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Year: 2006

First steps towards a floral structural characterization of the major rosid subclades

Endress, P K ; Matthews, M L

Abstract: A survey of our own comparative studies on several larger clades of rosids and over 1400 original publications on rosid flowers shows that floral structural features support to various degrees the supraordinal relationships in rosids proposed by molecular phylogenetic studies. However, as many apparent relationships are not yet well resolved, the structural support also remains tentative. Some of the features that turned out to be of interest in the present study had not previously been considered in earlier supraordinal studies. The strongest floral structural support is for malvids (Brassicales, Malvales, Sapindales), which reflects the strong support of phylogenetic analyses. Somewhat less structurally supported are the COM (Celastrales, Oxalidales, Malpighiales) and the nitrogen-fixing (Cucurbitales, Fagales, Fabales, Rosales) clades of fabids, which are both also only weakly supported in phylogenetic analyses. The sister pairs, Cucurbitales plus Fagales, and Malvales plus Sapindales, are structurally only weakly supported, and for the entire fabids there is no clear support by the present floral structural data. However, an additional grouping, the COM clade plus malvids, shares some interesting features but does not appear as a clade in phylogenetic analyses. Thus it appears that the deepest split within eurosids- that between fabids and malvids - in molecular phylogenetic analyses (however weakly supported) is not matched by the present structural data. Features of ovules including thickness of integuments, thickness of nucellus, and degree of ovular curvature, appear to be especially interesting for higher level relationships and should be further explored. Although features of interest are not necessarily stable at the level of a large clade, they do show a considerable concentration in particular clades and are rare or lacking in others. This may be viewed as a special trend for this feature to evolve in this group or to be conserved as a synapomorphy (or a combination of both)

DOI: https://doi.org/10.1007/s00606-006-0444-7

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-155761 Journal Article Published Version

Originally published at: Endress, P K; Matthews, M L (2006). First steps towards a floral structural characterization of the major rosid subclades. Plant Systematics and Evolution, 260(2-4):223-251. DOI: https://doi.org/10.1007/s00606-006-0444-7 Pl. Syst. Evol. 260: 223–251 (2006) DOI 10.1007/s00606-006-0444-7

First steps towards a floral structural characterization of the major rosid subclades

P. K. Endress and M. L. Matthews

Institute of Systematic Botany, University of Zurich, Switzerland

Received November 3, 2005; accepted January 23, 2006 Published online: July 20, 2006 Ó Springer-Verlag 2006

Abstract. A survey of our own comparative studies integuments, thickness of nucellus, and degree of on several larger clades of rosids and over 1400 ovular curvature, appear to be especially interesting original publications on rosid flowers shows that for higher level relationships and should be further floral structural features support to various degrees explored. Although features of interest are not the supraordinal relationships in rosids proposed necessarily stable at the level of a large clade, they by molecular phylogenetic studies. However, as do show a considerable concentration in particular many apparent relationships are not yet well clades and are rare or lacking in others. This may resolved, the structural support also remains ten- be viewed as a special trend for this feature to tative. Some of the features that turned out to be of evolve in this group or to be conserved as a interest in the present study had not previously synapomorphy (or a combination of both). been considered in earlier supraordinal studies. The strongest floral structural support is for malvids Key words: Rosids, eurosids, fabids, malvids, (Brassicales, Malvales, Sapindales), which reflects nitrogen-fixing clade, supraordinal relationships, the strong support of phylogenetic analyses. Some- floral structure, ovules. what less structurally supported are the COM (Celastrales, Oxalidales, Malpighiales) and the nitrogen-fixing (Cucurbitales, Fagales, Fabales, Introduction Rosales) clades of fabids, which are both also only weakly supported in phylogenetic analyses. The In the past decade new results of molecular sister pairs, Cucurbitales plus Fagales, and Malva- phylogenetic studies have brought tremendous les plus Sapindales, are structurally only weakly progress in our perception of plant relation- supported, and for the entire fabids there is no clear ships at all hierarchical levels. In the frame- support by the present floral structural data. work of the eudicots, which were established in However, an additional grouping, the COM clade morphological cladistic studies (Donoghue plus malvids, shares some interesting features but and Doyle 1989, Doyle and Hotton 1991) does not appear as a clade in phylogenetic analyses. Thus it appears that the deepest split within slightly before the onset of the ground eurosids–that between fabids and malvids - in breaking molecular works, orders were newly molecular phylogenetic analyses (however weakly circumscribed, and some quite substantially. supported) is not matched by the present structural Also there are new assemblages of orders that data. Features of ovules including thickness of constitute formerly unrecognized large clades 224 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

