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Developmental Genetics and Morphological Evolution Of Annals of Botany 88: 1173±1202, 2001 doi:10.1006/anbo.2001.1498, available online at http://www.idealibrary.com on REVIEW Developmental Genetics and Morphological Evolution of Flowering Plants, Especially Bladderworts Utricularia): Fuzzy Arberian Morphology Complements Classical Morphology ROLF RUTISHAUSER* and BRIGITTE ISLER Institut fuÈr Systematische Botanik und Botanischer Garten, UniversitaÈtZuÈrich, Zollikerstrasse 107, CH-8008, ZuÈrich, Switzerland Received: 6 November 2000 Returned for revision: 9 February 2001 Accepted: 28 May 2001 This review compares new developmental models on ¯owering and other vascular plants with evolutionary hypotheses formulated by Agnes Arber 01879±1960) and like-minded botanists. Special emphasis is laid on philosophical basics such as perspectivism, pluralism about evolutionary modelling, continuum way of thinking, and fuzzy logic. Arber's perspective is best labelled as Fuzzy Arberian Morphology 0FAM Approach). Its proponents 0`FAMmers') treat structural categories 0e.g. `roots', `shoots', `stems', `leaves', `stipules') in vascular plants as concepts with fuzzy borderlines allowing intermediates 0including transitional forms, developmental mosaics). The FAM Approach complements Classical Plant Morphology 0ClaM Approach), which is the traditional approach in botany. ClaM proponents 0`ClaMmers') postulate that the structural categories of vascular plants are regarded as concepts with clear- cut borderlines and without intermediates. However, during the evolution of vascular plants, the root-shoot distinction and the stem-leaf distinction have become blurred several times due to developmental changes, resulting in organs with unique combinations of features. This happened, for example, in the bladderworts 0Utricularia, Lentibulariaceae). When focusing on the `leaf', the FAM Approach is identical to Arber's `partial-shoot theory of the leaf' and Sinha's `leaf shoot continuum model'. A compound leaf can repeat the developmental pathway of the whole shoot, at least to some degree. For example, compound leaves of Chisocheton 0Meliaceae) with indeterminate apical growth and three- dimensional branching may be seen as developmental mosaics sharing some growth processes with whole shoots! We focus here on the FAM Approach because this perspective is especially promising for developmental geneticists studying ¯owering and other vascular plants. # 2001 Annals of Botany Company Key words: Review, body plan, developmental mosaics, leaf development, history of botany, homeosis, homeotic genes, Lentibulariaceae, morphological evolution, process morphology, stipules, Utricularia, ¯owering plants. INTRODUCTION Arberian Morphology 0 FAM Approach). `Arberian' refers to Agnes Arber and her way of thinking1. A special Agnes Arber )1879±1960), a giant in the history of botany )1) focus will be on papers published by Ge rard Cusset, Rolf Sattler and their colleagues propagating `continuum The year 2000 was the 50th anniversary of the publication of morphology', which is closely related to the FAM Approach Agnes Arber's book, The natural philosophy of plant form 0e.g. Sattler, 1996). New results in comparative morphology 01950). This book, and many of her earlier publications, were and developmental genetics speak in favour of the heuristic milestones on the way to a more open and dynamic approach value of the FAM Approach, as will be shown in this review. to plant morphology and developmental genetics, summar- In her writings, Agnes Arber anticipated various new ized in Sattler's 02001) contribution in this issue of Annals of explanatory models for vascular plant development pro- Botany. Since Arber's death in 1960, new methods and pers- posed by molecular geneticists. The fuzzy meaning of pectives have allowed a more dynamic and a more holistic structural categories in Utricularia and other vascular plants approach to the study of plant form. Nevertheless, some of will be discussed, putting emphasis on the heuristic value of Arber's hypotheses survived the decades and are still Arber's `partial-shoot theory of the leaf'. Cross-references refreshing our minds while we look for new ideas about the allow the reader to browse through the 29 sections evolutionary development of vascular plants. This review [labelled 1±29] to get the most out of this paper. covers examples from Agnes Arber's works 0published between 1920and 1957) as well as more recent publications giving credit to Arber's perspective, which is called Fuzzy 1We use the adjective `Arberian' similarly to already existing terms such as `Aristotelian' 0according to the philosophical school of * For correspondence. Fax 00 41 1634 8403, e-mail rutishau@ Aristotle), `Darwinian' 0in the sense of Charles Darwin and his systbot.unizh.ch followers), or `Victorian' 0pertaining to Queen Victoria). 