Structure of the Cyperaceae Inflorescence.
Abstract: This work presents the basics for interpreting the adult inflorescence structure in Cyperaceae. It provides an analysis of the variations of the synflorescence and inflorescence structure in the family. Three types of synflorescence may be recognized in this family: a synflorescence with a foliate stem, a terminal inflorescence and a variable number of lateral inflorescences; a synflorescence with a foliate stem and only the terminal inflorescence; and a synflorescence with a scape and a terminal inflorescence. Variations in the structure and form of the inflorescences are related to variations in inflorescence branching, inflorescence homogenization degree, presence or absence of the distal part of the inflorescence, phyllotaxis, inflorescence position, types of bracts and leaves subtending branches, elongation of inflorescence internodes and spikelet structure. These variations are correlated with some of the developmental processes that give origin to the inflorescence.

Keywords Cyperaceae * Synflorescence * Inflorescence. Homogenization process * Truncation process
Article Type: Report
Subject: Cyperaceae (Physiological aspects)
Fluorescence (Research)
Plant physiology (Research)
Authors: Reutemann, Andrea
Lucero, Leandro
Guarise, Nicolas
Vegetti, Abelardo C.
Pub Date: 06/01/2012
Publication: Name: The Botanical Review Publisher: New York Botanical Garden Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2012 New York Botanical Garden ISSN: 0006-8101
Issue: Date: June, 2012 Source Volume: 78 Source Issue: 2
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: Argentina Geographic Code: 3ARGE Argentina
Accession Number: 294894964
Full Text: Introduction

Cyperaceae, the third largest monocotyledonous family, comprise ca. 5.500 species in ca. 109 genera (Muasya et al., 2009) and constitute a specialized group of plants, particularly in relation to their reproductive structure (Kukkonen, 1994). In studying the Cyperaceae family, the characters of the inflorescence have played an important role in the diversification of many taxa, and have had significant phylogenetic value (Tucker & Grimes, 1999). Cyperaceae are difficult to classify due to the complex structure of their inflorescences, which leads to different interpretations and to establishing uncertain hypotheses of homology (Kukkonen, 1984, 1986, 1994; Simpson, 1995; Muasya et al., 1998; Vegetti, 2003). The establishment of hypotheses of structural homologies among different types of inflorescences is one of the main concerns of cyperologists (Raynal, 1971).

In the formal taxonomy of Cyperaceae, the misapplication of terms with regard to descriptions of the inflorescence morphology has led to wrong examples in the morphological sense, since uniformity or stability of terminology have been lacking (Kukkonen, 1994; Browning & Gordon-Gray, 1999). Within this context, homologous structures are named differently, and different structures are named alike (Simpson, 1992; Alves, 2000). The main problems in the interpretation of the inflorescence structure result from studies which did not consider the entire inflorescence (Vegetti, 2003); instead, attention was restricted to the position and arrangement of flowers in the final units of the often copiously branched inflorescence (Kukkonen, 1984).

In order to understand and compare inflorescences within this family, it is necessary to establish a terminology for the different components of the inflorescence; such terminology should refer to homologous structures and make it possible to determine variation paths from basic organizational plans (Mora-Osejo, 1987). Several broad approaches have been presented in the family (Haines, 1966; Guaglianone, 1970; Raynal, 1971; Meert & Goetghebeur, 1979; Haines & Lye, 1983; Tucker, 1987, 1994; Goetghebeur, 1998; Vegetti, 2003), however, a global view is lacking.

In view of this, this work aims at: a) stating the basics for interpreting inflorescence structures in Cyperaceae and their variations; and b) correlating such information with the various developmental processes that give origin to those structures. It must be noted that this work does not intend to comprise all of the variations occurring in the inflorescence structure in the family, but it includes some of the most relevant types.

The Structure of the Plant and its Floriferous Shoots

In Cyperaceae, as in many grass plants, the plant is composed of shoots of consecutive branching order. One of the shoots is the main axis of the plant and the others are axillary shoots (innovations = basal branches) generated in the basal zone of short internodes. Each of these shoots should be considered, in a morphological sense, as a synflorescence (Troll, 1964; Rua, 1999). The synflorescence is the floriferous shoot produced from an apical bud of the embryonic axis or from an innovation bud during the growth period (Troll & Weberling, 1989; Rua, 1999).

The structure and general shape of the synflorescence result from the activity of its meristems, which determines the number, size and relative disposition of its branches (Guarise & Vegetti, 2007).

The axillary basal shoots may develop and flower within the same vegetative period as their parental axis, or their branch development may be substantially delayed relative to the development of the parental axis (Mora-Osejo, 1960). These are silleptic innovation shoots or cataleptic innovation shoots, respectively (Rua, 1999; Vegetti, 2003). In most Cyperaceae, basal axillary meristems grow out to produce a highly tillered plant. As it occurs in other monocotyledonous plants, these buds are still under hormonal and environmental control (Shimamoto & Kyozuka, 2002; McSteen, 2009).

