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1592 the Predominantly Aquatic Order Alismatales (Sensu APG III, 2009 ) Displays a Diverse Range of Flower Morphology and Devel

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1592 the Predominantly Aquatic Order Alismatales (Sensu APG III, 2009 ) Displays a Diverse Range of Flower Morphology and Devel American Journal of Botany 99(10): 1592–1608. 2012. F LOWERS AND INFLORESCENCES OF THE SEAGRASS 1 P OSIDONIA (POSIDONIACEAE, ALISMATALES) M ARGARITA V. R EMIZOWA 2,5 , D MITRY D. SOKOLOFF 2 , S EBASTIANO C ALVO 3 , A GOSTINO T OMASELLO 3 , AND P AULA J. RUDALL 4 2 Department of Higher Plants, Faculty of Biology, Lomonosov Moscow State University, Moscow 119234, Russia; 3 Dipartimento di Scienze della Terra e del Mare, Viale delle Scienze, Edifi cio 16 90128 Palermo, Italy; and 4 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK • Premise of the study: The predominantly aquatic order Alismatales displays a highly variable fl ower groundplan associated with a diverse range of developmental patterns. We present the fi rst detailed description of fl ower anatomy and development in Posidonia , the sole genus of the seagrass family Posidoniaceae. Existing accounts provide confl icting interpretations of fl oral and infl orescence structure, so this investigation is important in clarifying morphological evolution within this early-divergent monocot order. • Methods: We investigated two species of Posidonia using light microscopy and scanning electron microscopy. Our observa- tions are interpreted in the framework of a recent molecular phylogeny. • Key results: Partial infl orescences are bracteate spikes, which are arranged into a botryoid or a panicle. The fl owers are perian- thless. The gynoecium is monomerous with the ventral carpel side oriented abaxially. The carpel contains a single pendent bitegmic ovule with a nucellus and long chalaza, both extending along the carpel wall. The ovule develops an integumentary outgrowth. Each fl ower is supplied by a vascular bundle, whereas the fl ower-subtending bracts are nonvascularized. • Conclusions: Our data support a racemose interpretation for the partial infl orescence of Posidonia and the presence of fl ower- subtending bracts. In common with some other Alismatales, Posidonia has simultaneous development of the fl ower and its subtending bract and loss of the bract vascular supply accompanied by innervation of the fl ower by a single vascular strand. The unusual carpel orientation could be an evolutionary reduction of a formerly tricarpellate gynoecium. The ovule of Posidonia is campylotropous and unusual within Alismatales in possessing an integumentary outgrowth. Key words: anatomy; Alismatales; embryology; fl ower; infl orescence; morphology; ovule; Posidonia ; vasculature. The predominantly aquatic order Alismatales (sensu APG explained by these two factors (early-divergent placement and III, 2009 ) displays a diverse range of fl ower morphology and adaptation to aquatic habitats). Alismatales is one of very few development (reviewed by Posluszny and Charlton, 1993 ; monocot lineages in which gynoecia with free carpels are pres- Posluszny et al., 2000 ). In contrast with most other monocot ent in some members. This feature, previously considered orders, Alismatales is characterized by a highly variable fl ower primitive (e.g., Takhtajan, 1987 ; Cronquist, 1988 ) is now com- groundplan ( Endress, 1995 ; Remizowa et al., 2010 ). The near- monly regarded as derived at the level of monocots ( Doyle and basal phylogenetic placement of the order in monocots ( Chase Endress, 2000 ; Chen et al., 2004 ; Endress and Doyle, 2009 ; et al., 2000 , 2006 ; Davis et al., 2004 ; Graham et al., 2006 ; APG Remizowa et al., 2010 ; Sokoloff et al., in press ). The core Alis- III, 2009 ; Iles et al., in press ), makes Alismatales potentially matales include the seagrasses, which are unique in possessing important in inferring early monocot evolution and the putative underwater pollination and fi liform pollen grains (the latter re- ancestral morphology of the monocot fl ower. On the other hand, viewed by Ducker et al., 1978 and Furness and Banks, 2010 ). specialized aquatic members of “core” Alismatales (i.e., ex- The seagrasses are adapted to permanently saline underwater cluding Araceae and Tofi eldiaceae) possess characteristically habitats, where they can occupy large areas, forming under- reduced fl owers that are adapted for underwater pollination water meadows that play a signifi cant role in the functioning of ( Posluszny and Charlton, 1993 ; Endress, 1995 ). However, marine ecosystems. the high fl oral diversity of core Alismatales cannot be fully Of 13 families of Alismatales recognized by the Angiosperm Phylogeny Group ( APG III, 2009 ), 12 have been well inves- 1 Manuscript received 13 May 2012; revision accepted 10 September tigated with respect to fl ower development ( Table 1 ). The only 2012. family for which such data