REVIEW The morphological relationship between carpels and ...

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Botanical Journal of the Linnean Society, 2019, 189, 201–227. With 1 figure.

© 2019 The Linnean Society of London, Botanical Journal of the Linnean Society, 2019, 189, 201–227

*E-mail: [email protected]

REVIEW

The morphological relationship between carpels and ovules in angiosperms: pitfalls of morphological interpretation

PETER K. ENDRESS*

Department of Systematic and Evolutionary Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland

Received 2 August 2018; revised 8 November 2018; accepted for publication 14 December 2018

Carpels and ovules have been differently interpreted over the past two centuries. In this review, some of these interpretations are highlighted, with particular emphasis on the current situation. Ovules are part of and are enclosed in carpels in all living angiosperms. Living angiosperms are monophyletic, and the evolutionary association between ovules and the leaf-like part, the carpel wall, had taken place at or before the time the clade of extant angiosperms was established. From what we know at present, there are no ‘cauline’ ovules in extant angiosperms. Developmentally, carpel walls and ovules are not always synchronous across all extant angiosperms. In early development ovules may be relatively precocious or relatively late compared with carpel walls. They are late in early-diverging angiosperms (ANITA grade, magnoliids, some early-diverging eudicots) but precocious in some more derived groups (e.g. some Caryophyllales and Primulaceae). Carpel primordia have a certain depth in the floral apex, and the entire activated area of a carpel primordium may be several cell layers thick. Thus, the carpel is ‘embedded’ or ‘rooted’ within the remaining floral apex. The parts of a carpel develop at different times in carpel ontogeny and probably evolved at different times on the line leading to the angiosperms, which needs to be considered in interpretations. Carpel development depends on a complex genetic network, which increased stepwise over evolutionary time and contains hundreds of genes revealed in molecular developmental biology. The evolutionary history of such networks in carpel walls and ovules is unlikely to be easily disentangled, as most of these genes are not transcription factors.

ADDITIONAL KEYWORDS: carpel primordium – congenital fusion – floral apex – floral development – gynoecium development – gynoecium evolution – post-genital fusion.

INTRODUCTION

Scientific questions change with the progress of our knowledge over time. There has been a long ongoing debate, especially in the first two-thirds of the 20th century, about the morphological and evolutionary relationship between carpels and ovules in angiosperms, which, 50 years ago, had repercussions on discussions of whether angiosperms were monophyletic or polyphyletic. However, the discussion has surfaced again more recently with new fossil finds and, especially, with the rise of

molecular phylogenetics and molecular evolutionary developmental genetics (evo-devo) in the past quarter of a century. A new avenue opened up with molecular work on model plants. Arabidopsis thaliana (L.) Heynh. (Brassicaceae) was chosen as the most prominent model plant in angiosperm developmental biology (e.g. Smyth, Bowman & Meyerowitz, 1990; Bowman, 1993; Ferrándiz et al., 2010). The choice of Arabidopsis Heynh. was based on technical advantages in handling the model organism, but it was somewhat unfortunate for discussion on the gynoecium because Brassicaceae have some unusually derived complex developmental traits that may easily lead to incorrect generalizations for angiosperm gynoecium structure. In Arabidopsis

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© 2019 The Linnean Society of London, Botanical Journal of the Linnean Society, 2019, 189, 201–227 © 2019 The Linnean Society of London, Botanical Journal of the Linnean Society, 2019, 189, 201–227

and most other Brassicaceae the syncarpous gynoecium has a ‘false’ septum and concomitantly two valves that fall off when the seeds are mature, enabling the seeds to be dispersed. The valves develop only late in gynoecium ontogeny. Nevertheless, the primary margins of carpels have been studied for a long time at the level of comparative morphology (Rohweder, 1967b; Hagemann, 1970; Guédès, 1979), and they have gained new attention in molecular developmental biology (e.g. Reyes-Olalde et al., 2013).

The great success of molecular phylogenetics of the angiosperms as summarized in APG IV (2016) and, in addition, progress in palaeobotany (Friis, Crane & Pedersen, 2011) with the discovery of fossil flowers now allows us to discuss some earlier controversies with much improved background knowledge. Other controversies have disappeared due to better knowledge of the phylogenetic tree of angiosperms, which allows us to trace evolutionary questions with more confidence (e.g. Sauquet et al., 2017, 2018; Sokoloff et al., 2018).

A discussion of the meaning of ‘axis’ in comparative plant morphology is also relevant in this respect. In early comparative morphology (especially in the era of Troll and earlier) a distinction and sharp delimitation between leaf (phyllome) and ‘axis’ played an important role in morphological discussions. However, the fact that these parts cannot be directly compared was overlooked in these discussions.

Firstly, the tip of a shoot or flower apex is morphologically undifferentiated, being neither axis nor leaves. Leaves or floral organs are lateral organs that are initiated slightly below this uppermost zone. Only as the first leaves are initiated does the axis also begin to develop inside, below the undifferentiated tip of the apex. According to the analyses of Rohweder (1963) and Hagemann (1970), most of the surface of a shoot apex and a shoot consists of parts of vegetative phyllomes or floral organs. In a developmental sense, the elongated part (the internode) between two successive phyllomes or floral organs consists of the elongated bases of these organs, which ‘cover’ the axis like a ‘skin’ (‘leaf-skin’ perspective; see, e.g. Hofmeister, 1868; Troll, 1937; Guédès, 1979; Rutishauser & Sattler, 1985). Thus, what is commonly called ‘axis’ is better seen as a combination of ‘leaf ’ and ‘axis’. In addition, because ‘axis’ and ‘leaf ’ are parts belonging to different levels of the structural hierarchy of a shoot (surface vs. internal region), they cannot logically be delimited from each other. They form a structural and functional unit. Attempts at such delimitation were made but do not make sense (e.g. Troll, 1957: figs 67, 70; Weberling, 1989: fig. 93). Some idealistic morphologists (Troll, 1933: fig. 22; Schaeppi, 1937: fig. 3, 1944: fig. 2; Troll, 1957: figs 67, 70; Weberling, 1989: fig. 10 II, III)

constructed abrupt demarcations between axis and leaf, which were unbiological.

Secondly, in the long developmental time from initiation to maturity of leaves, differential growth and differential tissue differentiation of the different areas of the shoot may become blurred. We should not forget that although the morphological parts of a shoot are initiated separately, they develop together as a complex functional entity, not as completely separate parts.

MATERIAL AND METHODS

This paper is a literature review. In addition, material of Tambourissa purpurea (Tul.) A.DC. (coll. Peter K. Endress 02-35, cult. Botanic Garden, University of Zurich, plant received from Botanic Garden, University of Heidelberg) was used to illustrate carpel primordia and young carpels in a gynoecium with numerous free carpels in whorled phyllotaxis (Staedler & Endress, 2009). Young flowers were fixed in ethanol, embedded in paraplast and sectioned with a rotary microtome at 10-µm thickness. They were stained with safranin and astra blue.

RESULTS AND DISCUSSION

Historical views of tHe morpHological relationsHips between carpels and ovules

De Candolle (1813) laid out the elements of the morphology of the flower with its present meaning. However, he used the term carpellum not for a female floral organ but for a fruiting organ. Instead, Dunal (1817: p. 13), a student of De Candolle, was the first to use carpellum for a female floral organ (Lorch, 1963; Brückner 1991). The ovules were called ‘grains’ by Dunal. However, De Candolle (1813) used the term ‘ovule’ for them before fertilization (for the origin of the word ovule, see Wagenitz, 2003). The term gynoecium for the sum of all carpels of a flower was introduced (as ‘gynoeceum’) by Roeper (1826: p. 438) according to Lorch (1963). At Dunal’s time there was no discussion on the morphological relationship between carpels and ovules. Subsequently, St. Hilaire (1833) viewed ovules as of axial nature, Brongniart (1844) of foliolar nature, and Schmitz (1872) as organs ‘sui generis’ (Worsdell, 1904; Scheckler & Rothwell, 1988). Čelakovský (1874, 1876, 1900) was a pioneer in evolutionary morphology. In particular, he discussed the evolutionary structure of the ovules and their origins from lower plants, but less so from gymnosperms, as important fossils from relevant gymnosperm groups were not yet known at his time. Broader discussions only arose in the 20th

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RELATIONSHIP BETWEEN CARPELS AND OVULES 203


century when the relationships of angiosperms with other seed plant groups became discussed more broadly, and when the ontogenetic development of carpels was studied in more detail. A first wave of studies debated whether some angiosperms were ‘acarpous’, meaning they did not have carpels. Thompson (1933), for example, thought that Zingiberales had no carpels as he did not accept that an ovary could become inferior in evolution, a notion immediately criticized by Parkin (1933). Thompson (1933) had the counter-intuitive idea that ovary, style and stigma were originally separate organs, and he did not accept that they must have formed a functional unit from the beginning. The original morphological uniformity of carpels is shown today with more clarity as we have much better knowledge of the phylogenetic relationships within angiosperms (e.g. APG IV, 2016) and the structure of the gynoecium of extant early-diverging clades (Endress & Igersheim 2000a; Endress & Doyle, 2009, 2015) and many Early Cretaceous fossil flowers are known (Friis et al., 2011), all of which support the early morphological unity of carpels in angiosperms.

For Fabaceae, Thompson (1931) assumed the carpels to be phylloclades, and thus that the ovules were borne on axes, without giving a clear explanation for his view. However, this idea has not found any followers.

In the early 20th century, several different interpretations of the evolutionary derivation of carpels were discussed based on assumptions concerning the closest relatives of angiosperms among gymnosperms, extant and fossil. The most popular view was that angiosperm carpels were derived from structures similar to macrosporophylls of pteridosperms or cycads, which bear ovules on the surfaces or margins of leaves or leaf-like organs (Hallier, 1902; Arber & Parkin, 1907). This view received strong support from most systematists up to the second half of the 20th century (e.g. Cronquist, 1968; Takhtajan, 1969). In contrast, Wettstein (1907, 1935) and a few others assumed the closest relationships to be with conifers and gnetophytes. Accordingly, they interpreted carpels as being composed of different organs of two axial orders, with an ovule surrounded by a bract. Other botanists assumed that angiosperms were polyphyletic (rather than monophyletic) and, accordingly, that the carpels were not homologous in all angiosperms (Karsten, 1918; Hagerup, 1934; Lam, 1948, 1950; Meeuse, 1963, 1986, etc.). These studies were not based on detailed comparative morphological analyses. For extinct groups such studies were not possible, and for living groups they were carried out with techniques that are no longer up to date and without present-day knowledge of developmental morphology regarding the background of angiosperm diversity (for a more detailed survey of different hypotheses, see Friis & Endress, 1990).

