AOBPreview originally published online on July 4, 2006
Annals of Botany 2006 98(5):901-926; doi:10.1093/aob/mcl133
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INVITED REVIEW |
Structure–Function Relationships in Highly Modified Shoots of Cactaceae
Section of Integrative Biology, 1 University Station, A6700, University of Texas Austin, TX 78712, USA
* E-mail j.mauseth{at}mail.utexas.edu
Received: 22 March 2006 Returned for revision: 28 April 2006 Accepted: 4 May 2006 Published electronically: 4 July 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONHABITORGANS OF THE CACTUS...TISSUES OF THE CACTUS...TISSUES OF THE CACTUS...ACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims Cacti are extremely diverse structurally and ecologically, and so modified as to be intimidating to many biologists. Yet all have the same organization as most dicots, none differs fundamentally from Arabidopsis or other model plants. This review explains cactus shoot structure, discusses relationships between structure, ecology, development and evolution, and indicates areas where research on cacti is necessary to test general theories of morphogenesis.
• Scope Cactus leaves are diverse; all cacti have foliage leaves; many intermediate stages in evolutionary reduction of leaves are still present; floral shoots often have large, complex leaves whereas vegetative shoots have microscopic leaves. Spines are modified bud scales, some secrete sugar as extra-floral nectaries. Many cacti have juvenile/adult phases in which the flowering adult phase (a cephalium) differs greatly from the juvenile; in some, one side of a shoot becomes adult, all other sides continue to grow as the juvenile phase. Flowers are inverted: the exterior of a cactus ‘flower’ is a hollow vegetative shoot with internodes, nodes, leaves and spines, whereas floral organs occur inside, with petals physically above stamens. Many cacti have cortical bundles vascularizing the cortex, however broad it evolves to be, thus keeping surface tissues alive. Great width results in great weight of weak parenchymatous shoots, correlated with reduced branching. Reduced numbers of shoot apices is compensated by great increases in number of meristematic cells within individual SAMs. Ribs and tubercles allow shoots to swell without tearing during wet seasons. Shoot epidermis and cortex cells live and function for decades then convert to cork cambium. Many modifications permit water storage within cactus wood itself, adjacent to vessels.
Key words: Cactus, epidermis, flower, leaf development, phase change, plant anatomy, shoot apical meristem, structure/function, wood evolution, xerophyte
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONHABITORGANS OF THE CACTUS...TISSUES OF THE CACTUS...TISSUES OF THE CACTUS...ACKNOWLEDGEMENTSLITERATURE CITED |
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The first two objectives of this review are to introduce readers to many of the exotic and extreme aspects of cactus biology, and also to show that even the most bizarre cacti are easy to understand because all have the fundamental tissues and organs of an ordinary dicot. People familiar with arabidopsis will find that cacti have the same basic body organization, just having a bit more cortex, smaller leaves, and axillary buds that develop as clusters of spines. A third objective is to emphasize the diversity of structure, ecology and reproduction in the family. Probably no other plant family exceeds Cactaceae in diversity of structure; its members include trees, vines, dwarfs, giants, epiphytes and geophytes. Many are dimorphic, producing different types of anatomy or morphology at different stages of their lives. The final and main objective is to point out that many research topics in many fields can be studied with this family; there is already a solid foundation of existing knowledge that can be a basis for further studies of morphogenesis, ecology, physiology, evolution and many more areas.
Cactus evolution has been a process of diversification. Starting from some ancestral organization of stems, leaves and roots, cacti have diversified into a multiplicity of body forms. Members of subfamily Pereskioideae (Fig. 1A and Table 1) are shrubs or large trees with thin, broad, ordinary-looking leaves and hard, woody, non-succulent trunks; they are not adapted to dry, hot conditions. Subfamilies Maihuenioideae and Opuntioideae contain plants with small but still easily visible foliage leaves, and plants vary from being trees to dwarfs (Fig. 1B and C). The largest subfamily, Cactoideae (Fig. 1D), differs from the others by having foliage leaves that are always microscopic: all photosynthesis is carried out by shoot cortex cells covered by a persistent epidermis and stomata, all of which live and function for decades or centuries, as long as the shoot is green. Members of Cactoideae and Opuntioideae occupy almost every terrestrial habitat: hot deserts; cold deserts; grasslands; shady forests; rainforests; and cold, wet or snow-covered alpine zones above the treeline (Mauseth et al., 2002). Several genera of Cactoideae display what appears to be unparalleled in any other group: an absolutely amazing morphogenetic phase change in which the adult body (able to flower) looks nothing at all like the juvenile body (unable to flower). Almost every aspect of shoot morphogenesis changes, each plant produces two totally distinct types of body (Figs 1E and F and 2E).
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Various aspects of cactus biology have been reviewed recently, so I will emphasize either newer discoveries or fields that have not received sufficient attention. Two monographs are recommended for numerous excellent photographs and general details of plant form and distribution: Anderson (2001) and Hunt (2006). The older work of Backeberg (1958–1962) lacks many recently discovered species and modern ideas but has much more detail than any other source (4041 pages in six volumes). Natural histories are provided by Rauh (1979) and Mauseth et al. (2002; A Cactus Odyssey being especially recommended for a less technical, more inclusive account of cactus biology). Cactus structure is reviewed by Buxbaum (1950), Gibson and Nobel (1986), Terrazas Salgado and Mauseth (2002) and Terrazas and Arias (2003). Ecophysiology is summarized by Nobel (1988). Techniques for extracting DNA from even mucilaginous cacti are now available (Griffith and Porter, 2003), and DNA-based phylogenies have been proposed (Nyffeler, 2002; Crozier, 2005; Edwards et al., 2005; Griffith, 2005).
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HABIT |
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TOPABSTRACTINTRODUCTIONHABITORGANS OF THE CACTUS...TISSUES OF THE CACTUS...TISSUES OF THE CACTUS...ACKNOWLEDGEMENTSLITERATURE CITED |
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In every species, the cactus body organization is fundamentally the same as that of ordinary dicots. Most cactus leaves are microscopically small (Fig. 1I) and the cortex of most species is gigantically enlarged, but still each cactus shoot has the basic dicot organization: all consist of internodes, nodes, leaves and axillary buds produced by shoot apical meristems (SAMs). Without exception their primary body has an epidermis (with stomata), cortex, eustele (single ring of collateral vascular bundles each with primary xylem and phloem) and pith. No cactus is an annual or an herb. All produce a secondary body consisting of secondary xylem (wood), secondary phloem and bark. All genetic programmes that guide basic dicot morphogenesis are probably still present and functional in cacti.
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ORGANS OF THE CACTUS SHOOT |
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TOPABSTRACTINTRODUCTIONHABITORGANS OF THE CACTUS...TISSUES OF THE CACTUS...TISSUES OF THE CACTUS...ACKNOWLEDGEMENTSLITERATURE CITED |
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Leaves
Evolutionary modification of leaf morphogenesis has been extensive in all cacti, and has resulted in great diversity of leaf types within each individual plant. All cacti produce foliage leaves (microscopically small in most) and spines (modified leaves); some also produce glands (modified spines), most have large, thin leaves on the surface of their floral shoots (Fig. 1C, D and G–I; see Floral shoots below).
