Terminology and classification of stomata and stomatal development—a critical survey

The literature on terminology of stomata and stomatal development is reviewed and the terminology rationalized. The classification of developmental types and of the developing cells should not be combined with the morphological classification of mature stomatal complexes. The cells involved in the development should be distinguished on the basis of their origin and position in the developing stomatal complex, and not on the basis of their future form and appearance. It is unsound to distinguish any kind of cell only on the basis of a presumed future division by which it is replaced by its two daughter cells. Development of stomata begins with the formation of a stomatal meristemoid by an unequal division of a protodermal cell. A meristemoid may divide unequally to produce a new meristemoid and a mesogene cell. Stomatal meristemoids eventually function as guard-cell mother-cells. The adjective perigene is restricted to those cells that have arisen by divisions of protodermal cells surrounding the future stoma. The undivided cells surrounding protodermal cells should be termed agene cells, and not neighbouring cells, a term which should be restricted to morphological terminology.     

Ultrastructure of stomatal development in early-divergent angiosperms reveals contrasting patterning and pre-patterning

Background and Aims

Angiosperm stomata consistently possess a pair of guard cells, but differ between taxa in the patterning and developmental origin of neighbour cells. Developmental studies of phylogenetically pivotal taxa are essential as comparative yardsticks for understanding the evolution of stomatal development.

Methods

We present a novel ultrastructural study of developing stomata in leaves of Amborella (Amborellales), Nymphaea and Cabomba (Nymphaeales), and Austrobaileya and Schisandra (Austrobaileyales), representing the three earliest-divergent lineages of extant angiosperms (the ANITA-grade).

Key Results

Alternative developmental pathways occur in early-divergent angiosperms, resulting partly from differences in pre-patterning and partly from the presence or absence of highly polarized (asymmetric) mitoses in the stomatal cell lineage. Amplifying divisions are absent from ANITA-grade taxa, indicating that ostensible similarities with the stomatal patterning of Arabidopsis are superficial. In Amborella, ‘squared’ pre-patterning occurs in intercostal regions, with groups of four protodermal cells typically arranged in a rectangle; most guard-mother cells are formed by asymmetric division of a precursor cell (the mesoperigenous condition) and are typically triangular or trapezoidal. In contrast, water-lily stomata are always perigenous (lacking asymmetric divisions). Austrobaileya has occasional ‘giant’ stomata.

Conclusions

Similar mature stomatal phenotypes can result from contrasting morphogenetic factors, although the results suggest that paracytic stomata are invariably the product of at least one asymmetric division. Loss of asymmetric divisions in stomatal development could be a significant factor in land plant evolution, with implications for the diversity of key structural and physiological pathways.     

Homology of posterior interray plates in crinoids: a review and new perspectives from phylogenetics,the fossil record and development

Despite their importance for understanding phylogeny, character evolution and classification, well-constrained homology relationships for posterior plating in crinoids have only recently been attempted. Here, we re-evaluate posterior plate homologies in all major crinoid lineages using development, fossil ontogenies and phylogenetic evidence. Based on these lines of evidence, we change terminology for some posterior plates to correct misnomers and make recommendations for updated terminology of others to better reflect homology. Among pentacrinoids (disparids, hybocrinids, eucladids, flexibles and articulates) the relative position of posterior interray plates, not their topology, reflects homology. From proximal to distal, pentacrinoid posterior plates are the radianal, anal X and right sac plate, regardless of the total number of plates in the adult calyx. Camerate posterior plating contrasts with pentacrinoids, but insufficient data are available to resolve homology relationships between these two clades. More examples of early post-larval ontogeny are needed in camerates and other Palaeozoic crinoids.     

