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Anatomy and Morphology |
School of Molecular and Cell Biology, University of the Witwatersrand, Johannesburg, Private Bag 3, WITS 2050, South Africa
Received for publication February 24, 2005. Accepted for publication July 12, 2005.
ABSTRACT
Structural features of leaves, including size, shape, and surfaces, vary greatly throughout the plant kingdom. In both functional and phylogenetic analyses of leaves, the various morphological aspects are often considered independently of each other, although it is likely that many combinations of features do not occur at random due to either functional constraint or genetic correlation. The distribution of variation in leaf morphology in the highly variable Begonia dregei species complex was examined in natural populations and in F2 offspring from a cross between plants from two populations. Leaf shape was quantified using several morphometric measures, and trichomes on leaves were counted and measured. Correlations between leaf shape and the numbers and size of trichomes were examined. There were significant correlations between the shapes of leaves and the presence, number, and size of trichomes among populations and in hybrid plants. Deeply incised leaves had larger numbers of longer trichomes at the sinuses. Higher numbers of trichomes on upper leaf surfaces occurred together with trichomes at the petiole and on the abaxial surface. The potential for independent evolution of leaf shape and trichomes in this group is limited. Hypotheses to explain the correlated development of leaf shape and trichomes are discussed.
Key Words: correlated evolution • developmental constraint • genetic correlation • leaf incision • leaf shape • morphological evolution
Multiple characters provide good support for the recognition of species and the determination of relationships among taxa. The strength of support for a lineage is based on the assumption that multiple characters have been acquired independently of each other. However, many suites of characters, such as the complex flowers of Asclepiadaceae and Orchidaceae, may be functionally integrated with each other and are probably not acquired independently. Others, such as the overall size of different organs (Midgely and Bond, 1989
), may have a common genetic and developmental basis in addition to functional integration. The assumption of genetic independence of multiple characters is difficult to examine directly above the species level, because hybridization to test for inheritance is difficult. However, the problem remains that multiple traits that are genetically correlated do not provide good evidence for evolutionary relationships (Shaffer, 1986
).
Genetic correlations between various aspects of plant morphology suggest that there is a genetic basis for the coordinated evolution of characters (Davis, 2001
; Conner, 2002
; Ungerer et al., 2002
). Two possible mechanisms for these correlations are pleiotropy, the association of more than one phenotypic characteristic with a single genotype, and linkage, when independent genes that determine different traits are inherited together because they are located near each other in the genome (Falconer and Mackay, 1996
).
Leaves throughout the plant kingdom have a wide diversity of shapes, sizes, surfaces, and other features. Correlations of structural features of leaves with environment and climate have been demonstrated (Givnish, 1987
; Wilf, 1997
). Within a single habitat plants possess a variety of characteristics (Givnish, 1987
), consistent with the idea that there are multiple solutions to the same environmental challenges (Gutshick, 1999
). The various functional aspects of leaf structure, such as shape and surface features, are often dealt with separately, while in reality, leaves function as integrated structures. Combinations of traits often occur nonrandomly, because of selection for their coordinated function, or they may have a common genetic basis for their correlated evolution.
To assess the importance of genetics in correlated evolution between traits it is necessary to be able to examine inheritance in a group that also has a variety of morphological features. The Begonia dregei Otto et Dietr. species complex has a wide variety of leaf shapes and sizes with high heritability (McLellan, 2000
). Genetic compatibility among forms, and their small size and rapid growth rate make them amenable to genetic analysis. There is little genetic variation within each small population (Matolweni et al., 2000
), so that wild plants are similar to inbred strains in being homozygous at most loci and distinctly different from each other, representative of the types of differences that often distinguish species. Irmscher (1961)
treated this group of plants as six species, differentiated by the shape and size of the leaves and foliar trichomes. In the most recent taxonomic treatment, Hilliard (1976)
recognized two species, distinguished by the size and shape of leaves. Neither quantitative comparisons of leaf shapes nor allozyme variation has provided any support for recognizing species according to the treatments of either Irmscher (1961)
or Hilliard (1976)
(Matolweni et al., 2000
; McLellan, 2000
).
The purpose of this paper is to examine correlations between leaf morphological traits among populations of the B. dregei complex and in the offspring of a cross between plants from different populations to investigate whether traits that are correlated in naturally occurring populations are genetically independent of each other. The results will allow an assessment of the utility of the characters to distinguish taxa within the group and serve as a basis for exploring the developmental mechanisms involved in correlated evolution.