(outlined in APG 2003, Soltis et al. 2005). The two subclusters, which receive weaker support: content of the rosids (in the premolecular era the ‘‘nitrogen-fixing clade’’ (Cucurbitales, Fa- called Rosidae, Rosiflorae, or Rosanae, Dahl- gales, Fabales, Rosales) and the ‘‘COM’’ clade gren 1980, Cronquist 1981, Takhtajan 1987, (Celastrales, Oxalidales, and Malpighiales). Thorne 1992) has considerably changed. Within the ‘‘nitrogen-fixing clade’’, Cucurbi- In great contrast to the progress in molec- tales and Fagales appear as sisters. A small ular phylogenetic research, understanding of order, Zygophyllales (Zygophyllaceae and structural features, not only for these newly Krameriaceae) appears as sister to fabids in circumscribed large clades but also for lower some analyses but with less than 50% support levels, orders, families, and genera, has not (Soltis et al. 2005); therefore we leave it in an advanced to the same degree. New structural unresolved position in rosids in our figures. characters must be explored that have not been Within malvids, Malvales and Sapindales discussed before in macrosystematic studies, appear as sisters, both with weak support and likewise characters that were earlier used (APG 2003, Soltis et al. 2005). The difficulties should be probed for new large clades. that have been encountered when trying to Rosids are a very large clade including resolve the phylogenetic topology at various about 30% of all angiosperm species. The levels may have been caused by the probable clade contains 14 mainly large orders, most of rapid early diversification of rosids and some which are well supported by molecular phylo- of their subclades in the Cretaceous (e.g. Davis genetic studies (Soltis et al. 2000, 2005; APG et al. 2005, Soltis et al. 2005), and perhaps, in 2003; Judd and Olmstead 2004; Scho¨ nenberger addition, because of the large size of these and von Balthazar 2006). However, it is clades, which may need more extensive sam- unclear for most of these orders how they are pling. related to each other (Fig. 1). Thus, despite These apparent largest subclades of the impressive progress in some respects, the rosids are new and have never been considered process of phylogenetic elucidation is only at as clades before. Their sheer size makes their its beginning. structural characterization a massive task, and Two major clusters of orders appear in fact, a structural characterization has not moderately to well supported as clades in yet been performed (see also Stevens 2001 molecular studies: fabids (=eurosids I), and onwards). malvids (=eurosids II). Within fabids there are This study is an attempt to make a first step towards this goal. We concentrate on the highest levels within rosids: assemblages of orders (but also this at different levels), while considering all current orders for data collec- tion, including Saxifragales and Vitaceae as potential sister groups of rosids. Our study is based on two sources: (1) the studies on several orders of rosids that we carried out over the past five years (Matthews et al. 2001; Scho¨ - nenberger et al. 2001; Matthews and Endress 2002, 2004, 2005a, b, 2006, Endress 2005; Endress and Matthews 2006) plus our earlier studies in other rosids and putative sister Fig. 1. Cladogram of rosids plus potential sisters groups (Endress 1967, 1977, 1989; Endress et (Saxifragales and Vitaceae) (modified after APG 2003 al. 1983; Hufford and Endress 1989; Endress and Soltis et al. 2005, with jackknife values from and Stumpf 1990, 1991; Sutter and Endress Soltis et al. 2005) 1995; Merino Sutter and Endress 2003; Blarer P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 225 et al. 2004; Merino Sutter et al. 2006) and (2) a following additional new molecular phyloge- search of over 1400 publications with original netic results (partly discussed in Soltis et al. information throughout all orders of rosids. 2005). To Saxifragales, Cynomoriaceae (Nick- Our studies of several orders (Matthews and rent et al. 2005) and Peridiscaceae (including Endress 2002, 2004, 2005a, b, 2006; Matthews Soyauxia) (Davis and Chase 2004) are added. et al. 2001; Scho¨ nenberger et al. 2001) To Malpighiales, Rafflesiaceae are added (Bark- acquainted us with some idiosyncrasies and man et al. 2004, Nickrent et al. 2004), and to features of potential interest. We have mainly malvids, Dipentodontaceae (Peng et al. 2003), concentrated on these features in our literature Tapisciaceae (Simmons et al. 1998; Savolainen search. The publications are on systematics, et al. 2000; Soltis et al. 2000, 2005), and floral structure and embryology. It was not Perrottetia (Zhang and Simmons, in press) are sufficient to use published compilations of added (but outside of the three major orders). data on morphology and embryology. Among Brassicales, Brassicaceae are subdi- Although handbooks on systematic embryol- vided into Brassicaceae, Capparaceae and Cle- ogy, such as Schnarf (1931b), Davis (1966), omaceae (Hall et al. 2002). To Malvales, and Johri et al. (1992), are highly useful for a Apodanthaceae and Cytinaceae are added quick survey on familial characters, these (Barkman et al. 2004, Nickrent et al. 2004). works were only used for a compilation of original literature, and not as a source for structural data. The bibliography by Nagen- Results dran and Dinesh (1989) was also used. By the Malvids (= Eurosids II) study of the illustrations in the original liter- ature and from our own work we found some Campylotropous ovules and zig-zag micro- features of systematic relevance for which the pyle (Fig. 2). In campylotropous ovules, in classical embryological terminology is not contrast to anatropous ovules, the curvature sufficiently differentiated, and therefore spe- encompasses not only the ovular base up to the cific mention of these features is lacking in the chalazal region, but also the upper part of text of such publications (see also Endress the ovule. As a consequence, the nucellus and 2003, 2005). In addition, one must be cautious the embryo sac becomes curved. Commonly, a even with the use of primary literature as campylotropous ovule has an anatropous terms are not always used in the same way. shape in early development before further This is another reason to carefully check the curving. In many cases, the campylotropous illustrations and not only the text. It is of form appears only after fertilization, during course not possible to cite every single piece of seed development (e.g. in part of Fabaceae and literature used in the present publication. part of Malvaceae) (Bouman and Boesewinkel However, we try to cite at least one publica- 1991). In this paper only ovules are considered tion for each feature and taxon mentioned (of as campylotropous that show this shape at the the focused groups), and preferably one of the time of fertilization. more recent ones. In angiosperms, campylotropous ovules The goal of this study is to find new are often associated with a zig-zag micropyle. features that represent idiosyncrasies of these This type of micropyle is formed by both clades and that are also interesting from an integuments, and in a median longitudinal evolutionary point of view, thus helping to section the micropylar canal is not straight better understand the biology of these clades. but zig-zag-shaped. The outer integument It is not to find new features for use in a exhibits excessive growth and overgrows the ‘‘determination key’’ for large clades. micropylar part of the inner integument such Circumscription of the families is according that the micropylar part of the outer integ- to APG (2003), with some modifications ument becomes displaced towards the funicle. 226 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

An ‘‘inverse zig-zag micropyle’’ also exists in ropous ovules but occurs rarely in anatro- which the zig-zag-shape goes in the opposite pous ovules (e.g. Batis, Bataceae, Alimova direction; however, it is absent in campylot- 1985a).

Figs. 2–7. Presence of features that are concentrated in malvids among rosids plus potential sisters (topology modified after APG 2003 and Soltis et al. 2005; soft polytomy setting of MacClade 4.07 used for illustration). Signatures: white: absent or rare; gray: present in at least 2 families, if the order has 5 or more families (or in less than 50% of the families, in which the feature has been studied); black: present in at least 50% of the families (in which the feature has been studied) and in more than 1 genus each, if the families are not too small P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 227

In rosids, campylotropous ovules are al- aceae, Tobe and Peng 1990; Capparaceae, most always associated with a zig-zag micro- Rodionova 1983; Cleomaceae, Maheshwari pyle (Fig. 2). (Interestingly, this is not the case and Khan 1953; Moringaceae, Puri 1941; in the campylotropous ovules of the non-rosid Resedaceae, Singh and Gupta 1968; Tovaria- Caryophyllales, in which the micropyle has no ceae, Mauritzon 1935), 5 families of Malvales zig-zag pattern because it is commonly formed (including 7 subfamilies of Malvaceae) by the inner integument alone.) Both campy- (Bixaceae, Nandi 1998b; Cochlospermaceae, lotropous ovules and zig-zag micropyles are Schnarf 1931a; Malvaceae, Rao 1954; Munt- concentrated in malvids (also in Fabales, and ingiaceae, Rao 1952; Thymelaeaceae, Gue´ rin less so in Geraniales). 1916), and 3 families of Sapindales (Meliaceae, The frequent co-occurrence of these two Prakash et al. 1977; Rutaceae, Starshova and patterns may be seen as a functionally linked Solntseva 1973; Sapindaceae, Weckerle and pair of features in malvids. However, there are Rutishauser 2003). also cases in malvids in which the ovules have Developmentally retarded inner integument. a zig-zag micropyle but are not campylotro- There are ovules in which the inner integument pous (e.g. Poncirus, Rutaceae, Boesewinkel is developmentally retarded in comparison to 1978). The same is known from some Fabales the outer integument and nucellus. In such (e.g. Fabaceae, Hardenbergia, Berg 1979; Po- ovules the inner integument is much shorter lygalaceae, Moutabea, Verkerke 1985). This than the outer and may not even be long gives the impression that either the two enough to take part in micropyle formation in features are not completely linked or, more the mature ovule. The tendency to form such interestingly, that a zig-zag micropyle, and ovules is present predominantly in the malvids. thus, an excessive growth of the outer integu- It is reported in Brassicales in at least 4 families ment may be a precondition for the excessive (Akaniaceae, Tobe and Raven 1995; Brassica- ovule curvature that leads to the campylotro- ceae, Sumner and Van Caesele 1988; Cappar- pous form. aceae, Narayana 1962; Cleomaceae, Campylotropous ovules are recorded in at Arunalakshmi 1989), among Malvales in 6 least 8 (of the 14) families of Brassicales subfamilies of Malvaceae (e.g. Rao 1949) and (Brassicaceae, Bowman 1994; Bretschneidera- among Sapindales in Rutaceae (Boesewinkel ceae, Tobe and Peng 1990; Capparaceae, 1977) and Meliaceae (Paetow 1931). Rodionova 1983; Cleomaceae, Khan 1950; This feature may also be developmentally/ Emblingiaceae, Melville 1969; Gyrostemona- functionally connected with campylotropy and ceae, Eckardt 1971; Resedaceae, Chaban and excessive growth of the outer integument. Such Yakovlev 1974; Tovariaceae, Mauritzon 1935; a connection may be supported by the addi- unknown in Koeberliniaceae and Pentadip- tional occurrence of a delayed inner integu- landraceae), at least 3 (of the 9) families of ment in a number of Fabaceae (Dnyansagar Malvales (Cochlospermaceae, Nandi 1998b; 1958), in which campylotropy and zig-zag Malvaceae, Chandra and Bhatnagar 1976; micropyle are also common. Neuradaceae, Murbeck 1916; unknown in Gynophores or androgynophores (or stipes Diegodendraceae), and at least 4 (of the 9) in free carpels) (Fig. 3). A gynophore is a families of Sapindales (Burseraceae, Narayana stalk-like part (or at least a constriction) 1960; Rutaceae, Boesewinkel 1984; Sapinda- between the ovary and the next outer floral ceae, Weckerle and Rutishauser 2005; organs, in bisexual flowers, the androecium. In Simaroubaceae, Narayana 1957; unknown in apocarpous gynoecia, each carpel may have a Biebersteiniaceae and Kirkiaceae). stalk-like base, which is called a stipe. An Similarly, zig-zag micropyles were recorded androgynophore is a stalk-like organ between in at least 7 families of Brassicales (Brassica- the androecium and the next outer floral ceae, Belyaeva and Fursa 1981; Bretschneider- organs, in flowers with petals, the corolla. 228 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

