Leaf Anatomy, Emphasizing Unusual Concertina Mesophyll Cells, of Two East African Legumes (Caesalpinieae, Caesalpinioideae, Leguminosae)

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1 Annals of Botany 78: 55 59, 1996 Leaf Anatomy, Emphasizing Unusual Concertina Mesophyll Cells, of Two East African Legumes (Caesalpinieae, Caesalpinioideae, Leguminosae) JOHN D. CURTIS*, NELS R. LERSTEN and GWILYM P. LEWIS Biology Department, Uni ersity of Wisconsin-Ste ens Point, Ste ens Point, WI 54481, Department of Botany, Iowa State Uni ersity, Ames, IA 50011, USA, and Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, UK Received: 1 September 1995 Accepted: 9 January 1996 Cordeauxia edulis (Somalia and Ethiopia), and Stuhlmannia moa ii (Tanzania, Kenya and Madagascar) are evergreen shrubs or small trees of dry areas. They have similar leaf anatomy as revealed by resin sectioning and scanning electron microscopy. The cuticle is extremely thick and all vascular bundles lack bundle sheath extensions. The most unusual feature is the mesophyll, three to seven layers consisting entirely of cylindrical palisade cells with lateral walls capable of changing vertical length by folding in a concertina-like manner. The matching outward folds of two adjacent cells always remain attached by means of a row of wall thickenings ( pegs ). The pegs can elongate, especially so between the widely separated mesophyll cells that occupy the substomatal chamber area. The unattached flexible inward wall folds enable these concertina cells to shorten or lengthen vertically without disrupting cell interconnections in the interior of each relatively long-lived leaf as it periodically loses and gains water. Concertina cells may be an anatomical adaptation allowing these leaves to remain evergreen and survive extended periods of drought and yet to store water quickly when it becomes available Annals of Botany Company Key words: Leguminosae, Caesalpinioideae, Cordeauxia, Stuhlmannia, concertina mesophyll cells, desert adaptation, hollow glandular trichomes, leaf anatomy, wall thickenings. INTRODUCTION During a comprehensive survey of leaf anatomy of representatives of 106 species from all 47 genera of the caesalpinioid legume tribe Caesalpinieae (Lersten and Curtis, 1993, 1994, 1996), we encountered two species with unusual features. Unlike the excellent cleared preparations obtained from leaves of all other species, these cleared leaflets remained opaque and unsatisfactory. We were forced to study their anatomy only from sections and by scanning electron microscopy. Cordeauxia edulis and Stuhlmannia moa i are both woody evergreen shrubs of African desert areas and are probably adapted to frequent droughts. We discovered that both species exhibit similar highly unusual and previously undescribed anatomical features. We describe these features here and hope to stimulate further study of their possible adaptive significance. Both species are members of the informal Caesalpinia group within tribe Caesalpinieae of the legume subfamily Caesalpinioideae (Polhill and Vidal, 1981). Cordeauxia edulis is the only species in its genus. Also monotypic is Stuhlmannia moa ii, which recently has been interpreted to include Caesalpinia insolita (Lewis, 1996). MATERIALS AND METHODS Leaflets were obtained from these herbarium specimens: Cordeauxia edulis Hemsh. (A. S. Hassan 232, Somalia- * For correspondence $ KEW; C. F. Hemming 1494, Ethiopia-KEW; J. B. Gillett et al , Somalia-MO BOT GARD), and Stuhlmannia moa ii Taub. (R. E. S. Tanner 3167, Tanzania-KEW) [also collected under its synonym Caesalpinia insolita (Harms) Brenan & Gillett (M. E. Archbold 2247, Tanzania-KEW; J. P. M. Brenan et al , Kenya-KEW; R. B. Faden et al , Kenya-KEW)]. In addition we were allowed to remove (and fix for SEM) two leaflets from a small potted plant of Cordeauxia edulis ( ) growing in a Missouri Botanical Gardens greenhouse. Herbarium leaflet pieces were cleared and stained (Lersten, 1986), and additional small pieces were processed by standard methods for thick plastic sections (Lersten and Curtis, 1994). External leaflet features were studied using standard SEM techniques; internal features were also observed by SEM using the cross section break technique described by Lersten and Curtis (1994). RESULTS The evergreen leaves of both species exist for more than one season, but the life span of an individual leaf is as yet unknown. Both adaxial and abaxial surfaces are covered by an extremely thick cuticle (Figs 1 3, 5 8 and 9). Vascular bundles (Figs 1, 5 7), including the midvein (Fig. 7), lack a bundle sheath extension. The mesophyll consists entirely of palisade parenchyma cells; there is no spongy mesophyll. The only obvious differences among the mesophyll strata are that cells of layers nearer the abaxial surface are 1996 Annals of Botany Company

56 Curtis et al. Concertina Mesophyll Cells in Two Caesalpinioid Legumes FIGS 1 7. Leaflet sections of rehydrated herbarium specimens. Fig. 1. Cordeauxia edulis.