During the vegetative phase, the apical meristems of the main axis and the axillary basal shoots generate leaves and shoots and, following floral induction, the terminal inflorescence (tIn). This inflorescence may be in the terminal portion of a long internode (scape) (Fig. 1C), or a foliate stem of somewhat developed internodes (Fig. 1B, C). The axillary buds in the foliate stem may develop (Fig. 1A) or not (Fig. 1B); thus, in some species, the tin appears alone in the distal portion of such foliate stem (Fig. 1C), while in other species the axillary buds develop floriferous shoots (enrichment shoots, Fig. 1A). Each of these enrichment shoots ends in an inflorescence (lateral inflorescence, lIn). The subtending leaves where the enrichment axes originate from bear developed blades and sheaths. The subtendig leaves (bracts) where the inflorescence branches originate from are modified leaves without sheaths.

[FIGURE 1 OMITTED]

Based on the aforementioned, the following synflorescence types may be recognized in the family: (1) a synflorescence with a foliate stem and a tin and a variable number of lIns (Fig. 1A), as in some species of Carex L., Fuirena Rottb., Rhynchospora Vahl, Scleria P.J. Bergius; (2) a synflorescence with only a tin and a foliate stem, as in some species of Hypolytrum Pers. (Fig. 1B); (3) a synflorescence with a scape and a tin, like Isolepis R. Br. and Cyperus L., Bulbostylis Kunth, Fimbristylis Vahl, Eleocharis R. Br, Scirpus L. (Fig. 1C).

Synflorescences with a foliate stem and terminal and lateral inflorescences (Fig. 1A) are a primitive condition in the family (Guarise & Vegetti, 2007). According to these authors, the inhibition of the development of enrichment shoots from the axils of the upper leaves makes it possible to obtain a synflorescence with only a tin and a foliate stem (Fig. 1B); while the shortening of the internode zone with the elongation of the internode above the last vegetative leaf leads to the formation of synflorescences with a scape and a tIn (Fig. 1C).

The change from a synflorescence with a foliate stem and tin and lIns (Fig. 1A) to a synflorescence with a scape and only a tin (Fig. 1C) takes place in the Arthrostylideae/Abildgaardieae clade (Guarise & Vegetti, 2007). According to these authors, reduction trends, starting from one structure like the plesiomorphic synflorescence proposed, were used to explain the variation observed in the inflorescences of Hypolitrum (Alves et al., 2000), Rhynchospora section Dichronema (Michx.) Griseb. (Thomas, 1984), Carex (Reznicek, 1990) and Kobresia Willd. (Zhang, 2001).

The presence of flowering branches in the axils of bracts with developed blade and sheath along an axis brings about a discussion on the limits and structure of the inflorescence in Cyperaceae. Several authors have considered the synflorescence with the elongated and foliaceous main axis, with or without branches emerging from the axil of leaves with developed blade and sheath, as a whole inflorescence termed paniculodium (Mora-Osejo, 1960; Raynal, 1971; Haines & Lye, 1983; Bruhl, 1995; Goetghebeur, 1998). However, other authors have considered the distal group of branches as the ultimate inflorescence (Thomas, 1992; Strong, 2001; Alves, 2003) or the terminal flowering unit (Reznicek, 1990); while the lateral branches produced at the axil of normal leaves with developed blade and sheath have been named lateral or partial inflorescence (Guaglianone, 1996; Alves, 2003) or lateral flowering unit (Reznicek, 1990).

There is some evidence in favor of considering the existence of terminal and lateral inflorescences in Cyperaceae. According to Mora-Osejo (1987), the enrichment axes (i.e. the flowering branches arising from the axils of bracts with a well-developed sheath) are differentiated from the inflorescence branch (i.e. the flowering branching which emerges from buds originating from the axils of bracts without a developed sheath) by their different development sequences. In this context, Sell (1980) suggested that the enrichment axes flower basipetally while the inflorescence branches develop acropetally. This sequence was observed in the reproductive meristem of Carex disticha Huds. by Mora-Osejo (1987).

Inflorescence Structure in Cyperaeeae

As a general model, during inflorescence development, the apical inflorescence meristem (IM) generates bracts and their axillary meristems, called branch meristems (BM), which are generally indeterminate and produce the inflorescence branches. After several branches are produced, the IM switches and generates axillary meristems that produce one spikelet (spikelet meristem, SM), which is determinate. Next, the IM may generate or not a varying number of bracts whose axillary meristems do not develop and, finally, it generates fertile leaves (glumes) with floral meristems (FM) in their axils, which make up the terminal spikelet.

In a few Cyperaceae, the IM does not produce branches, which means the inflorescence has a single terminal spikelet (unispicate inflorescence) (Fig. 2E, G, Goetghebeur, 1998; Vegetti, 2003). However, in most Cyperaceae, the IM produces lateral meristems that may behave either wholly as SMs and, consequently, do not produce other branches and end immediately in a spikelet (Fig. 2D, e.g. species of Ascolepis Nees ex Steud., Kyllinga Rottb., Lipocarpha R. Br.), or partially as BMs and partially as SMs, and then the former go on to branch again (Fig. 2A-C, F). As a consequence, based on the behavior of the meristems, the inflorescence may comprise one or several spikelets arranged in a branching system with varying degrees of complexity (Fig. 2).

In unispicate inflorescences (Fig. 2E, G), the 1M does not generate either a BM or an SM, and if it does, such axillary meristems do not develop--only the FMs show. Branching in spikes of spikelets (Fig. 2D) is controlled by two types of axillary meristems: the SM and the FM. Branching in an inflorescence with a branched axis (Fig. 2A-C, F) is controlled by three types of axillary meristems: BM, SM and FM.

