Wood Chemical Composition in Species of Cactaceae: The Relationship between Lignification and Stem Morphology

In Cactaceae, wood anatomy is related to stem morphology in terms of the conferred support. In species of cacti with dimorphic wood, a unique process occurs in which the cambium stops producing wide-band tracheids (WBTs) and produces fibers; this is associated with the aging of individuals and increases in size. Stem support and lignification have only been studied in fibrous tree-like species, and studies in species with WBTs or dimorphic wood are lacking. In this study, we approach this process with a chemical focus, emphasizing the role of wood lignification. We hypothesized that the degree of wood lignification in Cactaceae increases with height of the species and that its chemical composition varies with wood anatomy. To test this, we studied the chemical composition (cellulose, hemicellulose, and lignin content) in 13 species (2 WBTs wood, 3 dimorphic, and 8 fibrous) with contrasting growth forms. We also analyzed lignification in dimorphic and fibrous species to determine the chemical features of WBTs and fibers and their relationship with stem support. The lignin contents were characterized by Fourier transform infrared spectroscopy and high performance liquid chromatography. We found that 11 species have a higher percentage (>35%) of lignin in their wood than other angiosperms or gymnosperms. The lignin chemical composition in fibrous species is similar to that of other dicots, but it is markedly heterogeneous in non-fibrous species where WBTs are abundant. The lignification in WBTs is associated with the resistance to high water pressure within cells rather than the contribution to mechanical support. Dimorphic wood species are usually richer in syringyl lignin, and tree-like species with lignified rays have more guaiacyl lignin. The results suggest that wood anatomy and lignin distribution play an important role in the chemical composition of wood, and further research is needed at the cellular level.     

DEVELOPMENTALLY VARIABLE,POLYMORPHIC WOODS IN CACTI

Sixteen genera of cacti were discovered to have polymorphic wood, that is, the plants produce one type of wood while young but a different type when older. The polymorphisms are: fibrous wood (with vessels and scanty paratracheal parenchyma) followed by parenchymatous wood (with vessels but few or no fibers) (Hylocereus venezuelensis, Dendrocereus nudiflorus, Borzicactus humboldtii, Haageocereus australis, Morawetzia sericata, Stephanocereus leucostele, Trichocereus schickendantzii); WBT wood (with wide-band tracheids, vessels, and apotracheal parenchyma but few or no fibers) followed by fibrous wood (Buiningia aurea, Oreocereus celsianus, Vatricania guentheri); WBT wood followed by parenchymatous wood (Echinopsis tubiflora, Gymnocalycium marsoneri, G. oenanthemum, Notocactus warasii, Parodia maassii); trimorphic wood in which WBT wood is followed by fibrous wood, which is followed by parenchymatous wood (Melocactus intortus, Arrojadoa braunii). The different phases within each plant may differ in vessel cluster size, percentage of the vessels that are solitary, diameter of vessels, and lignification of ray cells. Several of these genera are not closely related to the others, so wood polymorphism may have arisen several times.     

Morpho‐anatomical diversity of the underground systems of Arrojadoa (Cactaceae), an endemic Brazilian genus

Members of Arrojadoa exhibit a variety of underground structures that can originate from roots or stems. Although the development of underground structures of stem origin in Arrojadoa represents a unique trait among Cactaceae of eastern Brazil, no detailed reports on the morphological diversity of such structures are available. The present morpho‐anatomical study of the underground systems of Arrojadoa has demonstrated that a single species can exhibit one or more structural types, such as single or branched stem tubers, short thick stems and/or long subterranean stems, thick and fleshy contractile roots and normal fibrous roots. Various morpho‐anatomical structures relating to the underground storage systems in Arrojadoa spp. have also been observed, including thick contractile roots consisting mainly of secondary xylem formed by fibrous wood with wide‐band tracheids (WBTs) and underground stems with a wide cortical region and WBTs‐type wood. Based on the evidence presented, we suggest that such traits, together with the occurrence of contractile roots associated with underground stems, are important adaptive strategies for the survival of the plants during seasonal drought in areas of cerrado (savannah), campo rupestre (rocky uplands) and caatinga (dry thorny scrubland). © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 108–128.     

