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. 2022 Aug 13;130(5):737–747. doi: 10.1093/aob/mcac104

Ontogeny and anatomy of Bouteloua (Poaceae: Chloridoideae) species display a basipetal branch formation and a novel modified leaf structure in grasses

Luis Fernando Cuellar-Garrido 1,2, Eduardo Ruiz-Sanchez 3,4,✉, Ofelia Vargas-Ponce 5,6, Clinton J Whipple 7
PMCID: PMC9670754  PMID: 35961673

Abstract

Background and Aims

Shoot ontogenesis in grasses follows a transition from a vegetative phase into a reproductive phase. Current studies provide insight into how branch and spikelet formation occur during the reproductive phase. However, these studies do not explain all the complex diversity of grass inflorescence forms and are mostly focused on model grasses. Moreover, truncated inflorescences of the non-model grass genus Urochloa (Panicoideae) with formation of primary branches have basipetal initiation of branches. Bouteloua species (Chloridoideae) are non-model grasses that form truncated inflorescences of primary branches with apical vestiges of uncertain homology at the tips of branching events and sterile florets above the lowermost fertile floret. Sterile florets are reduced to rudimentary lemmas composed of three large awns diverging from an awn column. Conflict about the awn column identity of this rudimentary lemma is often addressed in species descriptions of this genus. We test if Bouteloua species can display basipetal initiation of branches and explore the identity of vestiges and the awn column of rudimentary lemmas.

Methods

We surveyed the inflorescence ontogeny and branch/awn anatomy of Bouteloua species and compared results with recent ontogenetic studies of chloridoids.

Key Results

Bouteloua arizonica has florets with basipetal maturation. Branches display basipetal branch initiation and maturation. Branch vestiges are formed laterally by meristems during early branching events. The spikelet meristem forms the awn column of rudimentary lemmas. Vestiges and sterile floret awns have anatomical similarities to C4 leaves.

Conclusions

Basipetal initiation of branches is a novel feature for Chloridoideae grasses. Branch vestiges are novel vegetative grass structures. Sterile floret awn columns are likely to be extensions of the rachilla.

Keywords: Acropetal, anatomy, awn, basipetal, branch, grass, inflorescence, Kranz anatomy, ontogeny, phyllotaxy, rachilla, spikelet

INTRODUCTION

Shoot ontogenesis in grasses is made up of two phases; the vegetative phase (production of leaves and internodes) and the reproductive phase (inflorescence) (Tanaka et al., 2013). Organs in both phases are produced in phyllotactic arrangements by the shoot apical meristem (SAM), which transitions in identity from a vegetative meristem (VM) to an inflorescence meristem (IM) (Tanaka et al., 2013; Bartlett and Thompson, 2014). Following the reproductive transition, ordered initiation of branch meristems (BMs), spikelet meristems (SMs) and floret meristems (FMs) produces the distinctive inflorescence architecture of each species (Kellogg, 2000).

Moreover, structures formed during the vegetative and reproductive phase follow a general phytomer organization that is present in all grasses (Clark and Fisher, 1987; Forster et al., 2007). Phytomers are a series of iterative units. Each unit consists of the consecutive generation of an axillary meristem (AM), internode and leaf (Fig. 1A).

Fig. 1.

Fig. 1.

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Expected overview of the ontogeny of Bouteloua species and mature morphology of Bouteloua arizonica and Bouteloua chondrosioides vestiges. (A) Schematic of Bouteloua species inflorescence showing its expected ontogeny and B. chondrosioides vestiges. (B) Aerial shoots and vestiges of B. arizonica with a terminal inflorescence at maturity. Inserts in (A) and (B) show the main axis and branch vestiges of B. chondrosioides and B. arizonica. Small vertical bars in (A) indicate second-order branches.

