P. Barry Tomlinson

Cell longevity and sustained primary growth in palm stems

Longevity, or organismal life span, is determined largely by the period over which constituent cells can function metabolically. Plants, with modular organization (the ability continually to develop new organs and tissues) differ from animals, with unitary organization (a fixed body plan), and this difference is reflected in their respective life spans, potentially much longer in plants than animals. We draw attention to the observation that palm trees, as a group of monocotyledons without secondary growth comparable to that of lignophytes (plants with secondary growth from a bifacial cambium), retain by means of sustained primary growth living cells in their trunks throughout their organismal life span. Does this make palms the longest-lived trees because they can grow as individuals for several centuries? No conventional lignophyte retains living metabolically active differentiated cell types in its trunk for this length of time, even though the tree as a whole can exist for millennia. Does this contrast also imply that the long-lived cells in a palm trunk have exceptional properties, which allows this seeming immortality? We document the long-life of many tall palm species and their inherent long-lived stem cell properties, comparing such plants to conventional trees. We provide a summary of aspects of cell age and life span in animals and plants. Cell replacement is a feature of animal function, whereas conventional trees rely on active growth centers (meristems) to sustain organismal development. However, the long persistence of living cells in palm trunks is seen not as evidence for unique metabolic processes that sustain longevity, but is a consequence of unique constructional features. This conclusion suggests that the life span of plant cells is not necessarily genetically determined.

Variation in Leaflet Structure in Cycas (Cycadales: Cycadaceae): Does Anatomy Follow Phylogeny and Geography?

Premise of research. Cycas is the earliest-diverging extant lineage in the ancient order Cycadales, well separated phyletically from the other nine extant genera. Despite the ancient status of Cycas, all extant species are no more than 12 Myr old, and many extant species have become known only in recent decades. Given this context, a broad survey of variation in Cycas leaflet structure may show structural diversity that corresponds with and informs phylogeny and biogeography. Methodology. We investigated the leaflet anatomy of 48 Cycas species grown in a common garden to ascertain the variation of anatomical traits and compared this to available phylogenetic and geographic information to determine patterns in this variation. Pivotal results. We find a very strict anatomical bauplan within the genus and only limited qualitative variation in such features as epidermal cell type, stomatal structure, and extent of hypodermal specialization. Conclusions. Our findings thus sustain the well-accepted monophyly of the genus with a consistent series of synapomorphic features. The most distinctive character is the existence of pits within the outer wall of the epidermis, a feature almost unique for gymnosperms. Unlignified midrib fibers appear to be a unique synapomorphy for Australian and Papuan members of section Cycas. Encrypted stomata and epidermal cell shape confirm a close relationship between sections Asiorientales and Panzhihuaenses and suggest a distinction from section Stangerioides but do not show a clear geographic relationship. Mucilage canals are found only within section Stangerioides. No unique synapomorphy exists for section Indosinenses, but variation in epidermal cell shape appears correlated to the presence of an adaxial hypodermis in section Indosinenses.

Aspects of Vessel Dimensions in the Aerial Roots of Epiphytic Araceae

We measured vessel dimensions, most significantly vessel length, in the aerial roots of four epiphytic aroids using a digital camera to photograph sequential sections. Pendulous aerial roots in Araceae can grow from the forest canopy and so reach considerable length (>30 m) before they contact the ground, branch, and become anchored. In the free‐hanging state, the length over which tissue maturation occurs can exceed 1 m. We show that the distinctive medullary vessels do not anastomose and each series of vessels, end to end here termed a “pipe,” must differentiate without interruption throughout the length of the root and do not become fully functional until the ground is reached. Measurements show different vessel parameters, including vessel overlap at each vessel end, which is not usually considered in estimates of hydraulic conductivity. Our method of measurement is simple and direct and shows the topographic relation of all vessels in a single organ, suggesting that vessels in long plant organs can be measured precisely, giving results of value in considering the hydraulic properties of xylem elements.