Gynophores (or stipes) and androgyno- Petals with ventral elaborations (Fig. 5). phores are concentrated in malvids. In Petals with ventral elaborations are mostly Brassicales they are recorded in at least 8 associated with a nectary (Endress and Mat- families (Brassicaceae, Endress 1992; Cappar- thews 2006). They can be related to peltate aceae, Endress 1992; Cleomaceae, Endress carpel form and may be expressed as a ventral 1992; Moringaceae, Periasamy and Indira scale. They can also be more complicated, 1986; Pentadiplandraceae, Ronse De Craene exhibiting more than one scale either side by 2002; Resedaceae, Sobick 1983; Salvadora- side or one behind the other. The nectary can ceae, Khsetrapal 1970; Setchellanthaceae, be above or below the ventral scale (or one of Tobe et al. 1999), in Malvales in at least 3 the ventral scales), or make up the entire scale, families (Malvaceae, Correll and Correll 1982; or be on another organ next to the scale Sphaerosepalaceae, Horn 2004; Thymelaea- (Fig. 5). ceae, Venkateswarlu 1947), and in Sapindales Such petals tend to be concentrated in in at least 4 families (Burseraceae, Engler malvids. They were reported in Brassicales in 1931a; Meliaceae, Harms 1940; Rutaceae, at least 5 families (Cleomaceae, Emblingiaceae, Engler 1931b; Simaroubaceae, Endress et al. Pentadiplandraceae, Resedaceae, and Tropae- 1983). olaceae), in Malvales at least in the family Another clade in which these features are Malvaceae (in 4 subfamilies), and in Sapin- concentrated are Fabales in fabids (Fabaceae, dales in at least 2 families (Anacardiaceae, Lewis et al. 2005; Polygalaceae, Leinfellner Sapindaceae) (Endress and Matthews 2006). 1972; Surianaceae, Gutzwiller 1961). They are also reported in at least 6 families Gynoecium with more than five carpels in a of Malpighiales (Achariaceae, Dichapetala- whorl (Fig. 4). The tendency to form gynoecia ceae, Erythroxylaceae, Hypericaceae, Lina- with more than five carpels in a whorl is ceae, Turneraceae) (Endress and Matthews prominent in malvids. In Brassicales it is 2006). recorded in at least 3 families (Capparaceae, Monosymmetric flowers (Fig. 6). The ten- Ronse De Craene and Smets 1997; Gyroste- dency to form monosymmetric flowers is monaceae, Hufford 1996; Tovariaceae, Fisel conspicuous in malvids. They are reported in and Weberling 1990), in Malvales in at least 3 Brassicales in at least 8 families (Brassicaceae, families (Cytinaceae, Igersheim and Endress Rollins 1963; Bretschneideraceae, Ronse De 1998; Malvaceae, Correll and Correll 1982; Craene et al. 2002; Capparaceae, Vogel 1954; Neuradaceae, Ronse De Craene and Smets Cleomaceae, Endress 1992; Emblingiaceae, 1995), and in Sapindales also in at least 3 Leins 1969; Moringaceae, Olson 2003; Resed- families (Anacardiaceae, pers. obs.; Meliaceae, aceae, Sobick 1983; Tropaeolaceae, Ronse De Narayana 1959; Rutaceae, Engler 1931b). Craene and Smets 2001), in Malvales in at least Another clade with a certain concentration 2 families (Cochlospermaceae, Poppendieck of taxa with more than 5 carpels in a whorl are 1980; Malvaceae, Fryxell 1983), and in Sapin- Malpighiales of the COM clade of fabids. This dales in at least 4 families (Anacardiaceae feature is present in at least 11 (out of 37) families (monosymmetry by reduction), Mitchell and (Achariaceae, Gilg 1925; Caryocaraceae, Mori 1987; Rutaceae, Engler 1931b; Sapinda- Dickison 1990a; Clusiaceae, Engler 1925; ceae, Ronse De Craene et al. 2000; Meliaceae, Euphorbiaceae, Webster 1994; Medusagyna- Harms 1940). ceae, Dickison 1990b; Ochnaceae, Rao and In addition, in several malvids, monosym- Gupte 1957; Phyllanthaceae, Sutter 1994; metry may be oblique, i.e. the symmetry plane is Djarwaninshih 2004; Quiinaceae, Schneider et not the median plane that is formed by the al. 2002; Rafflesiaceae, Igersheim and Endress axillantaxisandthesubtendingleaf(pherophyll) 1998; Rhizophoraceae, Setoguchi et al. 1996; of the flower. This was reported for certain Salicaceae, van Heel 1967). Brassicales (Bretschneideraceae, Ronse De P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 229

