Clarification of the Carpel Number in Papaverales, Capparales, and Berberidaceae.

I. Abstract

For more than 170 years there has been a controversy about the organization of the siliqua, a fruit typical for the Brassicaceae and, in modified forms, also for members of Capparaceae, Papaveraceae, and Fumariaceae. Because in the Berberidaceae fruit forms resembling a "semi-siliqua" are produced, they are also controversial. A siliqua is typically furnished with two placental regions joined by a septum and dehiscing through detachment of two sterile valves. Modified forms lack a septum and have only one or more than two valves, or are indehiscent. The controversial issue is the number of carpels composing a siliqua, typical or modified. Aside from the fact that the nature and phylogeny of the angiosperm organ "carpel" are still insufficiently known and therefore speculative, carpel numbers of two, four, and six have been proposed for a bivalvate siliqua; moreover, an "acarpellate" state as an axis-derived structure has been postulated. Within the framework of these theories there are additional theories co ncerning the position, shape, and fertility or sterility of what are believed to be carpels. Each of these concepts is reviewed here, and its morphological basis is checked. Gynoecial features used as evidence of the manifold hypotheses are shape of the stigma, zones of dehiscence, structure of the placental regions, vascular pattern, ontogeny, and teratological transformations. They are discussed for each family and compared in the context of the conclusions derived from them. The result is that Robert Brown's (1817) classical theory, explaining the siliqua as a product of fusion of two transverse carpels with the valves being opercular structures and the septum formed of placental outgrowths, cannot be invalidated by any of the later theories. Stigmatic lobes should not a priori be equated with carpel tips, and their number is not a definite indication of carpel number. The zones of dehiscence are not carpel borders but secondary separation tissues within the carpel blade. Massive placental regions with com plex venation need not be solid carpels. Number and course of vascular bundles may be interpreted in ontogenetic and functional terms, and the concept of vascular conservatism is unsound. Gynoecial growth centers must not uncritically be equated with carpel primordia Terata, such as tetravalvate siliquac, are not atavisms. Thus, carpel numbers higher than those of placentae in the given gynoecium cannot be ascertained. The gynoecium of Berberidaceae is truly monomerous. The identical organization of the gynoecia in the families concerned demands their explanation by a single theory. Many textbooks, floras, and monographs should be revised from this point of view.

II. Introduction

The Papaveraceae Juss., Fumariaceae DC., Brassicaceae Burnett (= Cruciferae Juss.), and the majority of Capparaceae Juss. have superior paracarpous gynoecia with parietal placentation. These gynoecia produce various dehiscent or indehiscent fruit forms that are, however, predominantly a siliqua-like type. A siliqua s.str., the typical cruciferous fruit (Fig. 1), is characterized by a peculiar mode of dehiscence with two sterile sections of the pericarp (valves) separating from the persistent placental frame (replum). The latter bears the loosely attached seeds and is topped by the style and stigma remnants. The locule is two chambered, with a dissepimentum (septum) that covers the replum frame and, at fruit maturity, obtains a membraneous consistence. Modified siliquae include absence of the septum, valve numbers greater than two, and a differing degree of valve detachment in incompletely dehiscent fruit forms. The organization (in the sense of Froebe and Classen-Bockhoff, 1994) of all these modified siliqua e is essentially the same in the four families concerned. The dehiscent fruit forms of the Berberidaceae Juss. should also be considered, because their most important deviation from the bivalvate siliqua s.l. is a meristic one, for there is only one placental region and one valve formed, thus recalling "half a siliqua" (cf. Endress, 1995).

The composition of the fruits and especially of the siliquae (in a broad sense) has been debated for more than 170 years. The number and structure of the "congenitally fused" gynoecium units, the carpels, have been the subject of much discussion, as the many different concepts presented in the literature attest. The oldest and most widespread theory to explain the nature of the siliqua was first presented by Robert Brown in 1817. He and his successors proposed that bivalvate fruits with their placental regions in the median plane comprise two united carpels in transverse position. Other ideas-two median carpels, four carpels, six carpels, etc.--have been offered since then, sometimes defended in a long series of publications with concentrations around 1830, 1880, 1930, and 1980, or approximately every fifty years (Fig. 2). In the intervals, the supporters of the classical theory always hoped to give ultimate proof for the unsoundness of the deviating concepts, but, as Michel Guedes (1966b: 59) somewhat sadly states, they appeared to be of "palingenetic" nature. At that time he announced a historical review of carpel theories concerning Brassicaceae, but the manuscript was never published (A. Le Thomas, pers. comm.).

Due to temporal separation by about a half-century the creators of "new" concepts could hardly contact and exchange ideas with their mental predecessors. They referred to the literature but often did not know the whole array of papers relevant to the subject. Moreover, most of the concepts applied to only one of the families and often only to selected members, so theoreticians frequently did not know that the same phenomenon had already been discussed in detail for representatives of another family. The regular reappearance of the same arguments for "new" concepts is explained by these facts. Number and position of stigmatic lobes, course of the zones of dehiscence, structure of the placental regions, vascular pattern, ontogeny of the gynoecium, and teratological phenomena have been repeatedly stressed to found "new" hypotheses that, in reality, had already been established before. These character sets have been examined in increasing detail and with rapidly improving equipment. Nevertheless, no essentially new aspects have been revealed. So the relevant data are sufficiently known. The aims of this article are to analyze and discuss the data in broad comparison to elucidate whether the siliqua needs an interpretation different from the classical one and thus to terminate cyclical revival of deviating concepts. It will also show that the gynoecia of the five families can be explained by the same theory.

Most results of the author's practical studies preceding this widely theoretical paper have already been published (e.g., Bruckner, 1982, 1992a), so there is no need to discuss material and methods. The present paper is, for the most part, a translation of a postdoctoral thesis (Bruckner, 1996b).