Diversity of cactus leaves is associated with an extreme polymorphism present in all cactus shoots. The green, photosynthetic body of an unbranched cactus is a single shoot known as a ‘long-shoot’; if branched, all the green, fleshy branches are also long-shoots (Fig. 1A, C and D). Almost all familiar plants consist only of long-shoots so the term is usually unnecessary and rarely used. But in cacti, each axillary bud immediately produces leaf primordia, which in most other plants would become small, flat, waxy bud scales; in cacti, however, they develop into spines (Fig. 1D, G and I; Boke, 1944, 1952, 1967; Buxbaum, 1950). Many morphologists have considered a cluster of cactus spines to be just an axillary bud; others interpret it as a ‘short-shoot’, a shoot with extremely short, narrow internodes and without the broad, succulent tissues of the long-shoot. Long-shoot/short-shoot dimorphism is not unusual in seed plants. For example, most of an apple tree (Malus) consists of long-shoots which have ordinary photosynthetic leaves with axillary buds enclosed by bud scales, but the axillary buds themselves perennially produce both flowers and photosynthetic leaves on shoots with extremely short internodes: the axillary buds become short-shoots, often called spur shoots. In this case, long-shoots and short-shoots bear leaves that are virtually indistinguishable. In contrast, most of the body of a pine tree (Pinus) consists of long-shoots which bear small brown papery scale leaves (easily overlooked); the axillary buds of the scale leaves develop into short-shoots with needle-like leaves. The familiar pine needles are not the leaves of the familiar pine branches (long-shoots) but instead are the leaves of almost invisible short-shoots (Foster and Gifford, 1974).
Foliage leaves
In all cacti, SAMs (see below) of long-shoots produce leaf primordia (Boke, 1951, 1980; Mauseth and Halperin, 1975; Mauseth, 1976, 1977, 1978d, 1980a, 2004d). In Pereskia, these develop into large, thin, fully functional photosynthetic foliage leaves with a broad lamina (Fig. 1A; lamina to 23 cm long, 6 cm wide; Bailey, 1960; Leuenberger, 1986; Mauseth and Landrum, 1997). These are the main sites of photosynthesis and persist for months but abscise when plants become dormant. Pereskia foliage leaves may be slightly thickened but not remarkably so, and palisade and spongy mesophyll are only weakly differentiated. An extensive reticulate venation of collateral vascular bundles is present. In Maihuenioideae and Opuntioideae, green photosynthetic leaves are present and all are large enough to be easily visible by the naked eye (Fig. 1C; Mauseth, 1999a, 2005; Leuenberger, 1997). They are flattened with a small thick, succulent lamina in Pereskiopsis and Quiabentia, but are radially symmetrical in all other Opuntioideae and Maihuenia, and usually are narrow (2–5 mm), short (range 3–12 mm, but 120 mm long in Austrocylindropuntia subulata) and ephemeral (persistent in M. poeppigii, Pereskiopsis, Quiabentia and Austrocylindropuntia). Their photosynthesis is probably insignificant except when relatively large and long-lived. If an opuntioid long-shoot is more than 1 or two months old, there may be nothing other than a tiny leaf scar immediately below the cluster of spines.
Long-shoot leaves in all Cactoideae have been greatly reduced evolutionarily but most have all the tissue types typical of an ordinary foliage leaf (Fig. 1I; Boke, 1951, 1952, 1957b; J. D. Mauseth, unpubl. res.) and thus they probably still have leaf development genes similar to those of other plants (Fleming, 2005). They range from very small (maximum 2·3 mm long in Matucana aurantiaca) to microscopic, <500 µm long in most. All but the most miniscule have stomata, at least one vascular bundle, and dorsiventral asymmetry (the vascular bundle is located closer to the adaxial epidermis, and the abaxial mesophyll is slightly aerenchymatous). At least a few have a noticeable lamina (up to 1776 µm wide in Epiphyllum) but none has a petiole or abscission zone. The most reduced long-shoot leaves in Cactoideae do not develop beyond the leaf primordium stage, but instead remain as just a tiny bump (50 µm tall) of epidermis covering several mesophyll cells; their leaf trace typically runs only to the axillary bud SAM and spines, not to the leaf itself.
Evolutionary restriction of foliage leaf development had consequences other than the obvious ones of reducing the shoot's surface area and surface : volume (S : V) ratio, reducing transpirational water loss, and reducing photosynthetic surface area. It also reduced leaf venation, which is the site of vascular loading and unloading. Ordinary foliage leaves have an extensive set of leaf veins consisting of primary xylem and phloem and having a tremendous length and surface area in contact with living mesophyll. Shoots of Cactoideae with their highly reduced foliage leaves have little or no leaf vascular tissue, so water must be unloaded from bundles in the cortex (see Cortical bundles below), from leaf/bud traces or from secondary xylem (wood). But in most non-cactus woody plants, water is almost never unloaded from or loaded into secondary xylem (roots load water into primary xylem); vessels of wood are surrounded by a matrix of wood fibres or a bit of paratracheal parenchyma, and they do not have extensive surface contact with a voluminous parenchyma capable of absorbing the water they transport. Wood vessels instead transfer water to primary xylem of leaves, flowers, and so on. Loss of leaf venation in cacti almost certainly resulted in selection pressure to alter secondary xylem such that it has increased amounts of paratracheal tissues able to unload, store and transfer water [Fig. 3G; see Secondary xylem (wood) below].
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Loss of leaf venation also affected phloem loading; secondary phloem in the central vascular cylinder does not load sugars directly, it only receives them from primary phloem in leaf traces. Because cacti store water in a voluminous cortex, the outer photosynthetic cortex is too distant from the secondary phloem of the central cylinder to allow it to load sugars directly. All loading of sugars apparently must occur in cortical bundles or perhaps leaf/bud traces.
Spines
Cactus spines are the modified bud scales of an axillary bud; alternatively they can be considered the modified leaves of a short-shoot (Mauseth, 1976; Boke, 1980). Differences between the two interpretations are not obvious. Being leaves of an axillary bud, cactus spines almost always occur in clusters, a character which distinguishes this family from all others. Several cacti have only one spine per cluster, and spines are completely absent in Blossfeldia (Mauseth, 2006a) and some epiphytic rainforest cacti (some Epiphyllum, Lepismium, Rhipsalis; Fig. 3D). Almost as soon as the axillary bud SAM becomes recognizable, it develops zonation typical of any angiosperm, having a uniseriate tunica over a corpus composed of central cells, peripheral zone and pith-rib meristem. It immediately produces leaf primordia; these resemble long-shoot leaf primordia in being small swellings of ground meristem covered by protoderm. As the axillary bud's leaf primordia enlarge, their tip cells vacuolate and elongate, and quickly the young spine consists of three regions: a basal meristem; a zone of elongation/differentiation and an apical zone of mature; and dead lignified fibres (Fig. 1I; Mauseth, 1977).
The spine basal meristem consists of only a unistratose protoderm surrounding a mass of ground meristem. No vascular tissue or procambium has been reported. Most cell division produces daughter cells aligned parallel to the spine's long axis, but occasional divisions in other planes widen the basal meristem gradually, thus cactus spines taper from a narrow tip to a broader base (Fig. 1G). Spines are frequently circular in transverse section but can be flattened on one side (usually the adaxial side; Ferocactus latispinus) or their basal meristem becomes so broad but thin that the spine is flat and papery, mimicking a dry blade of grass (Leuchtenbergia principis, Tephrocactus articulatus: spines 4 mm wide, 0·3 mm thick, to 15 cm long). Factors that control morphogenesis in spine basal meristems are unknown, but in many cacti these meristems are accessible large masses of uniform meristematic cells which are active for weeks and thus could be an excellent experimental system. Genes that maintain SAM cells in a meristematic state, such as WUSCHEL and CLAVATA, may also act in spine basal meristems.