Water-storing and Cavitation-preventing Adaptations in Wood of Cacti

Ancestral cacti presumably had abundant, fibrous, heavily lignifiedwood, similar to that present in the relictual, leaf-bearinggenus Pereskia. During the evolutionary radiation of the subfamilyCactoideae, diverse types of bodies and woods arose. Severalevolutionary lines have retained an abundant, fibrous wood:all wood cells, even ray cells, have thick lignified walls,and axial parenchyma is only scanty paratracheal. Aside froma diversity of vessel diameters, there seems to be little protectionagainst cavitation during water-stress, and little water-storagecapacity. This strong wood permits the plants to be tall andto compete for light in their tree-shaded semi-arid habitats.In other evolutionary lines, the wood lacks fibres, and almostall cells have thin, unlignified walls. Vessels occur in anextensive matrix of water-storing parenchyma, and tracheidsare also abundant, constituting over half the axial tissue insome species. There is excellent protection against cavitation,but little mechanical support for the plant body; however, theseplants are short and occur in extremely arid, unshaded sites.Scandent, vinelike plants of two genera produce a dimorphicwood—while their shoots are extending without externalsupport, they produce fibrous, lignified wood, but after leaningagainst a host branch, they produce a parenchymatous, unlignifiedwood.Copyright 1993, 1999 Academic Press Cactaceae, cactus, water-stress, wood, evolution, xylem     

Wide-band tracheids in genera of Portulacaceae: novel, non-xylary tracheids possibly evolved as an adaptation to water stress

Wide-band tracheids (WBTs) are novel tracheids with wide, lignified secondary walls that intrude deeply into the cell lumen when viewed in transverse sections. These tracheids are found in a few genera in related families in the order Caryophyllales: Aizoaceae, Cactaceae, and Portulacaceae. WBTs in these three families vary in (1) systematic occurrence (found in more highly derived genera in each family), (2) location in plant organs, and (3) structure and dimensions. In addition, an analysis was conducted of WBT cell walls to test the hypothesis that WBTs evolved as an adaptation to water stress (i.e., the wide secondary walls should prevent collapse of the primary wall during water stress). The cell wall data show that primary cell walls in WBTs cannot inwardly collapse to occlusion, thus providing support for the water stress hypothesis of WBT evolution. With consideration of their systematic occurrence, the molecular phylogenetic data, and data here showing support for a water stress adaptive origin, it is logical to assume that WBTs evolved in genera that were adapting to environments undergoing a rapid trend toward aridification.     

Effect of light on seed germination and seedling shape of succulent species from Mexico

Aims Light requirements for cactus seed germination have been considered to be associated with their adult plant height and seed mass, but this has not been thoroughly studied for other succulent species. In order to understand seed photosensitivity from desert species belonging to Asparagaceae (subfamily Agavoideae) and Cactaceae, we performed a germination experiment with and without light for 12 species and 2 varieties from 1 species from the Southern Chihuahuan Desert. We also determined if adult growth is totally determined by seedling 'growth form' in cacti.Methods We performed a germination experiment using light and darkness for 13 species from Southern Chihuahuan Desert: 10 rosette species (Asparagaceae), as well as 1 globose, 1 columnar and 2 varieties from 1 depressed-globose species (Cactaceae). The response variables were seed germination percentage and relative light germination (RLG). In addition, in order to determine if adult-globose cacti could have cylindrical seedlings, we calculated the shape index (height/width ratio) for Coryphanta clavata and Mammillaria compressa .Important findings All species were considered neutral photoblastic. Eleven species had similar seed germination in both light and dark conditions, and three taxa (M. compressa and the two varieties of Ferocactus latispinus) showed higher germination with light than without it. Agave salmiana, M. compressa and the two varieties of F. latispinus had higher RLG than the other species. Seed mass was an important factor because with higher seed mass there was lower dependence to light. These findings support the hypothesis that small seed mass and light requirements have coevolved as an adaptation to ensure germination. One adult-globose cactus species, M. compressa, and one adult-columnar species, C. clavata, had small seeds and neutral fotoblasticism. Seedlings from these two species exposed to light were cylindrical and those under darkness conditions were columnar. Perhaps seeds from this species are able to germinate in the dark because they produce columnar seedlings with the ability to emerge from greater soil depths where sunlight cannot penetrate.     