In the vegetative phase, the leaves are initiated and mature acropetally (from the base to the apex) in a species-specific interval of time known as a plastochron (Itoh et al., 1998). In contrast, the ontogeny of the reproductive phase in grasses is more complicated (Kellogg, 2015). This complexity of grass inflorescence morphology is caused by a wide variation in morphology of the inflorescence main axis (e.g. phylotaxis, presence/absence of branches, determinate or indeterminate meristems, etc.), branching patterns and spikelets (Clayton, 1990; Soreng and Davis, 1998; Kellogg, 2000, 2006, 2015; Malcomber et al., 2006; Perreta et al., 2009). Moreover, some inflorescence structures can originate and/or mature not only acropetally (from the base to the apex), but also basipetally (from the apex to the base) (Kaplan and Specht, 2022). This makes it difficult to describe the grass reproductive phase since any combination of acropetal/basipetal initiation and/or maturation can vary among grass lineages (Kellogg, 2015) or even in different parts of the inflorescence of the same species (Le Roux and Kellogg, 1999; Reinheimer et al., 2009).

Categorical descriptions of the wide morphological variance of the mature grass inflorescence have been proposed (Troll, 1964; Vegetti, 1991; Cámara Hernández and Rua, 1991; Weberling et al., 1993; Vegetti and Anton, 1996). These have expanded into generalizations of the mature grass plant morphology as a whole (Vegetti, 1991; Vegetti and Anton, 1996; Vegetti and Weberling, 1996). However, these descriptions quickly become very complex to apply in practice and do not seem to be related to any clear biological process (Kellogg, 2015). Moreover, the grass spikelet has been described as a contracted inflorescence axis and is an evolutionary novelty that shares characteristics with branch systems and flowers that is clearly unique to the grass family (Kellogg, 2015).

Genetic studies provide insight into how branch (Vollbrecht et al., 2005; Bortiri et al., 2006; Satoh-Nagasawa et al., 2006) and spikelet (Chuck et al., 1998, 2002; Komatsu et al., 2003) formation occurs in model grasses. Suppressed bracts in the grass inflorescence (Wang et al., 2009; Chuck et al., 2010; Whipple et al., 2010; Houston et al., 2012) are proposed as one of many signalling centres producing mobile signals that regulate the determinacy of the meristem adjacent to the suppressed bract (Whipple, 2017; Xiao et al., 2022). However, these studies are not sufficient to explain all the complex diversity of grass inflorescence forms.

Moreover, non-model grasses in general have not been studied as thoroughly as grass model species, and provide an opportunity to investigate undescribed morphological patterns at early stages of inflorescence development that could further illuminate the constraints influencing grass inflorescence development and diversity. Specifically, an intriguing observation by Reinheimer et al. (2009) established that non-model grasses of the genus Urochloa (Panicoideae) with truncated inflorescences (not forming a spikelet at the distal end of the main axis) and formation of solely primary branches have basipetal initiation of branches that do not form a subtending bract.

We hypothesize that members of the PACMAD clade subfamily Chloridoideae (subfamily with most species after Panicoideae) (Soreng et al., 2017) with mature inflorescence morphology similar to Urochloa species with basipetal branch initiation can also share this developmental trait. To test this, we study Bouteloua arizonica (Fig. 1B), a recently described non-model C4 grass species that forms a mature inflorescence similar to its sister species Bouteloua aristidoides (Cuellar-Garrido and Siqueiros-Delgado, 2021). Both species form truncated inflorescences with one vestige at the distal end of the main axis and branches (Fig. 1A), first-order branches only, spikelets with a highly reduced rachilla (0.5 mm long) and two florets. The lower fertile floret has a lemma with three terminal awns and a two-keeled palea, while the upper floret is sterile, reduced to a structure commonly interpreted as a rudimentary lemma composed of three large awns that diverge from an awn column. The central awn of the upper floret bears a highly reduced leaf membrane at its basal periphery. Conflict about the awn column identity of this rudimentary lemma has often been addressed in species descriptions of this genus (Griffiths, 1912; Gould, 1979; Wipff, 2003; Herrera Arrieta et al., 2004).