Craene et al. 2002; Moringaceae, Olson 2003; dress 1999; Humiriaceae, Narayana and Rao Tropaeolaceae, Ronse De Craene and Smets 1969; Ixonanthaceae, Steyermark and Luteyn 2001) and Sapindales (Rutaceae, Engler 1931b; 1980; Linaceae, Endress 1999; Medusagyna- Sapindaceae, Ronse De Craene et al. 2000). ceae, Dickison 1990b; Ochnaceae, Amaral Monosymmetric flowers in eurosids are 1991; Turneraceae, Gonzalez 1993). also concentrated in Fabales (Fabaceae, Po- Outside of eurosids it is also present in lygalaceae) and, to some extent, in Malpighi- Geraniales (Geraniaceae, Hypseocharitaceae, ales (Chrysobalanaceae, Prance and White Ledocarpaceae) and Myrtales (Combretaceae, 1988; Dichapetalaceae, Engler and Krause Lythraceae, Melastomataceae, Onagraceae). 1931; Euphorbiaceae, Radcliffe-Smith 2001; Euphroniaceae, Lleras 1976; Lacistemaceae Fabids (=eurosids I) (monosymmetry by reduction), Endress 1999; Malpighiaceae, Vogel 1990; Ochnaceae, Ama- A feature of apparent concentration in fabids ral 1991; Passifloraceae, Sazima and Sazima that needs further exploration is idioblasts 1978; Podostemaceae, Razi 1955; Trigonia- with a conspicuously thickened, mucilaginous ceae, Kopka and Weberling 1984). However, periclinal internal cell wall on the outer sepal among Malpighiales, in most families in which surface (Matthews and Endress, submitted). monosymmetric flowers occur, they are rare. Anatropous ovules (as opposed to campylot- Outside of eurosids (fabids and malvids) ropous in malvids) are predominant in fabids there are concentrations of monosymmetric (except for some Fabales). However, anatro- flowers in Geraniales (Geraniaceae, Melianth- pous ovules are also predominant in non- aceae) and Myrtales (Lythraceae, Melastomat- eurosid rosids and are likely plesiomorphic in aceae, Myrtaceae, Onagraceae, Vochysiaceae). rosids. It appears easier to find synapomor- Contort petal aestivation (Fig. 7). Contort phies for the two major subclades of the fabids petal aestivation tends to be concentrated in than for the fabids as a whole. malvids. It is reported from at least 6 families in Brassicales (Akaniaceae, Ronse De Craene COM Clade et al. 2002; Capparaceae, Ronse De Craene et al. 2002; Caricaceae, Ronse De Craene and Relatively thin nucellus and presence of an Smets 1999; Koeberliniaceae, Mehta and integumentary endothelium (Figs. 8, 9). Most Moseley 1981; Limnanthaceae, Eichler 1878; prominent in the COM clade is ovule structure Moringaceae, Olson 2003), at least 6 families with respect to nucellus thickness and endo- in Malvales (Cistaceae, Nandi 1998a; Cochlo- thelium formation. However, the diversity of spermaceae, Poppendieck 1980; Dipterocarpa- form found in the nucellus is not sufficiently ceae, Rao 1962; Malvaceae, Bayer and Ku- captured by the commonly used terminology. bitzki 2002; Neuradaceae, Huber 1993; The two classically distinguished nucellus Sarcolaenaceae, Bayer 2002), and at least 6 types, crassinucellar and tenuinucellar, are families in Sapindales (Burseraceae Lam 1932; defined by the location of the meiocyte and Meliaceae, Murty and Gupta 1978; Pegana- resulting megaspores. In a crassinucellus, the ceae, Ronse De Craene and Smets 1996; meiocyte and megaspores are deeply buried Rutaceae, Correll and Correll 1982; Sapinda- under several cell layers. In a tenuinucellus, the ceae, Ronse De Craene et al. 2002; Simaroub- meiocyte and megaspores are situated imme- aceae, Correll and Correll 1982). diately below the epidermis and fill the entire A second centre of occurrence is in nucellus (apart from the epidermis). However, Malpighiales, where it is reported from at least there are also two intermediate forms, which 10 families (Bonnetiaceae, Maguire 1972; deserve distinction, weakly crassinucellar, with Clusiaceae, Gill et al. 1998; Ctenolophonaceae, a subepidermal cell or cell layer covering the Narayana and Rao 1971; Euphorbiaceae, En- meiocyte and megaspores, and incompletely 230 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

A B C D

Fig. 8. Types of ovules (schematic median longitudinal sections at meiocyte stage; shaded: integumentary endothelium). A Crassinucellar. B Weakly crassinucellar. C Incompletely tenuinucellar. D Tenuinucellar tenuinucellar, with the meiocyte and megasp- least 3 (of the 6) families (Cephalotaceae, ores subepidermal but not filling the entire Cunoniaceae, Oxalidaceae, Matthews and En- nucellus (Endress 2003). Tenuinucellar ovules dress 2002). and the two intermediate types tend to have an In addition, it is of special interest that in endothelium, i.e. a secretory tissue in the the COM clade even in crassinucellar ovules integument epidermis adjacent to the nucellus. the nucellus tends to be relatively narrow During embryo sac formation the thin nucellus (Matthews and Endress 2002, 2005b). And is dissolved by the growing embryo sac, and even in such crassinucellar ovules of the COM the embryo sac becomes contiguous with this clade, an endothelium may also be present, a endothelium. combination which is rare in other rosids. This Thin nucelli plus an endothelium are a good combination is reported in Celastrales from character for the COM clade. Weakly crassin- Celastraceae (Adatia and Gavde 1962), in ucellar or incompletely tenuinucellar ovules are Malpighiales from at least 5 families (Erythr- reported in Celastrales from 2 (of the 3) oxylaceae, Mametyeva 1985; Ixonanthaceae, families (Celastraceae, Matthews and Endress Narayana 1970; Linaceae, Narayana 1963; 2005b; Parnassiaceae, Matthews and Endress Putranjivaceae, Tokuoka and Tobe 1999; 2005b), in Malpighiales from at least 19 (of the Rhizophoraceae, Nikiticheva and Yakovlev 37) families (Balanopaceae, Merino Sutter and 1985), and in Oxalidales from at least 4 Endress 2003; Bonnetiaceae, Prakash and Lau families (Oxalidaceae, Boesewinkel 1985; Con- 1976; Chrysobalanaceae, Tobe and Raven naraceae, Mauritzon 1939; Cunoniaceae, 1984; Clusiaceae, Puri 1939 (endothelium not Mauritzon 1939; Elaocarpaceae, including mentioned); Dichapetalaceae, Boesewinkel and Tremandraceae, Matthews and Endress Bouman 1980; Elatinaceae, Dathan and Singh 2002). Also in Zygophyllaceae, which may be 1971; Erythroxylaceae, Boesewinkel and Gee- sister of fabids (but with less than 50% nen 1980; Humiriaceae, Boesewinkel 1985; support, Soltis et al. 2005), crassinucellar or Hypericaceae, Rao 1957; Ixonanthaceae, Rao weakly crassinucellar ovules combined with an and Narayana 1955; Linaceae, Boesewinkel endothelium are present (Phatak 1971). 1980; Lophopyxidaceae, Sleumer 1942; Ochna- Seeds with arils (Fig. 10). Seeds with arils ceae, Narayana 1973; Pandaceae Takhtajan are also conspicuous for the COM clade. They 1997; Podostemaceae, Murguı´ a-Sa´ nchez et al. are reported in Celastrales from 2 families 2002; Putranjivaceae, Singh 1970; Rafflesia- (Celastraceae, Kapil et al. 1980; Lepidobotry- ceae, Igersheim and Endress 1998; Rhizophor- aceae, Hammel and Zamora 1992), in aceae, Tobe and Raven 1988b; Trigoniaceae, Malpighiales from at least 13 families (Achari- Boesewinkel 1987), and in Oxalidales from at aceae, Steyn et al. 2002; Clusiaceae, Corner P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 231

1976; Ctenolophonaceae, Takhtajan 1997; Eu- Arils are also present but less prominent in phorbiaceae, Tokuoka and Tobe 2002, 2003; some other clades. In malvids they are Ixonanthaceae, Winkler 1931; Malesherbia- reported in Brassicales (Caricaceae, Corner ceae, Harms 1925; Passifloraceae, Kloos and 1976; Cleomaceae, Kers 1970; Setchellantha- Bouman 1980; Phyllanthaceae, pers. obs., ceae, Iltis 1999), Malvales (Malvaceae, Corner Picrodendraceae, Berg 1975; Rhizophoraceae, 1964), and Sapindales (Meliaceae, Corner Tobe and Raven 1987b; 1988b; Salicaceae, 1976; Sapindaceae, van der Pijl 1957, Weckerle van Heel 1979; Turneraceae, Kloos and Bou- and Rutishauser 2005). In Fabales they are man 1980; Violaceae, Kapil et al. 1980), and in reported from a number of Fabaceae and Oxalidales from at least 3 families (Connara- Polygalaceae. In Crossosomatales they occur ceae, Corner 1976; Elaeocarpaceae, including in Crossosomataceae, Stachyuraceae, and in Tremandraceae, Boesewinkel 1999; Matthews reduced form, in Ixerbaceae and Strasburgeri- and Endress 2002; Oxalidaceae, Corner 1976). aceae (Matthews and Endress 2005a).