Because none of the extant clades among gymnosperms appears to be most closely related to angiosperms (Chaw et al., 2000; Doyle, 2006, 2008, 2012, 2013; Hilton & Bateman, 2006; Herendeen et al., 2017), it is necessary to compare angiosperms with the entirety of the known fossil gymnosperm groups for potential hints about relationships. A detailed overview of fossil gymnosperms was provided by Friis et al. (2011). At present, two promising candidates based on morphological cladistic studies are glossopterids (Stebblins, 1974; Retallack & Dilcher, 1981; Doyle, 2006, 2008) and Caytoniales (Gaussen, 1946; Doyle, 1978, 2013). Both were also previously, without cladistic studies, discussed as potential angiosperm relatives. For both groups, new attempts at carpel interpretation were necessary. A carpel derivation from organs of glossopterids would imply that carpels were originally not simple macrosporophylls but biaxial structures composed of a macrosporophyll bearing ovules and a bract subtending a reduced short shoot with this macrosporophyll (Retallack & Dilcher, 1981) transformed into the outer integument. With a derivation from Caytoniales, a carpel would correspond to a pinnate leaf with each pinna modified into a cupule. Each cupule, if it became uniovulate, would correspond to an anatropous ovule in angiosperms. The inner integument would correspond to the original integument of the ovule, and the outer integument would correspond to the cupular wall (see Doyle, 1978, 2012). Earlier attempts to bring Caytoniales together with angiosperms (Thomas, 1934) were based on a different hypothesis. The closed cupules were seen as evolutionary precursors of angiospermous carpels (see also discussion in Unruh, 1939). For instance, Thomas (1931) compared the bulged ovaries of Alchemilla L. and other Rosaceae with the bulged cupules of Gristhorpia H.H.Thomas (Caytoniales). Therefore, Thomas (1933: p. 550) was able to state that ‘it is quite possible that the Rosaceae may be one of the more primitive families now living’. Today we know that the question is not a special relationship but rather a ‘basal’ position, such that structures could be homologous. Rosaceae are not phylogenetically early-diverging, but highly nested in angiosperms (APG IV, 2016). Other possibilities of evolutionary derivations of carpels were discussed in detail by Doyle (2006).

Regardless, there are phylogenetic indications that carpel and ovule were not a morphological unit from their evolutionary beginnings. However, they became tightly synorganized so that they appear as a unified organ in angiosperms. Given the similar developmental relationship of carpels to the floral apex even in early-diverging angiosperms, this synorganization must have evolved before or coincident with the origin of angiosperms. It is therefore problematic to call carpels sporophylls and simplest to call them ‘carpels’. To

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call them sporophylls is only possible if sporophylls are accepted as evolutionarily secondary structures because the carpel wall is derived from a ‘phyllome’ that was originally not associated with an ovule, or because it is a new formation of a scale on the ovule that evolved to a carpel wall.

earlier studies of carpel development and pitfalls of interpretation

The architecture of the shoot apex played a role in the interpretation of the organs originating from it. Schmidt (1924) conceived the tunica-corpus concept of apical organization. This described the occurrence of cell layers at the apex, called stratification. In angiosperms usually two outer cell layers are formed that are maintained by having only anticlinal (and no periclinal) divisions. Thus, these two cell layers remain stable during development. They form the tunica. In contrast, the inner area, the corpus, which is covered by the tunica in a shoot apex or floral apex before organ initiation, has anticlinal and periclinal cell divisions, and therefore does not show regular cell layers. Only in the area where the first leaves are initiated do periclinal divisions occur in the second tunica layer. Buvat (1952) made progress by focusing on the cytohistological and cytohistochemical zonation of the apex (for reviews, see also Gifford, 1954; Hagemann, 1970, 1973). He found areas of greater activity (cell divisions and other cell activity) at the flanks of the apex, and an area of reduced activity in the centre, which is also distinct in having reduced stainability (méristème d’attente, quiescent centre, more recently also termed the area of stem cells). A broad review on the structure and function of the shoot apex was presented by Robinson et al. (2013).

In the mid-20th century, so-called ‘histogenetic’ studies tried to interpret organs as foliar or axial (cauline) based on whether they were initiated in the second or third cell layer of the apical meristem, and thus from the ‘tunica’ or ‘corpus’. In studies on Datura stramonium L. (Solanaceae), Satina & Blakeslee (1941, 1943), working with periclinal chimaeras, found that sepals and petals are initiated by periclinal cell divisions in the second cell layer of the floral apex, but stamens and the placenta of the carpels by such divisions in the third layer. Because foliage leaves are usually initiated in the second layer and lateral shoots in the third layer, these authors concluded that in Datura L. sepals and petals are of ‘foliar’ nature, but stamens and the placenta of carpels are of ‘axial’ or ‘cauline’ nature. Datura stramonium became a model plant of developmental biology, and these studies became widely known at that time. Other angiosperm groups were also studied in the same way, including Poales (Barnard, 1955, 1957a, b, 1958) and several

others (Pankow, 1959, 1962; Taylor & Kirchner, 1994, 1996). These studies were illustrated by line drawings of microtome sections. Although Barnard (1955, 1957a, b, 1958) also included a few photographs of stained microtome sections, he did not use them in his discussion on the development of their presumed ‘cauline’ ovules.

A serious shortfall of these ‘histogenetic’ studies was that the authors concentrated solely on the location of periclinal cell divisions at the time of organ initiation in the second or third cell layer of the floral apex. Several authors criticized this. Prominent among them was Rohweder (1963). He had broad experience of the behaviour of young flowers in many different groups of angiosperms and did not base his assumptions solely on one model species such as D. stramonium. He realized that the results of Satina and Blakeslee were not universal for angiosperms. Instead he found that the site of periclinal divisions depends greatly on the final size of the organs. Large (thick) organs are generally initiated in the third layer, and small (thin) organs from the second layer, irrespective of their evolutionary derivation. Thus, while the results for Datura are in line with those for some other angiosperms, there are also many deviations from this pattern across the angiosperms. This means that the layer of periclinal divisions in organ initiation cannot be used for morphological implications of this sort, as also expressed by Joshi (1947) in a detailed review.

The research results of Rohweder and other morphologists of the 1960s and 1970s have been of lasting significance and are models for understanding flower development and evolution and should not be neglected simply because they are written in German. (A large body of important morphological literature was written in German or French in the 20th century and is a foundation for morphological research.)

floral apex and early carpel development

A flower primordium (a floral apex) starts to initiate the floral organs in a centripetal (acropetal) sequence. Because the gynoecium is in the centre of a flower, the carpel primordia are the last to appear. In longitudinal microtome sections of a floral apex, the carpel primordia are usually seen by an increase in meristematic activity, expressed by darker staining than the surrounding areas with appropriate stains (discussed by Endress, 1972a, b: see also Endress, 1994: fig. 2.18, and this paper, Fig. 1 and Table 1). The entire darker stained area gives rise to the carpel. As the young carpel grows and differentiates, new darker staining areas derived from the primary carpel meristem become visible (see below). They give rise to the placenta with the ovule or ovules. Hagemann (1970: p. 314) discussed this process for complex leaves

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(such as pinnate leaves) as ‘meristem incorporation’. It means that parts of the primary leaf meristem grow and form the parts of the leaf. Similarly, the ovule(s) develop(s) on the area already occupied by the carpel

and thus is (are) part of the carpel. After all carpels have been initiated and are developing, the floral apex usually ceases to be active. It is important to bear in mind that a carpel primordium has some volume but

Figure 1. Tambourissa purpurea (Monimiaceae). Median longitudinal microtome sections of young female flowers. A, B, flower at the stage of carpel initiation and young carpel development. A, entire flower. B, central part of the same flower showing the meristematic depth of the young carpels. Black arrows point to carpel primordia or young carpels. C, somewhat older flower. Red arrow points to a median longitudinal section of a young carpel with an ovule. Scale bars: A, B = 100 µm; C = 500 µm.

Table 1. Compilation of illustrations of carpel primordia in longitudinal microtome sections of gynoecia in major clades of angiosperms from the literature. The sequence of the families follows APG IV (2016)

Magnoliidae, Eupomatiaceae: Eupomatia laurina R.Br. (Endress, 2003, fig. 7C)Magnoliidae, Monimiaceae: Tambourissa purpurea. (Tul.) A.DC (Fig. 1; Endress 1980b, fig. 13)Magnoliidae, Winteraceae: Drimys winteri J.R.Forst. & G.Forst. (Tucker, 1959, plate 31d)Monocotyledoneae, Alismataceae: Alisma plantago-aquatica L. (Eckardt, 1957: plate IV, figs 1, 2; Singh & Sattler, 1972: fig. 25)Monocotyledoneae, Alismataceae: Echinodorus subalulatus (Mart. ex Schult.f.) Griseb. (Eckardt, 1957: plate VII, fig. 2)Monocotyledoneae, Alismataceae: Limnocharis flava (L) Buchenau (Kaul, 1967: figs 10, 11)Monocotyledoneae, Araceae: Anthurium sellowianum Kunth (Poli et al., 2015: fig. 5)Monocotyledoneae, Commelinaceae: Gibasis geniculata (Jacq,) Rohweder (Rohweder, 1963: figs 39–42)Ranunculales, Ranunculaceae: Ranunculus repens L. (Tepfer, 1953, plate 76a)Ranunculales, Ranunculaceae: Ranunculus sceleratus L (Grégoire, 1938: figs 1, 2)Saxifragales, Saxifragaceae: Tellima grandiflora (Pursh) Douglas ex Lindl. (Klopfer, 1968: fig. 9)Rosidae, Cucurbitaceae: Cucumis sativus L. (Bai et al., 2004: fig. 2a, b)Rosidae, Melastomataceae, Tibouchina clinopodifolia (DC.) Cogn. (Basso-Alves, Goldenberg & Teixeira, 2017, fig. 6B, D)Rosidae, Rosaceae: Rosa rugosa Thunb. (Rauh & Reznik, 1951: fig. 6V, VI)Rosidae, Rosaceae: Rubus fruticosus G.N.Jones (Grégoire, 1938: fig. 238)Rosidae, Rosaceae: Spiraea trifoliata (L.) Moench (Evans & Dickinson, 2005, fig. 3B, E)Caryophyllales, Caryophyllaceae: Uebelinia kiwuensis T.C.E.Fr. (Rohweder, 1965a: plate 22, fig. 2b)Ericales, Primulaceae: Primula sinensis Sabine ex Lindl. (Grégoire, 1938; fig. 195)Lamiidae, Apocynaceae: Trachelospermum asiaticum (Siebold & Zucc.) Nakai (Nishino, 1982: fig. 3E)Campanulidae, Apiaceae: Levisticum officinale W.D.J.Koch (Leins & Erbar, 1985, figs 1, 2, 10)Campanulidae, Araliaceae: Hedera helix L. (Erbar & Leins, 1988, figs 34, 35)Campanulidae, Asteraceae: Crepis capillaris (L.) Wallr. (Röthlisberger, 1970, fig. 28)Campanulidae, Campanulaceae: Downingia bacigalupii Weiler (Kaplan, 1967, fig. 20)

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that the major part of this volume is situated inside the floral apex and not just at its surface, although the surface is also part of it (Fig. 1). Thus, at the beginning this primordium is not noticeable from the outside (such as on scanning electron micrographs). It is only visible on stained microtome sections (Fig. 1). When the carpels begin to differentiate morphologically and histologically, the area of the initial primordium is no longer a primordium, but a young developing carpel, and is now also visible from the outside.

