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ASBP769K.QXD 12/2/06 6:33 PM Page 271 Vol. 75, No. 4: 271-279, 2006 ACTA SOCIETATIS BOTANICORUM POLONIAE '8" PHYLLOTACTIC PATTERN FORMATION IN EARLY :TAGES OF CACTUS ONTOGENY BDYTA M. GOLA Institute of Plant Biology, University of Wroc³aw Kanonia 6/8, 50-328 Wroc³aw, Poland e-mail: [email protected] (Received: February 27, 2006. Accepted: May 12, 2006) ABSTRACT Representatives of the family Cactaceae are characterized by a wide range of phyllotaxis. To assess the origin of this diversity, early stages of phyllotactic pattern formation were examined in seedlings. The analysis of the se- quence of areole initiation revealed intertribal differences. In seedlings from the Trichocereeae (Gymnocalycium, Rebutia) and Notocacteae (Parodia) tribes, two opposite cotyledonal areoles developed as the first elements of a pattern. Usually, next pair of areoles was initiated perpendicularly to cotyledonal areoles, starting the decussate pattern. This pattern was subsequently transformed into bijugate or into simple spiral phyllotaxis. In seedlings from the Cacteae tribe (Mammillaria and Thelocactus), cotyledonal areoles were never observed and the first are- oles always appeared in the space between cotyledons. It was either areole pair (mainly in Mammillaria), starting a decussate pattern, or a single areole (mainly in Thelocactus) quickly followed by areoles spirally arranged, usu- ally in accordance with the main Fibonacci phyllotaxis. Differences in the initial stages of pattern formation do not fully explain the phyllotaxis diversity in mature cacti. Only two, the most common phyllotactic patterns occurred in the early development of studied seedlings, i.e. the main Fibonacci and the decussate pattern. Discrepancy in the range of phyllotactic spectra in seedlings and in mature plants suggests that phyllotaxis diversity emerges during further plant growth. Initial phyllotactic trans- formations, occurring already in the very early stages, indicate great plasticity of cactus growth and seem to sup- port the hypothesis of the ontogenetic increase of phyllotaxis diversity due to transformations. FBD WORDS: phyllotaxis, phyllotactic transformation, cactus ontogeny, Cactaceae. INTRODUCTION spiral phyllotaxis, areoles are conspicuously and regularly arranged and can be easily connected by spiral lines for- The evolutionary modification of morphogenetic proces- ming two oppositely winding sets. Numbers of such inter- ses, adapting cacti to diversified and often severe environ- secting spirals represent subsequent elements of a phyllo- ments, has lead to emergence of the variety of morphologi- tactic series in which every element is the sum of two pre- cal forms in the family Cactaceae (Barthlott and Hunt ceding numbers. Two consecutive members of a phyllotac- 1993; Anderson 2001; Wallace and Gibson 2002; Mauseth tic series, corresponding to the number of spirals being in 2004). Within Cactaceae, there are shrubs and gigantic a contact at the stem surface, are called a contact parasti- candelabra-like trees, cylindrical or globular plants gro- chy pair (Church 1904). The pair identifies unequivocally wing alone or in compact clusters, flattened stems and tiny the phyllotactic series to which it belongs and a pattern rosettes (e.g., Anderson 2001). Likely, this variety of mor- expression. It also defines indirectly the configuration of phological forms may facilitate diverse distribution of lea- the ontogenetic spiral when orientation of opposite parasti- ves, and thus, formation of different phyllotactic patterns. chies is determined (Zagórska-Marek 1994). The most The phenomenon of phyllotaxis refers to regular patterning common patterns are identified by contact parastichy pairs of lateral organs in a shoot, e.g. areoles (=modified axillary belonging to the main Fibonacci series: 1, 2, 3, 5, 8, 13, buds or shoots; Boke 1953, 1961; Freeman 1970) in case 21, Other spiral patterns are mostly occasional in seed of cacti. Areoles, ontogenetically related to developing lea- plants (e.g., Schwabe 1984; Zagórska-Marek 1985, 1987, ves (Boke 1953, 1954, 1961; Mauseth 1980, 2004; Gibson "##-./ and Nobel 1986; Salgado Terrazas and Mauseth 2002), re- Despite quite intensive studies on cactus specific mor- flect positions of vestigial leaves and can be considered as phological features (e.g., Boke 1953, 1954, 1957, "#6"% elements of a phyllotactic pattern. In most of cacti with Mauseth 1978a, b, 1980, 2004), there is no detailed survey ASBP769K.QXD 12/2/06 6:33 PM Page 272 '8' INITIAL PHYLLOTAXIS IN CACTI Gola E.M. or systematic screening of phyllotactic patterns. Neverthe- MATERIALS AND METHODS less, information available in literature, although scarce, suggests an existence of pattern diversity within the