Distribution and Chemical Composition of Lignin in Secondary Xylem of Cactaceae

Cactaceae family has heterogeneity in the accumulation of lignocellulose due to the diversity of shapes and anatomy of the wood. Most studies focus on fibrous and dimorphic species; but the non-fibrous species are poorly studied. The aims of this work were to analyze the syringyl/guaiacyl ratio of lignin and its distribution in secondary xylem, especially in non-fibrous species. The syringyl/guaiacyl (S/G) ratio was quantified from 34 species of cacti by nitrobenzene oxidation of free-extractive wood. The distribution of lignocellulose in wood sections stained with safranin O/fast green was determined with epifluorescence microscopy. The S/G ratio was heterogeneous; most of the non-fibrous species had a higher percentage of syringyl, while the fibrous ones accumulate guaiacyl. Fluorescence emission showed that vessel elements and wide-band tracheids had similar tonalities. It is hypothesized that the presence of a higher percentage of syringyl in most cacti is part of the defense mechanism against pathogens, which together with the succulence of the stem represent adaptations that contribute to survival in their hostile environments.     

Allometric neoteny and the evolution of succulence in cacti

With the objective of analysing the role of heterochrony in the evolution of succulence in the cactus family, a comparative study of xylem development in six species with contrasting morphologies was carried out. Two woody leaf-bearing cacti and four succulent cactus species belong to different subdivisions within the family were analysed. In each species and for different ages, vessel-element length was measured, vessel-element lateral wall-pitting described and the percentage of xylem and parenchyma in the stem quantified. In the succulent species it was found that vessel element length did not change between juvenile and adult wood, that wall-pitting in adult plants was similar to that of seedlings, and that the woody tissue in adult plants was organized in vascular bundles as in the primary tissue of seedlingS. Leaf-bearing cacti, in contrast, changed in both vessel element length and wall-pitting when secondary wood was produced, and the secondary woody tissue of adult plants was organized in a continuous cambial cylinder as in most dicotyledonS. An allometric analysis suggests that a retardation in the developmental rate of woody tissues (allometric neoteny) is the main mechanism in the development of succulence in cacti.     

Basal cactus phylogeny: implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form

The cacti are well-known desert plants, widely recognized by their specialized growth form and essentially leafless condition. Pereskia, a group of 17 species with regular leaf development and function, is generally viewed as representing the "ancestral cactus," although its placement within Cactaceae has remained uncertain. Here we present a new hypothesis of phylogenetic relationships at the base of the Cactaceae, inferred from DNA sequence data from five gene regions representing all three plant genomes. Our data support a basal split in Cactaceae between a clade of eight Pereskia species, centered around the Caribbean basin, and all other cacti. Two other Pereskia clades, distributed mostly in the southern half of South America, are part of a major clade comprising Maihuenia plus Cactoideae, and Opuntioideae. This result highlights several events in the early evolution of the cacti. First, during the transition to stem-based photosynthesis, the evolution of stem stomata and delayed bark formation preceded the evolution of the stem cortex into a specialized photosynthetic tissue system. Second, the basal split in cacti separates a northern from an initially southern cactus clade, and the major cactus lineages probably originated in southern or west-central South America.     

Seeds photoblastism and its relationship with some plant traits in 136 cacti taxa

