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International Journal of Plant Sciences, Vol Phylogeny of Amaranthaceae and Chenopodiaceae and the Evolution of C₄ Photosynthesis Author(s): G. Kadereit, T. Borsch, K. Weising, H. Freitag Source: International Journal of Plant Sciences, Vol. 164, No. 6 (Nov., 2003), pp. 959-986 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/3691834 Accessed: 20/05/2010 19:46 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=ucpress. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. 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 Int. J. Plant Sci. 164(6):959-986. 2003. ? 2003 by The Universityof Chicago.All rightsreserved. 1058-5893/2003/16406-0013$15.00 PHYLOGENYOF AMARANTHACEAEAND CHENOPODIACEAEAND THE EVOLUTIONOF C4 PHOTOSYNTHESIS G. Kadereit,'l*T. Borsch,t K. Weising,t and H. Freitagt *lnstitut fOrSpezielle Botanik und Botanischer Garten der Johannes Gutenberg-Universitdit Mainz, D-55099 Mainz, Germany; tNees-Institut fOr Biodiversitditder Pflanzen, Friedrich-Wilhelms-Universitit Bonn, D-53115 Bonn, Germany; and tArbeitsgruppe Systematik und Morphologie der Pflanzen, Universitit Kassel, D-34109 Kassel, Germany A phylogeneticanalysis of Chenopodiaceaeand Amaranthaceaewas carriedout using sequencevariation of the chloroplastgene rbcL. Our samplingincluded 108 species of these two familiesalong with 29 species of Caryophyllalesserving as outgroups.Phylogeny inferences with maximumparsimony and maximumlike- lihood indicatethat the two familiesform a well-supportedmonophyletic clade that is sisterto Achatocarpaceae. Despite extensive sampling, we found that the relationshipbetween Chenopodiaceaeand Amaranthaceae remainsunclear as a result of short and weakly supportedbasal branches.The clearly monophyleticPolyc- nemoideae(traditionally considered a subfamilyof Chenopodiaceae)appear as sisterto Amaranthaceaesensu stricto. Within Amaranthaceae,most major lineages inferredexcept Gomphrenoideaeand Celosieaedo not correspondto recognizedsubfamilies and tribes. Bosea and Charpentierabranch first in the Amaranthaceae. WithinChenopodiaceae, the generaof Betoideaeoccur in basaland largelyunresolved positions. The remaining Chenopodiaceaeare divided into three major clades of unclear relationship:Chenopodioideae (Atripliceae s.str., ChenopodieaeI-III); Corispermoideae (Corispermeae); and Salicornioideae(Haplopeplideae, Salicor- nieae), Suaedoideae(Suaedeae, Bienertieae), and Salsoloideae(Camphorosmeae, Sclerolaeneae, Salsoleae I-II). The rbcL tree is discussedalso with regard to historicalclassifications and morphologicalsupport for the majorclades. The molecularresults are usedto elucidatethe evolutionof C4photosynthesis in the two families. C4 photosynthesishas evolved independentlyat least three times in Amaranthaceaeand at least 10 times in Chenopodiaceae.A survey of C4 leaf anatomy revealed 17 differentleaf types that in most cases mark an independentorigin of C4 photosynthesis.The applicationof a molecularclock indicates an age of C4 pho- tosynthesisof 11.5-7.9 Ma in Atriplex (Chenopodioideae)and 21.6-14.5 Ma in subfamilySalsoloideae. Keywords:Amaranthaceae, Chenopodiaceae, phylogeny, systematics, C4 photosynthesis,C4 leaf anatomy. Introduction treated as separate entities although most authors admitted difficultiesin identifyingdistinguishing characters. However, Amaranthaceae and Chenopodiaceae constitute the most di- Baillon(1887) treatedChenopodiaceae and Amaranthaceaeas verse lineage (ca. 180 genera and 2500 species) of the Cary- one family (table 1), as was later suggestedalso by Malligson ophyllales and have long been regarded as two closely related (1922) on the basisof serologicalstudies. Recently, it has again families (Brown 1810; Bentham and Hooker 1880; Baillon been proposed to merge both families into one family Ama- 1887; Volkens 1893; Ulbrich 1934; Aellen 1965-1968; Behnke ranthaceae(APG 1998; Judd et al. 1999). 