The different inflorescence phenotypes are the result of different developmental processes (Albert et al., 1998; Doust & Kellogg, 2002). These variations in the inflorescence structure within the family are determined by variations in: a) inflorescence branching, b) inflorescence homogenization degree, c) presence or absence of the distal part of the inflorescence, d) phyllotaxis, e) inflorescence position, f) types of bracts and leaves subtending branches, g) elongation of inflorescence internodes, and h) spikelet structure. All of these characters are controlled by the activity of a group of regulatory genes that respond to internal or external signals (Kellogg, 2000).

Inflorescence Branching

The inflorescence results from the activity of its own meristems, which defines the production or loss of iterative structures, and is finally determined by the number, size and relative arrangement of their branches (Guarise & Vegetti, 2007). The architecture of the inflorescence depends on its branching pattern (Vegetti, 2003). The unispicate inflorescence (Fig. 2E, G) lacks branches and consists of the terminal spikelet only. This reduction may concern an entire genus and characterize its type of inflorescence (as in Eleocharis), or it may only happen in some species of a genus (e.g. Bulbostylis, Goetghebeur & Groger, 1992; Isolepis, Vegetti, 1994) and even within the same species, as in Abildgaardia ovata (Burm. f.) Kral, Bulbostylis capillaris (L.) C.B. Clarke var. microstachys (Boeck.) Barros, B. brevifolia Palla (Reutemann et al., 2009), Schoenoplectus pungens (Vahl) Palla var. longispicatus (Britton) S.G. Sm. (Vegetti, 1992) and Bolboschoenus maritimus (L.) Palla (Browning & Gordon Gray, 1999).

However, in most species, the meristem forms lateral branches (primary branches). In some Cyperaceae, these primary branches are reduced to its terminal spikelet. When the internode below the spikelet (pedicel = hipopodium) is not elongated, the inflorescence is a spike of spikelets (Fig. 2D). The spike of spikelets is observed in Kyllinga, Lipocarpha and Ascolepis. In Carex, a spike of spikelets is also considered a specialized inflorescence (Reznicek, 1990); it is the result of one advanced degree of reduction and it is one of the most derivative types of inflorescence in the family (Guarise & Vegetti, 2007).

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

In other genera, the primary branches go on to branch again. Generally, there is a gradual transition in the number of spikelets in each inflorescence and in the branching order of the inflorescence branches (Fig. 2A). The branching degree becomes distally reduced and the branches become progressively shorter toward the apex (Fig. 2A). Therefore, the basal and median branches are branched, while the distal branches are not branched and reduced to their terminal spikelet. In many inflorescences of Cyperaceae, most of the primary branches have a lower similar order of branching, except for the very distal ones, which are reduced either to the minimum branching degree or to the terminal spikelet. These inflorescences with many branches of similar branching order are homogenized inflorescences (see next section).

For a proper interpretation of the inflorescence, it is important to know the inflorescence ramification pattern (Haines, 1966; Meert & Goetghebeur, 1979; Vegetti & Tivano, 1991) and the branch position in the inflorescences (Guarise & Vegetti, 2007). In the Cyperaceae inflorescence, three types of branching can be observed, namely (1) normal branching: the branch is produced by an axillary bud of a bract (Fig. 2A); (2) prophyllar branching: the prophyllar branch is produced by a prophyllar bud (Fig. 3A, B; E, F); (c) accessory branch: new branches are observed between an axillary branch and its bract (Fig. 3C-H). These accessory branches lack their own subtending bract; because of this, only one bract protects this entire ramification.

Prophyllar productions may have varying degrees of development in different species and even within one species (Reutemann et al., 2009); also, they may repeat themselves several times; thus, the prophyllar branching pattern may or not result in a whole series of prophyllar branches.

In the accessory branches, each of these accessory axes has its own prophyll, in whose axils a prophyllar branch can be produced. The accessory pattern is produced by serial or collateral buds. In the serial branches of Cladium P. Browne (Mora-Osejo, 1960), variations regarding the extent of development of these buds may be observed in different positions of the inflorescence: in the lowermost inflorescence region, the bottom enrichment axis is stronger and has more ramifications, while the opposite takes place in the distal region, where the top shoot is the one showing the highest degree of development. This means that accesory serial buds follow an upward pattern in one case and a downward pattern in the other.

Normal and prophyllar branching patterns have been described by several authors (Blaser, 1944; Haines, 1966; Guaglianone, 1970, 1980, 1981, 1982; Meert & Goetghebeur, 1979; Bruhl, 1995; Goetghebeur, 1998; Vegetti & Guaglianone, 2005). Branches arising from accessory serial buds are observed in Hypolytrum (Alves et al., 2000), Cladium mariscus (L.) Pohl (Mora-Osejo, 1960) and Cyperus (Guarise & Vegetti, unpublished), while supernumerary collateral buds are observed in Schoenus ferrugineus L. (Mora-Osejo, 1960) and Coleochloa setifera (Ridl.) Gilly (Kukkonen, 1986). Prophyllar and accessory-axillary productions can be either branched or reduced to their terminal spikelet.