DEVELOPMENT OF WOODY BRANCH ATTACHMENTS IN SCHEFFLERA (ARALIACEAE OR APIACEAE)

Attachment of branches in Schefflera is unusual in that it involves fingerlike woody extensions that originate in the cortex and pass gradually into the woody cylinder of the parent shoot. We tested the hypothesis that these structures could be roots since Schefflera is a hemi-epiphyte with aerial roots. These branch traces originate by secondary development in the many leaf traces (LTs) of the multilacunar node together with associated accessory traces. In the primary condition, the LTs may be described as cortical bundles. Leaves are long persistent and can maintain a primary stem connection across a broad cylinder of secondary xylem. Under the stimulus of branch development, the LTs form a template for secondary vascular development. Because the LT system is broad, with many traces, the branch attachment is also broad. The fingerlike extensions are attached to the surface of the woody cylinder of the parent stem but are progressively obscured as a continuous cambium is formed. Bark tissues are included within the branch axil because of the extended cortical origin of the initial attachment. The results are discussed in the context of branch-trunk unions in tropical plants, an important component of canopy development.

Wollemia nobilis (Araucariaceae): Branching, vasculature and histology in juvenile stages.

We present a preliminary description of the morphology and anatomy of contrasted axes in the recently discovered conifer Wollemia nobilis, based on clonally propagated material. The novelty of this discovery and the trees size and rarity has led to global interest and a comprehensive and successful conservation program. Our results should serve as a model on which future studies of this tree and other members of the Araucariaceae can be based. The specimens studied are mimics of the architecture of the mature tree, with precise distinction between orthotropic (= trunk) axes, which have radial symmetry (spiral phyllotaxy) and plagiotropic (= branch) axes with dorsiventral symmetry (as a modified decussate phyllotaxy). Trunk axes develop irregular pseudowhorls of branches that originate within the terminal bud by syllepsis, their extension coincident with that of the parent axis. The two kinds of axes show considerable anatomical differences, but are still based on the common feature of a single stelar-derived trace to each leaf that becomes subdivided in the cortex, a feature of the whole family. Trunk axes include extended cortical leaf and branch traces associated with abundant sclerenchyma, but branches have short cortical leaf traces, no branch traces, and limited sclerenchyma. Reiteration is limited and largely involves the formation of basal suckers on the trunk. Branches normally remain unbranched, but can do so most often when damaged. This study thus emphasizes the phenomenon of axis differentiation in conifers, which has been little investigated anatomically, but could be very important in the identification of fossils.

Phylogenetic and functional signals in gymnosperm ovular secretions

Background and Aims Gymnosperms are either wind-pollinated (anemophilous) or both wind- and insect-pollinated (ambophilous). Regardless of pollination mode, ovular secretions play a key role in pollen capture, germination and growth; they are likely also involved in pollinator reward. Little is known about the broad-scale diversity of ovular secretions across gymnosperms, and how these may relate to various reproductive functions. This study analyses the sugar and amino acid profiles of ovular secretions across a range of ambophilous (cycads and Gnetales) and anemophilous gymnosperms (conifers) to place them in an evolutionary context of their possible functions during reproduction. Methods Ovular secretions from 13 species representing all five main lineages of extant gymnosperms were sampled. High-performance liquid chromatography techniques were used to measure sugar and amino acid content. Multivariate statistics were applied to assess whether there are significant differences in the chemical profiles of anemophilous and ambophilous species. Data were compared with published chemical profiles of angiosperm nectar. Chemical profiles were placed in the context of phylogenetic relationships. Key results Total sugar concentrations were significantly higher in ovular secretions of ambophilous species than wind-pollinated taxa such as Pinaceae and Cupressophyta. Ambophilous species had lower amounts of total amino acids, and a higher proportion of non-protein amino acids compared with anemophilous lineages, and were also comparable to angiosperm nectar. Results suggest that early gymnosperms likely had ovular secretion profiles that were a mosaic of those associated with modern anemophilous and ambophilous species. Ginkgo, thought to be anemophilous, had a profile typical of ambophilous taxa, suggesting that insect pollination either exists in Gingko, but is undocumented, or that its ancestral populations were insect-pollinated. Conclusions Chemical profiles of ovular secretions of ambophilous gymnosperms show a clear signal of pollinator-driven selection, including higher levels of carbohydrates than anemophilous taxa, lower levels of amino acids, and the presence of specific amino acids, such as β-alanine, that are known to influence insect feeding behaviour and physiology.