2 56 Curtis et al. Concertina Mesophyll Cells in Two Caesalpinioid Legumes FIGS 1 7. Leaflet sections of rehydrated herbarium specimens. Fig. 1. Cordeauxia edulis. Concertina cells show regular rows of wall pegs (e.g. between arrowheads) where adjacent cell walls adhere. Wall pegs are stretched in substomatal chamber (arrows). Bar 50 µm. Fig. 2. C. edulis. Close-up of two abaxial substomatal chambers showing exaggerated wall pegs (arrow). Bar 20 µm. Fig. 3. As Fig. 2, a few sections away. Pegs traverse substomatal chambers. Fig. 4. C. edulis. Paradermal section through abaxial subepidermis. Regular alternation of thin and thick (pegged) wall areas are evident in these concertina cells. Included are two substomatal chambers traversed by pegs (arrowheads). Bar 20 µm. Fig. 5. Stuhlmannia moa ii. The four to five layers of concertina cells show rows of wall pegs (arrowheads) and stretched pegs in substomatal chambers (arrows). Bar 50 µm. Fig. 6. S. moa ii. The four to five layers of concertina cells have rows of wall pegs (arrowheads) and stretched pegs in substomatal chambers (arrows). Bar 50 µm. Fig. 7. Cordeauxia edulis. Section through midvein showing the lack of a bundle sheath extension. Note portion of hollow glandular trichome at lower right. Bar 50 µm.

Curtis et al. Concertina Mesophyll Cells in Two Caesalpinioid Legumes 57 FIGS 8 10. Fig. 8. Cordeauxia edulis.

3 Curtis et al. Concertina Mesophyll Cells in Two Caesalpinioid Legumes 57 FIGS Fig. 8. Cordeauxia edulis. Leaflet cross section including median view of sunken gland with prominent cavity (C) and only three layers of palisade mesophyll concertina cells. Bar 50 µm. Fig. 9. C. edulis SEM cross section break from fresh fixed leaflet showing a stomate (S), elongate pegs (P) in a substomatal chamber, lateral views (l) and face views (large arrows) of rows of pegs between concertina cells, and views of rows of pegs from the inside (i) of concertina cells. Bar 10 µm. Fig. 10. S. moa ii. SEM of cross section break through dried (not rehydrated) leaflet. Note that mesophyll cells have folded in concertina-like fashion. Rows of wall pegs are evident (arrows). Bar 10 µm.