MATERIALS AND METHODS
Plants
Begonia dregei was collected from 37 localities throughout its geographic range in South Africa, of 39 previously described (McLellan, 2000
), with the exception of Mnenu River Mouth and Nenga River Mouth, Coffee Bay (Table 1). Voucher specimens are on deposit at the C. E. Moss Herbarium at the University of the Witwatersrand. Plants were grown from either stem cuttings or seed collected in the wild near a large, south-facing window with a maximum light level of 80–90 µmol · m–2 · s–1 (McLellan, 2000
) for at least 24 mo. Leaf shape and size differ between wild populations and laboratory-grown plants; this was sufficient time for plants to acquire the characteristics of growth in the laboratory (McLellan, 2000
).
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; Falconer and Mackay, 1996
). It cannot be used to estimate genetic correlations in the sense the term is used in quantitative genetics (Falconer and Mackay, 1996
), and it does not allow for distinction of the genetic, environmental, and gene-by-environment interaction components of phenotypic variation.
Scanning electron microscopy
Immature leaves 1–5 mm long were dissected from leaf buds and placed in 2% glutaraldehyde in 50 mM sodium– potassium phosphate pH 6.8, then postfixed with 1% osmium tetraoxide (w/ v), dehydrated in an ethanol series, and critical-point dried with liquid CO2. They were mounted onto stubs, then sputter coated with gold and palladium, and examined at 20 kV in a JSM 840 scanning electron microscope (JEOL, Tokyo, Japan).
Quantification of morphology
Data were collected on trichomes in the four sinuses at the bases of the lobes of each leaf from two mature, adult leaves of each plant. One plant from each of the 37 populations, and 523 F2 hybrids were examined. In ovate and shallowly lobed leaves, areas homologous to the sinuses of incised leaves were defined by the pattern of venation, which is the same across all forms of B. dregei (McLellan, 1990
; McLellan and Dengler, 1995
). The length of trichomes was measured to the nearest 50 µm using a stage micrometer, and the trichomes at each of the four sinuses were counted. Trichomes on the adaxial and abaxial leaf surfaces and at the juncture of petiole and lamina were also counted.
Leaves were pressed and dried, and outlines of four leaves from each of 413 F2 hybrid plants were digitized by hand with a DT3613 digitizer (Seiko Instruments, Tokyo, Japan) with 1/500th inch resolution. The 110 plants for which there is data on trichomes but not on leaf shape never had four fully grown, adult leaves. Shape was quantified using dissection index, defined as the ratio of perimeter to the square root of area (Kincaid and Schneider, 1983
; McLellan, 1993
, 2000
; McLellan and Endler, 1998
). This is a measure that summarizes the extent of dissection in a single metric, with higher values corresponding to more incised leaves. Incision, defined as the ratio of the petiole-sinus distance to the mean of the lengths of the major lobe and the secondary lobe (Fig. 1), was also calculated as previously described (McLellan, 1993
, 2000
; McLellan and Endler, 1998
). Dissection index and incision are sensitive to different aspects of shape. Variation in the small details of the margin (teeth) will be detected with the dissection index, because the entire perimeter is a component of dissection index. The measure of incision is sensitive only to the extent of incision between lobes, because it is based on three linear measurements.
|
). Table-wide significance values of 
= 0.05 were calculated according to Rice (1989)
. Tukey's studentized range (HSD) test was used to determine the significance of differences between mean numbers of adaxial trichomes for hybrid plants with trichomes found on various parts of leaves and the Student's t test was used to determine the significance of difference between means of petiole trichomes on plants with and without abaxial trichomes. RESULTS
Trichomes in wild collected plants
All plants had small, ephemeral, short-stalked, glandular trichomes on developing leaves. Plants from 24 of the 37 populations had large, multicellular trichomes at the sinuses at the bases of the five lobes of the leaves (Fig. 2A, B). These structures might be appropriately called emergences if they are derived from subepidermal as well as epidermal cells (Esau, 1965
), but they were referred to as trichomes previously (McLellan and Dengler, 1995
). The trichomes occurred singly or in clusters of up to four, with a larger trichome in the center and smaller ones on either side of it (Fig. 2A). Trichomes with similar morphology were also found at the bases of smaller lobes and teeth of the leaves of some populations, as described previously (McLellan and Dengler, 1995
). There were evenly spaced trichomes on the adaxial leaf surface in plants from 12 populations (Table 1, Fig. 2C). Nine of these populations also had trichomes at the juncture of the petiole and the leaf blade. In six of them, there were trichomes on the abaxial leaf surfaces, usually on the veins or near them, in addition to those on the adaxial surface and at the petiole (Table 1). Trichomes on the leaf surfaces were without gland tips, while those around the petiole usually did have gland tips (Fig. 2C, D).