Stem anatomy in the spiny american palm Bactris (Arecaceae-Bactridinae)

Bactris trunks are made entirely by long sustained primary growth so that mechanical properties develop progressively as the trunk matures. Anatomical features vary throughout the stem so that one small sample is a limited representation. This limits the use for stem histology with systematic purposes. We examined stem anatomy in 17 out of 73 species representing all major sub-generic groups. Stem features do not associate well with the subdivision of the genus. Distinctive structural and developmental features: are the presence of fiber strands independent of the vascular tissues, the modified ground parenchyma with a late formation of air-lacunae, and the early inception of the mechanically significant outer central cylinder. Cell expansion and fiber wall thickening develop as the stem ages, but vary in their expression in stems of different diameter. Our example thus provides an explanation for the difficulty of identifying the systematic position of fossil palm stems.

A Novel Type of Fiber in the Leaves of the Cycad Dioon

Premise of research. The extant genera of cycads (order Cycadales) can be readily distinguished by the anatomy of their leaflets. In particular, the genus Dioon possesses a unique cellulosic fiber type in the leaflet mesophyll, not found in any other genus. We examine living material of all 15 species of Dioon to confirm preliminary observations and provide details of wall structure in comparison with fibers in the leaf axis. Methodology. Unembedded sample material was sectioned on a sliding microtome transversely and longitudinally, and standard histochemical tests were utilized to identify cell types. SEM was utilized to analyze fiber anatomy. Maceration of samples provided cell types for comparison. Pivotal results. All species of Dioon have the same configuration of cell types in the leaflets, the most conspicuous element being elongated fibers with multilamellate cellulosic cell walls. Such fibers do not appear in the leaf axis. This fiber type is seemingly unique among all cycad genera. Conclusions. Dioon leaflets possess a fiber type of distinctive wall structure, unique among the extant cycads. This finding clarifies an earlier report in which such fibers were described as “gelatinous fibers.”

How red mangrove seedlings stand up: an answer for Cheeseman (2012)

In a recent paper, Cheeseman (2012) sought to determine “how red mangrove seedlings stand up”. He investigated how such viviparous seedlings become erect after they detach from the tree, usually float away, and finally become lodged in the substrate in a horizontal position. He carefully measured movements of seedlings grown in the greenhouse and dark room using video and time lapse techniques. He states: “Neither how this occurs nor possible ecological benefits and costs have previously been considered”. Unfortunately the author does not cite earlier references about this topic. This literature noted the distinctive morphological feature of the Rhizophora seedling, the basal hook, illustrated (Fig. 1) as long ago as the 17th century in Rumphius (17411755) which was recently translated by Beekman (2011). The basal hook was illustrated in Rhizophora mangle in Van Steenis (1958). This structure is the site of the erectionmechanism, rather than the more general curvature of the hypocotyl, that Cheeseman emphasized. The hook can be seen in most uprooted seedlings in the wild and its significance has been discussed by a number of authors (LaRue and Muzik 1954; Lawrence 1949). The idea that the projectile shape of the Rhizophora seedling facilitates self-planting is dismissed, e.g. as the “plunk hypothesis” disparaged by Egler (1948). Marking experiments have shown that few seedlings remain in the vicinity of a parent tree (Yamashiro 1961). They are widely dispersed (Davis 1940) and are mostly stranded in a horizontal position, hence the requirement for self-erection. Unfortunately, Cheeseman failed to cite publications which, in fact, answered his own question. Tomlinson and Cox (2000) demonstrated the existence of selferection in all genera of the mangrove Rhizophoraceae (tribe Rhizophoreae) and showed that the hook is the site of reaction fibres (tension wood fibres), distributed eccentrically, which provided the necessary, but localized leverage. Repeated experiments by Fisher and Tomlinson (2002) on Rhizophora mangle presented quantitative anatomical measurements which showed that the elongated hypocotyl moved from a horizontal to vertical position over a period of many weeks by means of asymmetrical formation of tension wood fibres (also called gelatinous or G-fibres) at the base of the hypocotyl where roots form. This results in a bend of about 90° and so produces the hook. Furthermore, the Plant Soil (2012) 359:19–22 DOI 10.1007/s11104-012-1400-7