Although normal branching takes place along the inflorescence, the presence and position of prophyllar and accessory-axillary branches in the inflorescences may vary. In this context, whereas prophyllar branching is an important feature of the main branching system of the inflorescence, it is relatively rare in the spikelet clusters (Haines, 1966), except in the spikelet clusters of some species of Cyperus section Luzuloidei (Guarise & Vegetti, 2007), in Bulbostylis (Reutemann et al., 2009) and Rhynchospora (Haines, 1966). In different species, prophyllar and accessory-axillary axes may or may not be arranged in different ways along the main inflorescence axis and branches. In Bulbostylis, the development of prophyllar productions does not occur in a given region of the inflorescence, whereas in Cyperus incomtus Kunth var. incomtus and C. ochraceus Vahl, these branches are located in the distal region of the main axis. In some species of Cyperus section Luzuloidei Kunth, accessory-axillary axes of the 1st order can either develop from the proximal region upwards throughout the main axis (e.g. C. eragrostis Lam. var. compactus (E. Desv.) Ktik., C. fraternus Kunth, C. reflexus Vahl and C. surinamensis Rottb.), in the median-distal region (C. eragrostis var. eragrostis, C. intricatus Schrad. Ex Schult., C. luzulae (L.) Retz., C. virens Michx. var. drummondii (Torr. & Hook.) Kill and C. virens var. virens) or just in the distal region of the main axis (C. entrerianus Boeck., C. hieronymi Boeck., C. virens var. montanus (Boeck.) Denton). The presence or lack of prophyllar and accesory branches, as well as their position, have proved to be useful as taxonomic characters in some species of Cyperus section Luzuloidei (Guarise & Vegetti, 2007); whereas the presence or lack of prophyllar productions, as well as their degree of development, have turned out to be both taxonomically and phylogenetically useful in some species of Bulbostylis (Guaglianone, 1970; Lopez & Reutemann, unpublished).

Inflorescence Homogenization Degree

Homogenization is the process by which some or all branches positioned in consecutive nodes along one axis have the same ramification degree and become similar to one another (Rua, 1999). Homogenization may be total or partial. In a fully homogenized inflorescence (homogenized inflorescence), the degree of ramification is the same for all branches. In a partially homogenized inflorescence, only the distal and median parts have been affected by the homogenization process, while the basal branches are more extensively branched with respect to the distal and median branches (Rua, 1999). In homogenized inflorescences, two types of branches may be recognized: long branches (lBr = long paraclade) and short branches (shBr, the distal one reduced to the terminal spikelet).

In homogenized inflorescences (Fig. 2B), the axillary meristems made up by the BMs only form SMs, which, in turn, generate branches reduced to one spikelet. After generating a certain number of primary branches with secondary branches reduced to one spikelet, the 1M of the homogenized inflorescence switches abruptly to produce a certain number of branches reduced to their terminal spikelet. The BMs are indeterminate meristems and the SMs are determinate meristems. Indeterminate meristems make an indefinite number of organs, whereas determinate meristems are consumed after making a specific number of organs (Vollbrecht et al., 2005; Bortiri & Hake, 2007). The homogenization process of the inflorescence is related to the meristem determinancy (Perreta et al., 2009a). In this sense, the meristem determinancy would guide the degree of homogenization (Salariato et al., 2010).

The homogenization process is usually associated with the truncation process (Perreta et al., 2009a); however, this association is rare in Cyperaceae (see next section).

Presence or Absence of the Distal Part of the Inflorescence

After producing a certain number of branches, the IM generally ends in a terminal spikelet (Fig. 2A-C). In a few species, the IM forms a variable number of branches and then stops and does not develop the distal floral structures (Fig. 2F). The process characterized by the lack of formation of the distal floral structures has been called "truncation" (Troll, 1964; Weberling, 1989). Truncation may affect the development of the terminal spikelet only, or it may also affect the development of the distal region with short branches and some long branches (Perreta et al., 2009a).

Although truncation is not frequent in this family, a few species show truncated inflorescences. Truncation in Cyperaceae may affect only the terminal spikelet on the main axis (Cariceae, Reznicek, 1990; Vegetti, 2002), or it may also affect the primary shBrs (Fig. 2F) (Vegetti, 2002) and the primary 1Brs (e.g. Cyperus papyrus L., C. prolifer Lam., C. giganteus Vahl (Fig. 2F, Mora-Osejo, 1960; Raynal, 1971; Haines & Lye, 1983; Perreta & Vegetti, 2002; Vegetti, 2003). On the 1Brs, truncation may affect the terminal spikelet and the shBrs (Perreta & Vegetti, 2002; Vegetti, 2003).

In some families, such as grasses, truncation is a very common process which is frequently associated with homogenization, and both processes account for much of the diversity among grass inflorescences (Reinheimer & Vegetti, 2008; Perreta et al., 2009b). However, while most inflorescences show varying degrees of homogenization in Cyperaceae, truncation is not common in this family. In those few species of Cyperaceae where truncation does occur, inflorescences are homogenized (Fig. 2F).

Phyllotaxis and Branch Disposition

Phyllotaxis varies along the synflorescence (main shoot and branches); the disposition of the leaves in the vegetative zone is tristichous (phyllotaxis 1/3), whereas in the inflorescence branch zone the bracts, and their branches, have a spiral arrangement. The inflorescence primary branches emerge in an alternate arrangement, one per node; however, some inflorescences show branches with a subopposite or pseudo-verticillate arrangement (primary branches disposed in nodes very close around the main axis). In the inflorescence of some species of Cyperus (Guarise & Vegetti, 2007), the formation of more than three orthostichies can be observed. Each of these orthostichies is made up by branches from the basal and distal regions of the inflorescences; whereas the branches of the median region are not positioned over any orthostichies. If the number of primary branches on the main axis is not nine or more than nine, there are no orthostichies (e.g. some C. incomtus var. incomtus inflorescences). In the axillary and prophyllar branching, the disposition of branches can follow a fight-hand or left-hand spiral; showing an antidromic arrangement. This antidromic arrangement is not observed in the accessory-axillary ramification (Guarise & Vegetti, 2007).

