatomical and histological study of pollination-stage female cones of 45 species inferred that a seed envelope with three vascular bundles is the ancestral state and that two Fig. 1. Extreme rate heterogeneity within Gnetales and bundles evolved several times (Rydin et al., 2010). Fleshy gymnosperms based on matK and rbcL gene sequences. bracts characterize the fruiting cones of 38 species (Fig. 3B), A, Unrooted maximum likelihood tree obtained from 558 membranous (Fig. 4E) and winged bracts those of six or seven matK gene sequences, downloaded from GenBank in mid- other species (see section on Seed dispersal). The seed 2008. Values at nodes indicate statistical support from 100 envelopes are smooth (Fig. 4H) or papillate or bear transverse bootstrap replicates under the GTR þG model of substitution. ridges (Ickert-Bond & Rydin, 2011; Figs. 4F, 4G). B, Unrooted maximum likelihood tree obtained from 792 rbcL The male cones (staminate strobili, Fig. 4I) consist of two gene sequences, downloaded from GenBank in mid- 2008. lateral strobili with 2–3 sterile bracts at the base, followed Values at nodes indicate statistical support from 100 by 2–8 (10) fertile bracts, within each of which two median bootstrap replicates under the GTR þG model of substitution. bracts enclose the stalked antherophore (Cutler, 1939; Hufford, 1996; Ickert-Bond, 2003; Mundry & Stutzel,€ 2012, 2015; Hou et al., 2015); a few deep nodes within Ephedra 2004). Each antherophore consists of two fused micro- and Gnetum still remain statistically poorly supported. sporophylls and bears 2–8 stalked or sessile synangia, which result from the fusion of two (rarely three) microsporangia Ephedra (Ephedraceae) (Hufford, 1996; Ickert-Bond, 2003; Mundry & Stutzel€ All Ephedra are perennial and dioecious, and most species are 2004). Mundry and Stutzel€ (2004) interpret the male shrubs (Price, 1996; Ickert-Bond, 2003; Fig. 3A); a few are cones of Ephedra as consisting of two units with four climbers up to 4 m (e.g., Ickert-Bond, 2003: Fig. 3.1 E–F; simple sporophylls, and propose homologies with parts in Freitag, 2010: Fig. G2-02) or small trees up to 2 m (E. equisetina the female cones of Welwitschia and Gnetum (see respective in Freitag, 2010: Fig. G2-01A). The nodes bear narrow, sections below). lanceolate leaves arranged in decussate or whorled phyllo- The pollen of 45 species of Ephedra has been studied with taxis (Figs. 4A–4D). The leaves are 2–15 (40) mm long when light and scanning electron microscopy (Steeves & Barghoorn, fully expanded, but become non-functional (except for 1959; Zhang & Xi, 1983; Ickert-Bond, 2003; Ickert-Bond et al., E. foliata and E. altissima) when the vegetative shoot ceases 2003; Doores et al., 2007; Bolinder et al., 2015a, 2015b; our vegetative elongation (Ickert-Bond, 2003; Dorken,€ 2014). The Table 1). Pollen is ellipsoidal, with characteristic ridges, apical portion of each blade is free while the basal portions and rather large (27–58 mm in average equatorial diameter; are fused into a sheath, with the extent of fusion a species- Figs. 4J, 4K). Based on a phylogenetic analysis of pollen traits, characteristic trait (Figs. 4A–4D). grains with unbranched valleys in the exine (pseudosulci of J. Syst. Evol. 54 (1): 1–16, 2016 www.jse.ac.cn Biology and phylogeny of the Gnetales 3 Fig. 2. The distribution of the Gneales in the context of the World’s climates. A, Distribution plotted on WWW world ecoregions map (black line and at black arrowheads, Ephedra; yellow line, Gnetum; light blue line and at blue arrowhead, Welwitschia). B, Biomes in relation to mean annual temperature and mean annual precipitation based on worldclim climate layers (modified from Donoghue & Edwards, 2014). The distribution map of Old World Ephedra was kindly provided by H. Freitag, University of Kassel.
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