The carpel primordium, if there is only one carpel, or the carpel primordia if there are several, may occupy the entire rest of the floral apex or may not use up the entire remaining floral apex. For instance, in Pseudowintera Dandy, the entire remaining floral apex is used up for the single carpel (Sampson & Kaplan, 1970), whereas, in contrast, in Acacia Mill., the single carpel does not use up the entire floral apex (Newman, 1936a, b).

As a consequence of this early development, young carpels or gynoecia appear deeply ‘embedded’ (or ‘rooted’) in the floral apex as seen in longitudinal sections (Fig. 1). This organization of the floral apex including the gynoecium primordium is the same throughout the angiosperms, irrespective of whether the gynoecium will have a superior or inferior ovary (Table 1), with only the remarkable exception being the giant flowers of Rafflesiaceae (Nikolov et al., 2014), in which the inner space of the ovary originates by histological (schizogenous) splitting of massive tissue.

An interesting aspect here that has not been discussed in the papers cited and others is that each time a new part (within the gynoecium) is formed, the meristem becomes more extensive, as discussed for the different parts of the carpels in Laurales (Endress, 1972a, b), such as (1) carpel, (2) ventral part of carpel including primary margin, (3) ovule and (4) integuments. These new parts within the carpel or the gynoecium are not separate organs, as they originate in the carpel long after carpel initiation. Endress (1972b) showed this in detail based on a large number (>2500) of microtome section series of gynoecia or carpels. These included 793 series of Siparuna thecaphora (Poepp. & Endl.) A.DC. (as S. nicaraguensis Hemsl.) (Siparunaceae), 622 series of Laurus nobilis L. and 537 series of Cinnamomum camphora (L.) J.Presl (both Lauraceae), and 81 series of Doryphora sassafras Endl. (Atherospermataceae).

The floral apex is the area from which everything develops, floral organs and floral ‘axis’ (stem). Thus, the apex is neither axis nor leaves but is the place of origin of both (see also Rohweder, 1963: p. 83; Chandler, 2011; Perales & Reddy, 2012). Thus, the axis in seed plants is only what develops together with and after the first leaf formation.

different parts of a complex organ appear at different times in development and appeared

at different times in evolution

Different floral organs appear and differentiate at different times in development (Bowman et al., 1999; Endress & Igersheim, 2000a, Endress, 2006), namely sepals, petals, stamens, carpels and ovules. However, the evolutionary sequence was ovules, carpels, and perhaps stamens, sepals, petals. Thus, the developmental sequence is not congruent with the evolutionary sequence (Stewart, 1983; Endress, 2006). Also within single complex organs (e.g. carpels), the different parts do not appear synchronously but in a staggered fashion (e.g. Endress, 1972a, b).

A problem or pitfall is that the historical order of evolutionary changes is sometimes not considered in evolutionary interpretations and that ontogenetic changes are not properly considered, as will be shown in the following paragraphs. An example of unfortunate (incorrect) interpretation of the placenta as ‘cauline’ as a result of not considering the long ontogenetic temporal process of gynoecium development is the study by Pimentel et al. (2014) in Myrteae (Myrtaceae). An unfortunate example from evo-devo appears in Roe, Nemhauser & Zambryski (1997) who wrote (p. 351): ‘Recent studies suggest that whereas the carpel is a leaf homologue, the placenta is an axillary shoot (Taylor 1991; Doyle 1994). The genetic separation of carpel and placenta in the tsl ett double mutants would support this idea.’ However, these two sentences are misleading. As already mentioned, Taylor (1991) referred to the old, misinterpreted studies by Satina & Blakeslee (1941, 1943, see above), and Doyle (1994) just mentioned Taylor (1991) but did not support the hypothesis of Satina & Blackeslee (loc. cit.). Thus, Roe et al. (1997) actually distorted previous morphological concepts in this citation.

Centrifugal ovule initiation (i.e. away from the remaining gynoecium apex) is common in multiovulate gynoecia (Okamoto, 1984) and in free central placentation (Duchartre, 1844). In addition, the (anatropous) ovules appear to be curved away from the centre of the earlier floral apex (Duchartre, 1844). According to Kaplan (1968), there are four different patterns of ovule initiation sequence in multicarpellate ovaries: (1) basipetal in ovaries with axile placentation; (2) acropetal in parietal placentation; (3) bidirectional in gynoecia with axile placentaton at the base and parietal placentation higher up; and (4) interspersed initiation in long and slender ovaries of some Campanulaceae. The last also occurs in Orchidaceae, which have exceedingly numerous ovules in a gynoecium (Yeung & Law, 1997). A comparative study of these different developmental patterns is still missing.

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organ fusions in tHe gynoecium, and development and role of tHe carpel margin

The term ‘fusion’ is important in floral morphology in several ways and especially so in the gynoecium. Carpel fusion is intracarpellary and mostly also intercarpellary. The first process leads to angiospermy and the second leads to syncarpy. It is important to distinguish between the two. Another distinction is necessary between post-genital and congenital fusion (Baum, 1948a, b, 1949; Leinfellner, 1950, 1951; Cusick, 1966; Verbeke, 1992; Lolle & Pruitt, 1999), which are two completely different morphogenetic processes, although they lead to superficially similar results. Post-genital fusion occurs by coherence of two originally separate parts via the epidermis, whereas congenital fusion occurs by confluence of meristems and no participation of the epidermis. These two levels of distinction have led to confusions in the literature, such as in Raven & Weyers (2001). Free carpels usually show post-genital intracarpellary fusion of their margins or flanks. If free carpels are tubular (utriculate, ascidiate) as seen especially in members of the ANITA grade, the phylogenetically earliest-divergent angiosperms, carpel sealing above the ascidiate zone may be only by secretion, without any fusion (Endress & Igersheim 2000a; Endress & Doyle, 2015). In syncarpous gynoecia the walls of adjacent carpels are congenitally fused (united); in addition, in the upper zone of a gynoecium where congenital union is lacking and the carpels remain free, there is usually intracarpellary post-genital fusion of the margins. Rarely, the two carpels in Apocynaceae and Gentianaceae are flat and completely or almost completely post-genitally united (Fallen, 1985; Kissling, Endress & Bernasconi, 2009), or otherwise are post-genitally fused in some Ochnaceae (Matthews, Amaral & Endress, 2012). In species of a few more or less apocarpous groups (e.g. Anacardiaceae, Apocynaceae, Malvaceae), only the carpel tips are post-genitally united (Walker, 1975, 1978; Endress, 1982; Endress et al., 1983; Verbeke & Walker, 1985, 1986; Fallen, 1986; Verbeke; 1992; Endress, Lorence & Endress, 1997). In the order Crossosomatales at least four of the eight families have their carpels completely or partly post-genitally united (Matthews & Endress, 2005). In the special case of Brassicaceae, to which Arabidopsis belongs, the two carpels are congenitally united almost up to the stigma and the secondary flanks forming the septum are intracarpellarly post-genitally united. In addition, in the stigma the two carpels are post-genitally united. In this extreme case, angiospermy comes about by this apical post-genital union. Within the gynoecium, a ‘false’ septum is present, which is formed by post-genital fusion of the extended marginal or submarginal area of the two carpels. In

this additional post-genital fusion area the pollen tube transmitting tract is differentiated, encompassing parts of both carpels.

The carpel margin is the area where ovules are usually formed, where carpels may fuse post-genitally and where the pollen tube transmitting tract is differentiated, and thus where diverse functions are concentrated (e.g. Endress, 2006). Therefore, the carpel margin has found special attention in comparative developmental morphology (e.g. Rohweder, 1967b, c; Guédès, 1979) and in molecular developmental biology (e.g. Reyes-Olalde et al., 2013; Wynn et al., 2014; Vialette-Guiraud et al., 2016; Herrera-Ubaldo & de Folter, 2018). Rohweder (1967b, c) showed in detail that in Ranunculaceae and some magnoliids that are uniovulate or have a linear placenta, the ovules are initiated on the developmentally primary carpel margin, and what later appears as a margin is a developmentally secondary formation. Endress (1972a, b) showed the same for some Lauraceae and other Laurales. In carpels with laminar diffuse placentation, such as in Nymphaeaeae or Butomaceae, this is different (e.g. Leinfellner, 1973), as not all ovules can be located on a primary developmental margin. In these cases, it appears that the ovules are initiated only after the carpel margin has been established.

A problem is that the margin has not always been defined in the same way. How exactly should it be defined? The margin is not a geometrical line as it has some extension in thickness. Often an inner and an outer rim are formed where the two margins meet. Erbar (1983) and Leins & Erbar (2010) circumvented this problem by calling the inner rim ‘inner marginal ridge’ and the outer rim ‘outer marginal ridge’, and the area in between ‘marginal area’. The inner and the outer rim may appear sequentially, in which case the inner rim corresponds to the primary margin. The margin in a closed carpel is not exactly symmetrical as seen in transverse sections, because the inner side is smaller than the outer side by architectural necessity.