As cells are pushed upward in the meristem, at some point they cross into the spine's zone of elongation and maturation (Mauseth, 1977). All cells in both the surface (protoderm) and centre (mesophyll) develop into fibres. Mesophyll cells elongate greatly and have only a few simple pits in their extremely thick, hard walls. In most spines, cell elongation is uniform throughout, producing a remarkably straight spine, but some have predictable, differential growth rates, elongating more on their adaxial side and thus becoming curved or hooked downward (especially Ferocactus, Mammillaria, Parodia). Once mature, the cells die, but it is not known if they undergo programmed cell death or merely starve as they are pushed far away from the nutrient supply in the basal meristem and separated from it by younger cells that are also sclerifying. Spine protoderm cells also elongate, deposit a sclerified secondary wall then die. Cactus spine epidermis lacks stomata; in a few species some spine epidermis cells elongate outward as trichomes (Mammillaria plumosa, Turbinicarpus; Sotomayor and Arredondo, 2004). Spines of Cylindropuntia are covered by a loose sheath assumed to be deciduous epidermis.
At maturity, cactus spines lack almost all characters of leaves, even of the reduced long-shoot foliage leaves of Cactoideae (Fig. 1I; Mauseth, 1977). They have no guard cells, no stomata, no hypodermis, no chlorenchyma (except in the basal meristem), no spongy mesophyll, no phloem and no xylem. Instead they consist of just two cell types that never occur in long-shoot foliage leaves of cacti: libriform fibres and sclerified epidermis. Axillary bud leaf primordia must repress virtually all foliage leaf morphogenesis genes and instead activate genes that normally are only expressed in xylem or phloem fibres.
In tissue culture, cactus leaf morphogenesis is easily controlled by hormones. Cytokinins cause cultured axillary bud SAMs of Opuntia polyacantha to convert to long-shoot SAMs and produce primordia that develop as foliage leaves, whereas gibberellins cause cultured SAMs to continue as short-shoot SAMs, producing more spine primordia (Mauseth and Halperin, 1975; Mauseth, 1976, 1977). If cultured SAMs are transferred from one hormone to the other, or given both hormones simultaneously, lateral organs develop combinations of spine and foliage leaf characters (J. D. Mauseth, unpubl. res.).
A single axillary bud usually produces several types of spines, each differing in size, shape, colour and texture, varying in a predictable sequence (Figs 1G and 3B; Buxbaum, 1950). This is an extreme form of heteroblasty. The outermost spines (radial spines) are usually smaller, shorter, more delicate whereas those in the centre (central spines) are more robust and have different pigmentation. Radial and central spines are totally distinctive with no intermediates in many species, but intergrade in others. Spine colour may be important for camouflage (spines often have the colour of dry grass) or for recognition by pollinators and seed dispersers, but the basis of spine pigmentation is unknown. In a few species, all spines of an axillary bud are similar, differing only slightly from each other (Fig. 2A).
The phyllotactic arrangement of spine primordia around the axillary bud SAM in cacti is unusual and may challenge theories of phyllotaxy and leaf initiation. In most (all?) cacti, spines are produced only on the side of the axillary bud SAM adjacent to the subtending leaf, they are not produced in a radially symmetrical pattern centred on the SAM. An easily observed exotic phyllotaxy is that of Pelecyphora aselliformis, Turbinicarpus pseudopectinatus and Oroya peruviana (Fig. 2A; Boke, 1959); spines occur in two parallel rows, which at first appears to be distichous phyllotaxy, but both rows are located on the same side of the SAM, and all other sides are free of primordia. In some species, spine primordia remain small and quiescent after they are formed and none develops until the full complement is present, but then the most recently initiated primordia develop into spines first, and the first-initiated primordia are the last to enlarge (Boke 1952, 1955, 1957a, b, 1961a, b).
Unusual spines called glochids occur in all members of Opuntioideae (except Puna clavarioides; Kiesling, 1984) but no other subfamily. Glochids are short and narrow, occur in high numbers per axillary bud, have retrorsely barbed epidermis cells at their tip, and, unlike all other spines, glochids always abscise from their base (Robinson, 1974). After breaking away, they remain in place unless disturbed because they are so tightly crowded together. An incautious touch results in glochids in skin, clothing, equipment and laboratory. Glochids are modified spines and thus modified leaves; they are initiated by the axillary bud SAM as extremely slender leaf primordia in a phyllotactic pattern; these aspects of SAM function and leaf morphogenesis are unstudied.
Spines provide more than protection from herbivores. When abundant, they shade photosynthetic cortex from intense insolation and UV. Spine epidermis and mesophyll of several cacti have deep fissures as a part of normal development; in Turbinicarpus klinkerianus, Discocactus horstii and Opuntia invicta, radioactive phosphate or safranin dye applied to the spines was absorbed into the cactus body (Schill and Barthlott, 1973; Porembski, 1994); water absorption through such spines may be significant in fog zones. Spines are flammable, increasing damage to cacti during wildfires (Emming, 2005, 2006).
Spines as glands
Spines of several genera are secretory glands but this is almost completely unstudied. Ants are often seen at the glands of some species of Ancistrocactus, Coryphantha, Cylindropuntia, Ferocactus and Opuntia when they have droplets of clear liquid, presumably sugar and water (Fig. 2B). Ants are attracted to the glands of Cylindropuntia acanthocarpa and protect it from insects (Pickett and Clark, 1979), and ant visits to extra-floral nectaries of Opuntia stricta increase fruit set (Oliveira et al., 1999). Secretory spines on axillary buds of flowers of Neoraimondia arequipensis attract ants to the flower itself.
Glandular spines of Ancistrocactus scheeri are short, broad, and taper abruptly to a sharp, narrow spine-like tip; their mesophyll cells are short, blunt, living fibres with thin walls and large intercellular spaces (Mauseth, 1982). Sugars and water secreted by these fibres exude from the top of the glandular spine. After some unknown period, each gland collapses. In Ancistrocactus and Coryphantha, numerous glandular spines are formed in each axillary bud over a period of at least several months, perhaps >1 year; only one or two glands are active at any time, but any particular axillary bud will be producing secretory product for a protracted time (Dicht and Lüthy, 2005).
Secretory spines in Calymmanthium substerile produce a thick white material. This has been seen only in cultivated plants protected from rain. It has not been studied.
Axillary buds
In cactus literature, the region in a long-shoot leaf axil is called an ‘areole’, not simply an axillary bud. This term is useful because the bud's spines persist even if the axillary bud SAM goes on to produce a flower and fruit. Flowering in most angiosperms causes bud scale abscission, so after the fruit is shed, the region is little more than a set of scars, but in cacti the entire set of spines is still present. Furthermore, some cacti produce spines for a prolonged period, longer than most axillary buds produce bud scales, so these growing structures are more appropriately considered short-shoots rather than merely buds. ‘Areole’ refers to the region at all stages of its development.
