Leaf epidermal features of Lithocarpus (Fagaceae) from China and their systematic significance

The leaves of 52 species of Lithocarpus in China were studied. The adaxial leaf epidermis was investigated by light microscopy. Epidermal cells of the adaxial surface were classified into three types on the basis of the outline of their anticlinal walls, i.e. sinuate, straight and curved. The abaxial leaf epidermis was investigated by light microscopy and scanning electron microscopy. The following types of trichome were observed: appressed parallel tuft, stellate, fused stellate, papillae, stipitate fasciculate, solitary unicellular, appressed laterally attached unicellular, curly thin‐walled unicellular, bulbous and thin‐walled peltate. The fused stellate, appressed laterally attached unicellular and curly thin‐walled unicellular trichomes were reported in Lithocarpus for the first time. The appressed parallel tuft trichome, which is recognized as a salient characteristic of Lithocarpus, was not found in 15 species. A cladistic analysis was performed on the basis of the leaf epidermal features. According to the leaf epidermal features and several morphological characteristics, 26 of the 52 species could be divided into seven groups. Similar groups can be found in Barnett's and Camus' systems. The trichomes of four genera in Fagaceae are listed and compared. Lithocarpus had 14 types of trichome, 11 of which were identical to types found in Quercus, more than in Castanopsis and Cyclobalanopsis. The evolutionary trends of trichomes in Fagaceae are discussed and a new point of view is raised. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 216–228.     

Leaf epidermal features of Salix species (Salicaceae) and their systematic significance

? Premise of the study: The classification of the genus Salix has historically been intrinsically difficult due to its propensity toward plasticity and high variation in diagnostic morphological characters. We investigated leaf epidermal characteristics, focusing on the stomatal apparatus because it may provide critical insights into the evolution and taxonomy of Salix and its closely related genera. ? Methods: Light microscopy was used to examine the leaf epidermal features in 32 taxa of Salix. ? Key results: Characters such as shape, size, and density of stomatal complexes were very useful in differentiating Salix species. Variation in features of stomatal apparatus in Salix is wider than previously known. Moreover, the type of stomatal complex proved to be very helpful in discriminating Chosenia as members of the genus Salix. ? Conclusions: The results of the present study support the placement of Chosenia within Salix and the combining of subgenera Chamaetia and Vetrix because of similarities in their unique stomatal apparatus.     

中国杜鹃花属的叶表皮特征及其系统学意义

通过光学显微镜和扫描电镜对国产杜鹃花属Rhododendron6个亚属48种4变种植物的叶表皮特征进行观察,结果表明叶表皮的鳞片、腺体、表皮毛的有无和气孔器的类型具有一定的系统学意义。光学显微镜下可见：叶表皮细胞形状为多边形、不规则形,垂周壁式样为较平直、浅波状和波状．气孔器普遍存在于下表皮,上表皮未见气孔器分布,其类型均为无规则形。杜鹃亚属subgen．Rhododendron叶表皮具有鳞片,在扫描电镜下可见气孔器散生于指状突起之间,有别于无鳞类杜鹃花。常绿杜鹃亚属subgen．Hymenanthes和映山红亚属subgen．Tsutsusi有多种不同叶表皮类型;除了凯里杜鹃R．westlandii和弯蒴杜鹃R．henryi形态较特殊之外,马银花亚属subgen．Azaleastrum的马银花组sect．Azaleastrum和长蕊杜鹃组sect．Choniastrum微形态区别不明显。羊踯躅亚属subgen．Pentanthera的羊踯躅R．molle叶表皮有表皮毛,无腺体,气孔器密生,外拱盖形状不对称,外围有多层波形条纹突起可与其他亚属区分：而叶状苞亚属subgen．Therorhodion的叶状苞杜鹃R．redowskianum保卫细胞有明显的T型加厚,与其他亚属种类明显不同,与分子系统发育研究得到的“叶状苞亚属是杜鹃花属的基部类群”的结果吻合。本研究还依据叶表皮微形态特征讨论了一些近缘种类的关系。     

Leaf epidermal features of Rhododendron (Ericaceae)from China and their systematic significance