In addition, we attempt to elucidate the nature of vestiges and the identity of the sterile floret awn column in Bouteloua species by comparing the anatomy of the vestiges and sterile florets of B. arizonica with those of B. chondrosioides. The latter species morphology is similar to that of B. arizonica regarding sterile floret and main axis vestige, but differs by producing two twisted vestiges at the tip of its branches instead of only one upright vestige (Fig. 1). These comparisons give us additional insight into the nature of these structures in the genus since B. chondrosioides is phylogenetically distant from B. arizonica (Peterson et al., 2015). Moreover, we compare our findings with a recent ontogenetic study by Pilatti et al. (2019) of B. aristidoides which is described as having first-order branches with acropetal organogenesis and basipetal maturation, a basipetal spikelet organogenesis/maturation along the branch axis and the main axis distal vestige interpreted as the aborted portion of the main axis in this species and in other Chloridoideae species (Muchut et al., 2021) (Fig. 1A).

MATERIALS AND METHODS

Plant material

Seeds of B. arizonica collected at Sonora (Mexico) from Siqueiros 5220 (HUAA) were cultivated in greenhouse facilities at the California Botanic Garden (formerly known as the Rancho Santa Ana Botanic Garden). Aerial shoots from multiple individuals of this species were collected at different developmental stages. Leaf sheaths were removed with the help of dissecting scissors. Samples were collected at what appeared to be a vegetative phase of development (no apparent inflorescence formation by touch or visually), early reproductive stages (clear inflorescence formation by touch but still inside the leaf sheath), immature reproductive stages (clear inflorescence formation visually but with branches still inside the leaf sheath) and mature reproductive stages (with caryopsis formation). Seeds of B. chondrosioides collected from a population at 13 km south-east from Alpine (TX, USA) were cultivated in greenhouse facilities at Centro Universitario de Ciencias Biológicas y Agropecuarias (Universidad de Guadalajara). Mature awns and branches of these species were also removed with the help of dissecting scissors. After removal, all tissues were immediately fixed for 24 h at 4 °C in FPA (1:1:18 37 % formaldehyde:propionic acid:70 % ethanol) solution. Afterwards, FPA was replaced by 70 % ethanol for storage of samples at 4 °C (Kinney et al., 2008). Throughout the experiments, high-density polyethylene bottles with caps (Nalgene bottles) were used for fixation, storage and dehydration of tissues.

Scanning electron microscopy

Samples were placed in Petri dish covers with a constantly renewed surface covering of 70 % ethanol. Inflorescences were dissected by cutting from below their proximal stem node and removing leaf sheaths with the help of micro dissecting needles and a Leica stereo microscope. Dissected tissues were carefully put back in Nalgene bottles using dissecting forceps, and dehydrated in a series of increasing ethanol concentrations (90 % for 2 h, 95 % for 2 h, 100 % for 2 h and 100 % overnight) (Columbus, 1998). Dehydrated material was carefully deposited with the help of dissecting forceps inside base/top-covered embedding cassettes with cut-to-size Whatman paper and the cassettes were laid in a Petri dish cover with a surface covering of 100 % ethanol. Closed cassettes were immediately put inside a high pressurizing Pelco E3000 chamber and critical-point dried for 1 h with liquid CO2. The critical-point-dried plant material was very carefully grabbed from the stem node tissue and vertically mounted on scanning electron microscope stubs using dissecting forceps. Stubs were immediately sputtered coated with gold in an argon-based Pelco Sc-7 sputter coater. Imaging of the inflorescences was performed with an ISI model WB-6 scanning electron microscope.