Figs. 9–12. Presence of features that are concentrated in fabids among rosids and potential sisters (topology modified after APG 2003 and Soltis et al. 2005; soft polytomy setting of MacClade 4.07 used for illustration). Signatures: white: absent or rare; gray: present in at least 2 families if the order has 5 or more families (or in less than 50% of the families, in which the feature has been studied); black: present in at least 50% of the families (in which the feature has been studied) and in more than 1 genus each, if the families are not too small 232 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

Nitrogen-fixing clade Rhamnaceae, Tomlinson 1980; Rosaceae, Fell- ingham and Linder 2003; Ulmaceae, Urtica- Outer integument thicker than inner integu- ceae). ment. In the nitrogen-fixing clade the outer In all other large clades of fabids, the integument is commonly thicker than the incidence of apetaly is much more rare. In inner. However, this is also the case in putative Celastrales apetaly appears to be absent, and sister groups of rosids, such as Saxifragales in Malpighiales it is known from 9 families and Vitaceae. Thus it may be plesiomorphic (Achariaceae, Gilg 1925; Balanopaceae, for rosids (see below). Merino Sutter and Endress 2003; Chrysoba- Unitegmic ovules. There is a tendency lanaceae, Prance and White 1988; Euphorbia- towards unitegmic ovules in the nitrogen-fixing ceae, Webster 1994; Lacistemaceae, Agostini clade, which are otherwise very rare in rosids. 1973; Phyllanthaceae, Webster 1994; Picro- Unitegmic ovules are reported in Cucurbitales dendraceae, Merino Sutter et al., 2006; from Anisophylleaceae (Tobe and Raven Putranjivaceae, Webster 1994; Salicaceae, Gilg 1987a), in Fabales from 2 (of the 4) families 1925). In Oxalidales it is reported from 4 (Fabaceae (only Lupinus), Atabekova 1963, families (Brunelliaceae, Cuatrecasas 1970; Surianaceae, Heo and Tobe 1994), in Fagales Cephalotaceae, Matthews and Endress 2002; from 5 (of the 8) families (Nothofagaceae, Cunoniaceae, Moody and Hufford 2000, Mat- Poole 1952; Betulaceae, Endress 1967, Sogo thews et al. 2001; Elaeocarpaceae, only part of and Tobe 2005; Juglandaceae, Verhoog 1968; Sloanea, Coode 2004, Endress and Matthews, Myricaceae, Macdonald and Sattler 1973; in press). Ticodendraceae, Tobe 1991), and in Rosales Also in malvids apetaly is uncommon: in in 1 (of the 9) families (Rosaceae, Juel 1918). Brassicales it is reported from 2 families In contrast, in the COM clade unitegmic (Capparaceae, Pax and Hoffmann 1936; Gyr- ovules are unknown from Celastrales and ostemonaceae, Hufford 1996), in Malvales it is Oxalidales, and are only reported from few only present in part of Thymelaeaceae (Domke Malpighiales (Caryocaraceae, Dickison 1990a; 1934) and some cleistogamous flowers of Clusiaceae, Treub 1911; Salicaceae, Steyn et al. Cistaceae and Malvaceae, and in Sapindales 2004). it is reported from a few Anacardiaceae and In malvids, unitegmic ovules are unknown Sapindaceae (Leenhouts 1978). from Malvales. In Brassicales, they are only Outside of eurosids, there are two centres known from Limnanthaceae, and in Sapin- of apetaly. One is in Myrtales, in which it is dales only from very few Anacardiaceae (Co- reported from at least 7 (of 14) families peland 1955; Bachelier and Endress, unpubl. (Alzateaceae, Dahlgren and Thorne 1984; data), Burseraceae (Wiger 1935), Meliaceae Combretaceae, Correll and Correll 1982; (Wiger 1935), and Rutaceae (Boesewinkel and Crypteroniaceae, Takhtajan 1997; Lythraceae, Bouman 1978). Koehne 1903; Myrtaceae (although petal pri- Apetaly (Fig. 11). There is also a tendency mordia are present), Bohte and Drinnan 2005; towards apetaly in the nitrogen-fixing clade. In Onagraceae, Berry et al. 2004; Penaeaceae, Cucurbitales, apetaly is present at least in part Scho¨ nenberger and Conti 2003). The other in 4 (of the 7) families (Anisophylleaceae, centre is in Saxifragales, in which it is reported Begoniaceae, Datiscaceae, Tetramelaceae, from 10 (of 16) families (Altingiaceae, Wis- Matthews and Endress 2004), in all Fagales, niewski and Bogle 1982; Aphanopetalaceae, in Fabales in a few Fabaceae (e.g. Tucker Dickison et al. 1994; Cercidiphyllaceae, En- 1992) and in Stylobasium of Surianaceae dress 1986; Cynomoriaceae, Steindl 1945; (Carlquist 1978), and at least in part, in 7 (of Daphniphyllaceae, Endress and Igersheim the 9) families of Rosales (Barbeyaceae, Can- 1999; Haloragaceae, Orchard 1975; Hamam- nabaceae, Elaeagnaceae, Rao 1974; Moraceae, elidaceae, Endress 1970, 1978; Penthoraceae, P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 233