4 58 Curtis et al. Concertina Mesophyll Cells in Two Caesalpinioid Legumes somewhat shorter and have slightly larger intercellular spaces. The most unusual anatomical feature is all of the mesophyll consists of concertina palisade cells, approximately cylindrical in shape, with undulant lateral walls forming alternate inward and outward folds similar to a concertina. Along the outer edge of each outward fold, the wall is thickened where the matching outward fold of the adjacent cell is fused (Figs 1, 5 8, 9, 10). Adjacent cells adhere only along these regularly aligned thickenings, which must accommodate all plasmodesmata, and are separated elsewhere. In Cordeauxia, cells in all layers of the mesophyll display concertina cells (Figs 1 and 8); in Stuhlmannia, they are evident in the lower layers of mesophyll, but much less so in the upper layers (Figs 5 and 6). We did not attempt to identify the nature of the wall thickenings. They could be either additional ordinary wall deposits or some other substance such as pectin. Where the cells adhere, there is physical stress, which is often manifested by a stretching of the surrounding wall area into pegs that are variously drawn out depending on the extent of the intercellular space transversed. Most cells have five to seven rows of pegs, as seen in paradermal section, the plane that cuts the concertina cells in cross section (Fig. 4). The entire mesophyll of Cordeauxia, and to a somewhat lesser extent the lower mesophyll layers of Stuhlmannia, are composed of concertina cells. These cells surround both small (Figs 1, 5, 6) and large vascular bundles (Fig. 7), which is noteworthy because in most dicotyledons at least the larger vascular bundles have either parenchymatous or sclerified special cell extensions from the bundle sheath to the adaxial and or abaxial epidermis. In Cordeauxia edulis we saw large recessed hollow glands (Fig. 8) similar to those we reported from other members of Caesalpinieae (Lersten and Curtis, 1996). The mesophyll is thinner across the indentation, where it comprises only three layers of shortened concertina cells (Fig. 8) instead of the normal six or seven layers (Fig. 1). All figures but Fig. 9 are of rehydrated herbarium material; they show in sectional and SEM views the concertina cells expanded to their full vertical extent, or nearly so. Figure 9 is from the fresh fixed leaf, which appears nearly identical to those herbarium specimens that were rehydrated and fixed for SEM. Figure 10, in contrast, illustrates the deeply folded, shrunken appearance of the concertina cells in dried (not rehydrated) leaves, which approaches the configuration these cells would have in a living leaf during dry periods. Stomates occur on both surfaces in Cordeauxia (Fig. 1) but only on the abaxial surface in Stuhlmannia (Figs 5 and 6). Guard cells in both species have a prominent cuticular ridge (Fig. 2). Substomatal chambers seen in paradermal section (Fig. 4) and cross section (Figs 2, 3 and 9) did not show the typical large unimpeded space. Instead, the chamber area in both species consists of a rather small intercellular space of irregular shape traversed by several elongate pegs that form a simple lattice between adjacent concertina cells (Figs 1 6 and 9). In addition to restricted substomatal areas, which are anomalous compared to the substomatal chambers of vascular plants in general, intercellular spaces elsewhere in the leaf appear to be minuscule (Figs 1 8, 9, 10). DISCUSSION Mesophyll cells in both species exhibit unusual anatomical features. Wall thickenings of concertina cells resemble those we described for both palisade and spongy mesophyll cells of Caesalpinia ferrea (Lersten and Curtis, 1994), another species in the Caesalpinia group of tribe Caesalpinieae. Thickenings in that species, however, did not form pegs, and were not associated with any obvious leaf adaptation to dry conditions. We speculated that they might be pectic in nature, as per the review by Potgieter and van Wyk (1992), but van Wyk (pers. comm.) has opined that, since these thickenings do not abut an intercellular space, they are probably not pectic deposits. The excellent preparations we obtained from dried and rehydrated herbarium leaves and the limited live material we were able to examine, justify some speculation about how these unusual anatomical features might be related to leaf function. It seems likely that concertina cells under water stress lose water and compensate by shrinking vertically, thereby causing their cell walls to fold. In doing so, the entire leaflet also shrinks in thickness. Even areas above and below the vascular bundles, which lack bundle sheath extensions, shrink. When water again becomes available, perhaps even after only a brief rainfall, the concertina cells are probably capable of quickly and easily enlarging to store additional water, thereby collectively causing the leaflet to expand in thickness. In contrast to the orderly configuration of cells in leaves of Cordeauxia and Stuhlmannia, Mauseth (1995) recently described a somewhat less organized system of collapsible water storage cells in the stem cortex of certain leafless species of cacti. These cells collapse in all three dimensions and have intercellular spaces only at junctions of three or more cells, thus representing a somewhat different anatomical adaptation that seems to perform the same function as the concertina cells of the legumes. Since collapsible water storage cells appear in two unrelated families of dicotyledons, it may be a more widespread phenomenon, especially among evergreen species, than previously suspected. The occurrence of foliar rosette cells with involuted walls, well known in some evergreen conifers (e.g. Pinus), may be yet another modification of this anatomical adaptation to periodic drought. The unusual, perhaps unique, anatomical features of concertina cells could be important in adapting these evergreen leguminous shrubs to a xeric environment. Investigators with access to living plants will be able to test this hypothesis. Live plants will also be required to investigate the problems of gas exchange and temperature control in these dense leaves with reduced intercellular space. ACKNOWLEDGEMENTS The authors thank the Directors of the Herbaria at the Royal Botanical Gardens, Kew, UK and the Missouri Botanical Gardens, USA for permission to collect leaf

5 Curtis et al. Concertina Mesophyll Cells in Two Caesalpinioid Legumes 59 samples. Most of the light microscopy and darkroom work was done in the Bessey Microscopy Facility, Department of Botany, Iowa State University; scanning electron microscopy was done at the University of Wisconsin, Stevens Point. LITERATURE CITED Lersten NR Modified clearing method to show sieve tubes in minor veins of leaves. Stain Technology 61: Lersten NR, Curtis JD Subepidermal idioblasts in leaflets of Caesalpinia pulcherrima and Parkinsonia aculeata (Leguminosae; Caesalpinioideae). Bulletin of the Torrey Botanical Club 120: Lersten NR, Curtis JD Leaf anatomy in Caesalpinia and Hoffmannseggia (Leguminosae, Caesalpinioideae) with emphasis on secretory structures. Plant Systematics and E olution 192: Lersten NR, Curtis JD Survey of leaf anatomy, especially secretory structures, of Tribe Caesalpinieae (Leguminosae; Caesalpinioideae). Plant Systematics and E olution. (in press). Lewis GP Notes on Stuhlmannia Taub. and the correct placement of Caesalpinia insolita (Harms) Brenan & Gillett (Leguminosae: Caesalpinioideae: Caesalpinieae). Kew Bulletin. (in press). Mauseth JD Collapsible water storage cells in cacti. Bulletin of the Torrey Botanical Club 122: Polhill RM, Vidal JE Tribe 1. Caesalpinieae. Ad ances in Legume Systematics 1: Potgieter MJ, van Wyk AE Intercellular pectic protuberances in plants: their structure and taxonomic significance. Botanical Bulletin, Academia Sinica 33:

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