0305-7364/01/121173+30 $35.00/00 # 2001 Annals of Botany Company 1174 Rutishauser and IslerÐFuzzy Arberian Morphology FIG. 1. A lesson in perspectivism and as-well-as thinking. Street-car in the city of ZuÈ rich announcing `I am also a ship' 0see section 3). [Copyright by ZuÈ rcher Verkehrsverbund, ZuÈ rich, Switzerland.]. `The algorithmic beauty of plants'ÐRepetition and a developing whole. This can be observed in individuals of self-similarity )to some degree) )2) Sambucus nigra 0Fig. 3) and Phellodendron amurense 0Fig. 4) when some or all ®rst order lea¯ets 0pinnae) repeat Branching and repetition of developmental units 0cells, the branching pattern of the normally once-pinnate leaf. meristems, modules) are omnipresent in the plant kingdom. Arber 01941, 1950) described many examples of vascular Mathematical algorithms based on fractal geometry and L plants showing repetition during growth and development. systems allow branching patterns to be simulated The repeated unit can be totally identical to the one already 0e.g. Prusinkiewicz and Lindenmayer, 1990). Examples of formed 0i.e. complete repetition of a developmental path- self-maintenance and auto-reproduction at the cellular and way), or the structures formed afterwards may repeat the meristem level are provided by Barlow et al. 02001).At preceding ones only to some degree 0i.e. partial repetition of higher levels, the complex organization of branching in a developmental pathway) while deviating in other features. ¯owering plants can be understood as the repetition of Arber's work already implies the holographic paradigm: the modules. Instead of producing a single ¯ower, an individual whole is built up of the parts in such a way that each part ¯oral meristem can branch continuously giving rise to a bears something of the whole within it, as stressed by complex in¯orescence with many ¯owers 0Fig. 2: Nymphaea Kircho 02001) and Sattler 02001). The reiteration at prolifera). Developmental geneticists are gaining a better dierent size scales 0i.e. self-similarity) is reminiscent of understanding of pattern repetition 0reiteration) at dierent fractal geometry in which shapes are repeated at ever levels of structural complexity. Thus, there are develop- smaller scales 0McLellan, 1999). mental parallels between ¯ower level 0as a subsystem) and in¯orescence level 0as a system). By examining MADS box genes, Yu et al. 01999) have shown that gene activities found during ¯ower initiation are also found during early PHILOSOPHICAL BASICS development of the head-like in¯orescences of Asteraceae. This could explain why in certain taxa simple ¯owers and Perspectivism and the advertisements in the ZuÈrich public compound `¯owers' 0i.e. in¯orescences) are quite similar to transport system )3) each otherÐ`a resemblance sometimes carried into the If you visited ZuÈ rich in 2000 and 2001 you would have seen minutest details of form and coloration' 0Arber, 1947 street-cars bearing the message: `I am also a ship' 0Fig. 1). p. 233). Travelling on Lake ZuÈ rich, you may have been puzzled by Arber was convinced that the principle of repetition is ships announcing: `I am also a train'. Riding local trains to found everywhere in multicellular plants. Focusing on the suburbs, you could also have read the notice on the vascular plants, Arber was puzzled by the fact that some engine: `I am also a bus'. Not understanding the ®gurative steps of the developmental pathway of a whole shoot 0i.e. meaning of these sentences, foreign tourists may have leafy stem) can be repeated within a compound leaf. wondered whether the Swiss were crazy. No! They had just According to Arber 01950p.125) `a typical leaf is a shoot learnt a lesson in `as-well-as thinking'! The metaphorical in which the apex is limited in its power of elongation and in meaning of these sentences is obvious. As a passenger on its radiality'. Thus, Arber 01941, 1950) proposed the partial- the ZuÈ rich public transport system you need just a single shoot theory of the leaf in vascular plants, based on ideas ticket which is valid for all types of public transport. You already formulated in the 19th century 0see ¯owchart of can switch between street-cars, buses, trains and ships as ideas in Fig. 40). This theory was recently discussed under long as your ticket is valid. The philosophical background the label `leaf shoot continuum model' 0Sinha, 1999; Hofer of the ZuÈ rich public transport advertisements is known as et al., 2001). It is consistent with Fuzzy Arberian perspectivism, which coincides with as-well-as thinking. Morphology 0Table 1; see section 21). Compound leaves The concepts `street-car' and `ship' are overlapping when may repeat in each part what they have already produced
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