Seed germination triggered by light exposure (positive photoblastism) has been determined in quantitative studies for numerous plant families and species. For Cactaceae, positive photoblastism is thought to be associated with life form and seed mass, but this association has never been evaluated. To explore hypotheses on associations between seed mass, seed dispersal, seed dormancy, life form, taxa and plant height with Relative Light Germination (RLG) in Cactaceae, we evaluated the effect of light on seed germination of 136 taxa. The taxa studied are native to several countries: México, Chile, Argentina, Brazil, Perú, USA, and Venezuela. Seed traits contrasted with RLG were life form, seed mass, seed dispersal, seed dormancy, adult plant height and taxon. We found some differences between RLG among taxa; Cacteae, Pachycereeae and Trichocereeae had higher RLG than Notocacteae. RLG was lower for seeds from taller than for shorter taxa, and lower for taxa with heavier seeds than for taxa with lighter seeds. Dispersal syndrome groups varied with RLG. RLG did not differ between cylindrical and globose taxa. Trends found here were in agreement with expectations for small-seeded species to have a light requirement to germinate more often than large-seeded species. This is the first time that cactus height is related to photoblastism. It is possible that seeds from tall plants are larger and thus have the capacity to produce taller seedlings than those from small plants, and that seedlings from large seeds with more resources have the ability to emerge from greater soil depths than those from small seeds.     

Crassulacean acid metabolism photosynthesis in columnar cactus seedlings during ontogeny: the effect of light on nocturnal acidity accumulation and chlorophyll fluorescence

Columnar cacti have been traditionally classified as crassulacean acid metabolism (CAM) plants, though recent research indicates some cactus seedlings employ the C(3) pathway. To verify this last result, we measured acidity fluctuations for five columnar and one globular cactus species in seedlings from 1 to 48 d old after experimental exposure to 60% and 30% full sunlight, and in adult plants in the field. Using light-response curves of chlorophyll fluorescence, we determined photosynthetic efficiency (ΔF/Fm'), maximum electron transport rate (ETR(max)) and saturating photosynthetically active photon flux density (PPFD(sat)). All seedlings used the CAM pathway from their first day of development, and increases in nocturnal acidity depended on species, light treatment, and age. The CAM pathway was also found in adult plants. Cactus seedlings were able to acclimatize to light conditions by making photochemical adjustments, mainly by modifying the level of light at which photosystem II is saturated (PPFD(sat)). The presence of CAM in the seedlings of columnar cacti increases water-use efficiency and reduces the risk of photoinhibition. This could favor survival in the highly variable light levels characteristic of the desert environments of columnar cacti.     

Evolution of extreme xeromorphic characters in wood: a study of nine evolutionary lines in Cactaceae

Vessels of xeric-adapted woods have been predicted to be narrower than those of mesic-adapted woods, to occur at higher densities, to occur in larger clusters, and to have a greater percentage of them in clusters. These predictions were tested by comparing wood structure of several evolutionary lines of xeric-adapted cacti to that of mesic-adapted Pereskia, which probably resembles the ancestral cacti. Although derived cacti occur in habitats with water stress ranging from mild (rain forests) to severe (open deserts with little vegetation other than cacti), as long as plants retain wood with an ordinary fibrous matrix, wood characters are remarkably uniform and not correlated with habitat aridity. However, in several evolutionary lines, novel wood types occur with characters that fulfill the predictions for xeric-adapted woods listed above. However, conductive area (fraction of wood transverse-sectional area occupied by conduits) and estimated specific conductance (conductance per square millimetre) are correlated with shoot height (the need for mechanical support from xylary fibers) rather than with habitat aridity: tall plants transport water through relatively few, wide vessels, permitting much of the wood volume to consist of fibers. Small plants with little wood use large numbers of narrow vessels rather than small numbers of wide ones, thereby achieving conductive safety.     

Differentiation diversity of Argentine cacti and its relationship to environmental factors