Cactus axillary buds become active immediately and produce spine primordia while still within a few micrometres of the long-shoot SAM, still within its apical depression (Boke, 1944, 1952, 1980; Mauseth et al., 2002). Spine primordia themselves develop immediately, such that many spines project upward, protecting the shoot apex from herbivores (Fig. 1D). Young axillary buds are carried upward and outward with growth of the cortex, and leaf/bud traces elongate as well. Typically, cortex immediately interior to an axillary bud stops expanding slightly earlier than does surrounding cortex, thus the bud becomes located in its own well-like depression (only a few millimetres deep and wide; Figs 1D and G and 2A). This depression is lined by epidermis and hypodermis, both being more delicate and having thinner cell walls than epidermis and hypodermis cells located between areole depressions. In Blossfeldia liliputana, stomata are not present anywhere except in the areole depressions (Barthlott and Porembski, 1996; Mauseth, 2006a), and in Maihuenia poeppigii (Fig. 1B; Mauseth, 1999a) areole depressions are the only areas in which epidermis does not immediately convert to cork cambium, so in this species, too, areole depressions are the only regions of the stem that have stomata (M. poeppigii has persistent macroscopic foliage leaves, B. liliputana does not).
The axillary bud SAM produces an abundance of uniseriate, multicellular trichomes along with spine primordia. In most species, it appears as if every single areole epidermis cell becomes either part of a spine primordium or a trichome; there appear to be no ordinary epidermis cells within the areole. Trichomes in all species die immediately, thus the SAM is protected by an almost impenetrable mass of dead trichomes and spines.
After producing spine primordia and trichomes (and glochids in Opuntioideae), the axillary bud SAM remains capable of further growth, either as a floral bud (Fig. 2G), a vegetative branch (a long-shoot; Figs 1C and 3D), or as a short-shoot. In species that bloom with flowers on new growth near the shoot tip (many species), the axillary bud SAM develops as a floral bud as soon as spine primordium production is completed. If axillary bud SAMs become dormant for 1 or more years after forming spines, the plant blooms with flowers located farther from the shoot apex. In many species of Hatiora, Rhipsalis, Schlumbergera and Opuntioideae, young axillary buds immediately grow out as branches (Buxbaum, 1950), but, in most cacti, branching only occurs from axillary buds that are several to many years old and which are thus located in regions with enough strength to support the weight of branches. Many plants branch only from axillary buds located at the base of the trunk: their SAMs remain dormant for decades, yet develop as normal branches. Many giant columnar cacti and barrel-shaped cacti have few or no branches while growing normally; of their thousands of axillary buds (about 10 000 axillary buds in single shoots of Trichocereus pasacana; J. D. Mauseth, unpubl. res.), most do nothing other than produce spines and flowers. However, if these shoots are cut off near their base, one or several axillary buds become active and grow out as branches: they were suppressed by extreme apical dominance.
Axillary buds in some cacti are capable of more than producing only one flower and later one branch. Buds of Lepismium cruciforme, Myrtillocactus, Pachycereus gatesii, P. marginatus, P. schottii and Rhipsalis russellii bear several flowers or fruits simultaneously (Barthlott and Taylor, 1995; Arias et al., 2003), those of Neoraimondia (including Neocardenasia) produce several flowers per year for many years. Each time a flower is produced the axillary bud becomes slightly longer and the reason for calling it a short-shoot becomes more obvious. With extreme age (how old?), Neoraimondia short-shoots become up to 85 mm long, and may even branch; they have pith, secondary xylem and phloem, cortex and bark (Fig. 2C; Rauh, 1957; Mauseth and Kiesling, 1997; Kiesling and Mauseth, 2000).
Other unusual aspects of the growth pattern of Neoraimondia arequipensis are worth mentioning here. Their long-shoots are massively succulent, very broad and heavy (40 cm in diameter) and grow to 7 m tall. At that point, a long-shoot stops growing and one of its basal-most areoles grows out as a lateral shoot right at ground level, its eventual weight supported by the soil. Lateral shoots apparently grow rapidly because their apical-most 15 or 30 cm of epidermis has the clean, fresh look of being <1 year old; within a few years, this branch reaches its full length and stops, then another basal areole repeats the process. A typical plant has five to ten giant branches that have stopped elongating and one single branch that is growing: apparently the plant channels most resources to one branch at a time. But the non-growing branches are not moribund: they are photosynthesizing and their axillary buds all flower perennially (Mauseth et al., 2002). Neoraimondia biology has many intriguing aspects but these giant, frost-sensitive plants are not easy to cultivate.
Axillary buds of many Opuntioideae, a few Cactoideae and several Pereskia occasionally and sporadically produce a new spine from time to time over many years. These too are short-shoots but always remain only a few millimetres long; their anatomy has not been studied.
Unusual branching of axillary buds
In cacti and most other stem-succulents, cortex below and surrounding an axillary bud grows outward in the form of a cone (tubercle) or ridge (rib; Figs 1D and E and 3B and C; see Ribs and tubercles below). Growth of ribs and tubercles has not been studied, but they appear to have a basal growth zone located proximal to the axillary bud, between it and the stem. Consequently their growth causes the axillary bud to be carried outward along with the tip of the rib or tubercle, so axillary buds and all associated spines, flower parts or branches are located at the apex of a rib or tubercle.
In contrast, in a small subgroup of Cactoideae (e.g. Coryphantha, Mammillaria), the growth zone is located directly below the axillary bud SAM, which consequently is stretched as the tubercle grows (Boke, 1952, 1953, 1955, 1958, 1961a, b; Dicht and Lüthy, 2005). In Mammillaria, the bud SAM always divides dichotomously and one of the two new SAMs is carried outward along with the tubercle tip while the other remains stationary, at the base of the tubercle. Both new meristems become radially symmetrical but have different fates: the distal SAM at the tubercle tip produces only spine primordia, it never flowers or grows as a lateral branch, whereas the proximal one does produce flowers and lateral branches but almost never spines (Fig. 2D). Flowers or new branches of mammillarias emerge from between the crowded bases of the tubercles, not from the tubercle tips and not adjacent to the spines as is typical of most cacti. Remarkably, if tubercle tips are cultured with high levels of cytokinin, the spine-producing SAM can be induced to form a branch with microscopic foliage leaves on long-shoots (J. D. Mauseth, unpubl. res.).
In Coryphantha and Ancistrocactus, growth of the tubercle below the axillary bud causes the SAM to elongate but not divide dichotomously. Perhaps it acts as if forming a crest because it produces leaf primordia along its entire length. These leaf primordia develop into extrafloral nectaries (glandular spines; Fig. 2B; see Spines as glands above). In addition, radial growth of the tubercle cortex upward below the elongate SAM is inhibited, so the nectaries are located in a groove running along the tubercle's adaxial side (Boke, 1961b).
Phase change, heteroblasty and the transition from juvenile to adult
Seedlings of most angiosperms produce leaves and stems that differ at least slightly from those produced when the plant is older. This is called ‘heteroblasty,’ but additional characters differ between seedlings and older plants, and the term ‘phase change’ is more inclusive (Howell, 1998). Phase change is occasionally associated with conversion from the juvenile state (incapable of flowering) to the adult state (able to flower). In classic examples such as Citrus and Hedera, the juvenile/adult transition occurs simultaneously with phase change, but in many species, phase change is completed before the juvenile/adult transition occurs: the plant grows with its mature phase morphology for one to several years before becoming old enough to flower.
