Bradleya 22/2004 pages 9 – 14 Resolving the phylogenetic placement of Blossfeldia liliputana (Cactaceae): reticulate evolution, chloroplast inheritance, and graft-chimeras Root Gorelick School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, U.S.A. (email: [email protected]). Summary: The perplexing ancestral phylogenetic und solche Phylogenien werden durch reticulate placement of Blossfeldia liliputana based on Evolution verkompliziert. Das Problem mit der chloroplast DNA can possibly be explained by (1) zweiten Hypothese liegt darin begründet, dass the hybrid origin and uniparental inheritance of die meisten kultivierten Exemplare von chloroplasts in Blossfeldia and (2) the DNA Blosssfeldia gepfropft sind, und dass sich samples originating from the grafting stock niemand sicher ist, ob sich nicht leicht upon which the Blossfeldia was cultivated. The Pfropfchimären bilden. Solange diese beiden problem with the first of these hypotheses is that Hypothesen nicht ausgetestet worden sind, wird nobody knows whether chloroplasts are inherited Blossfeldia am Besten als hochabgeleitetes Glied from one or both parents in Blossfeldia nor how der Unterfamilie Cactoideae betrachtet, wie es this inheritance pattern may have changed in auch von den morphologischen Daten gestützt ancestors of Blossfeldia. Phylogenetic recon- wird. structions of species trees assume that the mode of organelle inheritance is known, and these phy- Introduction logenies are confounded by reticulate evolution. With trepidation, Nyffeler (2002) proposed that The problem with the second hypothesis is that Blossfeldia liliputana Werdermann is a basal most cultivated specimens of Blossfeldia are member of the subfamily Cactoideae Schumann. grafted and nobody is certain whether or not Yet, phylogenies based exclusively on morpho- these readily form graft-chimeras. Until both logical characters place Blossfeldia liliputana as hypotheses are tested, B. liliputana should be a highly derived taxon. Evidence for this place- considered a highly derived member of the sub- ment comes from such notable characters as family Cactoideae, as indicated by morphological having fewer stomata than any other terrestrial data. plant (other than parasites and aquatics), stomata that are sunken in areolar pits, Zusammenfassung: Die auf Grund von extremely thin epidermis, and lack of a hypo- Chloroplasten-DNA-Untersuchungen rätselhafte dermis (Barthlott & Porembski, 1996). phylogenetische Stellung von Blossfeldia The present consensus position is that liliputana kann möglicherweise (1) durch einen Blossfeldia Werdermann is in the tribe hybridogenen Ursprung von Blossfeldia und uni- Notocacteae Buxbaum, a position largely founded parentale Chloroplastenvererbung erklärt on a superficial resemblance to Parodia werden, oder (2) weil Chloroplasten untersucht Spegazzini and Frailea Britton & Rose, with wurden, die aus der Propfunterlage der kul- somewhat similar seeds and a hairy testa (Hunt tivierten Pflanzen stammen. Das Problem mit et al., 1990). Seeds, however, provide the only der ersten dieser beiden Hypothesen ist die similarity. Blossfeldia lacks several important Tatsache, dass niemand weiss, ob die characters of Notocacteae, such as presence of Chloroplasten bei Blossfeldia nur durch eine oder acicular bristles in the receptacle areoles. durch beide Elternpflanzen vererbt werden, und Blossfeldia flowers are much reduced in their ob dieses Vererbungsmuster bei Vorläufern von structures and seem to have more in common Blossfeldia anders gewesen sein könnte. with tribe Trichocereeae Buxbaum than with Phylogenetische Rekonstruktionen von Notocacteae. Blossfeldia flowers have a well- Artverwandtschafen gehen davon aus, dass der defined cauline zone, with a mass of white kinked Modus der Organellenvererbung bekannt ist, uniseriate trichomes at their base, which is not Bradleya 22/2004 9 found in tribe Notocacteae, but it is present in http://mobot.mobot.org/W3T/Search/ipcn.html) nal parent, or both. Three prickly pears (Opuntia tively small plants, especially for those taxa with subtribe Rebutiinae of the tribe Trichocereeae, and Ramsey & Schemske (1998) show that ane- basilaris Engelmann & Bigelow, O. engelmannii more than four sets of homologous chromosomes e.g. Rebutia Schumann sensu stricta (Mottram, uploidy is rare or absent in cacti. Salm-Dyck, O. vulgaris Miller) and one hedgehog (Pinkava et al., 1998), with the notable exception pers. comm.). Blossfeldia fruits also share many Intergeneric hybrids do occur in the cactus (Echinocereus engelmannii (Parry ex of Opuntia sensu stricta in which polyploids morphological characters with subfamily Cactoideae, albeit rarely. The tetraploid Engelmann) Rümpler) have strictly maternal appear to be more robust (Pinkava, 