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The Developmental Basis of an Evolutionary Diversification of Female Gametophyte Structure in Piper and Piperaceae

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The Developmental Basis of an Evolutionary Diversification of Female Gametophyte Structure in Piper and Piperaceae Annals of Botany 103: 869–884, 2009 doi:10.1093/aob/mcp011, available online at www.aob.oxfordjournals.org The developmental basis of an evolutionary diversification of female gametophyte structure in Piper and Piperaceae Eric N. Madrid and William E. Friedman* University of Colorado, Department of Ecology and Evolutionary Biology, Boulder, CO 80309, USA Received: 7 November 2008 Returned for revision: 3 December 2008 Accepted: 5 December 2008 Published electronically: 6 February 2009 † Background and Aims Fritillaria-type female gametophyte development is a complex, yet homoplasious devel- opmental pattern that is interesting from both evolutionary and developmental perspectives. Piper (Piperaceae) was chosen for this study of Fritillaria-type female gametophyte development because Piperales represent a ‘hotspot’ of female gametophyte developmental evolution and have been the subject of several recent molecular phylogenetic analyses. This wealth of phylogenetic and descriptive data make Piper an excellent candidate for inferring the evolutionary developmental basis for the origin of Fritillaria-type female gametophytes. † Methods Developing ovules of Piper peltatum were taken from greenhouse collections, embedded in glycol methacrylate, and serially sectioned. Light microscopy and laser scanning confocal microscopy were combined to produce three-dimensional computer reconstructions of developing female gametophytes. The ploidies of the developing embryos and endosperms were calculated using microspectrofluorometry. † Key Results The data describe female gametophyte development in Piper with highly detailed three- dimensional models, and document two previously unknown arrangements of megaspore nuclei during early development. Also collected were microspectrofluorometric data that indicate that Fritillaria-type female gametophyte development in Piper results in pentaploid endosperm. † Conclusions The three-dimensional models resolve previous ambiguities in developmental interpretations of Fritillaria-type female gametophytes in Piper. The newly discovered arrangements of megaspore nuclei that are described allow for the construction of explicit hypotheses of female gametophyte developmental evolution within Piperaceae, and more broadly throughout Piperales. These detailed hypotheses indicate that the common ancestor of Piperaceae minus Verhuellia had a Drusa-type female gametophyte, and that evolutionary transitions to derived tetrasporic female gametophyte ontogenies in Piperaceae, including Fritillaria-type female gameto- phyte development, are the consequence of key nuclear migration and patterning events at the end of megasporogenesis. Key words: Piper, Piperaceae, Piperales, magnoliids, female gametophyte, development, evolution, three- dimensional reconstruction. INTRODUCTION Asteraceae (Fagerlind, 1939; Maheshwari and Srinivasan, 1944; Howe, 1964). A modified form of this ontogeny, Perhaps one of the most complex developmental sequences Plumbagella-type female gametophyte development, is reported expressed among angiosperm female gametophytes is the in Plumbagella (Dahlgren, 1915; Haupt, 1934; Fagerlind, 1938; Fritillaria-type ontogeny. This developmental pattern, which Boyes, 1939). begins with a tetrasporic coenomegaspore, involves a free- The repeated origin of such a complex ontogenetic sequence nuclear division in which three haploid megaspore nuclei initiate makes Fritillaria-type female gametophyte development an mitosis and produce two triploid restitution nuclei (instead of six ideal subject for an evolutionary developmental investigation. haploid nuclei; Bambacioni, 1928; Maheshwari, 1950; Johri Yet, basic knowledge of this ontogeny in angiosperms is et al., 1992; Batygina, 2006). As far as is known there is no limited, and the developmental basis for the origin of this example of mitosis in any group of eukaryotes in which female gametophyte type has never been explored. Although fewer nuclei are present after a mitotic division is initiated several lineages of angiosperms contain members with than before. In spite of the peculiarity of this division, Fritillaria-type female gametophyte development (see above), Fritillaria-type female gametophyte development appears to it was decided to study this ontogeny within Piperales. There have independently evolved in angiosperms at least seven are reports in Piperales of transitions from monospory to times: in Liliaceae (Bambacioni, 1928; Romanov, 1957), bispory (Johnson, 1900c; Quibell, 1941; Raju, 1961) and tetra- Piperaceae (Kanta, 1962; Nikiticheva, 