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Phylogenetic Position and Floral Function of Siparuna (Siparunaceae: Laurales) Author(S): S

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Phylogenetic Position and Floral Function of Siparuna (Siparunaceae: Laurales) Author(S): S Phylogenetic Position and Floral Function of Siparuna (Siparunaceae: Laurales) Author(s): S. S. Renner, A. E. Schwarzbach and L. Lohmann Source: International Journal of Plant Sciences, Vol. 158, No. 6, Supplement: Morphology and Evolution of Flowers (Nov., 1997), pp. S89-S98 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2475169 Accessed: 24-09-2015 08:01 UTC REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/2475169?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/ info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to International Journal of Plant Sciences. http://www.jstor.org This content downloaded from 128.252.67.66 on Thu, 24 Sep 2015 08:01:58 UTC All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 158(6 Suppl.):S89-S98. 1997. C 1997 by The Universityof Chicago. All rightsreserved. 1058-5893/97/5806S-0007$03.00 PHYLOGENETICPOSITION AND FLORAL FUNCTION OF SIPARUNA(SIPARUNACEAE: LAURALES) S. S. RENNER,' A. E. SCHWARZBACH, AND L. LOHMANN Departmentof Biology, Universityof Missouri-St.Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121-4499, U.S.A. Nucleotide sequences for two chloroplastgenome regions, the rbcL gene and the trnL-trnFspacer region, were obtainedfor 22 genera and 30 species representingall major lineages of Laurales, witha special samplingeffort being made in the phylogeneticallyproblematic Monimiaceae sensu lato. Magnoliaceae, Winteraceae,Austrobaileyaceae, and Saururaceae were used as outgroups.A morphologicalcharacter matrix for the same taxa was compiled and includes new floral-anatomicaldata for Siparunaceae, a lineage traditionallyplaced in Monimiaceae. Phylogeneticanalyses of the molecular and morphologicaldata based on maximum parsimonyreveal that Siparuna and its sister taxon, the monotypicWest Africangenus Glossocalyx,are not closely relatedto the remainingMonimiaceae, supportingthe view thatthe Monimiaceae in the wide sense are polyphyletic.Based on morphologyand chromosomenumbers, Siparuna formsa clade with Atherospermataceaeand Gomortegaceae, while based on rcbL sequences, it is in a clade with Hernandiaceae, Atherospermataceae,and Gomortegaceae. The trnL-trnFsequences provide no resolutionfor basal nodes in Laurales but agree with the rbcL and morphologicalanalyses in stronglysupporting a placementof Siparun- aceae away fromMonimiaceae s.str.Based on the phylogenetichypotheses, we analyze some of the reportedfloral- morphologicaltrends noted in Monimiaceae and Laurales, such as miniaturizationof ovules, increasinglycomplete enclosure of reproductiveorgans, and aquisitionof functionalsyncarpy. Both Siparuna and Glossocalyx have polycar- pellate gynoecia embedded in massive receptacles covered by a membraneand uniovulate carpels with unitegmic ovules. The membrane,or floralroof, has a small, central pore for the styles or anthersto emerge at anthesis.It is more developed and thickerin female flowersthan in male ones. Consequently,the stylesin particularare forcedinto close physical contact.Flowers are pollinatedby gall midges thatoviposit into themthrough the pore in the floralroof, wherebythey contact stamens or styles.Anatomical studies of flowersrepresenting eight species show thatstyles fuse postgenitallyat the heightwhere theyemerge throughthe pore, resultingin a joint transmissiontrack for pollen tubes thatoriginally landed on differentstigmas. Lateral growthof pollen tubes,which resultsin switchingbetween carpels, was observed in an experimentallypollinated species thathad received large pollen loads. Introduction Endress (1979, 1980b, 1982; Endress and Lorence 1983) is fromcompletely free carpels, withoutany in- Comparativestudies of floralevolution in Monimi- tercellularcommunication between theirinner spaces, aceae have emphasized morphological trends that to "functionally syncarpous" gynoecia. Functional seem to characterizebasal angiospermlineages (En- syncarpycan be achieved in differentways, withmor- dress 1980a, 1980b, 1986, 1990, and 1994, pp. 230- phologicallyfree carpels sharingeither a joint pollen- 232). One such trenddiscerned by Endress (see esp. receiving region formed by massive secretions or a Endress 1990) is towardminiaturization of the ovules, pollen-exchange zone at their bases as in Illicium, resultingin unitegmicand/oi tenuinucellar conditions. where tubes can enter