2002). The Rebutiinae, such as fleshy scales overtopping the Bergerocactus emoryi (Engelm.) Britton & Rose inheritance. Two epiphytic cacti, both in the evidence is therefore equivocal for whether poly- rim of the umbilicus (Mottram, pers. comm.). hybridizes with both the diploid Myrtillocactus tribe Rhipsalideae A. P. de Candolle – Hatiora ploidy results in larger, smaller, or equal sized Thus, there is morphological evidence for place- cochal (Orcutt) Britton & Rose to form the hexa- gaertneri (Regel) Barthlott and Schlumbergera cacti. ment of Blossfeldia in either of the two closely ploid xMyrtgerocactus lindsayi Moran and the truncata (Haworth) Moran) – have many chloro- Rapid genetic and epigenetic changes follow- related tribes Notocacteae and Trichocereeae, tetraploid Pachycereus pringlei (S. Watson) plasts in their sperm cells and therefore most ing polyploid formation are believed to disrupt neither of which is generally considered ancestral Britton & Rose to form the octaploid likely have chloroplasts inherited from both development (Osborn et al., 2003) and could within the Cactoideae. xPacherocactus orcuttii (K. Brandegee) parents (Corriveau & Coleman, 1988). thereby explain general size reductions. Genetic Why did Nyfeller’s (2002) analysis result in a G.D.Rowley (Moran, 1962a, b; Pinkava et al., Furthermore, these two species do not have changes include gains or losses of DNA frag- glaringly anomalous phylogenetic position for B. 1998). The diploid Hylocereus undatus (Haworth) dimorphic sperm cells, providing further evi- ments (Osborn et al., 2003). The developmental liliputana amongst the Cactoideae? His phy- Britton & Rose has been hybridized with the dence of biparental inheritance (Corriveau, pers. pathways of most organisms, including plants, logeny was based solely on trnK/matK and trnL- tetraploid Selenicereus megalanthus (Schumann comm.). With dimorphism, one sperm cell might are largely regulated by epigenetic signals. trnF sequences of chloroplast DNA. Gorelick ex Vaupel) Moran to form a viable hexaploid (Tel- contain no chloroplasts and always end up fer- Epigenetic signals are often mediated by mole- (2002) proposed that the problem is that B. Zur et al., 2003). I hypothesize that the hexaploid tilising the egg cell, while the sperm cell with cules that are attached to DNA, such as cytosine liliputana is of hybrid origin and that chloroplast B. liliputana was similarly formed via hybridiza- chloroplasts always fertilises the polar nuclei. It methylation, heterochromatin formation, and DNA is only maternally inherited. Here, I review tion of a diploid and tetraploid parent. My sus- is not known whether chloroplast inheritance is histone acetylation (Holliday & Pugh, 1975; and critique that argument, noting that until picion is that both parents were members of the uniparental or biparental in B. liliputana or any Riggs, 1975; Russo et al., 1996). These epigenetic further cytological or molecular work with B. Notocacteae or Trichocereeae, which have several other member of the tribes Notocacteae or signals act by suppressing gene products (see liliputana is done, we will not know whether that tetraploid lineages (Pinkava et al., 1998). Trichocereeae. Gorelick, 2003a, b for review of mechanisms). argument is valid. I also discuss the mechanisms Most flowering plants have chloroplasts that Why might the fluidity of modes of organelle The proportion of the genome modified by epige- and equivocal evidence for Blossfeldia morphol- are solely inherited from the female parent inheritance over evolutionary time pose a netic signals, especially of cytosine methylation ogy arising via allopolyploidy. Additionally, I (Mogensen, 1996). Hence phylogenies based on problem in the phylogenetic reconstruction of the and heterochromatin, increases dramatically fol- propose an alternative hypothesis based on uniparentally inherited chloroplast DNA would Cactaceae? One reason chloroplast DNA is used lowing formation of a new polyploid (Matzke & graft-chimeras for why analysis of chloroplast only reflect half of the ancestry – the female half in phylogenetics of cacti is that organelle DNA Matzke, 1998; Liu et al., 2000), thereby disrupt- DNA may have incorrectly ascribed the phyloge- – of any plant of allopolyploid origin. Gorelick evolves much quicker than nuclear DNA because ing regulatory pathways. Such disruptions could netic placement of B. liliputana: The chloroplast (2002) argued that B. liliputana could then have organelle genomes are haploid. This means that mean that only neotenous (paedomorphic; repro- DNA sampled may have been from the stock a highly derived paternal parent and an ances- a maternally inherited haploid genome will have ducing in a juvenile state) individuals could rather than