1976; Thorne 1976; Carolin 1983; Kiihn et al. 1993). Nu- merous studies on the morphology, anatomy, and phytochem- The Position of Amaranthaceae/Chenopodiaceae istry of the two families revealed a number of shared, mostly within Caryophyllales derived features. These include minute sessile flowers arranged subf. were in cymose inflorescences; a five-merous, imbricate, uniseriate Traditionally,Caryophyllaceae Paronychioideae assumedto be the closest relativesof Amaranthaceae/Cheno- perianth; a single whorl of epitepalous stamens; a single basal and Hooker recent ovule; pantoporate pollen; chenopodiad embryogeny; sieve el- podiaceae(Bentham 1880). However, phy- based on characters ements with P-type plastids but without a central protein crys- logenetic analyses morphological (Rod- man rbcL and Savolainenet al. talloid; occurrence of the betacyanins amaranthin and celo- 1994), (Manhart Rettig 1994; and matK data et al. Hilu sianin; and presence of 6,7-methylenedioxyflavonol and 2000b), sequence (Cuenoud 2002; et al. have identifiedthe small Acha- isoflavones (Hegnauer 1964, 1989; Wohlpart and Mabry 2003) neotropicalfamily 1968; Behnke 1976; Natesh and Rau 1984; Sandersson et al. tocarpaceaeas sister to the Amaranthaceae/Chenopodiaceae. The 1988; Rodman 1990, 1994; Behnke and Mabry 1994; see also Amaranthaceae/Chenopodiaceae-Achatocarpaceae we refer to this as the ACA Judd and Ferguson 1999). The two families have mostly been clade (for convenience, clade) clearly belongs to the core Caryophyllales (Cuenoud et al. as is of the as tra- ' Authorfor e-mail 2002) and, such, part Centrospermae correspondence; [email protected]. ditionally circumscribed (Cronquist and Thorne 1994). Manuscript received April 2003; revised manuscript received July 2003. Early analyses of rbcL sequence data (Albert et al. 1992; 959 Table 1 HistoricalClassifications of Chenopodiaceaeand Amaranthaceae Kuiihnet al. 1993/ Moquin-Tandon 1840 Moquin-Tandon 1849 Baillon 1887 Bentham and Hooker 1880 Volkens 1893/Schinz 1893 Ulbrich 1934/Schinz 1934 Townsend 1993 This article Chenopodeae Salsolaceae Chenopodiacees Chenopodiaceae Chenopodiaceae Chenopodiaceae Chenopodiacea Chenopodiaceae Cyclolobeae Cyclolobeae Cyclolobeae Cyclolobeae Cyclolobeae Chenopodioideae Chenopodioideae Chenopodioideae Anserinae Chenopodieae Chenopodices EuchenopodiaeChenopodieae Chenopodieae Chenopodieae Chenopodieae I-IP Spinaciae Spinacieae Atripliceae Atripliceae Atripliceae Atripliceae Atripliceae Camphorosmeae Camphorosmeae Camphorosmeae Camphorosmeae Camphorosmeae Camphorosmeae - Salsoloideae (see below) Chenoleae Sclerolaeneae - Salsoloideae (see below) Corispermoideae Corispermoideae Corispermeae Corispermeae Corispermeae Corispermeae Corispermeae Corispermeae Corispermeae Betoideae Betoideae Beteae Beteae Beteae I-IVa Beteae Hablitzieae Polynemoideae Polynemoideae - Amaranthaceae (sub Amaranthaceae Polycnem&es Polycnemeae Polycnemeae Polycnemeae Polycnemeae Polycnemeae, subtr.) Salicornioideae Salicornioideae Salicornioideae Salicornieae Salicornieae Salicorni&es Salicornieae Salicornieae Halopeplideae Halopeplideae Halopeplideae Salicornieae Salicornieae Salicornieae Spirolobeae Spirolobeae Spirolobeae Spirolobeae Spirolobeae Suaedoideae Salsoloideae Suaedoideae Suaedinae Suaedeae Salsolees Suaedeae Suaedeae Suaedeae Suaedeae Suaedeae Bienertieae Bienertieae Salsoloideae Salsoloideae Salsoleae Salsoleae Salsoleae Salsoleae Salsoleae Salsoleae Salsoleae I-Ia Nucularieae Camphorosmeae (incl. Sclerolaeneae)a Sarcobatoideae (dubia sedis: Sarcobat&es Sarcobatideae Sarcobatideae Sarcobateae Sarcobateae - excl. as Sarcobataceae Sarcobatus) Eubaselleae - excluded Boussingaultieae - excluded Amaranthaceae Amaranthaceae Amaranthaceae Amaranthaceae Amaranthaceae Amaranthaceae Amaranthoideae Amaranthoideae Amaranthoideae amaranthoids I+IP CelosiaeClosilosieaeelosieae Celosieae Celosieae Celosieae Celosieae Achyrantheae Amarantees Amarantheae Amarantheae Amarantheae Amarantheae Amarantheae I-IV Gomphrenoideae Gomphrenoideae Gomphrenoideae Gomphrenoideae Gomphreneae Gomphrenees Gomphreneae Gomphreneae Gomphreneae Gomphreneae Gomphreneae (incl. Pseudoplantageae)• Guillemineae Brayulineae Pseudoplantageae Microtees - excluded Leucaster&es - excluded New tribal classification necessary. KADEREITET AL.-PHYLOGENY OF AMARANTHACEAEAND CHENOPODIACEAE 961 Giannasi et al. 1992; Rettig et al. 1992; Chase et al. 1993; smalltrees. Inflorescences are either complex cymose structures Manhart and Rettig 1994) had already indicated that Po- or the cymes are reducedto a single flower subtendedby one
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