Engler 1930; Peridiscaceae, Gilg 1925; Saxi- 2004; Cannabaceae, Eckardt 1937; Dirachma- fragaceae, Engler 1930). ceae, Ronse De Craene and Miller 2004; Wind pollination (Fig. 12). Similarly there Elaeagnaceae, Ronse De Craene and Miller is a tendency towards wind pollination in the 2004; Moraceae, Yamazaki 1982; Rhamna- nitrogen-fixing clade, which is functionally ceae, Laguna and Cocucci 1971; Rosaceae, linked with apetaly. It is present in Cucurbi- Juel 1918; Ulmaceae, Shattuck 1905; Urtica- tales in Coriariaceae, Datiscaceae, and, per- ceae, Fagerlind 1944). In other clades of haps, Tetramelaceae (Matthews and Endress eurosids the feature is less prominent. 2004), in all families of Fagales, among Vascular bundle(s) in integument(s). A ten- Fabales in Surianaceae (Stylobasium) (Carl- dency towards the presence of vascular bun- quist 1978), and in Rosales, at least in part, in dles in integuments is relatively prominent in Barbeyaceae, Cannabaceae, Elaeagnaceae, the nitrogen-fixing clade. In Cucurbitales it is Moraceae, Rosaceae, Ulmaceae, and Urtica- recorded in the outer integument of at least 3 ceae (Berg 1989, Fellingham and Linder 2003). families (Corynocarpaceae, Cucurbitaceae) Interestingly, most actinorrhizal genera out of and in the single integument in Anisophyllea- the 3 orders that have actinorrhiza, are wind- ceae (Matthews and Endress 2005), in Fagales pollinated (all respective genera in Fagales and in at least 6 families in the single or outer Cucurbitales, Hippophae in Elaeagnaceae, and integument (Betulaceae, Endress 1967; Casua- Cercocarpus in Rosaceae). rinaceae, Flores and Moseley 1982; Fagaceae, In the COM clade and in malvids, wind Fey 1981; Juglandaceae, Nast 1935; Myrica- pollination appears to be very rare. A system- ceae, Kershaw 1909; Ticodendraceae, Tobe atic centre of occurrence of wind pollination 1991), in Fabales in the outer integument in outside of eurosids are again Saxifragales, in Fabaceae (but only after anthesis) (Dnyansa- which wind pollination is reported from Alt- gar 1958), and in Rosales in the outer integ- ingiaceae (Endress 1977), Cercidiphyllaceae ument of Rhamnaceae (Laguna and Cocucci (Endress 1986), Daphniphyllaceae (probably 1971). wind-pollinated, but unstudied in this respect), Among the COM clade the presence of Haloragaceae (Orchard 1975), and some vascular bundles in integuments is less prom- Hamamelidaceae (Endress 1977). inent. In Oxalidales it appears to be absent. In Carpels or gynoecia with a single Celastrales it is recorded from Celastraceae in ovule. Another trend that is functionally the outer integument (only Stackhousia) (Mat- linked with wind pollination is the presence thews and Endress 2005b). In Malpighiales it is of only a single ovule per carpel or gynoecium reported from 6 families (Achariaceae, Steyn in many groups of the nitrogen-fixing clade. et al. 2002; Euphorbiaceae, Tokuoka and Tobe This feature occurs in at least 4 families of 1995, 2002, 2003; Phyllanthaceae, Tokuoka Cucurbitales (Anisophylleaceae, Tobe and and Tobe 2001), Putranjivaceae, Tokuoka and Raven 1988a, Matthews et al. 2001; Coriaria- Tobe 1999; Salicaceae, Dathan and Singh ceae, Matthews and Endress 2004; Coryno- 1979; Rhizophoraceae, Nikiticheva and carpaceae, Matthews and Endress 2004; rarely Yakovlev 1985). in Cucurbitaceae, Matthews and Endress In malvids, integumentary vascular bun- 2004), at least 4 families of Fagales (Betula- dles are only present in some small families ceae, Sogo and Tobe 2005; Juglandaceae, of Brassicales in the outer (or single) integu- Verhoog 1968; Myricaceae, Kershaw 1909; ment (Akaniaceae, Tobe and Raven 1995; Rhoipteleaceae, Zhang et al. 1994), at least 3 Bretschneideraceae, Tobe and Peng 1990; families of Fabales (Fabaceae, Joshi 1938; Limnanthaceae, Stenar 1925; Moringaceae, Polygalaceae, Leinfellner 1972; Surianaceae, Puri 1942), in Malvales in Dipterocarpaceae Carlquist 1978), and most families of Rosales (Rao 1955) and Malvaceae (Rao 1954), and in (Barbeyaceae, Ronse De Craene and Miller Sapindales in some Anacardiaceae and 234 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

Sapindaceae (but apparently only after anthe- of eurosids and rosids, Saxifragales should sis) (Corner 1976). be mentioned (Aphanopetalaceae, Mauritzon 1939; Crassulaceae, Mauritzon 1930; Hamam- elidaceae, Endress 1977; and Paeoniaceae, Cucurbitales plus Fagales Murgai 1962). The sister orders Cucurbitales and Fagales Elaborate apocarpy is here defined as free tend to have trimerous, unisexual flowers and carpels in which the upper part is postgenitally an inferior ovary, and most Fagales and at united at anthesis. This postgenital bond least 2 (of the 7) families of Cucurbitales are allows the formation of a compitum, a cen- wind-pollinated (Crane and Blackmore 1989; tralized pollen tube transmitting tract, in Matthews and Endress 2004). However, based which centralized pollen tube selection can on the occurrence of bisexual Cretaceous take place (Endress 1982, Endress et al. 1983, fagalean fossil flowers (Friis 1983; Sims et al. Armbruster et al. 2002). Within eurosids such 1998, 1999) and phylogenetic analyses of elaborate apocarpy seems to be restricted to extant Fagales, unisexual flowers and wind some Malvales and Sapindales. In Malvales it pollination may not be synapomorphic in the is known from Malvaceae-Sterculioideae (En- clade (Manos et al. 2001). However, most of dress et al. 1983, Jenny 1988), and in Sapin- the well preserved Upper Cretaceous fossil dales it is present in many Rutaceae and flowers of Fagales appear to be unisexual Simaroubaceae (Endress et al. 1983, Ramp (Friis and Crane 1989; Herendeen et al. 1995 1988). Among non-eurosid rosids it is known 1999; Scho¨ nenberger et al. 2001; Friis et al. from some Crossosomatales (although with 2003, 2006), which indicates that it is an old some basal syncarpy; Staphyleaceae, Ramp feature. Although Cucurbitales flowers are not 1987; Geissolomataceae, Ixerbaceae, Mat- known in the fossil record (Crepet et al. 2004), thews and Endress 2005a), and outside rosids, the complete unisexuality in Begoniaceae, in Saxifragales (Iteaceae, Hermsen et al. 2003). Cucurbitaceae, Datiscaceae, and Tetramela- ceae is an indirect indicator of it being an old Potential relationships between larger clades feature. not shown in molecular studies: Malvids plus COM clade Malvales plus Sapindales Inner integument thicker than outer (Fig. 13). The sister orders Malvales and Sapindales An especially interesting feature is an inner have a tendency towards the presence of integument that is thicker than the outer at the several (more than two) meiocytes in an ovule time of fertilization. It dominates in both and elaborate apocarpy. The regular occur- malvids and the COM clade of fabids, but is rence of several meiocytes in an ovule has been rare in other rosid orders. This feature must be reported in Malvales in Cistaceae (e.g. Kapil determined at comparable developmental and Maheshwari 1964) and in 4 subfamilies of stages in these clades, because the thickness Malvaceae (e.g. Kamalova et al. 1983), and in ratio of the two integuments may change Sapindales in Burseraceae (Shukla 1954), Me- during development. Both integuments may liaceae (Prakash et al. 1977), Simaroubaceae be two-cell-layered in the beginning but the (Nair and Joseph 1957), and Sapindaceae inner may become thicker up to anthesis (Alimova 1985b). Other centres of occurrence (Hakki 1974, Boesewinkel 1987). for this feature in eurosids are Fagales In malvids this feature is present in (Betulaceae, Zhang and Chen 1993; Casuarin- Brassicales, in at least 6 families (Brassicaceae, aceae, Sogo et al. 2004; and Fagaceae, Hjelm- Haughn and Chaudhury 2005; Capparaceae, qvist 1953), and Rosales (Rhamnaceae, Arora Rodionova 1983; Caricaceae, Stephens 1910; 1953; and Rosaceae, Hjelmqvist 1956). Outside Cleomaceae, Arunalakshmi 1989; Resedaceae, P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 235

Fig. 13. Presence of an inner integument that is thicker than the outer in eudicots (topology modified after APG 2003 and Soltis et al. 2005; soft polytomy setting of MacClade 4.07 used for illustration). Signatures as in Fig. 9