Rhododendron is the largest genus within the subfamily Rhododendroideae, which has about 1000 known species in the world and more than 500 species in China. Since the genus was established by Linnaeus, its infrageneric relationships have been well studied by many taxonomists on the basis of morphological characters and molecular data. In 1996, Chamberlain et al. proposed a new system of Rhododendron with eight subgenera, i.e., Azaleastrum, Candidastrum, Hymenanthes, Mumeazalea, Pentanthera, Rhododendron, Therorhodion, and Tsutsusi. In this paper, micromorphological characters of leaf epidermis in 4 varieties, 48 species, 6 subgenera of Rhododendron from China were examined using light microscopy (LM) and scanning electron microscopy (SEM). Leaf epidermal features are described and micromorphological types are distinguished here according to morphological characters such as scale, gland, foliar trichome and stomatal apparatus of leaf epidermis. It is shown that the leaf epidermal cells are usually irregular or polygonal in shape. The patterns of anticlinal walls are straight, arched or undulate. The stomatal apparatuses are anomocytic and are usually found on abaxial, not adaxial, epidermis. The results also show that: (1) the lepidote rhododendron (i.e., subgen. Rhododendron), which has both scales and papillae on leaf epidermis, differs distinctly from the elepidote rhododendron; (2) three types of leaf epidermis are identified in subgen. Hymenanthes (i.e., R. fortunei-type, R. chihsinianum-type and R. simiarum-type), whereas four in subgen. Tsutsusi (i.e., R. mariesii-type, R. simsii-type, R. mariae-type and R. flosculum-type); (3) except for R. westlandii and R. henryi, the species of subgen. Azaleastrum show similar morphological characters, i.e., dense stomatal apparatuses surrounded by ringed or discontinuous striates; (4) R. molle of subgen. Pentanthera differs from the species of other subgenera on morphological characters such as foliar trichomes, dense stomatal apparatuses with asymmetrical outer stomatal rims surrounded by undulate-striates, and no gland; (5) only R. redowskianum is found with distinct T-pieces at the polar region of guard cells in Rhododendron. The results support the conclusion inferred from molecular systematic studies that subgen. Therorhodion is the basal clade of Rhododendron. Finally, the relationships between the closely related species are also discussed on the basis of leaf epidermal features.     

Leaf epidermis of Quercus subgen. Cyclobalanopsis (Oerst.) Schneid. (Fagaceae)

The characters of leaf epidermis (mainly epidermal cells, stomata, trichomes) have been examined in 48 species of Quercus subgen. Cyclobalanopsis of the Fagaceae. The adaxial leaf epidermis was investigated under light microscope. The epidermal cells of this surface are of two types in terms of the outline of their anticlinal wall. One type is characterized by having straight wall, and this type has been observed in most of the species studied, while the other is characterized by having sinuate or sinuolate wall, and this type has been found only in eight species, such as Q. blakei and Q. hui. There exist two types of trichome-bases on this surface: in one type the bases are singlecelled, and this type has been found in most of the species studied, such as Q. oxyodon and Q. augustinii; while in the other the bases consist of a group of cells, and this type has been found only in nine species, such as Q. thorelii and Q. chungii. The abaxial leaf epidermis was investigated under light microscope and scanning electron microscope. The epidermal cells and the trichome-bases on this surface under LM are in morphology essentially similar to those on the adaxial surface. The stomata under LM include three types: cyclocytic, subcyclocytic and anomocytic. The stomatal density is of some diagnostic value to distinguish between closely related species, e.g. the stomatal density in Q. glauca is higher than that in Q. schottkyana. Under SEM the stomata are elliptical or roundish. The most noteworthy feature of the adaxial leaf epidermis is the trichomes. Eight types of trichomes have been observed under SEM: simple-uniseriate, solitary, papillae, stellate, fused-stellate, stipitate-fasciculate, multiradiate and jellyfish-like. The first type, i.e. the simple-uniseriate trichome, is glandular, other six types, i.e. the solitary, papillae, stellate, fused-stellate, stipitate-fasciculate and multiradiate trichomes, are non-glandular, and the last one, i.e. the jellyfish-like trichome, may represent an intermediate type in structure between the glandular and the non-glandular trichomes. Papillae are very common in subgen. Cyclobalanopsis although in the Fagaceae they were previously reported only in a few species of Lithocarpus. The jellyfish-like trichome, observed only in Q. sichouensis, is reported in the Fagaceae for the first time. The evolutionary trends of trichomes are discussed. The trichomes seem to evolve toward the direction of increasing complexity in structure. Papillae are considered as the pedomorphism of trichomes. From papillae the solitary trichomes and then the stellate ones have evolved. The complicated trichome types with more arms may be produced from relatively simple ones with fewer arms by means of varions fusion: several stellate trichomes are fused to form the fused-stellate ones by basal fusion, and by the same way the fused-stellate ones to form the stipitate-fasciculate ones; the multiradiate trichomes are formed by the stellate ones, in which the arms emerge in a variety of seemingly random directions from a typically rounded common base. Based on the above results, it is considered that the trichome features are of important significance for a better understanding of the infrageneric division of Quercus and the phylogenetic relationships between this genus and the other genera in the Fagaceae. The very common presence of papillae in Quercus subgen. Cyclobalanopsis and in a few species of Lithocarpus may indicate that subgen. Cyclobalanopsis is a quite natural group on the one hand, and may have close relationship with Lithocarpus on the other hand. The thin-walled, jellyfish-like trichomes found in Q. sichouensis are in structure similar to the “glandular” peltate trichomes in Trigonobalanus, a genus generally regarded as the most primitive in subfam. Quercoideae, indicating that the affinity between subgen. Cyclobalanopsis and Trigonobalanus may becloser than that between subgen. Quercus and Trigonobalanus.     