In the last branching order (spikelet), the glume phyllotaxis can be either spiral (e.g. Schoenoplectus (Rchb.) Palla) or distichous (e.g. Cyperus). In Cyperus sect. Luzuloidei (Guarise & Vegetti, 2007), all the glumes have a distichous arrangement (1/2 phyllotaxis), except for the prophyll. The distichous disposition of the glumes would indicate a change in the inflorescence phyllotaxis, from a spiral arrangement (3/8 phyllotaxis) to a distichous phyllotaxis (1/2 phyllotaxis), and this switch may be mediated by the prophyll of the spikelets in a transitional position, because it forms a 90 [degrees] angle with respect to the glumes (Guarise & Vegetti, 2007).

In species of Scleria, the glumes are disposed distichously in the pistillate spikelets, while the subandrogynous spikelet, staminate spikelet, and androgynous spikelet have one proximal portion with glumes disposed distichously and one distal portion with glumes disposed spirally (Camelbeke, 2002; Ahumada & Vegetti, 2009); this arrangement of the glumes is also characteristic of the bisexual spikelets of Abildgaardia ovata. In species of Scleria with the latter type of spikelet--considering each axis separately (the main axis and the branched paracladia)--, the phyllotaxy pattern changes first from spiral (in the vegetative part) to distichous and then again from distichous to spiral. The transition from the tristichous disposition, being characteristic of the leaves of the vegetative region, to the spiral arrangement in the inflorescence is a relevant feature that should be noted (Guarise & Vegetti, 2008). However, a double and bidirectional change in the phyllotaxy pattern along the same morphological axis is very unusual, as it occurs in the inflorescences of Scleria with subandrogynous, staminate, or androgynous spikelets. Extensive spikelet and floral ontogenetic research is needed to clarify these phyllotaxy changes.

The transition from the tristichous disposition, being characteristic of the leaves of the trophotagma region, to the spiral arrangement in the paracladial zone is a relevant feature that should be noted (Vegetti & Anton, 1995; Camara-Hernandez, 200la, b; Reinheimer & Vegetti, 2004; Reinheimer et al., 2005; Kern et al., 2008).

Inflorescence Position

The inflorescence position as related to the culm can be terminal or pseudolateral. When the inflorescence takes a pseudolateral position, the lower bracts and proximal inflorescence branches point into the same direction as the stem, turning the main axis aside. In this type of inflorescence, the first bract may be culmlike (e.g. Schoenoplectus: Vegetti, 2002) or foliaceous (e.g. Cyperus surinamensis, unpubl.). In Cyperaceae, pseudolateral inflorescences evolve independently more than once and can occur in isolation, as in the Cyperus genera (Heinzen & Vegetti, 1994; Guaglianone, 1996), or be a feature for all the species belonging to a genera, as in Schoenoplectus (Vegetti & Tivano, 1991; Vegetti, 1992) and Isolepis (Vegetti, 1994).

In terminal inflorescences, the main axis goes on the same direction as the stem. In some cases, in species with terminal inflorescences, the bracts and inflorescence branches are erect, as in the pseudolateral inflorescences (e.g. Cyperus intricatus). This feature, which has been observed in the family (Bruhl, 1995), could be considered as an intermediate position between terminal and pseudolateral. Some authors only refer to the pseudolateral arrangement when the bract goes on the same direction as the stem (Haines & Lye, 1983; Goetghebeur, 1998) and make no reference whatsoever to the inflorescence main axis. This type of consideration has led to considering one true terminal inflorescence as pseudolateral.

Bracts and Leaves Subtending Branches

The inflorescence main axis bears bracts that decrease in length up the axis; each bract subtends an axillary bud that produces a primary lateral inflorescence branch. Each primary branch has a prophyll and a variable number of bracts. Buds in the axils of the bracts and, in some species, in the axils of the prophylls expand and repeat the branching pattern in the successive branches (Richards, 2002; Vegetti, 2003).

Different types of bracts may be recognize in the inflorescence: (1) foliaceous, with a well-developed blade and a scarcely or not developed sheath; (2) setiform, without a sheath, the leaf blade enlarges at the base but the mid and upper portions are narrow and stretched (setalike), sometimes acuminate; and (3) glumaceous, similar to a glume, but with a short setiform appendix.

The length reduction of the inflorescence internodes of different order and the reduction of the branching degree of the inflorescence branches are generally correlated with the reduction in the shape of the bracts (Guarise & Vegetti, 2007). Because of this, the main axis may show, in acropetal succession, all three types of bracts (foliaceous-setiform-glumaceous), or two types (foliaceous-glumaceous, setiform-glumaceous) or only the glumaceous type. Given the clear acropetal development of its componentes, every inflorescence has glumaceous bracts, both in the distal portions on the main axis and on the inflorescence branches.