Abstract. We studied the differentiation diversity (β-diversity or species turnover) patterns of the three main cactus growth forms (columnar, opuntioid and globose) in 318 (1° × 1°) squares covering Argentina. We analysed the degree of association between species turnover of each growth form with the spatial variation of a set of 15 environmental variables. Species turnover was estimated in two ways: (1) by calculating species turnover along latitudinal and longitudinal gradients and (2) by evaluating the species turnover between each square and its eight surrounding neighbouring grid cells. For the three growth forms, species turnover in latitudinal transects was mostly related to the mean within-transect values of certain environmental variables, while in longitudinal transects it was related to the variation of some environmental variables within the transect rather than to their mean values. For columnar species, transect species turnover was mainly associated with variation in temperature, confirming the temperature-sensivity of this growth form. For opuntioid species, turnover along transects was mainly related to topographic variables. In the case of globose cacti, transect turnover was associated with variation in temperature and rainfall. For the three growth forms, areas of high turnover coincided with marked transitions between different biogeographic provinces, while the areas with lowest species turnover coincide with topographically and climatically uniform plains. Species turnover between individual squares was positively associated with the proportion of summer rainfall in globose cacti, the variation of mean annual temperature in columnar cacti and was negatively related to mean annual temperature in opuntioid cacti. Compared to the other growth forms, globose cacti presented a much larger proportion of squares with a high species turnover. In general, differentiation diversity was lower for the opuntioid and the columnar species, two growth forms with higher dispersal ability and was highest for the globose cacti, which have the lowest dispersal capacity. Environmentally heterogeneous areas, where large-scale transitions between biomes occur, have exceptionally high species turnover, and are important target areas for the conservation of biodiversity.     

miRNA control of vegetative phase change in trees

After germination, plants enter juvenile vegetative phase and then transition to an adult vegetative phase before producing reproductive structures. The character and timing of the juvenile-to-adult transition vary widely between species. In annual plants, this transition occurs soon after germination and usually involves relatively minor morphological changes, whereas in trees and other perennial woody plants it occurs after months or years and can involve major changes in shoot architecture. Whether this transition is controlled by the same mechanism in annual and perennial plants is unknown. In the annual forb Arabidopsis thaliana and in maize (Zea mays), vegetative phase change is controlled by the sequential activity of microRNAs miR156 and miR172. miR156 is highly abundant in seedlings and decreases during the juvenile-to-adult transition, while miR172 has an opposite expression pattern. We observed similar changes in the expression of these genes in woody species with highly differentiated, well-characterized juvenile and adult phases (Acacia confusa, Acacia colei, Eucalyptus globulus, Hedera helix, Quercus acutissima), as well as in the tree Populus x canadensis, where vegetative phase change is marked by relatively minor changes in leaf morphology and internode length. Overexpression of miR156 in transgenic P. x canadensis reduced the expression of miR156-targeted SPL genes and miR172, and it drastically prolonged the juvenile phase. Our results indicate that miR156 is an evolutionarily conserved regulator of vegetative phase change in both annual herbaceous plants and perennial trees.     

Demographic trends in the Cactaceae

Although our biological knowledge regarding cactus species is thorough in many areas, only in recent years have ecologists addressed their demographic behavior. Here we attempt a first review of the present knowledge on cactus demography, including an analysis of the published information on species with different growth forms and life-history traits. Our review shows that cactus distribution ranges are determined by environmental heterogeneity and by species-specific physiological requirements. Temperature extremes may pose latitudinal and altitudinal distribution limits. At a more local scale, soil properties dramatically affect cactus distribution. Most cacti show a clumped spatial distribution pattern, which may be the reflection of a patchy resource distribution within their heterogeneous environments. The association of cacti with nurse plants is another factor that may account for this aggregated distribution. Many cacti grow in association with these perennial nurse plants, particularly during early life-cycle phases. The shade provided by nurse plants results in reduced evapotranspiration and buffered temperatures, which enhance cactus germination and establishment. In some cases a certain degree of specificity has been detected between particular cactus species and certain nurse plants. Yet some globose cacti may establish in the absence of nurse plants. In these cases, rocks and other soil irregularities may facilitate germination and establishment. Cacti are slow-growing species. Several abiotic factors, such as water and nutrient availability, may affect their growth rate. Competition and positive associations (i.e., mycorrhizae and nurse-cacti association) may also affect growth rate. Age at first reproduction varies greatly in relation to plant longevity. In general, cactus reproductive capacity increases with plant size. Populations are often composed of an uneven number of individuals distributed in the different size categories. This type of population structure reflects massive but infrequent recruitment events, apparently associated with benign periods of abundant rainfall. A few cactus species have been analyzed through the use of population-projection matrices. A total of 17 matrices were compiled and compared. Most of them reflect populations that are close to the numerical equilibrium (λ = close to unity). Elasticity analyses revealed that the persistence of individuals in their current size category (“stasis”) is the demographic process that contributes the most to population growth rate. Also, adult categories (rather than juveniles or seedlings) show the largest contributions to λ. No differences were apparent regarding this matter between cacti with different life-forms. This review shows that our knowledge of cactus population ecology is still incipient and rather unevenly distributed: some topics are well developed; for others the available information is still very limited. Our ability to preserve the great number of cactus species that are now endangered depends on our capacity to deepen our ecological understanding of their population processes.     