栎属青冈亚属（壳斗科）的叶表皮研究

利用光镜和扫描电镜观察了栎属青冈亚属Quercus subgen. Cyclobalanopsis 48种植物的叶表皮,尤以对叶下表皮的毛被特征观察较为仔细。共观察到8种不同类型的叶表皮毛：单列毛、单毛、乳突、星状毛、溶和星状毛、具柄束毛、多出毛和水母状毛。其中乳突在青冈亚属中较常见,而在壳斗科其他属中仅在石栎属 Lithocarpus 少数种类中有报道;水母状毛首次在壳斗科中发现。毛被可能遵循以下的演化规律：乳突→单毛→星状毛;星状毛依照从简单→复杂的演化途径,分化出各种形态各异和结构复杂的毛系。初步讨论了毛被以及叶表皮其他特征(如毛基细胞和表皮细胞的形态、气孔的类型和密度等)的分类和系统学意义。     

Comparative leaf surface morphology and molecular data of five oaks of the subgenus Quercus Oerst (Fagaceae)

Abstract

Comparisons between different data sets are important in taxonomic studies, particularly for complex taxa such as the genus Quercus. However, there is scarce literature on comparative morphological and molecular analyses in oaks. Here we describe an experimental approach based on the correlation between micromorphological features and molecular data in order to characterize and discriminate among five closely related species: Q. robur, Q. petraea, Q. frainetto, Q. pubescens and Q. virgiliana.     

A Study on the Morphology of Foliar Trichomes of Evergreen Oaks (Quercus) in China and Its Implication in Taxonomy