are hitherto lacking is the monoge- The authors thank Peter Endress, Will Iles, and Usher Posluszny for neric seagrass family Posidoniaceae, which is distributed in the suggestions on the manuscript, Will Iles and Sean Graham for discussion Mediterranean and the southern coast of Australia. This excep- of the phylogeny of Alismatales, Ivan I. Shamrov for discussion on ovule tion is primarily due to technical diffi culties in obtaining suit- morphology, and Evgeny Mavrodiev for providing some literature. This able material; reproductive development of Posidonia K. D. work was supported by an International Joint Project grant from the Royal Koenig occurs at some depth in the sea ( Campey et al., 2002 ). Society (to M.V.R., D.D.S., P.J.R.) and grants from the Russian Foundation for Basic Research and Ministry of Education and Science of Russia (FCP Furthermore, in the Mediterranean species P. oceanica (L.) ‘Kadry’, NK-541P/P314) (to M.V.R., D.D.S.). Delile, fl owering is infrequent, and clonal growth is important 5 Author for correspondence (e-mail: [email protected]) in maintenance of populations ( Procaccini and Mazzella, 1998 ; Balestri and Cinelli, 2003 ; Calvo et al., 2006 , 2010 ; Diaz-Almela doi:10.3732/ajb.1200227 et al., 2006 ). Large, vegetative clones of P. oceanica are American Journal of Botany 99(10): 1592–1608, 2012; http://www.amjbot.org/ © 2012 Botanical Society of America 1592 October 2012] REMIZOWA ET AL.—FLOWERS AND INFLORESCENCES OF THE SEAGRASS POSIDONIA 1593 T ABLE 1. Summary of literature on fl oral development in families of season. Because young infl orescences of Posidonia are not vis- Alismatales sensu APG (2009) . Note that fl ower development is still ible externally on the plant, a developmental series is obtain- unknown in Maundia , for which a monogeneric family Maundiaceae able only by collection of ample material and careful laboratory can be adopted ( von Mering and Kadereit, 2010 ). dissection to reveal relatively few infl orescences. Flowers of Family Reference Posidonia are morphologically unusual and lack close ana- logues in monocots, especially in possessing stamens with large Alismataceae Kaul, 1967a , b ; Singh and Sattler, 1972 , 1973 ; tepal-like outgrowths. As Tomlinson (1982) noted, the various Charlton and Ahmed, 1973 ; Sattler and Singh, 1973 ; interpretations of fl ower and infl orescence morphology of Posi- Leins and Stadler, 1973 ; van Heel, 1988 ; Ronse De Craene and Smets, 1995 ; Charlton, 2004 donia are highly controversial, and information from anatomy Aponogetonaceae Singh and Sattler, 1977 and particularly development are urgently needed to provide Araceae Lehmann and Sattler, 1992 ; Scribailo and Tomlinson, useful interpretative evidence. Kamelina (1990 , 2011 ) noted 1992 ; Barabé, et al., 2000 , 2002 , 2011 ; Buzgo, 2001 that the embryology of Posidoniaceae is almost unknown, a gap Butomaceae Singh and Sattler, 1974 that was only partially fi lled by a recent paper on megasporo- Cymodoceaceae Tomlinson and Posluszny, 1978 ; McConchie et al., 1982 genesis and embryo development in Australian Posidonia ( Ma Hydrocharitaceae Kaul, 1969 ; Scribailo and Posluszny, 1985 et al., 2012 ). In particular, no detailed data are available on Juncaginaceae Lieu, 1979 ; Charlton, 1981 ; Posluszny et al., 1986 ; Buzgo et al., 2006 ; Remizowa et al., in press ovule morphology in Posidoniaceae, even though this feature Posidoniaceae This study represents an important taxonomic marker in Alismatales. Potamogetonaceae Sattler, 1965 ; Posluszny and Sattler, 1973 , 1974a , 1976 ; Molecular phylogenetic data indicate that Posidoniaceae Posluszny and Tomlinson, 1977 ; Posluszny, 1981 ; are close relatives of Cymodoceaceae and Ruppiaceae ( Les Sun et al., 2000 et al., 1997 ; Iles et al., in press ). These results contradict the Ruppiaceae Posluszny and Sattler, 1974b ; Kaul, 1993 ; traditional views that Cymodoceaceae are most closely related Lock et al., 2011 ; Lock, 2012 Scheuchzeriaceae Posluszny, 1983 to Zannichelliaceae and Ruppiaceae to Potamogetonaceae Tofi eldiaceae Remizova and Sokoloff, 2003 ; Remizowa et al., 2005 , ( Eckardt, 1964 ; Dahlgren et al., 1985 ; Takhtajan, 1987). Thus, 2006 , in press detailed morphological data on Posidonia are needed to rein- Zosteraceae Soros-Pottruff and Posluszny, 1995a , b vestigate the evolutionary history of Alismatales in the new phylogenetic context. estimated to be hundreds to thousands of years old ( Arnaud- Haond et al., 2012 ). MATERIALS AND METHODS Here, we present the fi rst detailed description of fl ower anat- omy and development in Posidonia , including specimens spe- Specimens were obtained from three sources. (1) Material of the Mediter- cifi cally collected by underwater diving several times during a ranean species Posidonia oceanica (L.) Delile including developmental fl oral Fig. 1. Posidonia oceanica . (A) Scheme of shoot and infl orescence morphology. (B) Diagram of a lateral
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