family Genera representing different tribes of the subfamily Cactaceae related indirectly to taxonomic position of an in- Cactoideae (Cactaceae) were selected to compare the initial vestigated plant. For instance, in leaf-bearing shrubs repre- stages of phyllotactic pattern formation. Their choice was senting the primitive subfamily Pereskioideae (Boke "#5-% based on differences in phyllotaxis occurring in mature Bailey 1960; Gibson 1976), as well as morphologically di- plants. This is why genera Mammillaria and Rebutia were verse cacti from the subfamily Opuntioideae (Bailey "#6-% analyzed in a first place their phyllotactic patterns were Freeman 1970; Gibson 1976; Gibson and Nobel 1986), the previously screened (Gola 1997). The choice of other cac- most common phyllotactic pattern the main Fibonacci J tus species was partly limited by the seed availability. Se- is reported. Surprisingly, this pattern is frequently maintai- eds were obtained from the cactus collection of the Botani- ned during formation of flat cladodes in opuntias (Gibson cal Garden of University of )roc³aw and from the private 1976; Gibson and Nobel 1986) despite changes of the sho- collection of Ms. Zofia Pyjek. ot symmetry. Within the more succulent subfamily Cactoi- Regarding the most recent changes in classification and deae, distichy characterizes majority of flattened stems, nomenclature within the family Cactaceae, a majority of especially in genus Epiphyllum (the Hylocereee tribe; Rauh cactus names is given according to the International Organi- 1979) whereas spiral phyllotaxes, conspicuous due to zation for Succulent Clant Study (IOS) checklist (Hunt "##'% a dense areole packing and a limited internodal growth Anderson 2001). Synonyms of chosen species are available (Gibson and Nobel 1986), are typical for globular and cy- at the website: www.cites.org. In few cases, obtained Mam- lindrical cacti. Among these, the short columnar Echino- millaria seeds belonged to taxa which species names were psis representing the tribe Trichocereeae was possibly the not accepted or only provisionally accepted by the IOS. first genus for which few unusual phyllotactic patterns we- Such species are marked in the list by an asterisk. Higher re reported (Church 1904). Church, in his classical work on units, such as tribes and subfamilies, are distinguished based phyllotaxis (1904), showed the extensive range of patterns on the classification of Barthlott and Hunt (1993) recently in Echinopsis, comprising of either true whorls or typical supported by molecular data (Wallace and Gibson 2002). spiral patterns with much the same numbers in a contact Below is given the complete list of cactus species used parastichy pair, e.g. 6:6, 6:7, 6:8, etc. Cactus adaptation to during the study. Letters in square brackets show the sour- harsh environmental conditions was a suggested reason for ce of seeds: the Botanical Garden of University of )ro- occurrence of such patterns (Church 1904). Rebutia, ano- c³aw LBG] or Ms. Z. Pyjeks collection [ZP]. An asterisk ther genus from the Trichocereeae tribe, shares phyllotaxis before Mammillaria species name indicates not known/not variety 1ith Echinopsis. The broad spectrum of various accepted by the IOS position of the taxon. phyllotactic patterns, including many infrequent accessory ones, is characteristic of Rebutia/ Patterns other than the Tribe Trichocereeae: main Fibonacci often co-dominate or even prevail in this Gymnocalycium bodenbenderianum (Hoss. ex Berg.) genus (Gola 1997). For Mammillaria, belonging to the tri- Hill [BG]; G. knebelii Friè [BG] at present it is a doubt- be Cacteae, spiral areole arrangements are so conspicuous ful species; G. ochoterenae Backeb.[BG]; Rebutia deminu- that the numbers of connecting spirals (= parastichies) have ta (Weber) Br. P R. [BG]; R. fiebrigii (Gürke) Br. P R. ex frequently been given in plant descriptions (Britton and Bailey [BG]; R. pseudodeminuta Backeb. [BG]. Rose 1923; Craig 1945; Krainz 1956-75; Backeberg "#6"% Rauh 1979). Comparing with the extensive pattern range in Tribe Notocacteae: the similar in form tribe Trichocereeae, it can be quite sur- Notocactus eugeniae Vliet [BG] provisionally accepted prising that, in Mammillaria, again the main Fibonacci is species name in Hunt (1992), although the entire genus is almost exclusively occurring pattern. Even the ontogenetic currently included into Parodia (Hunt 1992, Anderson changes in this genus alter the pattern expression only (Go- 2001); Parodia ottonis (Lehm.) Taylor [ZP]. la 1997). Still, observations of the changeable numbers of ribs in Ferocactus and few genera belonging to this group Tribe Cacteae: (Gibson and Nobel 1986) as well as the numbers of parasti- RMammillaria flavovirens Salm-Dyck [ZP]; RM. fuscata chies in one set in few other