The primary bracts are often described as involucral bracts, the lowermost bracts are usually foliaceous (sheathing or not) or setiform, and the uppermost bracts are very small and glumaceous; however, not rarely, primary bracts can be all foliaceous (Cyperus imbricatus Retz.) or all glumaceous (Cyperus papyrus). The bracts of the ultimate branchlets (spikelet bracts) are often barely distinct from glumes (Goetghebeur, 1998). In some species, bracts can be patent or reflex; also, in some species, the lower bracts can be upright, continuing the culm and culmlike (see Inflorescence Position). Lower bracts may be longer or shorter than the inflorescence.

The prophylls can be well developed, but they are often reduced or even absent. They show an acropetal variation in size and form: tubular (cladoprophyll), laminar and glumaceous. All of them are two-keeled, a hardly observable character in the glumaceous ones. The length of the lowermost prophylls varies among species, whereas the length of the distal ones (glumaceous) is smaller in all species studied.

The occurrence of the different types of bracts and prophylls varies according to the region of the inflorescence (Guarise & Vegetti, 2007). Some authors (Haines, 1966; Tucker, 1983) consider the length and shape of the bracts to bear taxonomic significance.

Elongation of the Inflorescence Internodes

The length variation in the internodes both on the main axis and on the branching axes of different order determines important variations in the external appearance of the Cyperaceae inflorescence. Internodes lengthening is related to the time of development of each species (Tucker & Grimes, 1999); it is genetically determined (Kellogg, 2000).

In Cyperaceae, the inflorescence main axis may show long or short internodes, determining the so-called panicle (Fig. 2A) and anthela (Fig. 2B) respectively or, in the sense of Troll's terminology, the paniculodium and the anthelodium (Rua, 1999; Guarise & Vegetti, 2008). Raynal (1971) and Goetghebeur (1998) consider the panicle of spikelets as the basic cyperaceous inflorescence which can be modified by the contraction of the internodes and various reductional trends.

In the inflorescence branches, the internode length is variable; with the epipodium being the internode showing the main variations. The variations in the anthela of spikelets depend on the length of the epipodium of their branches (see Inflorescence Form). A capitate inflorescence may derive from a paniculodium, an anthelodium, or from a spike of spikelets because of the reduction of the internode length of the main axis and the inflorescence branches. There is no reason to suppose that the reverse pathway might happen to produce a type of inflorescence with an epipodium developed from any more congested form (Guarise & Vegetti, 2007).

The internode growth from the inflorescence branch axes (except the epipodium) affects the inflorescence shape, especially in the manner in which branches group in the distal portion of an inflorescence branch with a developed epipodium; these groups can be simply described as a contracted head or glomerulous (e.g. Cyperus sect. Luzuloidei), digitate inflorescences (C. laxus Lam.), lax (C. esculentus L.) or congested spikes (C. aggregatus (Willd.) Endl).

Structure of the Spikelet

In Cyperaceae, the spikelet is the morphological unit of the inflorescence (Eiten, 1976). Studies of inflorescences in Cyperaceae focus mainly on the spikelet, whose reduced size and complexity have led to varying interpretations. In this context, there is much controversy over the spikelet in the family and until now its interpretation has remained unclear (Vrijdaghs, 2006). This author considers that this confusion partially results from old discussions influenced by the euanthial and pseudanthial hypotheses and related monopodial or sympodial interpretation of spikelets. There is plenty of literature on the structure and development of flowers and spikelets in the family (Payer, 1857; Pax, 1886; Celakovsky, 1887; Schonland, 1922; Mattfeld, 1938; Blaser, 1941, 1944; Holltum, 1948; Mora-Osejo, 1960, 1987; Kern, 1962; Raynal, 1971; Meeuse, 1975a, b; Eiten, 1976; Haines & Lye, 1976; Kukkonen, 1986; Meert & Goetghebeur, 1979; Goetghebeur, 1986, 1998; Bruhl, 1991, 1995; Muasya, 1998; Timonen, 1998; Vrijdaghs et al., 2003, 2004, 2005a, b, c, 2007, 2009, 2010; Zhang et al., 2004a, b; Richards et al., 2006), that is why this subject is not covered in this review. Based on findings from many ontogenetic studies (Vrijdaghs et al., 2003, 2004, 2005a, b, c, 2007, 2009; Richards et al., 2006; Reutemann et al., 2009), we consider spikelets to be monopodial ramifications.

Many variations which are valuable from a taxonomic or systematic point of view have been observed in spikelets (see Eiten, 1976; Bruhl, 1995). The most important variations include: a) flower sexuality: spikelets with male and female flowers may be gynandrous (with the female flower distal), androgynous (with the male flower distal) and mesogynous (with female flowers proximal and distal to the male flowers); b) shape (shortly ovate, elliptical, lanceolate, linear, ovate, etc); c) compression (laterally or dorsiventrally compressed or more or less terete); d) rachilla internodes more or less straight, zigzag or flexuose; e) rachilla prolongation exceeding (e.g. Uncinia Pers.) or not the flowers; f) rachilla persistent or deciduous at maturity; g) type of rachilla disarticulation at maturity (not disarticulating, disarticulating above the prophyll, disarticulating below the prophyll, shattering with points of abscission at the base of each fruit or not shattering); h) rachilla with wings or wingless, i) wings deciduous or persistent; j) glumes spirally or distichously disposed; and k) glumes persistent or deciduous (completely, incompletely, individually or collectively deciduous).