The role of peristomatal transpiration in the mechanism of stomatal movement

Abstract. Peristomatal transpiration is defined as the relative high local rate of cuticular water loss from external and internal surfaces around the stomatal pore and its decisive role in the control of stomatal movement is re-emphasized. As the resistance towards changes in air humidity is low in the pore surroundings, the state of turgor is particularly unsteady there. Due to the inherent instability the guard cell 'senses' fluctuations in the supply-demand relationship of water and is thus the control unit proper. The environmental variables (supply and demand) are cross-correlated within the subsidiary cell and the information is transmitted to the guard cell through the water potential gradient between the two cells. A conceptual segregation of a 'humidity response' by 'passive' stomatal movements is rejected.
As ions always accumulate at the most distant point of the liquid path and as this point varies with pore width according to the prevailing water potential gradients, it is felt that the water stream is causing the characteristic pattern of ion distribution within the epidermis. Passive import of ions is attributed to local concentration gradients which are steepened by continuous supply and by water uptake into the guard cell in response to starch hydrolysis. A mechanistic model supplements the discussion.     

Variations in stomatal density and index: implications for palaeoclimatic reconstructions

The variation in stomatal characters in leaves from one Alnus glutinosa (L.) Gaertn. tree is analysed. Measurements were taken from over 70 sites on the abaxial surfaces of representative ‘sun’ and ‘shade’ leaves having the same insertion point. The mean values of stomatal density and index in the shade leaf were significantly lower (71 and 93%, respectively) than those for the sun leaf. Within leaves, up to 2.5-fold differences in stomatal density values were observed. Contour maps derived from the data reveal non-random trends over the leaf surface. Correlations between stomatal density, epidermal cell density and stomatal index indicate that the variation in stomatal density within leaves arose primarily from local differences in stomatal differentiation, rather than from local differences in leaf expansion. This research demonstrates that a high level of variation in stomatal characters occurs both within and between leaves. We conclude that a well-defined sampling strategy should be used when estimating stomatal characters for (tree) leaves. Furthermore, the leaf's insertion point and situation within the tree crown should be taken into account. We discuss the implications of these findings for palaeoclimatic interpretations and emphasize the need for great caution when drawing conclusions based solely on stomatal characters.     

Clonal analysis of stomatal development and patterning in Arabidopsis leaves.

Cell lineage has been used to explain the stomatal distribution in several plant species. We have used transgenic plants carrying a 35SGUS::Ac construct that produces clonal sectors to analyze the possible role of cell lineage during the establishment of stomatal patterning in Arabidopsis leaves. The analysis of sectors ranging from two to eighteen cells supports the conclusion that most stomatal complexes derive from a single and immediate precursor cell through a stereotyped pattern of three unequal cell divisions followed by a final equal one. In addition, it shows that the successive cell divisions take place at a constant angle (approximately 60 degrees ) with respect to the previous one. Interestingly, this angular dimension shifts from 60 degrees to 0 degrees in the last cell division that gives rise to the stoma. These sectors also reveal the development of both clockwise and counterclockwise patterns of cell divisions during stomatal development in approximately equal numbers. Our clonal analysis indicates that cell divisions involved in the development of stomatal complexes are probably the last ones contributing to epidermal growth and development. Finally, the stereotyped pattern of cell divisions that culminates in the formation of stomatal complexes indicates that cell lineage plays a very important role during stomatal pattern establishment.     

Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record

Major fluctuations in the concentrations of atmospheric CO₂ and O₂, are predicted by historical long-term carbon and oxygen cycle models of atmospheric evolution and will have impacted directly on past climates, plant function and evolutionary processes. Here, palaeobotanical evidence is presented from the stomatal density record of fossil leaves spanning the past 400 Myr supporting the predicted changes in atsmopheric CO₂. Evidence from experiments on plants exposed to long-term high CO₂, environments and the newly-assembled fossil data indicate the potential for genetic modification of stomatal characters. The influence of the changes in fossil stomatal characteristics and atmospheric composition on the rates of leaf gas exchange over the course of land plant evolution has been investigated through modelling. Three contrasting eras of plain water economics emerge in the Devonian (high), Carboniferous (low) and from the Upper Jurassic to the present-day (high but declining). These patterns of change result from structural changes of the leaves and the impact of atmospheric CO₂, and O₂, concentrations on RuBisCo function and are consistent with the fossil evidence of sequential appearances of novel plant anatomical changes. The modelling approach is tested by comparing predicted leaf stable carbon isotope ratios with those measured on fossil plant and organic material. Viewed in a geological context, current and future increases in the concentration of atmospheric CO₂, might be considered as restoring plant function to that more typically experienced by plants over the majority of their evolutionary history.     