1981; Prakash and Kin, spory (Johnson, 1900a, b, 1914; Swamy, 1944; Lei et al., 1982; Prakash et al., 1994), Plumbaginaceae (Dahlgren, 1916; 2002) and at least six of the ten standard female gametophyte Haupt, 1934), Euphorbiaceae (Carano, 1925, 1926; Tateishi, ontogenies recognized by Maheshwari (1950) are known to 1927; Kapil, 1961), Cornaceae (D’Amato, 1946; Chopra and exist in Piperales (Fig. 1) (Maheshwari, 1950; Davis, 1966; Kaur, 1965), Tamaricaceae (Mauritzon, 1936; Sharma, 1939, Johri et al., 1992; Batygina, 2006; Madrid and Friedman, 1940; Battaglia, 1941, 1943; Johri and Kak, 1954) and 2008). Piperales has also been the subject of several recent * For correspondence. E-mail [email protected] phylogenetic analyses (Nickrent et al., 2002; Zanis et al., 2003; # The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 870 Madrid & Friedman — Female gametophyte structure in Piper Monosporic A 8-nucleate Polygonum-type Bisporic B 8-nucleate Allium-type Tetrasporic C 8-nucleate Adoxa-type Tetrasporic D 16-nucleate Peperomia-type Tetrasporic E 16-nucleate Penaea-type Tetrasporic F 16-nucleate Drusa-type Tetrasporic G 8-nucleate Fritillaria-type F IG. 1. Selected monosporic (A), bisporic (B) and tetrasporic (C–G) patterns of female gametophyte development from Maheshwari (1950). Each of these ontogenies is found in Piperales. Neinhuis et al., 2005; Wanke et al.,2007a, b). This wealth of up to 3 m in height, and has stems with distinct nodes that may developmental diversity and robust phylogenetic sampling become woody at the base. The leaves are peltate and about make Piperales an excellent candidate in which to study female 40 cm across. Developing infloresences of P. peltatum were gametophyte developmental evolution, and Piper an informative collected from greenhouse collections at the University of clade in which to study the evolution of Fritillaria-type female Colorado in the springs and summers of 2006 and 2007. gametophyte development. Each inflorescence was immersed in a modified PIPES All members of the genus Piper reported until now show the buffer (60 mM PIPES, 25 mM HEPES, 5.4mM CaCl2, Fritillaria-type (Joshi, 1944; Swamy, 1944; Maugini, 1953; 1.97 mM MgCl2) where it was dissected into smaller pieces Murty, 1959; Yoshida, 1960; Kanta, 1962; Nikiticheva, that each contained about 12 flowers. These infloresence por- 1981; Prakash and Kin, 1982; Prakash et al., 1994) and tions were then chemically fixed. female gametophyte development in Piper peltatum was investigated. Nuclear positioning, nuclear migration and nuclear division throughout the syncytial stages of female Histology gametophyte development were documented. The ploidy levels of several cell types within the mature female gameto- Developing flowers were placed in a fixative solution con- phyte and the seed were also measured. The goals were to taining either 3:1 95 % ethanol:acetic acid or 4 % paraformal- . characterize better the specific developmental processes that dehyde, 2 5 % gluteraldehyde, and 4 % acrolein in a modified are associated with female gametophyte development in PIPES buffer (above) for 12 h. Specimens were dehydrated in Piper, and use these detailed ontogenetic insights to generate a graded ethanol series, infiltrated, embedded with glycol hypotheses about how diverse patterns of female gametophyte methacrylate (JB-4 embedding kit; Polysciences, Warrington, development may have evolved in Piperaceae. PA, USA), and serially sectioned into 5-mm-thick ribbons using a Microm HM330 rotary microtome and glass knives. Sections from flowers that were fixed in the 3:1 sol- MATERIALS AND METHODS ution were stained with a solution of 0.2 mgmL21 of 40,6-diamidino-2-phenylindole (DAPI) and 0.1mgmL21 phy- Plant collection lenediamine in 0.05 M Tris (pH 7.2). Sections from flowers that Piper peltatum is a herbaceous shrub that is native to Mexico, were fixed with paraformaldehyde, gluteraldehyde and ethanol Central America and South America. Piper peltatum may grow were stained with 0.1 % toluidine blue. All slides were viewed Madrid & Friedman — Female gametophyte structure in Piper 871 with a Zeiss Axiophot microscope using brightfield, differen- template to identify equivalent female gametophyte nuclear tial interference contrast, and epifluoresence optics. Digital positioning events in other previously studied species of micrographs were taken with a Zeiss Axiocam digital Piperaceae. Character distribution and estimation of ancestral camera. Post-processing of all images was done with the and derived states were inferred using the programs Adobe Creative Suite 2 software package (San Jose, CA, MacClade (Maddison and Maddison, 1992) and Mesquite USA). Digital image manipulations were restricted to pro- (Maddison and Maddison, 2008). Characters were traced cesses that applied to the entire image unless otherwise using the
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