Hypothesized Evolutionary Processes

Reduction is the most frequent way of modification in the inflorescences of Cyperaceae (Thomas, 1984; Zhang, 2001), and it is considered the main trend of synflorescence evolution among and within the tribes (Guarise & Vegetti, 2008). The reductive processes do not always affect equivalent areas. Indeed, reductive processes can occur in branches, resulting in less complex inflorescences, as in supra-decompound and simple anthelas in Cyperus; they can affect the proximal region of the inflorescence and complex branches, resulting in a spike of spikelets (with this inflorescence being the most derived stage in Cyperaceae, Guarise & Vegetti, 2008); or they may affect the entire inflorescence, which is then reduced to its terminal spikelet. In other cases, it is the distal part of the inflorescence that is reduced in a sequence that can affect either the terminal spikelet alone, the short branches or some of the long branches (Fig. 2F), as occurs in truncated inflorescences of Cariceae (Vegetti, 2002) and Cyperus giganteus (Perreta & Vegetti, 2002). Truncation is not frequent in this family.

The broad diversity shown by inflorescences in the family can be explained by the analysis of some processes that operate in different ways, either combined or independently (Guarise & Vegetti, 2007). These authors characterize 25 processes that have contributed to variations in the Cyperaceae inflorescence. These processes may be grouped into the following classes: (1) reduction/elongation of the internodes; (2) branch development; (3) reduction/development of foliar structures; (4) homogenization; and (5) truncation.

Several trends and processes create morphological differences and similarities between and within the tribes, and even in the same genus. This may cause parallelism and reversions in the evolutionary course. Examples of parallelism can be observed in the synflorescence of different genera such as Chrysitrix L. and Eleocharis R. Br., among certain synflorescences of Hypolytrum (Alves, 2003) and Eriophorum L., or among Scleria, Fuirena and Rhynchospora (Guarise & Vegetti, 2008). Ficinia Schrad. and Bolboschoenus (Asch.) Palla might be good examples of reversion because these genera show synflorescences with a foliate stem (considered an ancestral state) but belong to clades where the synflorescence has all basal leaves and the inflorescence is supported by a scape (considered a derived state) (Guarise & Vegetti, 2008).

Beyond parallelism and reversion within the inflorescence architecture, it is possible to identify groups of taxa in which particular types of inflorescences have evolved (Stebbins, 1974; Tucker & Grimes, 1999). This allows to identify basic structures for a given group and to understand the way in which the processes have changed the synflorescence architecture.

Inflorescence Form

The following inflorescence forms have been described in the Cyperaceae family:

--Panicula of spikelets (or paniculodium): conical indeterminate inflorescence; the terminal spikelet and the distal branches emerge distinctly higher than the proximal branches (Fig. 2A) (e.g. the panicle-like inflorescences of Hypolytrum, Alves et al., 2000; Alves, 2003). In the panicula of spikelets, the branches may have their internodes more or less lengthened or completely shortened, looking like lateral capitula or heads (densely paniculate inflorescence; Scirpodendron Zipp. ex Kurz, Goetghebeur, 1998).

The panicula of spikelets, as an inflorescence, evolved early in basal groups in the phylogeny of the family, as in some species of Hypolytrum (Hypolytreae I), Scleria and Rhynchospora. Raynal (1971) and Goetghebeur (1998) consider the panicle as the basic cyperaceous inflorescence which can be modified through the elongation or contraction of the internodes in various reduction trends. This type of inflorescence is also observed in Juncaceae (e.g. Oxychloe Phil. and Luzula DC.; Pedersen, 1968; Barros, 1969) and it can be considered plesiomorphic based on the outgroup comparison criterion (Guarise & Vegetti, 2008).

--Anthela of spikelets (or anthelodium): crateriform indeterminate inflorescence, with the terminal spikelet and the short and distal branches hidden among the long and proximal ones, which overtop them. This results from the inhibited lengthening of the main axis intemodes and the distal branch epipodium, with an important development of the basal branch epipodium (Fig. 2B). The anthela of spikelets may be simple, compound, decompound and supra-decompound depending on the branching order with expanded epipodium (either first, second, third, or fourth and above, respectively). This variation in the form of the anthela of spikelets has been described in species of Cyperus (Wilson, 1991; Guaglianone, 1996; Guarise & Vegetti, 2007, 2008).

--Corymb of spikelets (or corymbodium): indeterminate inflorescence with the primary branch spikelets arranged like the flowers of a corymb (Rua, 1999). In this inflorescence, the variable epipodium length determines the spikelets to be disposed all at the same level (Fig. 2H). Haines & Lye (1983) describe terminal and lateral corymbs in Rhynchospora corymbosa (L.) Britton.

--Umbel of spikelets (or sciadodium or umbelliform inflorescence): indeterminate inflorescence, with the spikelets disposed like the flowers of an umbel (Rua, 1999). Haines & Lye (1983) only recognize as true umbels the truncated inflorescences of Cyperus papyrus and C. prolifer. We consider that true umbelliform inflorescences do not exist in Cyperaceae. In the umbel, the stalks arise from a same point (Weberling, 1989), while in umbelliform Cyperaceae inflorescences, the branches follow a one-per-node disposition (alternately arranged) and are separated by very short internodes. In this context, the inflorescence of C. papyrus and C. prolifer depicted as a true umbelliform inflorescence is a truncated anthela of spikelets as it has been described for C. giganteus (Perreta & Vegetti, 2002).