Anatomical sections

Previously fixed samples were desilicified with 30 % aqueous hydrofluoric acid for 2 d (Breakwell, 1914). Dehydration, paraffin embedding, sectioning and slide affixation of whole samples was done according to Columbus (1998) with the modification of not using tertiary butyl alcohol during dehydration. Tissues were oriented longitudinally or transversely during embedding and microtome sectioning to produce 10 μm thick sections. Slides with affixed tissues were stained in a slide carrier and a stain dish (500 mL volume) for each step solution according to Sharman (1943) (with modifications provided by J. Travis Columbus) (Supplementary data Table S1) and according to Johansen (1940) for awns and B. chondrosioides branches. Sections were evaluated under a Leitz Laborlux D light microscope (Leica Instruments) and digitally photographed using a SPOT digital camera with SPOT 3.2.4 imaging software (Diagnostic Instruments).

RESULTS

Inflorescence transition and branch initiation

The B. arizonica vegetative SAM develops lateral organs distichously until it transitions to the reproductive phase. After the reproductive transition, two structures that are engulfed by a common sheathing leaf can be formed; one corresponds to the terminal inflorescence while the other is a lateral inflorescence preceded by a prophyll that envelops it (Fig. 2). The terminal inflorescence creates three structures. Two of them are separated by 180° and the third one is medial (approx. 90°) from the other two (Figs 2A and 3A–C). The medial structure of the terminal inflorescence is born opposite from the last vegetative leaf (Figs 2A and 3A–C, J) and develops into a small vestige that does not enlarge very much (Fig. 3A–C, F, I–L), forms a central vascular bundle with two vertical rows of chlorenchyma cells surrounding it and bears a reduced blade-like tissue distally at maturity (Fig. 3M, N). The other two structures initiate opposite each other, but rotated 90° relative to the vestige and correspond to branch primordia (BPs) (Fig. 3A–I, K). The inflorescence elongates basipetally as the inflorescence matures, forming the inflorescence main axis (Figs 2 and 3A–L).

Fig. 2.

Fig. 2.

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Development of a Bouteloua arizonica arrested lateral inflorescence. (A) Scanning electron microscope picture of the terminal and lateral inflorescence at early stages of development. (B–D) Longitudinal anatomy sections of terminal and lateral inflorescences (circles) at successive developmental stages. LI, lateral inflorescence; TI, terminal inflorescence. Black scale bars = 250 μm.

Fig. 3.

Fig. 3.

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Bouteloua arizonica inflorescence main axis and primary branch development. (A–C) Scanning electron microscopy (SEM) pictures of the terminal inflorescence and lateral inflorescence at early stages of development. (B) Rotated view of (A). (D, F, H–J) SEM pictures of terminal inflorescence development. (D) Terminal inflorescence with only three branches formed and maturing basipetally, the uppermost with spikelets initiating basipetally. (F) Terminal inflorescence with several branches initiated and forming spikelets. (H) Uppermost branches of the terminal inflorescence with spikelets forming florets while the proximal branches are still at the stage of primordia and the the lowermost recently initiated. (I) Rear view of (H) terminal inflorescence showing the main axis vestige size unaltered with respect to earlier stages. (J) Terminal inflorescence with the apical spikelet of the uppermost branch covered by glumes. (E, G, K) Longitudinal anatomy sections of terminal inflorescences at successive developmental stages. (E) Branch primordia with apparent basipetal initiation. (G) Apical branch with distal vestige and spikelets formed. (K) Main axis elongated with vestige size unaltered and lowermost branches forming spikelet primordia. (L) Mature inflorescence main axis vestige. (M) Longitudinal anatomy section of the proximal portion of the mature inflorescence main axis vestige indicated by the lower box in (L). (N) Longitudinal anatomy section of the distal portion of the main axis vestige indicated by the upper box in (L). (O) Terminal and lateral consecutive inflorescences, the lateral inflorescence preceded by a prophyll. B, branch; BP, branch primordium; BV, branch vestige; IM, inflorescence meristem; IV, main axis inflorescence vestige; LB, leaf blade portion of the main axis vestige; LG, lower glume; MA, inflorescence main axis; P, prophyll; S, spikelet; SFM, sterile floret meristem; SL, sheathing leaf; SM, spikelet meristem; TIV, terminal inflorescence main axis vestige; UG, upper glume. Other abbreviations are as in Fig. 2. Inserts in (O) show a dissected lateral inflorescence early in development and preceded by a prophyll. The box in (H) highlights the resemblance between this branch and branch 1 in (D). Yellow arrows in (M) and (N) indicate vertical rows of chlorenchyma (dyed brown) surrounding central vascular tissues of the vestige. Asterisks in (M) indicate vascular tissues (dyed purple). White scale bars = 100 μm.