Most of the evergreen oaks (Quercus L.) are endemic to China and distributed in a large moutainous area of southwestern China at an altitude of 2600-4000m. The delimitation of sections and species in the group has not been satisfactorily solved. The foliar trichomes are very an important character in identifying species of oaks. As a result of observation on 17 species and 2 varieties of evergreen oaks in China under scanning electron microscope, ten types of foliar trichomes are recognized: Simpleuniseriate, Simple-branched, Bulbous, Rosulate, Solitary, Stipitate-fasciculate, Fasciculate, Multiradiate, Stellate and Fused-stellate. The first four types fall into glandular trichomes and the last six non-glandular trichomes. The taxa examined have a combination of various types of the trichomes. All the evergreen oaks have non-glandular trichomes on their foliar epidermis, but glandular trichomes occur solely in certain taxa. These two types of foliar trichomes are obviously different in structure and function, which represent different adular trichomes and the last six non-glandular en oaks are divided into two groups: the glandular group and the non-glandular group according to the types of foliar trichomes and it is reasonable to divide the evergreen oaks into two sections: Sect. Suber (Reichenb.) Spach and Sect. Englerianae (A. Camus) Hsu et Jen. Foliar trichomes of the evergreen oaks show a continuity in density from species predominately with glandular trichomes at a high altitude to species solely with non-glandular trichomes at a low elevation. The characters of branching of foliar trichomes, especially the number of branches, can imply to some extent the evolutionary position of a given evergreen species. Considering the types, density and branches of foliar trichomes combined the evolutionary relationships among the evergreen oaks in China are proposed. Q. gilliana is the startpoint, from where evolution took place in two directions: glandular and non-glandular. In the glandular direction envolved are Q. aquifolioides, Q. longispica and Q. guyavaefolia. Q. pannosa is a species with the most types and highest number of glandular trichomes. In non-glandular line aligned are Q. spinosa, Q. senescens, Q. senescens var. muliensis, Q. monimotricha with the reduction of glandular trichomes and increase of non-glandular trichomes. After Q. tungmaiensis no glandular trichomes appear and it solely depends on non-glandular trichomes to protect itself. Q. granchetii is the climax in the non-glandular line with the highest density and number of branches of foliar trichomes. And then some species, such as Q. engleriana, Q. phillyraeoides, have few or no trichomes. Q. dolicholepis, Q. baronii and Q. baronii var. capitata show the close re-lationships because they share fused-stellate trichomes.     

Two-year cycles of synchronous acorn and leaf production in biennial-fruiting evergreen oaks of subgenus Cyclobalanopsis (Quercus, Fagaceae)

Many masting species switch resources between vegetative growth and reproduction in mast and non-mast years. Although masting of oak species is well known, there have been few investigations of the relationship between vegetative growth and reproduction based on long-term monitoring data, especially in evergreen oaks of subgenus Cyclobalanopsis. We investigated annual variations over 13?years in acorn and leaf production of three evergreen oak species in subgenus Cyclobalanopsis, genus Quercus (Fagaceae)??Q. acuta, Q. salicina and Q. sessilifolia??in western Japan. In these species, the maturation of acorns occurs in the second autumn after flowering, which is known as a biennial-fruiting habit. We found a pattern of acorn production and masting in alternate years that was synchronized in all three species. Masting was not correlated with temperature and precipitation. Annual leaf-fall also showed 2-year cycle in the three oak species; peak years were synchronized between species and peak leaf-fall alternated with acorn production in all three species. Furthermore, there was a significant negative correlation between acorn and leaf production in all three species. Data showing 2-year cycles of acorn and leaf production and the negative correlation between them supports the hypothesis of resource switching between vegetative growth and reproduction. The 2-year cycle might be the basic, intrinsic rhythm of resource allocation in biennial-fruiting Cyclobalanopsis species.     

First record of Erysiphe quercicola (Ascomycota: Erysiphales) on species of Quercus subgenus Cyclobalanopsis (evergreen oaks,Fagaceae)

During the DNA sequence analyses of specimens on Quercus subgenus Cyclobalanopsis deposited as Erysiphe gracilis or Cystotheca wrightii, some specimens exhibited DNA sequences that are different from the sequences of the two species. Based on BLAST search and morphological observations, the true causal agent was identified as E. quercicola. This is the first record of E. quercicola on species of subgenus Cyclobalanopsis. Previous studies revealed that E. quercicola is plurivorous infecting a wide range of tropical fruit trees and woody plants. Further studies are needed to address the question as to why only E. quercicola infect species of subgenus Cyclobalanopsis.     

Competitive suppression of Quercus douglasii (Fagaceae) seedling emergence and growth

Reduced recruitment of blue oak (Quercus douglasii) seedlings in California grasslands and woodlands may result from shifts in seasonal soil water availability coincident with replacement of the native perennial herbaceous community by Mediterranean annuals. We used a combination of container and field experiments to examine the interrelationships between soil water potential, herbaceous neighborhood composition, and blue oak seedling shoot emergence and growth. Neighborhoods of exotic annuals depleted soil moisture more rapidly than neighborhoods of a perennial grass or "no-neighbor" controls. Although effects of neighborhood composition on oak seedling root elongation were not statistically significant, seedling shoot emergence was significantly inhibited in the annual neighborhoods where soil water was rapidly depleted. Seedling water status directly reflected soil water potential, which also determined the extent and duration of oak seedling growth during the first year. End-of-season seedling height significantly influenced survival and growth in subsequent years. While growth and survival of blue oak seedlings may be initially constrained by competition with herbaceous species, subsequent competition with adult blue oak trees may further contribute to reduced sapling recruitment.     