--Capituliform inflorescence (or capitate inflorescence or cephalodium): indeterminate inflorescence, similar to a capitulum or head, due to a pronounced shortening of the internodes on the main axis and branches of different order. In some cases, there is also a reduction of the branching degree (Fig. 2C). Many of the above described inflorescences may be reduced to a capitate inflorescence; in many cases, probably due to unfavorable environment conditions (Raynal, 1971; Browning & Gordon-Gray, 1999; Rua, 1999).

--Spike of spikelets (or stachyodium): indeterminate inflorescence with spikelets disposed sessile on the main axis (Fig. 2D). In some cases, the terminal spikelet is absent (truncation) and only branches reduced to final spikelets remains (Cariceae, Vegetti, 2002). The spike of spikelets can be composed of spikelets with perfect flowers (e.g. Schoenoplectus, Isolepis and Cyperus) or unisexual flowers (e.g. Cariceae). In some spikes of spikelets, the unisexual flowers may form bisexual spikelets (male and female flowers on a same rachilla) or unisexual spikelets (male and female flowers on different rachillae) (Meert & Goetghebeur, 1979; Timonen, 1998). The spikes with unisexual and bisexual spikelets (in given cases) may be gynandrous (i.e. with the female-only spikelet distal) or androgynous (i.e. with the male-only spikelet distal) (Bruhl, 1995).

In extremely complex inflorescences, the distal region of the main axis, as well as the distal region of the many branches (especially the basal branches with long epipodium), can also show a branch arrangement similar to one of the above described forms. This leads to a set of combinations including: panicula of congested spikes (e.g. Carex uruguensis Boeck.; Carex trachycystis Griseb.; Scirpodendron), anthela of spikes of spikelets (e.g. Cyperus digitatus Roxb.), anthela of fascicles of spikelets, anthela of capitula (e.g. Bulbostylis consanguinea (Kunth) Clarke, B. junciformis (H.B.K.) Clarke, Cyperus entrerrianus); anthela with monostachius axis (e.g. Fimbristylis robusta K. Lye; F. dipsaceae (Rottb.) C. B. CL).

Within the various forms that have been characterized, it is important to describe, in turn, subtypes of inflorescences according to: (1) the truncation process (truncated or non-truncated inflorescences, Perreta & Vegetti, 2002); (2) the homogenization proccess (fully homogenized inflorescences, partially homogenized inflorescences, non-homogenized inflorescences, Guarise & Vegetti, 2007; Lucero et al., 2009; Reutemann et al., 2009).

Conclusions

The structural diversity of the Cyperaceae inflorescences may be analized at the spikelet level or at the inflorescence branch level. In this review, we analyze the variations at the inflorescence and synflorescence branch level. The most significant variations that affect the inflorescence branches determine that inflorescences may be composed of numerous spikelets, arranged in a more or less complex branching system, or consist of a few spikelets or even one spikelet. Variations at the level of the inflorescence branches are related to:

* number of primary inflorescence branches;

* number of the primary branches in each node: alternate, subopposite or pseudo-verticillate branches;

* development degree of the primary branches:

--reduced to the terminal spikelet,

--formed by the terminal spikelet and a variable number of branches of consecutive order (only secondary branches or branches of order n);

* different elongation of the internodes of : (1) the main axis; (2) the epipodioum; and (3) the rest of the intemodes of the inflorescence branches;

* disposition of the branches of consecutive order;

* development of the bracts and prophylls;

* development of the prophyllary buds;

* development of the accessory buds;

* homogenization degree;

* truncation degree.

Variations at the synflorescence level are related to:

* presence of scape or of foliate stem;

* absence or presence of enrichment shoots and its axillary inflorescences in the foliate stem.

In this work, we analize the structure of the mature inflorescence. The extensive variation in adult inflorescences of Cyperaceae is the result of the diverse inflorescence development patterns, as it has been shown in Grasses (Doust & Kellogg, 2002; Reinheimer, 2007; Perreta et al., 2009a). Research on the evolution of morphological diversity of the Cyperaceae inflorescences in large clades and the combination of developmental and mature structure studies are essential; these will contribute to a more detailed interpretation of the inflorescences in the family's different genera as well as to a description of a larger morphological variability. Such studies will help to establish new characters that may be useful in future taxonomic and phylogenetic studies.

It is important to characterize the inflorescence and the synflorescence properly. For comparative purposes, only homologous structures should be compared, that is, inflorescences should only be compared with inflorescences but not with synflorescences.

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Andrea Reutemann (1,2) Leandro Lucero (1,2) * Nicolas Guarise (1), Abelardo C. Vegetti (1,2,3)

(1) Facultad de Ciencias Agrarias, Universidad Nacional del Litoral, Esperanza, Pcia. Santa Fe, Argentina

(2) Instituto de Agrobiotecnologia del Litoral, Facultad de Ciencias Agrarias, Universidad Nacional del Litoral, Kreder 2805, S3080HOF Esperanza, Provincia de Santa Fe, Argentina

(3) Author for Correspondence; e-mail: avegetti@fca.unl.edu.ar

Published online: 5 April 2012

DOI 10.1007/s12229-012-9098-z
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