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). Those from Ntumeni had short, single trichomes at the sinuses and longer trichomes on the adaxial and abaxial surfaces of the leaves and around the petiole. Plants from Eagle's Nest had clusters of long trichomes at each sinus and no large laminar trichomes (Table 1). The shapes of leaves of the F2 plants varied in the extent of incision between lobes and the size and number of teeth on the margins (Fig. 4). The values of the shape indices extend beyond the values for both parents in a small number of plants, while the numbers of sinus trichomes and petiole trichomes are transgressive traits, with values in 46% and 32% of the plants, respectively, above that of the parent with the higher number (Fig. 5). All F2 plants had trichomes at the sinuses either singly or in clusters, with a maximum of seven. Mean sinus trichome length and adaxial trichome number are within the range of parental values. The distributions of all traits are continuous (Fig. 5), with no evidence of the bimodal or trimodal distributions expected if traits were determined by single loci.
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Leaf shape was correlated with trichome length and number across natural populations and in the offspring of a cross between plants of different morphology. Trichomes on leaf surfaces and surrounding the junction of the petiole and lamina also had similar patterns in populations and in hybrid plants, with adaxial trichomes occurring more frequently, and higher numbers of adaxial trichomes associated with the presence of trichomes in other areas. The combinations found in one or the other of the parents of the cross occurred more often in the F2 generation than expected if the traits were controlled by different, unlinked genes.
The presence and distribution of foliar trichomes corresponded with the species recognized by Irmscher (1961)
. Those with only short glandular trichomes were recognized as B. rudatisii Irmsch., B. homonyma Hook., or B. natalensis Steudl., which differ in shape and size of leaves. However, some populations are intermediate between these categories (McLellan, 2000
). Begonia partita Irmsch. was distinguished from the others by the trichomes on the upper leaf surface. The number of adaxial trichomes varies greatly among populations, higher in the northern part of the range than in the more southern populations. Two of the species recognized by Irmscher, B. suffruticosa Meissn. and B. dregei, have trichomes at the sinuses but not on the upper surface and can be distinguished by the extent of incision; B. suffruticosa is deeply incised like the plants from Eagle's Nest. The shorter and less numerous sinus trichomes of plants with less incised leaves cannot be considered a character that has evolved independently of leaf shape. Previous analyses of leaf shape and molecular studies do not support the recognition of more than one taxon in the B. dregei complex (Matolweni et al., 2000
; McLellan, 2000
), and the data reported here are consistent with that conclusion.
The lack of independent evolution of trichomes and leaf shape does not, however, extend to the entire genus Begonia, which contains more than 1000 species (Smith et al., 1986
; Plana, 2003
). Many species have elliptic to obovate leaves and entire or dentate margins with trichomes along the margins (ciliated margins) (Burt-Utley, 1985
; Sosef, 1994
), including B. geranioides Hook.f., which appears to be the sister group to B. dregei (L. Matolweni, University of the Witwatersrand et al., unpublished manuscript). The parted leaf shape of the plants from Eagle's Nest is unusual in Begoniaceae (Smith et al., 1986
), however, and the occurrence of large trichomes at sinuses in other species is unknown.
Causes of correlations
One explanation for adaptive significance of the correlations between leaf shape and trichome size is that trichomes in different parts of the leaves are functionally equivalent. It is possible that the trichomes function to inhibit herbivory on leaves as soon as the leaves grow longer than stipules and are no longer protected by them, until leaves are fully expanded. The long trichomes of highly incised leaves cover much of the adaxial surface in the expanding leaf. The adaxial surface trichomes also cover much of the unfolding leaf. In the unlobed leaves from several populations, where sinus trichomes are missing, a ring of emergences at the vein endings surrounds the unfolding leaf (McLellan, 1990
; McLellan and Dengler, 1995
). Therefore, the various arrangements of trichomes have provided different solutions to the same problem of distributing trichomes over developing leaves, possibly to protect them from small herbivorous insects. Although this explanation of functional equivalence of the different morphologies may be valid, it does not explain a genetic basis for the correlations between leaf dissection and trichome distribution found in the F2 plants.
The mechanisms for genetic correlations can be either pleiotropy or linkage (Falconer and Mackay, 1996
). A different crossing design, with many generations that allowed for more recombination than in the design used here, supported a role for pleiotropy rather than for linkage in correlated floral traits of wild radish (Conner, 2002
). However, segregation distortion, in which a deviation occurs from expected Mendelian proportions in a segregating population from linkage between genes, is not uncommon in crosses between different species, subspecies, or strains (Falconer and Mackay, 1996
; Rieseberg et al., 1996
; Xu et al., 1997
; Schwarz-Sommer et al., 2003
). Alleles from one of the parents are found much more frequently in the offspring than expected due to differential fertility or viability of individuals with some combinations of alleles. Distributions of traits in the F2 did not reveal much bias toward one parent or the other, but those distributions depend on mode of inheritance and interactions between genes, and therefore cannot provide a test for segregation distortion, although they are consistent with a lack of distortion. Molecular markers could resolve whether segregation distortion has occurred.