Evolution and patterning of the ovule in seed plants

The ovule and its developmental successor, the seed, together represent a highly characteristic feature of seed plants that has strongly enhanced the reproductive and dispersal potential of this diverse group of taxa. Ovules encompass multiple tissues that perform various roles within a highly constrained space, requiring a complex cascade of genes that generate localized cell proliferation and programmed cell death during different developmental stages. Many heritable morphological differences among lineages reflect relative displacement of these tissues, but others, such as the second (outer) integuments of angiosperms and Gnetales, represent novel and apparently profound and independent innovations. Recent studies, mostly on model taxa, have considerably enhanced our understanding of gene expression in the ovule. However, understanding its evolutionary history requires a comparative and phylogenetic approach that is problematic when comparing extant angiosperms not only with phylogenetically distant extant gymnosperms but also with taxa known only from fossils. This paper reviews ovule characters across a phylogenetically broad range of seed plants in a dynamic developmental context. It discusses both well-established and recent theories of ovule and seed evolution and highlights potential gaps in comparative data that will usefully enhance our understanding of evolutionary transitions and developmental mechanisms.     

The relation between stomatal aperture and gas exchange under consideration of pore geometry and diffusional resistance in the mesophyll

The quantitative relation between stomatal aperture and gas exchange through the stomatal pore can be described by physical models derived from Fick's first law of diffusion. Such models, usually based on a simplified pore geometry, are used to calculate leaf conductance from stomatal pore dimensions or vice versa. In this study a combination of gas-exchange measurements and simultaneous microscopical observations of stomatal apertures was used to empirically determine this relationship. The results show a substantial deviation between measured stomatal conductance and that calculated from the simplified models. The main difference is a much steeper increase of conductance with aperture at small apertures. When the calculation was based on a realistic pore geometry derived from confocal laser scanning microscopy, a good fit to the experimentally found relationship could be obtained if additionally a significant contribution of a mesophyll diffusional resistance was taken into account.     

Preface: The phylogeny, fossil record and ecological diversity of ostracod crustaceans

After more than two centuries of research, more than 65,000 living and fossil ostracod species have been described and studied, yet much remains to be learned about this ancient, widespread and diverse group of bivalved arthropods. Their higher classification and phylogeny are subjects of vigorous debate, as is their position in the broader picture of crustacean phylogeny. At the same time, major advances in our understanding of ostracod lineages and their relationships are resulting from the application of innovative approaches and techniques. This preface provides a contextual overview of the 15 contributions to this volume, which resulted from the 14th International Symposium on Ostracoda (ISO2001) held in 2001at Shizuoka, Japan. As such it provides a cross-section of topics at the forefront of research on the evolution and diversity of Ostracoda, and indicates directions for future work.     

Egg size evolution in tropical American arcid bivalves: the comparative method and the fossil record

Marine organisms exhibit a wide range of egg sizes, even among closely related taxa, and egg size is widely considered to be one of the most important components of the life histories of marine species. The nature of the trade-off between egg size and number and the consequences of variation in egg size for offspring growth and survivorship have been extensively modeled. Yet, there is little empirical evidence that supports the relative importance of particular environmental parameters in engendering the tremendous variation in egg size seen in marine organisms. This study compares egg sizes between six geminate species pairs of bivalves in the family Arcidae to determine whether egg size differs in predictable directions between geminate species in the two oceans separated by the Central American isthmus, and whether the direction and timing of egg size evolution among geminates in this family is correlated with both modern and paleoceanographic patterns of oceanic productivity. In all modern members of six geminate pairs, egg size was larger in the species in the western Atlantic than in its sister species the eastern Pacific. This pattern supports the hypothesis that optimal egg size differs in the two oceans due to the low productivity and poor larval feeding environment in the western Atlantic relative to the eastern Pacific. The fossil record of one geminate pair shows that egg size has remained consistently large in the western Atlantic from the Miocene to the Recent, while egg size in the eastern Pacific has decreased to the current small size in less than 2 million years; this suggests that modern-day differences between egg sizes in the western Atlantic and eastern Pacific are due to either an increase in productivity in the eastern Pacific and subsequent selection for smaller eggs in that ocean, or differential patterns of extinction that occurred well after the rise of the isthmus. These results agree with ancestral character state reconstruction using linear parsimony, but differ from squared-change parsimony reconstructions.     