In peltate carpels (with an ascidiate base) with a single ovule, such as in Lauraceae and some Ranunculaceae, the position of the ovule may be on the primary margin and the apparent cross-zone may be the secondary margin (Rohweder, 1967b, c; Endress, 1972a, b). Two other terms that are easy to confuse because they are similar but are used differently are median and medial. ‘Median’ means in the middle of a carpel (or other single elementary organ) in comparative morphology (e.g. Rohweder, 1967b, c; Hagemann, 1970), whereas ‘medial’ is used for the middle of an entire gynoecium (and thus not for a single organ) in evo-devo studies (e.g. Reyes-Olalde, 2013, 2017). Two domains, medial and lateral, can be distinguished in the gynoecium of Arabidopsis. ‘The medial domain includes the carpel margin meristem (CMM) that is key for the production

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of the internal tissues involved in fertilization, such as septum, ovules and transmitting tract’ (Reyes-Olalde et al, 2017: p. 1). It may be expected that the marginal zone is morphogenetically active in younger stages than the medial zone, as the margins are already post-genitally fused and the young ovules are present when the medial zone is activated. Reyes-Olalde et al. (2013) found at least 86 genes that play a role in carpel margin tissue development. However, there was no discussion on the relationships between the development of margins proper and the ovules. Important genes for marginal tissue formation in Arabidopsis are LEUNIG and AINTEGUMENTA (Liu, Franks & Klink, 2000) and SPATULA (Heisler et al., 2001). Intercarpellary fusion is also regulated by LEUNIG (Chen et al., 2000).

Unfortunately the valves of the fruits of Arabidopsis are described in molecular developmental literature as having a margin (e.g. Alonso-Cantabrana et al., 2007; Montes et al., 2015; de Folter, 2016). This easily leads to misinterpretations. A margin in the original sense of developmental morphology is a developmentally primary structure: the transitional area between upper (adaxial) and lower (abaxial) surface of leaves or carpels or other organs (e.g. Hagemann, 1970, 1973; Bowman et al., 1999). It is present as soon as the upper and lower surface become distinct from each other. It should also be emphasized that the rim of the valve does not develop at the site where one would expect a virtual border line between the two carpels of the gynoecium. Thus, it is recommended to use the term ‘margin’ only in its restricted sense for primary margins and to use ‘rim’ for the periphery of valves.

‘acarpous’ or ‘acarpellate’ gynoecia witH ‘cauline’ placentation

In the course of time and up to now some authors have claimed that some or all carpels in angiosperms were not macrosporophylls, i.e. phyllomes bearing ovules, but that they were ‘cauline’ or ‘axial’, sometimes irrespective of whether angiosperms were monophyletic or polyphyletic. Some of these authors argued phylogenetically. Others argued only morphologically.

Wettstein (1907, 1935) assumed that carpels or carpel walls were derived from bracts that bear ovules in their axil. Thus, according to him, carpels are not sporophylls and ovules were not originally borne on sporophylls. This hypothesis may still be correct in some sense. Ovules are first known from seed ferns from the Late Devonian and Early Carboniferous (c. 350 Mya) and they were not associated with typical leaf-like structures (Long, 1966; Rothwell & Scheckler, 1988; Doyle, 2013). It is not clear how ovules became associated with leaf-like structures, giving rise to sporophylls. In addition, as shown above, other

structures such as subtending leaves or cupules were associated with ovules.

Thompson (1929) introduced the term ‘acarpy’ for the female organs of some angiosperms and referred to the ‘acarpous interpretation of the inferior ovary of the Scitamineae’ (Thompson, 1933). This view was then criticized by Parkin (1933). Hagerup (1934) used the terms ‘false’ and ‘true’ carpels. He assumed that angiosperms with ‘false’ carpels are derived from Gnetales, and those with ‘true’ carpels are derived from Cycadales. For instance, Hagerup (1939) assumed that Lamiales have ‘false’ carpels.

The most extensive discussion on carpellate vs. acarpellate flowers was by Sattler (Sattler, 1974a; Sattler & Perlin, 1982; Sattler & Lacroix, 1988). Sattler was not interested in the question of whether angiosperms are monophyletic or polyphyletic. According to him at least some ‘acarpellate’ gynoecia can be derived from ‘carpellate’ gynoecia in angiosperms, whereas other acarpellate angiosperms are derived from other, gymnospermous groups. Cresens & Smets (1989, 1990) criticized Sattler’s types as irrelevant for systematic considerations. Sattler was primarily interested in ontogeny, not phylogeny. Such a narrow view makes no sense in the present time of rapidly growing knowledge on plant phylogeny and evolution. Sattler & Lacroix (1988: p. 925) assumed ‘transgressions between the extreme types of gynoecial construction during the evolution of angiosperms due to the fluidity of organization patterns’. On the other hand, Sattler (1974a, fig. 1A–C) drew an unbiological borderline between carpellate and acarpellate gynoecia, which is not even developmental. He depicted the ovule and gynoecium as if glued on the surface of the gynoecium or the floral apex, respectively. Such a demarcation does not occur in nature. What Sattler (1974a: fig. 2) called ‘imaginary lines’ are in no way imaginary, but are instead rather the contours of areas of greatest meristematic activity in the young carpels. Thus, these lines outline the area of the young carpels, which are ‘rooted’ within the remaining floral apex. The carpels of the phylogenetically earliest-diverging extant angiosperms, in the ANITA grade (Endress, 2015; Endress & Doyle, 2015), clearly show that carpels including the ovules are fundamental organs in angiosperms. That in the evolution of more derived angiosperms carpels should freely come and go is an absurd concept. In addition, in Sattler (1974a: fig. 1D) and also in Leins (1972: fig. 1) and in Erbar (1993: fig. 53), two processes are intermingled: (1) morphogenesis of the organs, and (2) intercalary growth of the flower. They should be separately regarded, as they occur at different times of development and involve different cellular processes: the ovule(s) is (are) initiated long before intercalary elongation takes place. Schaeppi (1944: fig. 2b) made a similar mistake as Sattler in

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‘gluing’ a carpel to the floral base. However, his error concerns the schematic demarcation of the carpels from the ‘axis’, and not the demarcation of the ovules from the carpel.

An example with ‘acarpellate’ flowers mentioned by Posluzny & Sattler (1976: p. 1146) is Najas flexilis (Willd.) Rostk. & W.L.E.Schmidt: ‘We showed that the ovule primordium, including the nucellus, is the transformed floral apex, i.e. the ovule is initiated in an exactly terminal (basal) position and not laterally on the gynoecial appendage (i.e. the gynoecial wall). Therefore, it is not possible to apply the carpel concept to this situation (see Sattler, 1974a [which corresponds to 1974b in the present paper]). The gynoecium of Najas is clearly acarpellate. Whether this acarpellate condition is primitive or derived from a carpellate gynoecium is a different question (Sattler, 1974a)’. [Note that in ‘Sattler, 1974b’ there is no mention of carpellate and acarpellate gynoecia, and thus this is an incorrect citation in Posluszny & Sattler (1976)]. However, these authors did not really show what they proclaimed. They did not study the initiation of the gynoecium. There are no critical illustrations of this stage in the literature on Najas L. In the meantime, it has also been resolved that the alismatidean gynoecia that were described as ‘acarpellate’ by Sattler in various papers are phylogenetically derived within Alismatales, and not in positions where their features could be ancestral (APG IV, 2016).

According to Greyson (1994: p. 149), ‘Ovule initiation is most often restricted to what is generally interpreted as carpellary tissue. As mentioned earlier, it is now generally acknowledged that, in some cases, ovules are formed from the floral apex as distinct from the tissues of the gynoecium.’ The second sentence is incorrect because such cases were not critically studied. On the other hand, Greyson (1994: p. 134) also expressed in the same book: ‘Regardless of morphological complexity, however, all functional carpels and ovaries generate ovules and, ultimately, receptive embryo sacs.’ Thus, he was not consistent in his own view.

As discussed above, carpels (and other floral organs) develop from relatively deep meristematic areas at the floral apex (which were formed after flower initiation). Thus, all the ovules (or the single ovule if there is only one) develop from the meristem of the carpel, which may occupy the whole floral apex in some cases, and not from the floral ‘axis’. Thus, the ovules are carpellate. This is also the case if a single ovule in small, reduced flowers grows in the same direction as the floral ‘axis’ lower down. The developmental sequence of a normally developing flower does not change, and it may be predicted that the sequence of molecular events in the floral apex remains stable, although there may be changes in the relative times of specific events.

Along these lines, Breuil-Broyer et al. (2016: p. 905) proposed ‘the concept of meristematic “transference” (cascade) – a regulatory bridging process redundantly and sequentially co-ordinating the triggering and completion of flower meristem termination, and carpel margin meristem and placenta patterning … resolving male/female gradients into sharp male and female entities (whorls, organs) and enforcing flower homeostasis during evolution. This has probably been achieved by incorporating the meristem patterning system of the floral [apex] into the female (carpel) programme.’

In many publications the end of the spent floral apex has been seen as the end of the axis and the ovules have been interpreted as axis-borne. Thus, researchers fell into a trap of short circuits. For instance, Barnard (1955: p. 1) wrote ‘The ovule is derived directly from the apex of the flower primordium’ (in Triticum L.). According to Sajo, Longhi-Wagner & Rudall (2007: pp. 184, 185) ‘the single ovule arises in a basal position in the locule and initially is not related to the carpel walls but arises directly from the pedicel’ (in Pharus P.Browne). This is an incomplete and illogical description. Sattler & Perlin (1982: p. 181) wrote: ‘One cannot deny that their gynoecium [i.e. that of Nyctaginaceae] consists of an appendage which encloses an ovule. However, the ovule which is enclosed is basal, that is, cauline.’ Here the authors neglected the fact that a carpel always has a solid base and that the ovule develops from this solid base, which is part of the carpel, and not of the floral ‘axis’. Also, Leinfellner (1950) described the remaining floral apex in Asphodeline Rchb. and Asphodelus L. as the end of the floral axis, without, however, addressing the position of the ovules.

The placenta has often been interpreted as a special part, separate from the carpels, especially in cases where the placenta is massive. However, the placenta is merely a transitional zone from the carpel wall to the ovules. It becomes thicker as the number of ovules increases. Thus, it is especially thick in some derived groups of angiosperms, such as Orchidaceae in monocots and some Gentianales and Lamiales in eudicots with high ovule numbers, whereas, in phylogenetically early-diverging angiosperms that often only have one or few ovules per carpel it is inconspicuous (Endress & Igersheim, 2000a, Endress & Doyle, 2015). Taylor & Kirchner (1994, 1996) unfortunately adopted the long-outdated Datura model for their Nicotiana L. studies as critically discussed by Rohweder (1963) (see above). Chiurugwi et al. (2007: p. 85) maintained: ‘The findings provide a clear indication that placentation in Impatiens L. is neither axile nor free central in the classical sense of the terms. Impatiens ovules are cauline, and come from a floral meristem-derived placenta; yet the placenta is still attached to the

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carpels.’ It needs to be added that their study was made from a teratological mutant.