杜鹃花属映山红亚属植物叶表皮显微形态特征及其分类学意义

为澄清映山红亚属(Rhododendron subg. Tsutsusi)内的系统关系问题,该研究选择杜鹃花属映山红亚属37种植物作为对象,其中29种为首次报道,通过扫描电镜观察其叶表皮显微特征。结果表明:(1)气孔器均为无规则型且均在远轴面。(2)根据叶片微形态特征将映山红亚属的种类分为杜鹃型(R. simisii-type)、岭南杜鹃型(R. mariae-type)、皋月杜鹃型(R. indicum-type)、崖壁杜鹃型(R. saxatile-type)及丁香杜鹃型(R. farrerae-type)5种类型。(3)杜鹃型植物的气孔器周边无或具间断的条形突起。(4)岭南杜鹃型植物的气孔器周围有多层条形突起环绕,保卫细胞两极不具T型加厚。(5)皋月杜鹃型植物的叶表皮保卫细胞两极具有T型加厚,与叶状苞亚属(Subg. Therorhodion)叶状苞杜鹃(R. redowskianum)的气孔器特征相似,推测其与叶状苞亚属具有一定的亲缘关系。(6)崖壁杜鹃型植物的叶表皮毛单一,多呈卷曲状,与其他类型有所不同且未见腺体。(7)丁香杜鹃型植物的叶表皮仅有腺体。(8)依据叶表皮微形态特征讨论了一些近缘种类的关系,如倾向于将背绒杜鹃(R. hypoblematosum)和千针叶杜鹃(R. polyraphidoideum)处理为独立的种,支持保留紫薇春(R. naamkwanense var. cryptonerve)作为南昆杜鹃(R. naamkwanense)的变种地位,不支持将腺花杜鹃(R. adenanthum)并入细瘦杜鹃(R. tenue)作异名处理等。该研究结果表明叶表皮显微特征在映山红亚属内物种划分上具有重要价值。     

Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae).

Quercus is one of the most abundant and economically important genera of woody plants in the Northern Hemisphere. To infer phylogenetic relationships within Quercus subgenus Quercus, chloroplast DNA (cpDNA) restriction sites and nucleotide sequences of the internal transcribed spacers (ITS) and the 5.8S coding region of the nuclear ribosomal DNA repeat were obtained for 44 individuals, including 25 species, intraspecific samples, and three outgroups. Separate parsimony analyses of each data set showed that individual gene trees were congruent and often complementary in supporting clades that generally corresponded to previously recognized taxonomic groups. Only one instance of strongly supported gene tree incongruence was detected and this anomalous pattern was explained best by ancient introgression of cpDNA across sectional boundaries. Simultaneous parsimony analysis of the pruned data sets supported the recognition of the strictly Eurasian section Cerris and resolved a novel hypothesis for the major infrageneric groups (Cerris- (Lobatae- (Protobalanus + Quercus sensu stricto))). The biogeographic hypothesis that all major oak lineages evolved locally at middle latitudes within the general distribution of their fossil ancestors was fully supported. This set of relationships also suggested a New World origin for the widespread white oaks of the Northern Hemisphere (section Quercus s. s.). For both data sets, inter- and intraspecific sampling within section Protobalanus showed little correspondence to morphological species. Greater cladistic structure among the samples was obtained by cpDNA restriction sites and two well-delimited plastomes types comprising a total of 15 distinct haplotypes were resolved. Haplotypes of 2 of the peripheral species in this species complex occupy terminal portions of one of the plastome clades, suggesting a more recent origin relative to those of more widespread species. The phylogeography of the two divergent plastome types suggested a north-south pattern, consistent with a Late Tertiary disjunction in the ancestral distribution of section Protobalanus.     