SEM studies on the early larval development of Triops cancriformis (Bosc)(Crustacea: Branchiopoda, Notostraca)

We investigated early larval development in the notostracan Triops cancriformis (Bosc, 1801–1802) raised from dried cysts under laboratory conditions. We document the five earliest stages using scanning electron microscopy. The stage I larva is a typical nauplius, lecithotropic and without trunk limbs. The stage II larva is feeding and has trunk limb precursors and a larger carapace. Stage III larvae have larger trunk limbs and a more adult shape. Stage IV larvae have well developed trunk limbs, and stage V larvae show atrophy of the antennae. We describe the ontogeny of selected features such as trunk limbs and carapace, discuss ontogeny and homologization of head appendages, follow the development of the feeding mechanism, and discuss trunk limb ontogeny.     

长春花叶片发育过程中气孔密度和气孔指数的动态变化

对长春花叶片近轴面和远轴面上的气孔密度和气孔指数在不同发育阶段的动态变化进行了研究.结果表明:在各个发育阶段,近轴面上的气孔以叶脉两侧居多,远轴面上的气孔则在整个叶片上均匀分布.将一个枝条上的10对真叶按发育顺序界定为10个发育阶段,即从枝条的顶端到基部,分别将第10、第9、第8……第1节位的叶片定义为第1、第2、第3...     

Comparative development in Moenkhausia pittieri and Paracheirodon innesi (Ostariophysi: Characiformes) with comments on heterochrony and miniaturization in the Characidae

Developmental heterochronies between the small‐sized Moenkhausia pittieri and the miniature Paracheirodon innesi were determined by describing and comparing external morphological development in both species. Despite being classified as miniature, P. innesi was larger and more developed in the flexion and post‐flexion larval stages than M. pittieri. Broader patterns within the Characidae suggest that body size reduction in P. innesi is tied to accelerated development and higher growth rate along with early maturation and precocious cessation of growth, which are characteristic of miniature species. Comments on adipose‐fin loss in Characidae as a consequence of developmental truncation are included.     

Recognising angiosperm clades in the Early Cretaceous fossil record

Studies of the earliest Cretaceous angiosperms in the 1970s made only broad comparisons with living taxa, but discoveries of fossil flowers and increasingly robust molecular phylogenies of living angiosperms allow more secure recognition of extant clades. The middle to late Albian rise of tricolpate pollen and the first local dominance of angiosperm leaves mark the influx of near-basal lines of eudicots. Associated flowers indicate that palmately lobed ‘platanoids’ and Sapindopsis are both stem relatives of Platanus, while Nelumbites was related to Nelumbo (also Proteales) and Spanomera to Buxaceae. Monocots are attested by Aptian Liliacidites pollen and Acaciaephyllum leaves and Albian araceous inflorescences. Several Albian–Cenomanian fossils belong to Magnoliidae in the revised monophyletic sense, including Archaeanthus in Magnoliales and Virginianthus and Mauldinia in Laurales, while late Barremian pollen tetrads (Walkeripollis) are related to Winteraceae. In the basal ANITA grade, Nymphaeales are represented by Aptian and Albian flowers and whole plants (Monetianthus, Carpestella and Pluricarpellatia). Epidermal similarities of lower Potomac leaves to woody members of the ANITA grade are consistent with Albian flowers assignable to Austrobaileyales (Anacostia). Aptian to Cenomanian mesofossils represent both crown group Chloranthaceae (Asteropollis plant) and stem relatives of Chloranthaceae and/or Ceratophyllum (Canrightia, Zlatkocarpus, Pennipollis plant and possibly Appomattoxia).     