All cacti undergo phase change. Compared with older plants, seedlings have narrower primary stems with fewer cortex and pith cells; more delicate epidermis and hypodermis; shorter ribs or tubercles (and species with ribbed adults may have tuberculate seedlings); shorter, more delicate spines. Most produce wide-band tracheids (WBTs; see Wide-band tracheids below; Fig. 3E, F and H) in their primary and secondary xylem (Loza-Cornejo et al., 2003; Mauseth, 2004c). As the seedling ages, each successive bit of growth becomes more robust, its characters progressively more similar to those of an older plant. Species that will grow to have slender shoots stop producing WBT wood and switch to making fibrous wood instead (see Dimorphic wood below). These changes are not accompanied by a juvenile/adult transition because almost no cactus can bloom before it is 1 year old (in many cases, several years or decades old), so most cacti grow with their mature morphology for years even though they are still juvenile.
The juvenile/adult transition is accompanied by no obvious morphological changes in most cacti, but in others there are stunning changes in anatomy, morphology and physiology. The differences between juvenile and adult phases are much more extensive and dramatic than those of any other group of plants. Once old enough to flower, these cacti produce an adult body called a cephalium.
Terminal cephalia
Melocactus and Discocactus (do not confuse with Disocactus) have terminal cephalia. Young plants grow as juveniles with unbranched globose to short cylindrical shoots with prominent ribs and areoles, each with a small number of stout spines (Fig. 1E; Mauseth, 1989). Most of the green shoot surface is unobscured, visible and photosynthetic because ribs are large, areoles small and spines are few. The juvenile phase lasts several to many years, varying with species and growing conditions, and the biochemical trigger to become adult is unknown: plants of M. matanzanus (commercially available) grown with fertilizer, water and full sunlight become adults while only 3 years old, during which time they have produced about 160 leaves and areoles. As a plant converts from juvenile to adult, almost all aspects of its growth change. The adult shoot—the cephalium—is produced by the same SAM that produced the juvenile shoot (juvenile shoot and cephalium are the two ends of one shoot) (Niklas and Mauseth, 1981; Mauseth, 1989). Phyllotaxy becomes very high, and the adult SAM produces small, closely spaced tubercles rather than prominent ribs as it did while it was juvenile. Spine number per areole increases greatly and cephalium spines are short and slender. Trichomes are produced in abundance. Because areoles are so closely spaced and the density of spines and trichomes is so high, the surface of the adult shoot is completely hidden under an impenetrable, solid mass (about 1·0 cm thick) of spines and dead trichomes (Mauseth et al., 2002). No light penetrates this mass, photosynthesis is impossible, and there are no stomata, no guard cells, no ordinary epidermis cells. The adult SAM becomes smaller, produces a narrower cortex free of chloroplasts but with cortical bundles and closely spaced leaf/bud traces. Cephalium pith is also narrow, so the entire adult region is much narrower than the juvenile. The transition is abrupt with little or no intermediate tissues. Adult shoot secondary xylem consists of WBTs and vessels, and that of the juvenile shoot consists of an inner region of fibrous wood surrounded by an outer, more recently produced layer of WBT wood; apparently the juvenile/adult transition also affects the vascular cambium such that once the SAM begins producing adult morphology at the shoot's apex, the cambium begins producing wood with adult morphology throughout the shoot.
Axillary buds in the cephalium produce flowers. Being located on a tiny tubercle below a thick layer of spines and trichomes, each flower bud is remarkably well protected from predation. During anthesis flower buds elongate and petals curve outward just above the spines. Ovules and nectaries, still located at the base of the mass of spines, are accessible to pollinators through a petal-lined flower tube. Flowers close after just 1 d, the perianth withers and remains in place, protecting the ovary. When ready, the mature fruit swells, pushing itself up above the mass of spines, becoming visible to seed dispersers (Cortes Figueira et al., 1994).
A cephalium in this position is a terminal cephalium because it is at the apex of the shoot, not because it terminates the plant's growth. Instead, the plant continues its growth for many years, but as with any other species that undergoes a juvenile/adult transition, all further growth is with the adult organization (the cephalium is not an inflorescence, is not ephemeral). The cephalium becomes longer every year, every year there are more flowers and fruits, but every year the juvenile portion merely becomes older—and it is the only photosynthetic tissue the plant has. Because the shoot is produced by one single SAM and does not branch, no new photosynthetic cortex can be added, so the ratio of photosynthetic tissue to heterotrophic tissue decreases every year. Melocacti easily become 20 or 30 years old in cultivation, continuing to rely on the same, old chlorenchyma cells they produced when they were juveniles. Under normal conditions, melocacti never branch, but if a mature plant is decapitated, an axillary bud of either the cephalium or the juvenile body will grow out as a lateral branch with juvenile characters. At some point this switches to adult growth, a new cephalium. All 33 species of Melocactus have this morphology; no known species retains intermediate stages in cephalium evolution (Taylor, 1991).
Discocacti resemble melocacti, but their cephalia grow more slowly and even old plants that have bloomed for years have only extremely short cephalia. Discocacti grafted onto hardy rootstocks are easy to cultivate.
Plants of Backebergia militaris (Pachycereus militaris) are giant columnar cacti, up to 5 m tall (Fig. 2E). They grow as juveniles with broad stems and prominent ribs until at least 3–4 m tall, then they add several ribs and soon switch to producing tubercles (Cattabriga, 2004; Mauseth et al., 2005). In this short transition region, spines are shorter, narrower, more brittle and translucent. Production of trichomes increases. The adult body is only slightly narrower than the juvenile, and the thick layer of long, densely packed spines causes the cephalium to appear broader than the juvenile body. Unlike Melocactus, the adult body of B. militaris does have a few cells that become ordinary epidermis cells, and stomata are present; the outer cortex is weakly chlorophyllous, but certainly little light penetrates the spines. Just as in Melocactus and Discocactus, each year the cephalium becomes longer, whereas the juvenile body remains the same length.
Backebergia, however, periodically abscises its cephalia, which releases one of the uppermost axillary buds on the juvenile portion from apical dominance. The bud grows out as a new lateral branch with juvenile morphology and fresh chlorophyllous tissue. Once the branch becomes 2–3 m long, it too converts to adult growth and becomes topped with a terminal cephalium. This process occurs repeatedly, resulting in giant, highly branched plants. Backebergia militaris cannot tolerate frost but small plants grow readily in a greenhouse. Adult portions of Pachycereus schottii have more and longer spines than do juvenile portions.
Terminal, temporary cephalia occur in Arrojadoa, Cephalocereus (Neodawsonia) apicicephalium and Stephanocereus leucostele (Table 2). After the shoot has bloomed with a set of flowers emerging from a cephalium encircling the shoot tip, its SAM returns to vegetative growth and then makes a segment (many centimetres long) of green stem incapable of flowering. In the following year, it makes another terminal, temporary cephalium. The shoot alternates between non-flowering zones and ring-shaped flowering zones, which remain recognizable for years, long after all flowers and fruits have matured and abscised; internal anatomy is not known.
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Stephanocereus luetzelburgii, a poorly known species, grows as a broad column until about 20 cm tall, then it switches to growing as a much narrower column, perhaps accompanied by a juvenile/adult transition (Taylor and Zappi, 2004).