adjacent carpels via theirun- While most basal angiospermshave bitegmic ovules fused margins (Williams et al. 1993). Ecologically, with abundantendo- or perisperm,minute ovules oc- these mechanismscould be increasingreproductive ef- cur in both Laurales and Piperales: Calycanthaceae, ficiency.This may be particularlyimportant in groups Lauraceae, and Hernandiaceae have endospermless in which flowershave numerous carpels but solitary seeds; Peperomia has ovules with a single integument ovules: if insect-depositedpollen loads can be distrib- (Tucker 1980; Tucker et al. 1993). Within Laurales, only Siparuna was known untilrecently to have a sin- uted to more than one carpel, this must increase the gle integument(Heilborn 1931; Endress 1972; S. Ren- numberof ovules that can be fertilized.In Laurales, ner,personal observation),but a screeningof potential functionalsyncarpy via a common pool of mucilage relativesof Siparuna revealed the presence of uniteg- is known fromthe monimiaceous genera Faika, He- mic ovules in the monotypicWest Africangenus Glos- dycarya,Hennecartia, Tambourissa,and Wilkiea (En- socalyx, thus providinga potentialsynapomorphy for dress, 1979, 1980b, 1982, and 1994, p. 232). Below a clade consistingof these two genera. Siparuna com- we reporta new type of functionalsyncarpy by post- prises ca. 72 species of shrubs,straggling shrubs, and genital fusion of stylesin Siparuna. trees, occurringfrom tropical Mexico throughoutthe A thirdtrend noticed by Endress in the Monimi- West Indies and northernSouth America to Bolivia aceae is towardan increasinglycomplete enclosureof and Paraguay (Renner,ongoing revision). The flowers the reproductiveorgans in massive cup-like recepta- are strictlyunisexual and measure a few millimeters cles thatraise the floralperiphery around or above the in diameter(figs. 1, 2). gynoecium.While fleshycupules were presentin now A second floral evolutionarytrend emphasized by extincthigher seed plants (K. Nixon, personal com- munication),within angiospermsthey characterizea 'Authorfor correspondence and reprints. groupof familiesfirst united under the name Laurineae Manuscript received May 1997; revised manuscriptreceived July by Hallier (1905). The Laurineae (or Laurales) include 1997. the Calycanthaceae (threegenera; includingIdiosper- S89 This content downloaded from 128.252.67.66 on Thu, 24 Sep 2015 08:01:58 UTC All use subject to JSTOR Terms and Conditions S90 INTERNATIONAL JOURNAL OF PLANT SCIENCES _~~~ _, Figs.l, 2 Female flowersof Siparuna. Fig. l, S. thecaphora.The floralroof in this species is glabrous and consists of an outerbulge and an inner,narrower collar just visible to the rightof the stylarcomplex. (Real heightof flowerca. 1.6 mm) Fig. 2, S. muricata. The floral roof consists of a wide outer area (not shown) and an innermostcollar thattightly surrounds the styles. Pollen grains visible on stigmatic papillae. mum), Gomortegaceae (monotypic), Hemandiaceae also examines the hypothesisthat Monimiaceae in the (five genera; including Gyrocarpus), Lauraceae (50 wide sense are polyphyleticas suggestedby R. Brown genera), and Monimiaceae s.l. (i.e., Atherospermata- (1814), Schodde (1969, 1970), Endress (1972), and A. ceae with seven genera, Siparunaceae with two or C. Smith (1972). Our understandingof (floral) evolu- three genera, and Monimiaceae with ca. 18). These tionary trends in Monimiaceae, Siparunaceae, and taxa share several charactersbesides the cup-like re- Atherospermataceaestands to be improvedby knowl- ceptacles, includinginaperturate pollen (except Caly- edge of their closest relatives in Laurales. However, canthaceae and Atherospermataceae)usually withspi- trendsalso need to be relatedto the functionof flowers nulose exines, unilacunartwo-trace nodes (also present in pollinationor seed dispersal. To do this we report in some potentialoutgroups and perhapsplesiomorph- new resultsof floral-anatomicalstudies on Glossocalyx ic), decussate leaves (perhaps plesiomorphicand lost and Siparuna and observationson pollen tube growth in Lauraceae and Hernandiaceae), and carpels with a in Siparuna and relate themto the pollinationof these single ovule (except Calycanthaceae,which have two plants by ovipositinggall midges. ovules of which only one formsa matureembryo sac The molecular data presentedare part of ongoing [Nicely 1965], and Gomortegaceae,which have a 2- work on the phylogeneticsystematics of Laurales. or 3-merous syncarpous gynoecium). Four of seven lauralean familieshave stamensdehiscing by apically- Materialand methods hinged valves
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