Singh and Gupta 1968; Tovariaceae, Mauritzon 2002; Caryocaraceae, Dickison 1990a; 1935; 6 families, Bataceae, Emblingiaceae, Gyr- Chrysobalanaceae, Tobe and Raven 1984; ostemonaceae, Koeberliniaceae, Pentadip- Dichapetalaceae, Boesewinkel and Bouman landraceae, Setchellanthaceae, are unstudied 1980; Elatinaceae, Dathan and Singh 1971; in this respect, and for Limnanthaceae the Erythroxylaceae, Boesewinkel and Geenen feature is not applicable because the ovules are 1980; Euphorbiaceae, Tokuoka and Tobe unitegmic), in Malvales in 9 families (Apo- 2002, 2003; Humiriaceae, Boesewinkel 1985; danthaceae, Endriss 1902; Bixaceae, Mauritzon Phyllanthaceae, Singh 1972; Picrodendraceae, 1936; Cistaceae, Kapil and Maheshwari 1964; Berg 1975; Putranjivaceae, Tokuoka and Tobe Cytinaceae, Bernard 1903; Dipterocarpaceae, 1999; Rafflesiaceae, Ernst and Schmid 1913; Kaur et al. 1986; Malvaceae, Rao 1954; Munt- Rhizophoraceae, Tobe and Raven 1987b; ingiaceae, Rao 1952; Neuradaceae, Murbeck Salicaceae, Steyn et al. 2005; Trigoniaceae, 1916; Thymelaeaceae, Venkateswarlu 1947), Boesewinkel 1987; Turneraceae, Kloos and and in Sapindales in 3 families (Meliaceae, Bouman 1980), and in Oxalidales in 4 families Prakash et al. 1977; Rutaceae, Boesewinkel (Brunelliaceae, Cephalotaceae, Cunoniaceae, 1984; Simaroubaceae, Nair and Sukumaran Elaeocarpaceae, incl. Tremandraceae, Mat- 1960). thews and Endress 2002). In the COM clade the feature is present in In the seed this feature corresponds to the Celastrales, in Celastraceae and Parnassiaceae predominant differentation of the mechanical (Matthews and Endress 2005b), in Malpighi- tissues in the inner integument (exo- and ales in 16 families (Achariaceae, Steyn et al. endotegmic seeds, as opposed to exotestal, 236 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades mesotestal and endotestal seeds, in the termi- Ovules with a much thicker inner than nology of Corner 1976). outer integument are of special interest Other features. There are also other fea- (Fig. 13). This feature is not present in basal tures that tend to be present in malvids and eudicots; only in Trochodendron and Tetra- Malpighiales of the COM clade but are less centron is the inner integument slightly thicker common in the other two orders of the COM than the outer (Endress and Igersheim 1999). clade. These features include (1) contort petals Among core eudicots outside of rosids it is (see also above); (2) a tendency towards absent in Gunnerales, Berberidopsidales, polystemony (15 or more stamens in a flower): Caryophyllales, Santalales and asterids (van in at least 18 families of Malpighiales Heel 1984, Endress and Igersheim 1999), and (Achariaceae, Bonnetiaceae, Caryocaraceae, only present in Dilleniaceae (Sastri 1958), Chrysobalanacae, Clusiaceae, Euphorbiaceae, which do not appear as the likely sister to Humiriaceae, Hypericaceae, Medusagynaceae, rosids. Thus it is a clear synapomorphy for a Ochnaceae, Pandaceae, Passifloraceae, Phyl- part or parts of the rosids, especially the lanthaceae, Picrodendraceae, Putranjivaceae, COM clade and malvids. There are several Quiinaceae, Rhizophoraceae, Salicaceae), 5 scenarios for the evolution of this feature. (1) families in Brassicales (Capparaceae, Cleoma- It evolved once at the base of a clade ceae, Gyrostemonaceae, Resedaceae, Setchel- consisting of the COM clade and malvids lanthaceae), 5 in Malvales (Bixaceae, Cistaceae, (however, such a clade is not supported by Cochlospermaceae, Malvaceae, Sarcolaena- phylogenetic analyses). (2) It evolved sepa- ceae), and 3 in Sapindales (Anacardiaceae, rately twice at the base of the COM clade and Rutaceae, Sapindaceae); (3) a tendency to- the malvids. (3) It evolved separately many wards polycarpelly (more than 5 carpels in a times in families of the COM clade and of whorl) (see also above); (4) integuments tend to malvids. As the feature does not occur in all be free from each other and from the nucellus. families or genera of the COM clade and the This feature was mentioned as a side observa- malvids, there are also different scenarios to tion in a number of publications and was explain this pattern. (A) It evolved only once sometimes only illustrated without any men- or twice (as in 1 and 2) and was lost again in tion; however, it was never focused upon (see, a number of families or genera. (B) The e.g. Sutter and Endress 1995; Merino Sutter et tendency to form the feature was not ex- al., 2006). pressed in all families or genera. The combination of campylotropous ovules with a zig-zag micropyle is not present Discussion in basal eudicots (except for some papaver- aceae). In core eudicots it occurs in Dillenia- Promising features of potential interest ceae, among rosids in some Geraniales and at various higher levels (order and above) Myrtales, and among eurosids, in malvids (and Ovule structure. Ovules have yielded especially some Fabales). It appears to be a separate interesting floral features in this study. Re- apomorphy for each of these clades (or of cently, attempts have been made (1) to find parts thereof). Campylotropous ovules with- previously unrecognized features in ovules and out a zig-zag micropyle (because only the inner (2) to redefine the classification of ovules (e.g. integument forms the micropyle) are common Shamrov 1999, Batygina 2002). However, in Caryophyllales. Otherwise most eudicots these two goals require that further studies have anatropous ovules, and this is most are carried out in a phylogenetic framework, probably the plesiomorphic state for rosids. and that both are explored for their potential Mucilage cells. At the histological level the significance at different systematic levels (see presence in sepals of a cell layer or single cells also Endress 2003, 2005). with a thickened, mucilaginous periclinal inner P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 237 cell wall may be of interest. This feature seems is higher flexibility in the expression of curva- to be new for flowers (Matthews et al. 2001, ture, and both types, anatropy and campylot- Matthews and Endress, 2006). ropy are able to develop. Another interesting situation is where a suite of exceptional features are known to Patterns of occurrence of interesting features occur exclusively in very few (potentially Floral structural features of macrosystematic related) groups, such as unusually structured interest in rosids are commonly ‘‘tendential’’ stamens. In angiosperms stamens have a con- features. They are not ubiquitous in a clade servative organisation comprising an anther but occur much more frequently there than in with two lateral thecae. The absence of a thecal related clades. The evolutionary interpretation structure in the stamens (Endress and Stumpf of such tendential features is an interesting 1990) and presence of single pollen sacs that and unresolved problem in evolutionary biol- open individually is extremely rare in angio- ogy. In principle there are different possibil- sperms. Among rosids it is only known from ities to assess for the presence of such a few Malvaceae (von Balthazar and Nyffeler pattern: (1) The feature itself is not a 2002) and from Apodanthaceae (Blarer et al. synapomorphy, but only the predisposition 2004). As Apodanthaceae (for a long time of for it to easily evolve is. (2) The feature is a uncertain position, APG 2003), are at present synapomorphy, however, it is simply not best placed in Malvales (Nickrent et al. 2004), expressed in each component of a clade, but their unique stamen structure may help to suppressed in some. (3) The unusual concen- support their position in this order. This tration of a feature in a clade has arisen by stamen structure may be an apomorphic ten- coincidence, and thus represents separate dency in Malvales. autoapomorphies for each clade in which it occurs. (4) Also combinations of 1–3 are Unexplored correlations of features independent possible. Tendential features have often been of systematic position addressed in evolutionary studies (e.g. San- derson and Hufford 1996). When surveying a number of features through An example for (1) is the feature expressed a large clade, unexpected correlations between in the informal name of the ‘‘nitrogen-fixing features may appear, especially in such cases clade’’. Each of the four orders of this clade in which pairs of unusual features tend to contains one or a few families in which occur in combination. There are two impor- nitrogen fixation by symbiontic bacteria (Fran- tant aspects involved in the occurrence of kia and Rhizobium) in the roots is present. This such correlations. (1) Why are these features feature is not known from any other angio- correlated? (A) Are there general functional sperm group. It appears that in the common constraints that tend to always bind them ancestor a precondition was present that together, also in distant relatives? Or (B) do allowed for the full evolution of this feature these features occur associated only in certain relatively easily (Soltis et al. 1995, 2005; clades but not in others? Thus, are there Swensen et al. 1996). Similarly, such a situa- developmental constraints causing the fea- tion may be assumed for other features as well. tures to occur together in this clade? (2) Does A potential example in floral structure for (1) the presence of such a correlation in a clade or (2) is campylotropy of ovules in malvids, constitute an especially strong systematic which may be seen as a further development of marker for this group? This would only be anatropy by a prolonged process of curvature. the case if (B) were correct. These questions If the development stops earlier, anatropy does are currently not resolvable, however we not develop into campylotropy. Thus, once the would like to present them for further potential for campylotropy has evolved, there consideration. 238 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