Lateral cephalia
Lateral cephalia are regions with adult characters located on one side of the shoot, not at its apex (Fig. 1F). They have been studied in Cephalocereus (Vásquez Sánchez et al., 2005) and Espostoa (including Vatricania; Buxbaum, 1952, 1959; Rauh, 1957; Mauseth, 1999b; Mauseth et al., 2002). A seedling grows as a juvenile green column with prominent ribs and stout, sparse spines on all sides for several years. When old enough to undergo the juvenile/adult transition, development of only some ribs on one side is altered, all tissues being added to the other ribs on the rest of the body continue to develop with juvenile characters; as the shoot continues to grow from one single SAM, some leaf primordia and their associated node and internode tissues develop with adult morphology, the rest develop with juvenile characters. Adult characters are similar to those in Melocactus: cortex is thin and non-chlorophyllous; short, small tubercles with long, slender spines are produced instead of large ribs and stout spines; and there are also abundant trichomes and bark. Only areoles in the cephalium produce flowers; other areoles at the same level (thus with the same age) but in juvenile regions do not. Differential growth of cortex and ribs/tubercles disrupts phyllotaxy but the SAM is not affected and continues to grow for years, simultaneously producing reproductive adult tissues and chlorophyllous juvenile tissues. Lateral cephalia occur in numerous genera (Table 2).
In Pilosocereus, areoles that produce flowers simultaneously produce copious amounts of long trichomes, giving the shoot the appearance of having a cephalium. However, internal portions of the shoot are not affected, and once the trichomes break off after several years, that portion of the shoot looks like any other; such regions are pseudocephalia. Cephalocleistocactus produces exceptionally long spines on just one side, giving the impression of a weakly formed lateral cephalium, but flowering is not restricted to those areoles. All areoles are adult, so the role of the cephalium-like region is unknown.
Other types of phase change
The juvenile/adult transition of Browningia candelaris is more or less the opposite of producing a terminal cephalium. Juvenile plants grow as vertical, unbranched determinate columns with prominent ribs and abundant long spines. Once the shoot reaches about 2 m tall, it stops growing and five to ten apical areoles grow out as lateral branches. These are slightly narrower than the juvenile shoot (the trunk), have many low ribs with short weak spines that could almost be overlooked. These branches constitute the adult body and are the only part that bears flowers (Mauseth et al., 2002).
Several species, especially Lepismium (Pfeiffera) ianthothele appear to be neotenous: their adult bodies strongly resemble the seedling phase of other lepismiums (Barthlott and Taylor, 1995).
Dwarfism, gigantism
Evolutionary dwarfism of shoots appears common in cacti. The ancestors of cacti were probably woody, non-succulent trees or large shrubs; this body form occurs in Pereskia (Pereskioideae), Maihuenia patagonica (Maihuenioideae), Pereskiopsis (Opuntioideae) and Cactoideae (Leptocereus, Calymmanthium, Acanthocereus and many others). However, many clades now have genera or species whose plants consist of dwarf shoots <10 cm tall, often <3 cm (Kiesling, 1995; Table 2). These have WBT wood (see Wide-band tracheids below), a type of wood characteristic of seedlings, so dwarfism may be linked to neoteny.
In contrast, many species of Pachycereus (P. fulviceps, P. weberi), Trichocereus (T. atacamensis, T. pasacana, T. terscheckii), Cephalocereus senilis and Neobuxbaumia tetetzo are gigantic. Within Opuntioideae, O. echios of the Galapagos Islands must be the result of tremendous evolutionary increase in body size from a smaller ancestor. Griffith (2004a, b) has pointed out that all subfamilies of Cactaceae except Pereskioideae also contain small, dwarf geophytic plants, thus it is theoretically possible that very small body size is basal in the family.
Floral shoots
Most cactus flowers are inside out, with perianth located physically above stamens, both located above carpels, all buried deeply within a shoot (Fig. 2F; Boke, 1963, 1964, 1966, 1968; Leuenberger, 1986). When a cactus axillary bud produces a flower, it first initiates several to many leaf primordia, nodes and internodes, then switches to producing the primordia of petals (there are often no distinctively sepal-like structures), stamens and carpels. All primordia are present in an ordinary acropetal sequence while the bud is microscopic (Ross, 1982). When cell enlargement occurs, it stops earlier in the centre of the bud than in peripheral regions, so the ovary is elevated little, stamens are elevated a bit more and petals are elevated most. All floral organ primordia become located on the inside of a conical depression in the end of the elongating floral shoot (Fig. 2F). At the rim-like apex of the depression are the first-formed, most proximal perianth primordia and the last-formed, most distal leaf primordia; on the outside of the floral shoot are progressively older leaves and areoles in ordinary phyllotactic sequence (Fig. 2F and G). The object we see when viewing a cactus ‘flower’ from the side is really just a long-shoot (not flower) surmounted by petals. The true flower (except for the petals) is completely hidden inside the long-shoot. Floral shoots are >10 cm long in many cacti and reach 30 cm in Epiphyllum crenatum and E. oxypetalum (Anderson, 2001): ovary and ovules are 30 cm below the uppermost leaves. After pollination and fertilization, the true fruit develops inside the base of the long-shoot, which itself develops as a false fruit; just as in an apple fruit, the boundary between inner true fruit and outer false fruit is not readily apparent. Only the region immediately exterior to the ovary converts to false fruit, all the distal long-shoot tissue is abscised along with the style, stamens and perianth (most cacti have dozens of stamens and petals, an important consideration for the ABC model of floral morphogenesis).
Each node of the floral branch often has a scale-like leaf and an axillary cluster of spines. In Cylindropuntia fulgida (‘chain fruit cholla’), C. leptocaulis, Pereskia sacharosa and a few others, the axillary buds on the ‘flower’ produce floral shoots which later become ‘fruits’ whose axillary buds repeat the process. Axillary buds on the false fruits of C. leptocaulis even produce non-floral branches. Calymmanthium substerile goes one step farther: the apical rim with the last leaves and the first petals does not grow radially as the floral shoot elongates, so it remains just a tiny hole. During anthesis, the flower's expansion actually rips the floral shoot open such that petals, stamens and style elongate through ruptured, dying long-shoot tissues (Mauseth et al., 2002).
The long-shoot nature of the exterior of a cactus ‘flower’ is important because in many genera its nodes bear large, thin photosynthetic leaves (Fig. 1H). They are referred to as ‘scales’ or ‘bracts’ but they develop from leaf primordia, have a lamina (23 mm long, 14 mm wide in Browningia candelaris; Mauseth et al., 2002) with extensive leaf venation, axillary buds, and some have an abscission zone. Thus almost all ‘leafless’ cacti (subfamily Cactoideae) have not only microscopic long-shoot foliage leaves (see Leaves above) but also large, relatively ordinary leaves as well (they differ from petals, which are pigmented and lack axillary buds and spines). Many cacti are adapted to mesic habitats in which virtually all associated plants have photosynthetic leaves, and rainforest epiphytic cacti occur in very moist habitats. Yet none of these uses floral leaf genes to produce large, photosynthetic leaves on their vegetative body. As most cacti evolved to be exclusively stem-photosynthetic, they gave up the beneficial capacity that drought-deciduous plants have; modern cacti (other than pereskias, maihuenias and some Opuntioideae) cannot have an extensive photosynthetic surface area (large leaves) during rainy seasons and then abscise that extra surface area during drought. Many Euphorbia and Pachypodium combine stem-succulence with stem-photosynthesis and drought-deciduous leaves; it seems as if cacti should have the genetic capacity to do this also, but instead remain ‘leafless’ except when flowering.