Chemical Composition of Cacti Wood and Comparison with the Wood of Other Taxonomic Groups

The aims of this study were to determine the wood chemical composition of 25 species of Cactaceae and to relate the composition to their anatomical diversity. The hypothesis was that wood chemical components differ in relationship to their wood features. The results showed significant differences in wood chemical compounds across species and genera (P < 0.05). Pereskia had the highest percentage of lignin, whereas species of Coryphantha had the lowest; extractive compounds in water were highest for Echinocereus, Mammillaria, and Opuntia. Principal component analysis showed that lignin proportion separated the fibrous, dimorphic, and non‐fibrous groups; additionally, the differences within each type of wood occurred because of the lignification of the vascular tissue and the type of wall thickening. Compared with other groups of species, the Cactaceae species with fibrous and dimorphic wood had a higher lignin percentage than did gymnosperms and Acer species. Lignin may confer special rigidity to tracheary elements to withstand desiccation without damage during adverse climatic conditions.     

Anatomical Adaptations to Xeric Conditions in Maihuenia (Cactaceae), a Relictual, Leaf-Bearing Cactus

Maihuenia and Pereskia, constitute Pereskioideae, the subfamily of Cactaceae with the greatest number of relictual features, but the two genera differ strongly in habit and ecological adaptations. Plants of Maihuenia occur in extremely xeric regions of Patagonia and are small cushion plants with reduced, terete leaves and soft, slightly succulent trunks. Plants of Pereskia occur only in mesic or slightly arid regions and are leafy trees with hard, woody trunks and thin, broad leaves. Maihuenias have many more anatomical adaptations to arid conditions than do pereskias: maihuenias lack sclerenchyma in their phloem and cortex (M. poeppigii also lacks xylem sclerenchyma and can contract during drought); their wood consists of vessels, axial parenchyma, and wide-band tracheids and can store water as well as minimize embolism damage; one species channelizes water flow by producing intraxylary bark; and at least some stem-based photosynthesis occurs because maihuenias have small patches of persistent stem epidermis that bears stomata and overlies a small amount of aerenchymatous chlorenchyma. Pereskias lack all these features. Although closely related, maihuenias have fewer relictual features than do pereskias, and plants of Pereskia probably are more similar to the ancestral cacti. Received 8 March 1999/ Accepted in revised form 29 May 1999     

Spatial relationships between cacti and nurse shrubs in a semi-arid environment in central Mexico

Abstract. The Zapotitlán de las Salinas valley, central Mexico, harbours a high diversity of cacti. Pattern analysis indicated that the establishment of two columnar cacti, Neobuxbaumia tetetzo and Cephalocereus hoppenstedtii, and of three small globose cacti, Coryphantapallida, Mammillaria colina andM casoi, is aggregated and associated with perennial nurse shrubs. Some nurse species, Castela tortuosa, Caesalpinia melanadenia and Eupatorium spinosarum have a higher number of cacti beneath their canopies than would be expected by chance. A replacement pattern was found between the columnar cacti and their nurses, an aspect which was not found with the globose cacti. Following the assumption that protection against excessive radiation is the main factor determining the nurse effect, the azimuth orientation of the cacti with respect to their nurses was evaluated. Only Coryphanta pallida presented a non-random distribution with a tendency towards the North and West. The difference in maximum temperature between the soil surface under the different nurse species and of open spaces, which is reached at midday, was 16 °C. No significant differences were found in beneath-canopy temperatures for the three nurse species considered. Soil nitrogen levels were significantly lower beneath the different nurse plants than in open spaces. This result suggests that soil fertility is not an important factor in the nurse-plant phenomenon in Zapotitlán.