Lobed or fringed petals and instability grow more slowly than the outer integument between presence and absence of petals (Table 1). and nucellus. Hypothesis: for differential elon- Those orders in which lobed of fringed petals gation non-contiguity (to avoid coherence) is occur, also show much fluctuation between necessary. If the elongation of the inner the presence and absence of petals. Addition- integument does not keep pace with the ally they often have small and narrow petals elongation of the outer integument and the in some members, and often have valvate or nucellus, contiguity is not possible. This cor- united sepals (Endress and Matthews 2006). relation is especially prominent in malvids and Such orders are, for example, Rosales of Malpighiales. eurosids, Myrtales of ‘‘basal’’ rosids (Scho¨ - Thickness of integument and presence of nenberger and Conti 2003), and Saxifragales vascular bundles. Vascular bundles are present (Crane and Blackmore 1989, Endress 1989) in the seed coat in a number of angiosperm outside of rosids. What is the morphogenetic groups. In some groups one or more vascular or functional significance of such suites of bundles are present in one of the integuments features? This should be compared in more of the ovules already at anthesis, and these detail in the different groups where they integuments tend to be relatively thick. occur. As a hypothesis for this correlation it Hypothesis: if early vascular bundle formation may be speculated that lobed or fringed in an integument is needed for later massive petals, if they are not in any way especially seed coat development, a certain integument elaborate, may already exhibit a state of thickness at anthesis is necessary. An only two- reduction of form. cell-layered integument cannot develop vascu- Campylotropous ovule and zig-zag lar bundles. micropyle. In several larger clades campylo- Thickness of integument and its contribution tropous ovules are often accompanied by a zig- to seed coat formation. The outer and the inner zag micropyle. Hypothesis: the convex periph- integument variously contribute to the ery of the ovule develops excessively and mechanical layer(s) of the seed coat (testal or especially also the outer integument on the tegmic seed coat, Corner 1976). It appears that convex side, so that its tip grows over the the integument that contributes most to the micropyle. This correlation is especially prom- mechanical part of the seed coat is thicker than inent in malvids and Fabaceae. However, in the integument that contributes least, and this these clades it is also of interest that in some already at anthesis. Hypothesis: if a massive cases only one of the two features is present, seed coat has to be formed, the contributing such as anatropous ovules with zig-zag micro- integument has to have a certain thickness (see pyle, or (less often), campylotropous ovules also Corner 1976). with straight micropyle. Obturator and nucellar beak. Ovules in Retardation of inner integument and which a nucellar beak is present (i.e. the apex non-contiguity of integuments and nucellus. In protruding out of the micropyle), also tend to some groups the inner integument tends to have an obturator (i.e. a plug formed by an

Table 1. Correlation of tendencies in perianth differentiation within orders (based on Endress and Matthews, in press). 1. Fluctuation between presence and absence of petals; 2. Petals small and narrow; 3. Petals lobed/fringed; 4. Sepals valvate or united Saxifragales 1 2 3 (4) Myrtales 1 2 3 4 Cucurbitales 1 2 3 (4) Rosales 1 2 3 4 Oxalidales 1 2 3 4 Brassicales 1 2 (3) (4) P. K. Endress and M. L. Matthews: Floral structure of rosid subclades 239 adjacent part of the carpel, commonly the have crassinucellar ovules, while others have placenta, pointing to the micropylar region). incompletely tenuinucellar ovules. It appears Hypothesis: There are morphogenetic interac- that those with arillate seeds have crassinucel- tions between obturator and nucellus apex; an lar ovules. As an additional example, outside obturator tends to intrude into the micropyle of rosids, in asterids, ovules are tenuinucellar, and a nucellar beak tends to extrude out of the seeds are commonly small, and arils are not micropyle thus making contact with the obtu- common or absent. rator. One or the other part may become dominant in this interplay. This correlation Floral structure and systematics in rosids was observed in Euphorbiaceae (Sutter and Endress 1995), Thymelaeaceae (Gue´ rin 1916), In this study we originally screened numerous Rosaceae (Sharma and Narayana 1971), and features but finally focused on only a few Urticaceae (Fagerlind 1944). especially informative ones that appeared Presence in the ovule of several meiocytes relatively stable in their distribution. These and tubular embryo sacs. If there are several features tend to be congruent with molecular meiocytes in an ovule and several embryo results to a large degree. However, there are sacs develop, they tend to be tubular with also some differences (Table 2). the largest diameter around the egg apparatus In molecular results the deepest split within and the antipodal cells. Hypothesis: there eurosids appears between the fabids (nitrogen- is competition between the female gameto- fixing clade plus COM clade) and malvids phytes, pushing each other aside, or there is (Soltis et al. 2000, 2005; APG 2003). However, just lack of space to expand sidewards. Among from our floral structural results, one would rosids and relatives this is conspicuous in rather expect the deepest split to be between Crassulaceae, Sedum (Subramanyam 1968), the nitrogen-fixing clade and a clade of malvids Paeoniaceae, Paeonia (Walters 1962), and plus COM clade. Although the malvids are Casuarinaceae, Casuarina (Sogo et al. 2004) especially well characterized, there are also (see also above). This combination is also special shared features between the COM clade known from some other angiosperm groups. and malvids. Gynobasic style and single, tenuinucellar It is interesting that of all apparent supra- ovule. Gynoecia with a gynobasic style (in ordinal clades (clusters of orders) within rosids which the dorsal ovary region is bulged up and the best supported in phylogenetic studies the style appears to be inserted at the base) (Soltis et al. 2000, 2005), the malvids, are also tend to have a single ovule (or not more than 2 the best supported by floral structural features. ovules) per carpel and this ovule is small, often This clade also appears in the combined rbcL incompletely or completely tenuinucellar. and non-molecular analysis by Nandi et al. Hypothesis: A gynobasic style produces a (1998), although with the inclusion of Myrtales. reduction of space within the ovary locule. The second major group, the fabids (Cuc- This combination is present among rosids in, urbitales, Fagales, Fabales, Rosales, Celast- e.g. Limnanthaceae (Maheswari and Johri rales, Malpighiales, Oxalidales) are less well 1956), Chrysobalanaceae (Juel 1915), and characterized than the malvids. Among the Ochnaceae (Chikkanaiah and Mahalingappa fabids, the COM clade (Celastrales, Oxali- 1974). dales, Malpighiales) appears to be best char- Aril and crassinucellar (not tenuinucellar) acterized by floral features. ovules. Arils tend to form on crassinucellar The two sister pairs of orders within and not on tenuinucellar ovules. Hypothesis: eurosids, Cucurbitales plus Fagales and Mal- for the formation of an aril the ovule has to be vales plus Sapindales, both poorly supported relatively massive. This is especially well exem- by molecular studies, are also structurally not plified by Malpighiales, in which some families (yet) well characterized. 240 P. K. Endress and M. L. Matthews: Floral structure of rosid subclades

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