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TISSUES OF THE CACTUS SHOOT: PRIMARY BODY |
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TOPABSTRACTINTRODUCTIONHABITORGANS OF THE CACTUS...TISSUES OF THE CACTUS...TISSUES OF THE CACTUS...ACKNOWLEDGEMENTSLITERATURE CITED |
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Shoot apical meristems
Evolutionary modification of one aspect of plant biology often affects other aspects. Such interactions are extensive in cacti, and the co-evolution involving SAMs, increased cortex succulence and decreased branching is especially interesting. All cacti with relatively narrow stems (diameter <1·0 cm) have SAMs between 90 and 300 µm, a rather ordinary size for seed plants (Boke, 1941; Gifford, 1954; Mauseth, 1978d, 2004d). However, all cacti with greatly enlarged stems (due to having a very thick cortex, which is possible due to having cortical bundles; see Cortex below) have exceptionally large SAMs, up to 2565 µm (>2·5 mm) diameter in Echinocactus platyacanthus (also E. grusonii, which is commercially available and easy to cultivate). The only other plants with such large SAMs are cycads, which also have broad-diameter primary bodies and high phyllotaxy (Foster, 1940). The exceptionally broad cortex makes cactus shoots exceptionally heavy per unit length; e.g. a 1·0-m-long section of Trichocereus pasacana shoot weighs about 32 000 g (J. D. Mauseth, unpubl. res.) while an equal length of Arabidopsis thaliana would weigh <0·5 g. Almost certainly, this increased weight caused selection of mutations that decrease branching, and many cacti with broad stems have few or no branches (Cody, 2002; Table 2).
Related to reduced branching is a reduced number of SAMs that produce the shoot system. In non-succulent trees such as Pinus or Acer, each plant is highly branched, each has thousands of twigs and thus thousands of SAMs. Even if each SAM is of ordinary size with only a few hundred cells, the shoot is being produced by hundreds of thousands of apical meristem cells. In contrast, sparsely branched cacti have only a few SAMs, and unbranched cacti have just one single SAM that produces the entire shoot body (reminder: the bulk of cactus shoots consists of primary tissues derived directly from a SAM, not secondary tissues produced by cambia). If unbranched cacti had a SAM of ordinary size with just a few hundred meristem cells, each cell would have to undergo tens of thousands of rounds of cell division, and the number of copy-error mutations created with each replication would accumulate to unacceptable levels (Klekowski, 1988) before a cactus shoot had reached maturity. But because sparsely branched cacti have gigantic SAMs, each with thousands of cells, the number of rounds of cell division required of each meristem cell is reduced, as is the risk of introducing copy-error mutations.
The evolution of SAMs up to 2500 µm in diameter from ancestors whose SAMs were much smaller must have required extensive modification of genes that control shoot apex morphogenesis. SAM genes in Arabidopsis thaliana and other model plants probably play the same roles in cacti but must have evolved to interact over much greater distances and greater volumes of meristematic cells (Mauseth, 2004d).
Rate of leaf production and length of plastochron vary tremendously in the family, although studies are needed. SAMs in Ariocarpus, Lophophora, Pediocactus and Sclerocactus may produce only one to five leaf primordia per year (Table 2), but plants of Cleistocactus, Espostoa and several other genera probably have the highest leaf production rates and the shortest plastochrons in the entire plant kingdom. Shoots of C. strausii have up to 30 ribs, each with leaves and axillary buds (spines clusters) located every 3 mm; a shoot may grow 300 mm per year, which is 100 leaves per rib, and 3000 leaves on all 30 ribs. The growing season is about 9 months or 270 d, thus each SAM produces about 11 leaves per day with a plastochron of 2·2 h (J. D. Mauseth, unpubl. res.).
Cactus SAMs are located in depressions at the shoot tip, they are not the most apical point physically (Fig. 1D). Newly formed cortex cells grow upward slightly sooner than do newly formed pith cells, so cortex actually protrudes beyond the SAM. The apical depression may be as much as 3·0 cm deep and 20 cm wide in large globose cacti such as Echinocactus or Echinopsis, so newly formed epidermis and leaf primordia are carried upward and outward by growth of subapical tissues. Following a row of leaf primordia in its phyllotactic spiral from oldest to youngest, you would follow them up the outside of the shoot, across the ring-shaped top of the shoot and then down the inside of the apical depression.
Indeterminate SAMs and monopodial growth
The orderly nature of ribs and phyllotactic spirals of tubercles indicates that shoot growth is monopodial and indeterminate in most Cactoideae. Cactus SAMs become dormant in winter or dry seasons but never form terminal buds and, in almost all cases, the first-formed nodes and internodes of one year grow to be as wide as those of the previous year, so columnar cacti tend to have uniform, straight ribs and globose cacti have uniform spirals of tubercles. Seasonal growth increments along a shoot's length can occasionally be identified due to constrictions of the ribs or markings in their cuticle (Otis and Buskirk, 1986). In Backebergia militaris immature portions of ribs in the dormant shoot apex form a bit of bark, which prevents them from expanding fully in the following growing season: the shoot's longitudinal growth increments are marked by constrictions (Fig. 2D; Mauseth et al., 2005). Constricted monopodial shoots are especially pronounced in Armatocereus, whose shoots consist of vertically aligned segments, strongly resembling the jointed bodies of an Opuntia or Cylindropuntia (but these latter have determinate shoots and sympodial growth). Demographic studies may be possible with Armatocereus; each segment demarcated by a constriction indicates a single growth episode. In A. procerus, they may be correlated to episodic El Niño rains rather than annual growth cycles (Mauseth et al., 2002).
Determinate SAMs and sympodial growth
In contrast to the evolution of giant SAMs in many Cactoideae, SAMs in Opuntioideae evolved to be determinate, functioning briefly before being replaced by a branch derived from an axillary bud (Fig. 1C). This is almost universal in Opuntioideae; only Pereskiopsis, Brasiliopuntia, Consolea and Tacinga have any indeterminate shoots. Plants of Pereskiopsis are highly branched shrubs with many indeterminate shoots (Arias Montes, 1996); those of Brasiliopuntia and Consolea have a single indeterminate, radially symmetrical trunk but all branches are determinate, laterally flattened cladodes. Another species, Tacinga funalis, has radially symmetrical, indeterminate shoots. All other opuntioid genera grow with determinate SAMs only (Mauseth, 2005). The jointed cylindrical stems of chollas (Cylindropuntia) are each determinate shoots; the flat ‘pads’ or ‘ears’ of prickly pears (genus Opuntia or subgenus Platyopuntia) are determinate cladodes. Less familiar opuntioid genera such as Maihueniopsis, Pterocactus and Tephrocactus consist of sympodial sets of globose determinate shoots (Kiesling, 1982, 1984; Hunt and Taylor, 2002; Mauseth et al., 2002; Griffith, 2005). Typically, the SAM has finished producing all internodes, nodes, leaf primordia and axillary buds while it is still <1·0 cm long. Apparently their SAMs convert to masses of large parenchyma cells at maturity. In contrast, a seedling's epicotyl SAM persists longer, although it too is ultimately determinate; this needs study (Table 3).