Species in the primate fossil record

Species in the fossil record are population pools of genetic and phenetic variation at a place and time, morphologically recognizable and distinguishable from others by empirical standards. Change through time can be substantial, requiring subdivision of lineages that becomes more arbitrary as they become more complete. Evolution is about form, space, and time; it is about variation and change. Interpretation of species in the fossil record touches all of these.     

Association genetics,geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade‐offs

Stomata are essential for diffusive entry of gases to support photosynthesis, but may also expose internal leaf tissues to pathogens. To uncover trade‐offs in range‐wide adaptation relating to stomata, we investigated the underlying genetics of stomatal traits and linked variability in these traits with geoclimate, ecophysiology, condensed foliar tannins and pathogen susceptibility in black cottonwood (Populus trichocarpa). Upper (adaxial) and lower (abaxial) leaf stomatal traits were measured from 454 accessions collected throughout much of the species range. We calculated broad‐sense heritability (H²) of stomatal traits and, using SNP data from a 34K Populus SNP array, performed a genome‐wide association studies (GWAS) to uncover genes underlying stomatal trait variation. H² values for stomatal traits were moderate (average H² = 0.33). GWAS identified genes associated primarily with adaxial stomata, including polarity genes (PHABULOSA), stomatal development genes (BRASSINOSTEROID‐INSENSITIVE 2) and disease/wound‐response genes (GLUTAMATE‐CYSTEINE LIGASE). Stomatal traits correlated with latitude, gas exchange, condensed tannins and leaf rust (Melampsora) infection. Latitudinal trends of greater adaxial stomata numbers and guard cell pore size corresponded with higher stomatal conductance (g_s) and photosynthesis (A_max), faster shoot elongation, lower foliar tannins and greater Melampsora susceptibility. This suggests an evolutionary trade‐off related to differing selection pressures across the species range. In northern environments, more adaxial stomata and larger pore sizes reflect selection for rapid carbon gain and growth. By contrast, southern genotypes have fewer adaxial stomata, smaller pore sizes and higher levels of condensed tannins, possibly linked to greater pressure from natural leaf pathogens, which are less significant in northern ecosystems.     

Anatomy and early development of the pectoral girdle,fin, and fin spine of sturgeons (Actinopterygii: Acipenseridae)

Acipenseriformes hold an important place in the evolutionary history of bony fishes. Given their phylogenetic position as extant basal Actinopterygii, it is generally held that a thorough understanding of their morphology will greatly contribute to the knowledge of the evolutionary history and the origin of diversity for the major osteichthyan clades. To this end, we examined comparative developmental series from the pectoral girdle in Acipenser fulvescens, A. medirostris, A. transmontanus, and Scaphirhynchus albus to document, describe, and compare ontogenetic and allometric differences in the pectoral girdle. We find, not surprisingly, broad congruence between taxa in the basic pattern of development of the dermal and chondral elements of the pectoral girdle. However, we also find clear differences in the details of structure and development among the species examined in the dermal elements, including the clavicle, cleithrum, supracleithrum, posttemporal, and pectoral‐fin spine. We also find differences in the internal fin elements such as the distal radials as well as in the number of fin rays and their association with the propterygium. Further, there are clear ontogenetic differences during development of the dermal and chondral elements in these species and allometric variation in the pectoral‐fin spine. The characters highlighted provide a suite of elements for further examination in studies of the phylogeny of sturgeons. Determining the distribution of these characters in other sturgeons may aid in further resolution of phylogenetic relationships, and these data highlight the role that ontogenetic and comparative developmental studies provide in systematics. J. Morphol. 276:241–260, 2015. © 2014 Wiley Periodicals, Inc.     