Development of leaves and trichomes
Many genes have been characterized in Arabidopsis thaliana and other species that effect leaf morphogenesis when their expression is modified by mutation or overexpression (Berná et al., 1999
; Bharathan and Sinha, 2001
; Pérez-Pérez et al., 2002
). Multiple independent origins of compound leaves through plant evolution have been attributed to the differential expression of the KNOX family of genes (Bharatan et al., 2002
; Gleissberg, 2002
). A single gene responsible for variation in leaf incision can be ruled out in B. dregei by the continuous distribution of leaf shapes in the hybrid offspring, rather than two or three classes expected from a single gene. Leaf shape has high heritability between populations of B. dregei (McLellan, 2000
), and if a single gene were involved, discrete groups should have been observed.
Numerous genes in the developmental pathway for the initiation and morphogenesis of the unicellular trichomes in Arabidopsis have been characterized (Hülskamp et al., 1994
; Szymanski et al., 2000
; Schiefelbein, 2003
), as well as the Antirrhinum gene MIXTA, involved in the development of multicellular trichomes (Glover et al., 1998
; Payne et al., 1999
). The different pathways in trichome initiation suggest that trichomes are not homologous between species (Payne et al., 1999
). The large Begonia trichomes may be influenced by yet another set of genes not known from model systems.
There is little precedent in the literature for a common genetic basis for leaf shape and the presence of trichomes. A few papers report mutants with effects on both leaf shape and trichome presence or type (Qiu et al., 2002
; Cho et al., 2005
). Mapping of quantitative trait loci in cotton identified many QTL for leaf shape and one for the presence of trichomes that mapped to another chromosomal region (Jiang et al., 2000
). However, there are coordinated changes in the presence of trichomes and the shape and size of leaves during shoot maturation from seedling to a flowering plant, a process called phase change (Poethig, 1990
; Telfer et al., 1997
). The presence and abundance of trichomes on juvenile leaves of Arabidopsis is related to gibberellin concentration, consistent with a model that an inductive signal has a higher threshold for inducing trichome initiation on the abaxial surface than on the adaxial surface. Higher concentrations of exogenous gibberellin induced higher numbers of adaxial trichomes and initiated trichomes on the lower surface than did lower concentrations (Telfer et al., 1997
). This effect is similar to the pattern of trichomes on the leaf surfaces of B. dregei, with more adaxial trichomes on leaves that also have abaxial trichomes.
Several plant hormones affect the development of both leaf shape and trichomes, and the expression of genes in the KNOX gene family. In leaves overexpressing KNOX genes, gibberellin downregulation makes leaves more deeply lobed (Hay et al., 2002
). Cytokinins and ethylene also affect the development of both trichomes and leaves (Martin and Glover, 1998
; Frugis et al., 1999
; Hamant et al., 2002
; Greenboim-Wainberg et al., 2005
). The lobing of leaves of B. dregei is determined early in development (McLellan, 1990
). Initially, the area that will become the sinus between lobes grows much more slowly than the lobes in deeply incised leaves, and the sinus area grows faster as the leaf matures. It would appear that there is some inhibition of growth in this area early in leaf development, at the same time as sinus trichomes are being initiated. Therefore, the same mechanism that inhibits growth of the lamina at the sinuses may also be encouraging sinus trichome initiation (higher numbers result) and growth (greater lengths). It is possible that increased gibberellin concentration causes an increase in the number of sinus trichomes and more deeply lobed leaves. These hypotheses provide a base for the design of experiments to elucidate the developmental basis for correlations observed in B. dregei. Pleiotropy might not be due to the action of a single gene that is directly involved in the morphogenesis of different types of organs, but instead the determination of the concentration of a hormone could simultaneously affect many genes that are involved in the development of both traits.
FOOTNOTES
1 The author thanks Arthur Baloyi and Johannes Baloyi for maintaining living plants and Sarah Taylor for assistance with data collection. Michele Ramsay, Ed Witkowski, and two reviewers made substantial comments on the manuscript. Funding was provided by the South African National Research Foundation, GUN 2034570. 
2 Author for correspondence (e-mail: mclellan{at}gecko.biol.wits.ac.za
)
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