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Determinate SAMs are associated with unusual branching patterns and shoot polymorphism in several rainforest epiphytes in Cactoideae (Barthlott and Taylor, 1995). In Hatiora salicornioides, each determinate shoot has one narrow, long basal internode (1 mm by 3–4 mm) followed by four to six broad, short internodes (3 mm x 1 mm), followed by five to eight internodes that form a concave disc at the shoot apex; shoots are shaped like inverted beer or wine bottles (common name: ‘drunkard's dream’). Its SAM disorganizes into a plate of parenchyma, and three to five of the axillary buds in the topmost flat disc become active simultaneously, forming a whorl of shoots identical to the one to which they are attached. This pattern repeats indefinitely. In Rhipsalis mesembryanthemoides, an axillary bud near the base of a shoot grows out as a long (20 cm) determinate shoot; almost all its axillary buds grow out as short (1·5 cm) determinate shoots which do not branch under ordinary circumstances but which bear flowers. Once the long shoot stops growing, one of its basal-most branches grows out as another long shoot. In Rhipsalis burchellii, a basal axillary bud grows out as a long (60 cm) determinate shoot. Once it stops growing, several apical-most axillary buds grow out as a whorl of shorter determinate shoots, and when they stop, several apical-most axillary buds on each of them grow out as a whorl of even shorter determinate shoots. This repeats until the last determinate shoots grow to be only about 6·0 cm long, then the pattern repeats as one of the basal-most axillary buds on the original long shoot grows out as another very long determinate shoot.
Dichotomous branching of SAMs
Dichotomous branching occurs in at least two species of Mammillaria (M. perbella and M. parkinsonii; Boke, 1976) and one Echinocereus (E. reichenbachii; Boke and Ross, 1978) and sporadically in several other genera. For several years, plants grow as unbranched short columnar shoots with radial symmetry and a set of intersecting phyllotactic spirals of tubercles. At some point in time, the shoot apex becomes oval rather than round and phyllotaxy becomes abnormal. The shoot apex becomes even more elongate and gradually the phyllotaxy resolves itself into two separate sets of phyllotactic spirals, each set centred on the ends of the oval-shaped apex: the apex has divided into two separate SAMs, each producing ordinary radially symmetrical shoots. After several years, both apices of M. perbella divide dichotomously again, this time perpendicular to the previous division.
During dichotomous branching the SAM temporarily switches to bilateral symmetry, and, if viewed in median longitudinal section, it is extremely broad due to a lateral expansion of the central cell zone and pith-rib meristem. The peripheral zone appears unaffected (Boke, 1976; Boke and Ross, 1978). Cells in the centre of the broadened SAM begin dividing regularly, giving rise to a layered pattern typical of a peripheral zone, and leaf primordia are formed in the centre of the broad apex. At this point, the SAM has divided into two separate meristems. If the SAM is viewed in a median longitudinal section perpendicular to that described above, it appears normal throughout the process.
Perhaps related to dichotomous branching is formation of crested shoots. A SAM becomes extremely broad in one plane as described above, but instead of dividing, it continues to broaden (Boke and Ross, 1978). SAMs as much as 1 m wide are known, and despite having dimensions on the order of 50 µm tall x 200 µm thick x 1000 000 µm wide, they produce leaf primordia, nodes, internodes and axillary buds. Phyllotaxy is irregular in most crests. Crested cacti are often propagated by cuttings; many can be obtained for research. Colour-based chimeras are also now available commercially.
Cortex
Cortical bundles
A key innovation in the evolution of many cacti (in particular Cactoideae) must have been the acquisition of cortical bundles, a network of collateral bundles that vascularizes the cortex and permitted it to evolve to a thickness not found in any other plant of any kind (Fig. 2H). Although several cactus clades have narrow shoots with a relatively thin cortex, most Cactoideae have cortexes that range from extremely broad to extraordinary compared with shoots of all non-cactus plants; the cortex is 300 mm thick in Echinocactus platyacanthus (compared with 0·048 mm in Arabidopsis thaliana), and a range of 10–70 mm is common in Cactoideae (mean thickness is 19·9 mm; Mauseth, 2000).
Cortical bundles apparently were not an early step in cactus evolution. They are completely absent from subfamilies Pereskioideae, Maihuenioideae and Opuntioideae; they are present in all Cactoideae except Blossfeldia liliputana (Boke, 1980; Mauseth and Sajeva, 1992; Mauseth and Landrum, 1997; Mauseth, 1999a, b; Terrazas and Arias, 2003; Mauseth, 2005, 2006a). DNA cladograms suggest B. liliputana is the earliest-divergent member of Cactoideae (Nyffeler, 2002; Crozier, 2004, 2005), so presence of cortical bundles is a synapomorphy for the rest of Cactoideae.
Cortical bundles are critically important for the evolution of a broad cortex because, even if a stem has a thick, wax-covered cuticle, it gradually loses water to dry desert air, so epidermis, hypodermis and outer regions of cortex must be kept hydrated by some means. If the cortex is unvascularized (as it is in almost all vascular plants; Howard, 1979), then water must move from the central vascular cylinder to epidermis by diffusion, which is slow over distances of more than a few millimetres (Barcikowski and Nobel, 1984), thus limiting any increase in cortex thickness. But with the evolution of cortical bundles, water can be transported rapidly in bulk and distributed throughout the outermost regions of the stem, keeping chlorenchyma, hypodermis and epidermis hydrated no matter how distant they are from the xylem in the central ring of bundles. Similarly, as cortex evolved to be thicker, the chlorenchyma and the sugars it produces became located farther from central cylinder phloem, but cortical bundles allow mass flow of phloem sap across the thickest cortex. In contrast, other stem-photosynthetic succulents, such as euphorbias and stapelias, lack cortical bundles and never have a truly thick, truly voluminous cortex similar to that common in Cactoideae (Mauseth, 2004a, b). Although they are excellent examples of evolutionary convergence with cacti, their shoots are not as wide, they never have giant globose or columnar primary bodies; the euphorbia that are broad achieve their width by accumulation of wood.
The molecular genetic basis of cortical bundle morphogenesis is not known, but these bundles greatly resemble leaf venation (Fig. 2H; Mauseth and Sajeva, 1992). Cortical bundles are collateral, slender with just a few narrow conducting cells, they have a similar spacing between veins, they form a network (three dimensional whereas leaf venation is two dimensional), and in many species they end in a cluster of short, broad terminal tracheids. Also like leaf veins, cortical bundles never extend to the epidermis or hypodermis but instead lie just at the base of the photosynthetic tissues, the palisade mesophyll of leaves, the palisade cortex in cacti (see below in this section). Cortical bundles may have evolved by means of mutations that allowed cortex cells to ectopically activate genes normally expressed only in leaves.
Unlike leaf veins, cortical bundles must remain functional for decades, as long as the cortex is photosynthetic and the epidermis is permitting gas exchange (cactus epidermis lives for years; see Epidermis below). A vascular cambium arises in each cortical bundle and produces abundant secondary phloem and, in most cases, at least a bit of secondary xylem (Mauseth and Sajeva, 1992). As is typical of all vascular plants, sieve tube members and companion cells collapse af