It should not be surprising that if there is a single ovule at the base of the gynoecium, then if the placenta is at the base, it is not developmentally necessary that the carpel wall should show much growth in early stages. What is functionally most important is that the carpel should be closed at the time of pollination and later. This is crucial for protection of the ovule at this stage (1) because the stigma is now exposed and (2) because a closed pollen tube transmitting tract is favourable for compatibility/incompatibility reactions, and for pollen tube competition inside the gynoecium (see, e.g. Mulcahy, 1979). Some plants have been said to have open carpels or gynoecia at anthesis. In most cases this is not true, but a misinterpretation of dried herbarium material or a result of non-recognition based on disregard of carpel sealing by secretion (see discussion in Endress & Igersheim, 2000a; Endress, 2015).

gynoecia witH a free central placenta

A free central placenta occurs in genera of several angiosperm orders (Myrtales, Malpighiales, Santalales, Ericales, Lamiales) and thus presumably evolved several times in angiosperms. This has puzzled morphologists and has led to unfortunate interpretations. It is of interest that this feature is associated with some other unusual developmental features.

primulaceae

For Primulaceae, Duchartre (1844) first described how the gynoecium appears as a uniform united ring wall. He also described how the free central placenta secondarily makes contact with the stylar canal by a thin apical protrusion, and he further observed a centrifugal (basipetal) ovule development. Other authors mentioned that gynoecia in the family have slow carpel wall development. Cusick (1966: p. 177) cited for Primula L.: ‘The ovary wall contains five (sometimes a multiple of five) vascular strands (Dickson, 1936). If the inception of vascular tissue occurs in relation to growth centres or, at least, to peaks of metabolic activity, a similarity to the common pattern of syncarpous ovary in which five carpels appear simultaneously as separate growth centres is easy to see. The placenta of Primula has no connection with the ovary wall but an examination of its vasculature reveals a minimum of five vascular strands. Dickson points out that in Lysimachia L. each of the five strands is clearly double, an arrangement strongly reminiscent of the associated marginal veins of adjacent carpels in the five-locular

ovary of Geranium robertianum L. Douglas (1936) confirmed the inverted orientation of the placental bundles of the Primulaceae, thereby providing overwhelming evidence of homology between the free central placentation of this family and the commoner axile placentation of syncarpous five-locular ovaries.’ Another case of gynoecia with cryptic pentamery occurs in Emmotum Ham. (Metteniusaceae; Stull et al., 2015), also in early-diverging asterids. There are also five vascular bundles in the gynoecium, which has three fertile and two sterile carpels, whereby the sterile carpels are highly reduced (Endress & Rapini, 2014).

Also in former Theophrastaceae (now Primulaceae), the gynoecium wall develops as a ring with only faintly expressed carpel tips. ‘The free-central placenta starts as a spherical outgrowth of the floral axis, becomes conical, and ovule primordia arise on it in a downward spiral’ (Caris & Smets, 2004: p. 639). Unfortunately, this is not entirely correct. The figures show that there is no continuous downward spiral. There are only smaller groups of organs that appear to be spirally disposed starting from the apex, but this pattern is often interrupted. It is impossible on geometrical grounds to produce a regular downward spiral. A spiral can only be formed from an apex by enlarging of its periphery, leading to an acropetal pattern. Thus, in a free central placenta with basipetal ovule initiation, there are a number of short spiral-like patterns, each encompassing groups of several ovules, and not a single (ontogenetic) spiral that would encompass all ovules. Only the latter could be called spiral organotaxis. Such short ‘spirals’ of few organs are simply the expression of relatively regular local organotaxis (see Endress, 2006).

In abnormal proliferating flowers of Primula, Caris & Smets (2004) interpreted the top of the placenta as the top of the floral axis. Rather, this is the remaining floral apex that has been transformed again into a new floral apex, as is often the case in such abnormal proliferating flowers.

There is a good discussion on the morphology of the free central placenta in Sundberg (1982) (see also Pax, 1889, and early work by Sattler, 1962). The discussion by Pankow (1959) is insufficient, because it is based on histogenesis only, and is thus one-sided. In Roth (1959), despite similar one-sidedness, the discussion is more differentiated because aspects other than the apex are also included.

AmarantHaceae, lentibulariaceae and santalaceae

In Amaranthaceae usually one or a few ovules occur on a basal placenta. Pleuropetalum Hook.f. is one of

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the few genera with numerous ovules on a free central placenta. It also has a more-or-less circular gynoecial rim as in Primulaceae and has only faintly expressed carpel tips. The ovules also appear in a centrifugal direction (Ronse De Craene, Volgin & Smets, 1999). In Lentibulariaceae (Hartl, 1956; Degtjareva & Sokoloff, 2012), as in Primulaceae (Duchartre, 1844; Caris et al., 2000; Caris & Smets, 2004), both with a free central placenta, the gynoecial rim is circular and individual carpels are not recognizable (at least not in early development).

The same is the case in some Santalaceae (Ram, 1959). According to Stauffer (1959), carpel number in Anthoboleae (Santalaceae) could often not be determined with absolute certainty (see also Endress, 2015). In Thesium L., stigmatic lobes are only weakly recognizable (Schaeppi, 1942). In contrast, in Osyris L. (Santalaceae) with basal locule formation the number of carpels is clear based on more pronounced stigmatic lobes (Schaeppi & Steindl 1937).

summary for development of gynoecia witH free central placenta

In Primulaceae (Duchartre, 1844; Caris et al., 2000; Caris & Smets, 2004) and Lentibulariaceae (Degtjareva & Sokoloff, 2012), the gynoecial rim is completely circular in early stages, like a diaphragm, and carpel number cannot be recognized from the surface in early gynoecium development. Only later, when the gynoecium closes, are irregular lobes formed. These lobes appear to be an architectural necessity for closure, a developmental by-product, and should not be misinterpreted as carpel tips. Such architectural necessity for closure of a circular diaphragm (or aperture) in plants was first discussed for the closure of micropyles in ovules by Endress (2011, 2015). The same is probably the case in Santalaceae mentioned, such as Thesium, but they have not been studied by scanning electron microscopy. What is the developmental relationship between these two features, the diaphragm-like circular rim of the young gynoecium (without recognizable carpel tips) and the free central placenta? This has not yet been studied. It may be speculated that during the formation of a syncarpous gynoecium the signal for the formation of individual carpel tips has been lost such that no or only weak signature of a morphological carpel differentiation remains.

It is also interesting to see how a free central placenta in an anthetic gynoecium may develop ontogenet ica l ly f rom an axi le p lacenta , as shown by gynoecium development in Avicennia L. (Acanthaceae; Borg & Schönenberger, 2011). Here, early stages are more distinctly septate,

but the upper part of the placenta becomes more prominent during development so that the septa are no longer obvious at anthesis. Accordingly, there are two distinct stigmatic lobes, corresponding to the two carpel tips. There are also intermediate forms that still appear in mature gynoecia in families that normally have septate ovaries. In Limosella L. (Scrophulariaceae) the placenta is similar to the free central placenta type (Svensson, 1928), but septa are present at the base of the gynoecium. Likewise, in Sauvagesia erecta L. (Ochnaceae) the ovary is septate only at the base. Here also the young gynoecium rim is circular without any morphological indication of carpel number (Farrar & Ronse De Craene, 2013). Another family, Podostemaceae, also has normally septate ovaries. Inversodicraea Engl. ex R.E.Fr. lacks a septum and has a free central placenta (Thiv et al., 2009). However, the gynoecium has two free stigmatic tips and the early opening is not circular.

misinterpretations on free central placentation witH early ovule formation, and

early and late ovule formation in general

The misinterpretation that a free central placenta is not formed by the gynoecium but by the axis has been most often evoked when the ovules become visible before gynoecium closure. It then looks as if the placenta with the ovules might be something independent of the carpel, as discussed by Endress (2015).

There is a wide spectrum of early and late ovule formation across angiosperms. Another extreme is very late ovule formation, such as in Fagales (Sogo & Tobe, 2006), in which the ovules appear only long after carpel closure (in the extreme several months later in some Betulaceae) (Endress, 1967, 1977).

In early-diverging angiosperms (ANITA grade) ovules appear conspicuously late in development compared with carpel development, e.g. Amborella Baill. (Endress & Igersheim, 2000b; Yamada et al., 2001; Posluszny & Tomlinson, 2003; Buzgo, Soltis & Soltis, 2004; Endress, 2015), Nymphaeaceae (Igersheim & Endress, 1998), Trimeniaceae (Endress & Sampson, 1983), Austrobaileyaceae (Endress, 1980c, 1983) and Schisandraceae (Endress, 2001). This feature is also common in magnoliids (Endress, 1980a, 2015; Endress & Igersheim, 1997; Igersheim & Endress, 1997; Staedler, Weston & Endress, 2009) and also occurs in a number of early-diverging eudicots, such as Eupteleaceae (Endress, 1969) and Buxaceae (von Balthazar & Endress, 2002a, b), and monocots, such as Acorus L. (Buzgo & Endress, 2000) and Anthurium Schott (Poli, Temponi & Coan, 2015).

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carpel vasculature: patterns and plasticity

Some basic principles of vascular bundle formation in angiosperms should be mentioned here to understand vascular patterns in the carpels.

(1) In angiosperms, vascular bundles are initiated as procambium in a developing leaf or floral organ. From the base of the organ the procambium then develops basipetally to become connected with vasculature of the young stele. Within the developing leaf or floral organ, the procambium also develops acropetally during further development of the growing parts of the leaf. Thus, the vasculature is initiated by the leaf or floral organ, and not by the stele. This has been revisited and discussed by a number of developmental botanists (e.g. Brooks, 1940; Esau, 1943; Hagemann, 1970). Exceptions where procambium was visible before the leaf primordia have also been described (reviewed by Esau, 1965a, b). A hypothesis to reconcile the different observations is the following. The most developmentally active meristem parts within the apex may function as attraction centres for the needed growth substances from the nearest existing vascular bundles that are at the right developmental stage. This attraction and connection with a vascular bundle results in a flow of substances, which triggers the origin and development of a procambial strand. The leaf apex could be the organizer of procambium formation. Thus, the initiation of an organ and its procambium would go hand in hand (Hagemann, 1967: p. 295; 1970: p. 319). Auxin has been identified as playing a key role in the initiation and differentiation of vascular bundles (reviewed by Scarpella, Barkoulas & Tsiantis, 2010).