Stem xylem features in three Quercus (Fagaceae) species along a climatic gradient in NE Spain

 Stem xylem features in two evergreen Quercus species (Q. coccifera and Q. ilex) and a deciduous one (Q. faginea) were analysed along an Atlantic-Mediterranean climatic gradient in which rainfall and winter cold experience strong variation. Mean maximum vessel diameter, vessel density, vessel element length, xylem transverse sectional area, Huber value (xylem transverse sectional area per leaf area unit), theoretical leaf specific conductivity (estimated hydraulic conductance per leaf area unit) and total leaf area were determined in 3-year-old branches. Q. faginea presented the widest vessels and the highest theoretical leaf specific conductivity while Q. coccifera showed the lowest total leaf area and the highest Huber value. Studied features did not exhibit significant correlations with mean minimum January temperature in any species but did show significant relationships with rainfall. In Q. coccifera, mean maximum vessel diameter, vessel element length and theoretical leaf specific conductivity increased with higher rainfall while vessel density decreased. Mean maximum vessel diameter and total leaf area in Q. ilex increased with precipitation whereas variables of Q. faginea did not show any significant trend. Results suggest that aridity, rather than minimum winter temperature, controls stem xylem responses in the studied evergreen species. Q. faginea traits did not show any response to precipitation, probably because this species develops deep roots, which in turn makes edaphic and topographic factors more important in the control of soil water availability. In response to aridity Q. coccifera only exhibits adjustment at a xylem level by reducing its water transport capacity through a reduction of vessel diameter without changing the amount of xylem tissue or foliage, whereas Q. ilex adjusts its water transport capacity in parallel to the foliage area. Received: 13 January 1997 / Accepted: 8 April 1997     

Evolution of trichomes and its systematic significance in Salvia (Mentheae; Nepetoideae; Lamiaceae)

We have investigated the trichome characteristics in representative species of Salvia and Pleudia in order to evaluate this source of morphological evidence for addressing problems regarding generic delimitation and subgeneric classification. Trichomes of 46 Salvia spp., representing three subgenera in Iran, were investigated using light microscopy and scanning electron microscopy. General trichome characteristics were constant among different populations of a certain species, but showed a degree of variability useful in the delimitation of taxa, specifically at lower taxonomic levels. Trichome characters of taxonomic interest are as follows: types of glandular hair; number of composing cells (uni‐, bi‐ or multicellular); size and thickness; branching pattern; and presence of papillae on the surface. Non‐glandular trichomes can be simple and branched. Glandular trichomes can be stalked, subsessile or sessile. Our investigation reveals the usefulness of such characters in providing fundamental taxonomic criteria for taxon delimitation in these genera at various levels, especially at the specific rank. Furthermore, the data presented here indicate the potential applicability of such characters in the determination of evolutionary trends in Salvia and allies. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 241–257.     

Geometric morphometric analyses of leaf variation in four oak species of the subgenus Quercus (Fagaceae)

Abstract

This paper defines a protocol for the study of leaf morphology and morphometric relationships among Quercus frainetto, Quercus robur, Quercus petraea and Quercus pubescens. Leaf shapes were investigated in an attempt to characterize and discriminate among these four species. Landmark and outline data were compared in order to ascertain their relative efficacy for describing variation in leaf morphology. MANOVA was performed to assess intra‐specific differentiation and to compare the distribution of variance in individuals, populations and species. A strong correlation was found between landmark and outline datasets of the four species: both methods proved capable of discriminating among the four species. Finally, a Two‐Block Partial Least‐Squares analysis was performed for each species in order to assess the correlation between intra‐specific shape variation and environmental factors.     

Foliar trichomes of the evergreen and semi-deciduous species of the genus Quercus (Fagaceae) in the Iberian Peninsula

The leaf trichomes of the evergreen and semi-deciduous species of the genus Quercus living in the Iberian Peninsula were studied by means of SEM and LM. The SEM has been particularly useful because of the high quality of the illustrations and the possibility of recognizing the structures under LM or the stereomicroscope afterwards. The studied species were-. Quercus coccifera, Q. ilex, Q. rotundifolia, Q suber, Q canariensis, Q. faginea, Q. broteroi and Q. lusitanica. All species show some exclusive particularities that permit their identification using these characters. The abaxial surface of the leaf always has more trichomes than the adaxial and hence provides more characters for identification. Quercus alpestris Boiss. shows the same features in the leaf trichomes as Q. faginea Lam. A key for identification using these characters is provided.