小麦进化过程中叶片气孔和光合特征演变趋势

根据小麦属内种间的进化关系选取21种小麦品种为实验材料,研究了小麦进化过程中气孔特征和光合特征的演变趋势。结果表明,无论是A,B,D染色体组还是A,G染色体组,气孔长度、宽度、周长、面积均随倍性水平的升高而呈增大趋势,而气孔指数无显著变化;A,B,D染色体组气孔密度随倍性升高呈减少趋势。二倍体小麦的Pn值最高,六倍体小麦的Fv/Fm值较高,二倍体小麦叶片叶绿素含量显著高于四倍体和六倍体小麦。不同倍性小麦的净光合速率与气孔导度间均存在极显著相关关系,表明气孔传导力是小麦光合能力的主要限制因素之一。气孔导度与单一气孔特征之间无显著相关关系。A,B,D染色体组不同倍性小麦叶片气孔密度差异显著,其大小顺序为二倍体〉四倍体〉六倍体;A,B,D染色体组不同倍体小麦叶片的气孔长度、宽度、周长、面积差异显著,顺序均为六倍体〉四倍体〉二倍体,气孔密度降低可能是A,B,D染色体组六倍体小麦光合能力降低的原因。随着倍性的升高,小麦的抵抗光抑制能力越强,因此光化学能转换效率可能不是小麦进化过程中光合能力变化的原因。A,B,D染色体组中二倍体的叶绿素含量显著大于四倍体和六倍体,而A,G染色体组中倍体间叶绿素含量差异不显著,说明叶绿素的降低可能是A,B,D染色体组六倍体光合能力降低的原因之一。     

Phylogeny and biogeography of Zelkova (Ulmaceae sensu stricto) as inferred from leaf morphology, ITS sequence data and the fossil record

To address the evolution and geographical diversification of the genus Zelkova (Ulmaceae) a phylogenetic analysis of morphological data and the sequences of the internal transcribed spacers (ITS1 and ITS2) of nuclear ribosomal DNA were used. Cladistic analyses suggested that the Chinese species Z. schneideriana and Z. sinica are basal within Zelkova. The western Asian Z. carpinifolia either appears nested between the East Asian Z. schneideriana and Z. sinica and a clade formed by the Japanese Z. serrata and two Mediterranean species, Z. abelicea and Z. sicula (ITS), or forms a clade with Z. serrata that is sister to a clade Z. abelicea plus Z. sicula (morphology). Nucleotide data suggested that gene flow occurred between Z. schneideriana and Z. serrata, and Z. carpinifolia and a lineage ancestral to Z. abelicea/sicula. Character evolution in Zelkova appears to have gone from long leaves with numerous secondary veins, coarse to shallow teeth with blunt or slightly pointed apex and small stomata, to leaves that are either long or short with numerous or few secondary veins, coarse teeth with cuspidate or obtuse apex or conspicuously shallow teeth, and dimorphic stomata displaying ‘giant stomata’ surrounded by a ring of small stomata or uniform large stomata. These results are in agreement with fossil data. Early Cainozoic fossils attributed to Zelkova from North America and Central Asia closely resemble the modern Z. schneideriana and Z. carpinifolia. The genus could have originated in the northern Pacific area and migrated to Europe after the Turgai Strait was closed during the Late Oligocene. Geographical differentiation may have started with the isolation of Chinese populations (leading to modern Z. schneideriana and Z. sinica) from high‐latitude Eurasian (North American) populations. This widespread Early Cainozoic type may have diversified into the western Asian Z. carpinifolia and the more derived Japanese and Mediterranean species during the latest Cainozoic. The modern Japanese and European/western Asian species would have differentiated relatively late, while two locally endemic Mediterranean species are the result of the cooling and development of a Mediterranean climate belt in Europe during the Pleistocene. Fossils from the Miocene and Pliocene of Europe resemble modern Z. carpinifolia and Z. serrata. Differentiation of the two Mediterranean species Z. abelicea and Z. sicula in the Late Cainozoic cannot be traced by leaf morphology. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147 , 129–157.