(2) In complex organs, such as pinnate leaves or carpels, the different parts do not originate all at once but in a certain sequence. In a young organ that is still morphologically undifferentiated, the meristematic areas leading to the different parts of the complex organ are, correspondingly, active at different times. Likewise, the vasculature of the parts is initiated not synchronously but one by one over a time span (Hagemann, 1970; Endress, 1972a, b). Carpels are morphologically more complex than simple vegetative leaves. However, there are also different degrees of complexity among carpels. In general, they are more complex the larger they are, the larger they become in fruit, and the more ovules and seeds they have, as also discussed by Carlquist (1969). The large flowers of Magnoliaceae are an example, which should be mentioned here also because of morphological misinterpretations of this phenomenon. These flowers have two vascular systems, a normal

stele in the centre, which develops first, and a more peripheral cortical system that develops later (Ozenda, 1949; Canright, 1960; Eames, 1961; Skipworth, 1970). It is normal in leaves and carpels that the median vascular bundle develops earlier than the lateral bundles. This is plausible because it develops from the primary procambium in the centre of the organ, which is always first differentiated. In Magnoliaceae, this time difference is especially exaggerated compared to plants with smaller carpels, and the median bundle, i.e. the dorsal bundle of the carpel, is formed much earlier (Tucker, 1972). Because of this sequence the earlier formed dorsal bundle tends to connect with the vasculature of the stele, whereas the lateral (ventral) bundle, with the vasculature of the ovules, tends to connect with the vasculature of the cortical bundles (Canright 1960; Skipworth & Philipson, 1966). However, Canright (1960: p. 140) showed that ‘the vascular pattern is decidedly unstable: in Michelia champaca L. the middle carpels of the gynoecium are vascularized by both the cortical and stelar systems, similar to the manner previously described for other genera. However, not uncommonly the basal carpels of a gynoecium are vascularized entirely by the cortical system, and the apical carpels entirely by the stelar system.’ This variation may depend on the great change in shape and diameter of the floral apex (Tucker, 1961) during the extended time of carpel formation in the elongate gynoecium. Variability in the carpel bundles within one and the same flower was also recorded for Magnolia decidua Q.Y.Zheng (Deroin, 2010). In those Annonaceae that also have an additional cortical vascular system, ‘the distal parts of the cortical system are used up in the formation of carpel traces, three to each carpel’ (Eames, 1961: p. 393). Deroin (1989) found various patterns of cortical bundles in the flowers of Annonaceae that may take part in vascularization of the gynoecium. Other examples of great variability of vascular patterns in flowers of angiosperms were discussed by Schmid (1972).

(3) Vascular bundles exhibit high plasticity in occurrence and structure. They are formed where they are needed. If an organ is not initiated, consequently a vascular bundle is not initiated. Thus, there are no vestigial bundles when an organ is no longer present. In other words, the vascular bundle disappears (in evolution) at the same time or before the organ completely disappears (Rohweder, 1972). (An exception is when in this transition phase of vanishing an aborted organ is still initiated and leads to a rudimentary vascular bundle even though the organ is no longer visible at maturity.) For instance, in Actinidia Lindl. the

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lateral (ventral) carpel bundles are only formed in functionally female flowers but not in functionally male flowers with much smaller gynoecia and reduced ovules (Löfstrand & Schönenberger, 2015). This is different from vestigial bones in vertebrates, which have a different pattern of development than plants. The earlier view of ‘conservatism of vascular bundles’ (Henslow, 1888; Eames, 1931) was abandoned in the past 50–100 years (Arber, 1933; Venning, 1948; Rohweder, 1967a, 1972; Carlquist, 1969; Hagemann, 1970; Kaplan, 1971; Schmid, 1972; Nuraliev & Sokoloff, 2014). Another, long-extinct theory based on vascular bundles was that on ‘carpel polymorphism’ by Saunders (1925). It was criticized early by Parkin (1926, 1933) and later by Brückner (2000) and no longer has any supporters.

In species of Dysphania R.Br. (Amaranthaceae), which has minute flowers, there are no vascular bundles in the gynoecium wall, which has only two cell layers apart from some islands with three cell layers. This was found in D. glomulifera (Nees) Paul G.Wilson (as ‘D. myriocephala’) (Eckardt 1967a) and in M. plantaginella F.Muell. (Eckardt, 1967b, c). The early vascular bundle in the gynoecium extends from the gynoecium base into the ovule (Eckardt, 1967a, b) in D. glomulifera. The ovule has several cell layers in transverse section, in contrast to the two cell layers of the carpel wall.

In minute unitegmic, tenuinucellar ovules of some Gentianaceae, Rubiaceae and Scrophulariaceae (all lamiids), vasculature is completely lacking (reviewed by Endress, 2011), and likewise in ovules of orchids (Yeung & Law, 1997). The minute size apparently removes the necessity for special vasculature for water, nutrient or hormone supply.

earlier and recent misinterpretations based on vasculature in comparison witH non-

angiosperm seed plants

Bailey & Nast (1943) found that ovules in some Winteraceae are supplied not only by branches from ventral vascular bundles, but also by branches from dorsal bundles. This led to a misinterpretation of carpel morphology by Doweld (1996). He interpreted such a carpel as consisting of two organs and compared them with two-parted organs of fossil gymnosperms (Leptostrobus Heer, Czekanowskiales, a group of ginkgophytic plants of the Jurassic to Early Cretaceous; see Friis et al., 2011). Although the development of carpels in Winteraceae was not studied by Bailey & Nast (1943) (or later authors), the vascular pattern appears to show that the ventral vascularization of the ovules develops later than the dorsal bundle, which is the primary vascularization, as expected for

a carpel. The ventral branches appear later and are less regularly arranged. Such secondary vasculature is common, especially in massive organs, such as here, which develop into fleshy fruits (see also Carlquist 1969: his Commentary 4). Doweld (1996) uses the term ‘vascular skeleton’ for the vascular bundles in Bubbia Tiegh. (now Zygogynum Baill., Winteraceae). This is unfortunate because vascular bundles of plants and the skeleton of animals are not comparable and behave differently in development, functional roles and evolution. In contrast to the skeleton of vertebrates, vasculature in flowering plants is a developmentally secondary structure, which is governed by the development of organs and usually disappears in evolution before organs disappear or together with the organs as mentioned before (critical discussion, e.g. by Carlquist, 1969, and Rohweder, 1972).

These aspects of vasculature attracted much attention and there is an extensive literature. However, there is recent literature that falls into a trap of blatant misinterpretation of carpels because of lack of knowledge of the literature on the behaviour of vasculature in angiosperms. Variation and flexibility in structure occurs not only in patterns of arrangement of the vasculature but also in the histology of the vascular bundles themselves. Liu, Hilu & Wang (2014) interpreted ‘amphicribral’ bundles as a feature of ovules and ‘collateral’ bundles as a feature of the ovary wall. This is incorrect and does not take into account the flexible behaviour of vascular bundles in angiosperms. ‘Collateral’ and ‘concentric’ (‘amphicribral’ or ‘amphivasal’) are not different ‘types’ of vascular bundles but they may occur within one and the same bundle, with continuous transitions from one pattern into another (Esau, 1965a: p. 369). They have no significance for evaluation of organ homology but differentiate depending simply on position and neighbourhood of the bundle in the vascular system. Liu et al. (2014) based their belief on the simple vascular bundles in ovules of fossil plants that are only distantly related to angiosperms. Liu et al. (2014) further claimed that Endress’s (2005) statement that all vascular bundles in the carpel of Brasenia Schreb. are collateral ‘is nullified in his own figure’. However, all figures of Endress (2005) show that the xylem is on the inner side of the vascular bundle and not in the centre. Endress (2005) marked the bundles with the xylem simply to show that they are vascular bundles and not other structures, and he did not indicate other tissues, such as phloem and parenchyma. Regardless, this procedure shows how authors may misinterpret the results of other authors. A similar discussion on Actinidia based on the same incorrect assumption can be found in Guo et al. (2013). Furthermore, Zhang, Liu & Wang (2017) studied teratological material of magnoliaceous carpels. They described abnormal

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open carpels with exposed ovules. They claim that ‘these atypical and typical carpels for the first time demonstrate clearly how the naked ovules get enclosed’ and ‘each atypical carpel, with naked ovules, clearly comprises two parts, namely, subtending foliar part and branches bearing ovules, suggesting that a typical carpel is actually an end-product of the fusion between the ovuliferous branches and subtending foliar parts’ (Zhang et al., 2017: p. 1). Apparently, the authors were unaware of the vast literature on terata that was produced from the 19th century onward, which, among many other things, also showed terata with open carpels (e.g. Brongniart, 1844; Masters, 1869; Penzig, 1921–22, Guédès, 1966; Leinfellner, 1973; Komaki et al. 1988; Jabbour et al. 2015). In addition, Zhang et al. (2017) did not recognize that normal ontogeny always starts with open carpels. Malformations can hardly be used to understand the evolution of normal formations. That there seem to be two different parts in carpels may be simply because they have different functions today, and not because they have two separate evolutionary origins. Such short circuits were also criticized by Deroin (2015) and Herendeen et al. (2017). An especially misleading paper is that by Guo et al. (2017) on the gynoecium of Dianthus chinensis L., in which it was claimed that they have a free central placenta. They did not know that flowers of several genera of Dianthoideae (Caryophyllaceae) were studied in an extremely careful and circumspect paper by Rohweder (1967a), which can serve as model paper in comparative developmental floral morphology. Fifty years later, Guo et al. (2017) published a paper based on a superficial and erroneous interpretation of the structures. They also mentioned that the notion of sporophylls in angiosperms is problematic, but they overlooked the long-standing discussion in the literature. It is a pity that the wheel has been invented again but in a form that does not work.

It is likely that the ovules and the carpel wall part have separate evolutionary origins and the ovules are evolutionarily older than the carpels, and there are several hypotheses about angiosperm ancestors and the organs involved in carpel origin, as mentioned earlier in this paper (see, e.g. Stebbins, 1974; Doyle, 1978, 2008; Retallack & Dilcher, 1981; Meyen, 1988; Friis & Endress, 1990; Frohlich & Parker, 2000; Endress, 2006; Frohlich & Chase, 2007; Friis et al., 2011). However, the ovules appear developmentally long after the carpels in some angiosperms (as discussed before), and this has nothing to do with any evolutionary sequence. Rather, it reflects their present function: young angiosperm ovules generally need to be protected by the carpel walls from the beginning of their development. It is also not surprising that the genetic networks activated in the young ovules are different from those in the young carpel wall given

that they have completely different functions. Thus, this also does not necessarily say anything about the different origins of the placenta and other parts of the carpel. It does not make sense to assume that a compound structure such as the carpel would have been governed for >200 Myr by the different origin of its parts, and not by its present functional needs. Furthermore, an evolutionary origin from two different parts does not mean that these two parts were not synorganized long ago in the evolutionary history (not later than the origin of the angiosperms as we know them today) and that they now appear as one unified organ, which we call carpel.

In sum, it is quite possible that the distant precursors of angiosperm carpels were not originally unified structures. However, the constituent parts have adjusted to each other such that today the ovules and their surrounding part behave as a unified organ. It may be better not to call them sporophylls, to avoid a potentially incorrect phylogenetic context. The term ‘carpel’ is perfectly sufficient. Unfortunately, in Guo et al. (2017) and similar papers, such as Guo et al. (2013) on Actinidia and Liu et al. (2014) and Zhang et al. (2017; as Michelia L.) on Magnolia L., the authors did not recognize the developmental plasticity and biology of vascular bundles, leading to serious errors in their interpretations.

Pitfalls in the interpretation of vascular bundles of angiosperms may be summarized as follows. (1) A vascular bundle often changes its anatomy along its length. The anatomy is influenced by its immediately adjacent histological environment. (2) The structure of a vascular bundle is not organ-specific. Thus, it cannot be used to determine the kind of organ in which it was formed. (3) A vascular bundle is connected with other vascular bundles in the plant body, and its histology is greatly influenced by the next older vascular bundle to which it connects. For instance, fusing bundles may be concentric below the place of fusion, irrespective of the morphological location of this fusion, and they may be inversely collateral in the two counterparts above the place of fusion because their xylem portions need to approach each other before they become concentric. These kinds of plasticity were described in detail by Esau (1943, 1965a, b); see also Puri (1944).

earlier misinterpretations based mainly on incorrect pHylogenetic assumptions:

monopHyly vs. polypHyly of angiosperms and pHyllospory vs. stacHyospory

The monophyly vs. polyphyly of angiosperms was debated until the 1960s. Polyphyly was favoured by several authors (Karsten, 1918; Hagerup, 1934; Fagerlind, 1947; Lam, 1948, 1950, 1959; Suessenguth & Merxmüller, 1952), and by some authors still

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later (Melville, 1983; Meeuse, 1986; reviewed by Friis & Endress, 1990). However, detailed studies on comparative floral development of the late 1960s and early 1970s showed that the dissimilarities in gynoecium structure between putatively basically different angiosperms adduced by these authors did not hold (critiques in Baum & Leinfellner, 1953; Rohweder, 1963, 1972; Endress, 1967; Carlquist, 1969; Eyde, 1971; Kaplan, 1971; Schmid, 1972; Tucker, 1972).

For a long time, up to the early 1970s and even later, authors including Pankow (1962), Maze, Dengler & Bohm (1971) and Sattler (1974a), who invoked acarpellate gynoecia and cauline placentae, restricted their attention to histogenetic studies. Thus, they studied only the cellular pattern (resulting from anticlinal and periclinal cell divisions) in young flowers without considering the cytological zonation of the apical region (see, e.g. critique in Hagemann, 1970; Endress, 1972a, b). Thus, the study of areas of meristematic activity shown by differential cytohistological staining was neglected.

In the premolecular era, before nucleotide sequences were used for phylogenetic reconstruction, macrosystematic reconstruction of phylogeny was mainly based on comparative morphology. A breakthrough of molecular phylogenetics took place with the first large seed plant analysis based on rbcL by Chase et al. (1993). This has been continuously refined since with the use of more genes from all three genomes and with the application of improved phylogenetic analytical techniques for large data sets (reviewed, e.g. in Soltis et al., 2018).

Better knowledge of phylogeny increasingly became a forceful guideline for understanding the evolution of features. Thanks to optimization of characters on molecular trees, we are no longer at a loss about what is ‘primitive’ or ‘advanced’. Thus, there was a shift from morphological to molecular data in phylogenetic studies, with the exception of fossils for which morphological studies are still the only possible approach (e.g. Doyle & Endress, 2000, 2018).

An additional new line of research was the successful study of mesofossils (mostly flowers) from the Cretaceous, starting in the 1980s (survey in Friis et al., 2011). In concert, refined morphological and developmental studies are ever more important for the reconstruction of evolutionary changes. Sattler (1974a) did not consider any evolutionary aspects, which, of course, were more difficult to address four decades ago than at present. However, some valid interpretations were not impossible, and Rohweder (1963, 1967a) was successful in this endeavour. His circumspect and cautious views have been supported since by molecular studies as shown below. Today, if neither phylogenetic nor developmental aspects are considered, evolutionary interpretations make no sense.

tHe cases of Phytolacca and hyPericum

In two species of Phytolacca L., pollen tube growth was observed on the area that developed from the former floral apex between the seemingly free carpels and was interpreted as an extragynoecial pollen-tube pathway (Zheng et al., 2018). This is a possible interpretation. However, Rohweder (1965b) had already studied floral development of two Phytolacca spp. He recognized the gynoecium as syncarpous and found a stigma-like differentiation of the area in question. He discussed this tissue as potential carpel tissue.

To show the careful discussion by Rohweder (1965b: p. 515) I reproduce some sentences (translated from German): ‘While the ovary bulges, periclinal cell divisions in the floral apex begin to encompass also the outermost cell layer. Thus a tunica is no longer present. It is interesting that the same takes place in the carpel margins, especially in the symplicate zone. The free central protrusion is usually regarded as the non-used up part of the floral apex and, without discussion, as the sterile end of the floral axis. This is not as self-evident as is usually assumed. The periclinal cell divisions in the second tunica layer [of the floral apex] after carpel initiation cannot simply be understood as a reduction in number of the cell layers in the remaining floral apex from two to one. It is the beginning of a development that scarcely has anything to do with that of an apex, but is similar to development at carpel margins. It is further obvious that the stele contracts to a small remainder in the centre of the protrusion in spite of the intensive growth of the surrounding area (especially impressive in P. clavigera W.W.Sm. and P. americana L.). The possibility that at least the surface of the protrusion can be interpreted in some sense as carpellary tissue cannot be completely disregarded.’

Hypericum calycinum L. may be a similar case. Here, ‘besides many ordinary carpel-borne ovules, some further ovules exist that in all probability are inserted directly on top of the floral axis and are vascularised by its residual stelar tissue. In this genus there appears to occur a fairly clear instance of partial stachyospory’ (Dupuy & Guédès, 1975: p. 39). However, the interesting proposal for Phytolacca by Rohweder (1965b) may also apply here. One could tentatively say that in both cases there is an extended area of morphogenetic potential of the gynoecium extending out from the normal area of the carpels.

tHe cases of cerastium and stellaria

An especially critical case was the incorrect interpretation of the gynoecium of Stellaria Ség. and Cerastium L. by Moeliono (1959, 1966, 1970). As Rohweder published an exellent critical review in German, part of it will be reproduced here, translated to English:

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‘The stimulating effect even of erroneous assumptions should not be underestimated; however, the carelessness with which many new theories have been advanced today – in this case based even on a wrong interpretation of long correctly interpreted evidence’ (Rohweder, 1970: p. 263). And further: ‘A special case is Cerastium, because the central placental protrusion extends outside the attachment point of the septa and also bears ovules (Payer, 1857; Lister, 1884; Roth, 1963). As always these are also arranged here in two rows opposite the dorsal median bundle. In Cerastium triviale Link the free septum edges protrude between each of two double rows [of ovules] and are mostly more or less tightly contiguous with the placental plug (Fig. 38 a, b). On their surface, during the development of the ovules, there are numerous periclinal cell divisions in the area of the septum edges. Such phenomena may have led Moeliono (1966) to the idea of post-genital fusion between the septa and the placenta. However, such fusion effectively does not occur. The periclinal cell divisions correspond to those that occur everywhere together with the differentiation of the pollen tube transmitting tissue, not only on these alleged areas of fusion. Furthermore, at that time the synascidiate and the symplicate zone are already well formed. A later shifting of the border between the two by post-genital fusion does not occur. It should also be emphasized that the growth in the septa in the crucial, much earlier morphogenetical phases is in no way transverse, from the ovary wall inwards, but longitudinal, i.e. parallel to the floral axis’ (Rohweder (1970: p. 230f.).

The following discussion by Rohweder (1963) relates not only to Moeliono but in general to works on carpels with basal or central ovules: ‘If it could be shown that there is no tissue that would be part of a phyllome between the floral axis and the ovule, it would hardly be doubtful that this would be an axis-borne ovule.

However, at first one should realize that with such a statement come several unresolved questions that are commonly simply overlooked. One would need to ask (with Unruh, 1939) whether it is permissible to count the floral apex as part of the axis or whether it needs to be viewed as a part that is not yet the one or the other, but that it will differentiate only later into the one or the other part. It is therefore not obvious that an ovule or a placenta that immediately arises by “transformation” from an apex has to be viewed as axis-generated (stachyosporous) or even of caulinary nature. As mentioned earlier, it is also well possible that a placental protrusion that is formed by the marginal areas of several carpels resembles in its mode of growth that of a shoot axis in the usual (conventional) sense. Because such an organ complex is initiated and the axis ceases to grow, the possibility that the upper end of the axis without a [morphologically] noticeable change

transits into the placenta apex can not be ruled out. Examples of corresponding processes in the vegetative region are found in the seedlings of certain monocots (Haccius, 1952) and some special cases of dicots (e.g. Rauh, 1956). Furthermore, we have to consider that it is scarcely possible to draw a sharp and unequivocal borderline between leaf and axis. […] It is also well known that the peripheral layers of the part of the shoot that is commonly briefly called “axis” has its closest relationship to the leaf, and in many cases this is conspicuously demonstrated by a decurrent leaf base or by hair lines, which continue the ciliation of the leaf margin etc. In any case, it is not possible to deny at the outset that also certain parts of the floral receptacle can be viewed as of foliar nature, even if they do not appear clearly separated from the floral “apex” and therefore do not even stand out in their histogenesis. Admittedly, these are questions that can find a clear answer only with difficulties, and perhaps in part a clarification is not even possible. Therefore, a discussion would result in a dispute about arbitrary notions and definitions. Just for this very reason it is advised to be careful with far reaching conclusions’ (Rohweder, 1963: pp. 83, 84).

molecular developmental studies

Consistent with the complexity of carpel (gynoecium) structure, the gene regulatory network involved in the formation of these organs is also highly complex (Reyes-Olalde et al., 2013; Montes et al., 2015). Reyes-Olalde et al. (2013) mentioned 86 genes, including 62 transcription factors involved in gynoecium development in Arabidopsis. Montes et al. (2015) mentioned 282 transcription factors. This was 25 years after a carpel identity (homeotic) gene (AGAMOUS) was described in Arabidopsis (Yanovsky et al., 1990; Bowman et al., 1999). ETTIN is another important gene that is active in morphogenesis of the Arabidopsis gynoecium (Sessions & Zambryski, 1995). The YABBY gene family is active in adaxial–abaxial differentiation in both leaves and carpels (Eshed, Baum & Bowman, 1999; Bowman, 2000; Finet et al., 2016) and in other functions in carpel development (Fourquin et al., 2005; Gross, Broholm & Becker, 2018). A number of valve and replum genes were found to be active in the gynoecium of Arabidopsis (Alonso-Cantabrana et al., 2007). At least 23 961 genes were recorded for entire flowers of Arabidopsis (Zhang et al., 2015). Most of these genes are not homoeotic but form complex networks of functions (Montes et al., 2015). In addition to transcriptional regulators, hormonal signals also play a role in this complexity of development. It should also be re-emphasized that the development of a carpel or gynoecium takes some time, weeks or months, and many genes may be activated sequentially. In addition, development may not proceed evenly but

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in distinct phases in the young gynoecium (Crone & Lord, 1991) and in the young flower (Bellaire et al., 2014), which may make the entire process even more complex. A broad study by Pfannebecker et al. (2017a, b) involving many plant groups showed that a number of gene families in which genes play a role in carpel development in modern plants were already present in the most recent common ancestor of all land plants or in the most recent common ancestor of seed pants. They discussed the potential evolution of gene regulatory networks acting in carpel development. The authors assumed that some of these genes were recruited from pre-existing networks and others arose from duplication and neo- and sub-functionalization and changes occurred at different times in plant evolution.

Despite the presence of such complex networks, the basic order of carpel development across the angiosperms indicates that the developmental pattern is stable and the molecular developmental events take place in a fixed cascade. It is possible that there is some flexibility in the relative duration of some events but it is not expected that the sequence of events should change and it appears that this aspect is highly resilient (e.g. role of SHI/STY/SRS genes in early-diverging eudicots and asterids; Gomariz-Fernández et al., 2017).

Post-genital fusion of carpels in Arabidopsis is regulated by CUP SHAPED COTYLEDON (CUC) genes (Aida et al., 1997). In unicarpellate gynoecia of legumes the NAM/miR164 genetic module was found to play a role in intracarpellary fusion (Vialette-Guiraud, 2016). The CUC genes play a role in organ separation or loss of organ separation resulting in ‘fusion’ (Sieber et al., 2007). It appears that both congenital and post-genital fusion are affected. Their common denominator is that in both cases organ separation may be inhibited, in which case inhibition may be complete (in congenital fusion) or partial (in post-genital fusion). In Zea mays L., micro RNAs were found to play a role in carpel fusion (Li et al., 2017).

The antagonistic hormones auxin and cytokinin are important modulators of carpel development in Arabidopsis (Deb, Bland & Ostergaard, 2018). ‘Auxin promotes carpel initiation, gynoecium growth, and proper style and stigma formation’, whereas ‘cytokinin participates in the carpel margin meristem and derived tissues, and valve margin’ (Marsch-Martínez et al., 2012a, b; Marsch-Martínez & de Folter, 2016). However, later it was found that auxin is also necessary for valve dehiscence (van Gelderen et al., 2016; de Folter, 2016). Also, ovule number and development are regulated by auxin and cytokinin (Cucinotta et al., 2016), and apical–basal patterning of the gynoecium is affected by cytokinin (Zuñiga-Mayo et al., 2014). The antagonistic interaction of cytokinin and auxin also regulates floral meristem determinacy (Zhang et al., 2018).

SUMMARY

There has been confusion in morphological interpretation based on several misconceptions: (1) the dichotomy between phyllome and axis (lateral vs. intercalary structures); (2) the nature of the shoot apex or floral apex (‘axis’ instead of undifferentiated); and (3) the view that the primordium originates only by cell divisions (stratification, histogenesis) instead of tissue activation (zonation, morphogenesis). In reality: (1) an organ primordium extends from the surface to deep down in the apical meristem; (2) there are no sharp demarcations in congenitally fused organs or uniform parts of organs – a sharp demarcation is present only between free organs (Aida & Tasaka, 2006); and (3) the use of the term ‘axis’ may also be confusing because ‘axis’ has been used in different senses, as a morphological and as a geometrical term. In addition, different adjectives, namely axial, axile and axillary, have sometimes been confused. Axial relates to the axis, axillary relates to the position of a lateral branch (vegetative or floral) in the axil of a leaf, and axile relates to the position of the placenta in the inner angle of a carpel in a syncarpous ovary.

The first good discussion of the fact that ovules in angiosperms are never axis-generated was by Čelakowský (1874), who was one of the first evolutionary morphologists. Despite the in-depth studies and detailed discussions of comparative morphologists in the 1950s to 1970s, which clearly showed that in extant angiosperms ovules always develop on carpels (e.g. Eckardt, 1954, 1957; Rohweder, 1967a, 1970; Endress, 1972b; Rohweder & Huber, 1974; Hagemann, 1975), publications on ‘axial ovules’, ‘cauline placentation’ (e.g. Sattler & Lacroix, 1988) and ‘acarpellate gynoecia’ have continued to appear until recently (e.g. Satina & Blakeslee, 1943; Pankow, 1959; Roth, 1959; Moeliono, 1970; Sattler, 1974a; Sattler & Perlin, 1982; Sattler & Lacroix, 1988; Taylor & Kirchner, 1996; Chiurugwi et al., 2007; Sajo et al., 2007; Zheng et al., 2018). These publications were based on incorrect observations (Moeliono, 1970) and/or on fundamental misconceptions about how floral organs develop and their patterns of diversity, apparently because the authors were not aware of the relevant literature, and they did not provide well-founded reasoning for their beliefs. Sattler (1962) was more circumspect in his first paper than later and discussed several viewpoints. Even Schaeppi (1937), who accepted ‘Karpellsohlen’ as part of the gynoecium, unfortunately interpreted the central protrusion of the placenta as part of the ‘axis’.

Some of these papers concentrated on ‘histogenesis’, which by itself is one-sided, and, second, they did not consider the diversity of angiosperms (e.g. systematics and evolutionary changes), which was, of course, much

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less well understood at their time than at present. A common misconception is that the floral apex is regarded as ‘axis’. The shoot apex is the primordium of a shoot, and a shoot primarily produces leaves. Likewise, the floral apex is the primordium of a flower or of the inner part of a flower, and a flower primarily produces floral organs. The axis of angiosperms is a developmentally secondary structure, which develops behind the shoot apex or floral apex only when leaves or floral organs have been initiated. Thus, it is an anatomically and morphologically internal structure, surrounded by (and congenitally fused with) organ bases, whereas leaves or floral organs are ‘appendages’ or ‘lateral structures’. This makes it easier to delimit leaves than ‘axes’. This is also true for carpels, but the gynoecium as a whole has a special position because it terminates the development of a floral apex. The floral apex either is used up completely from the developing gynoecium or a residual part is left in the centre of the gynoecium, especially when the gynoecium consists of a larger number of carpels (e.g. Endress, 2006, 2014) or to the side of the gynoecium if it consists of a single carpel. If the gynoecium consists of a single carpel, this carpel primordium also may use up the entire remaining floral apex so that there are no remains of the apex at maturity, as in Pseudowintera (Winteraceae) (Sampson & Kaplan, 1970) as discussed above. When a carpel or a syncarpous gynoecium is initiated, an area within the floral apex, encompassing several cell layers, becomes active, which can be visualized by differential staining (e.g. Eschscholzia Cham.; Stammler et al., 2013). This pattern is the same for any organ arising from an apex (e.g. Hagemann, 1970). This activation occurs before any cell division takes place. The entire activated area is the carpel or gynoecium primordium. This is independent of whether this area is slightly lateral to the midpoint of the apex or whether it encompasses the midpoint. Everything that develops from this activated area, the carpel or gynoecium primordium, belongs to the developing carpel or gynoecium and is thus not cauline. Ovules always develop from this area. A major misconception, as seen from the figures in Sattler (1974a), is the view that the carpel or gynoecium sits on the floral apex as if it was glued onto its surface. This is not how development proceeds. Another misconception is that an organ primordium originates by cell divisions only, and without considering cytohistological activation of an entire area. With molecular techniques this can be analysed in more detail today. Cell division without morphogenesis primarily provides growth and not form.

CONCLUSIONS

At present we are fortunate for the following reasons. (1) We have a much better knowledge on the

phylogenetic relationships among extant angiosperms than 50 years ago based on molecular phylogenetic studies. (2) We know more about the relationships among gymnosperms thanks to better knowledge on fossils and application of phylogenetic techniques. Extant angiosperms are clearly monophyletic and the ANITA lines make up their early-diverging grade (e.g. Mathews & Donoghue, 1999; Qiu et al., 1999; Soltis, Soltis & Chase, 1999; APG IV, 2016; Soltis et al., 2018). (3) Many well-preserved fossil flowers have been recovered from the Early Cretaceous, the time when angiosperms began their main diversification (Friis et al., 2011). (4) We know more about evo-devo in angiosperms (e.g. Coen & Meyerowitz, 1991; Smyth, 2018). Despite this progress, however, much is still unknown in all these fields.

From this present knowledge it can be stated that the ovules of all angiosperms are carpel-borne. There are no critically studied cases in which this appears not to be the case. However, this does not mean that ovules were associated with carpels in pre-angiosperms. Rather, it has to be assumed that ovules and a leaf-like structure were synorganized in an earlier phase of evolutionary history. This synorganization was highly successful and probably relatively rapid (as no intermediate fossils have yet been found); it has never been abandoned in angiosperm evolution.

ACKNOWLEDGMENTS

I thank Rosemarie Siegrist for microtome sections and Alex Bernhard for graphical work. I am greatly indebted to James A. Doyle and an anonymous reviewer for careful text reviews and Julien B. Bachelier for welcome suggestions on the arrangement of the sections.

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