The subsequent BPs initiate distichously and basipetally along the inflorescence main axis without evidence of subtending bracts. All branches are formed at about 90° from the main axis vestige. The branches mature basipetally at all developmental stages of the inflorescence and display formation of a branch vestige at their branch tips that is oriented at about 90° from spikelets (Fig. 3D–K). We did not find any signs of secondary branch formation.

Lateral inflorescence development

The development of the lateral inflorescence remains arrested during the formation and maturation of the terminal inflorescence (Fig. 2). This is apparent from early stages of development, where it is already clear that the terminal inflorescence enlarges its main axis and branch primordia while the lateral inflorescence does not (Fig. 2B–D). Longitudinal anatomical sections demonstrate that during later developmental stages of the terminal inflorescence, the lateral inflorescence size remains almost unaltered (Fig. 2B–D).

Spikelet development

Spikelet meristems are formed basipetally along each branch axis. Adjacent SMs appear to initiate as a common primordium that has a non-spherical morphology. The common primordium develops into two distinct convex protuberances that initiate sequentially. The upper (distal) protuberance is initiated before the lower protuberance, suggesting that adjacent emerging SMs are partially fused initially and subsequently separate (Figs 3D, H and 4A). Each SM creates two glumes with a substantial difference in size when they are formed (Fig. 4A, D, E). The sterile floret meristem (SFM) sits on top of the rachilla when it starts to form three protuberances that arise from a single lemma primordium (Fig. 4D, E). Two of them are separated by 180°. The third one is medial from the other two at about 90°, and is formed in the same longitudinal plane as glumes and opposite from the lower floret lemma (Fig. 4E). Each of the three protuberances develops into an awn that arises directly from the highly reduced lemma leaf blade (i.e. they are a single organ) while the rachilla on which the SFM rests elongates as the sterile floret matures (Fig. 4A, B, D, E). The lemma lateral awns initiate first (Fig. 4D, E) while the medial awn develops last and is connected to the lateral awns from the periphery of the highly reduced lemma leaf blade that is conspicuous at maturity (Fig. 4A, B, D, E).

Fig. 4.

Fig. 4.

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Successive developmental stages of Bouteloua arizonica spikelets. (A) Scanning electron microscopy (SEM) pictures of early spikelet development stages. (B) Mature sterile floret. (C) Transverse anatomical section of the medial awn at the location indicated by the dashed line in (B). (D) Top-down view SEM picture of spikelet development showing basipetal maturation of florets. (E) Top-down view SEM picture of spikelet development with the distal branch tip removed and showing asynchronous awn formation. AWP, awn primordium; FFM. fertile floret meristem; GP, gynoecium primordium; L, lemma; PA, palea; Par, parenchyma cells; Sc, sclerenchyma cells; SP, stamen primordium. Other abbreviations are as defined in Figs 2 and 3. The insert in (A) is a close-up view of a sterile floret meristem indicated with a box in the picture. Scale bars = 50 μm.

The fertile floret meristem (FFM) begins to develop shortly after the SFM (Fig. 4D, E). The lemma is already conspicuous when the palea initiates. Both lemma and palea initiate in the same distichous plane as the glumes, after which the FFM forms three stamen primordia, two of them separated by 180°. The other stamen primordium is medial from the other two (in about 90°) and distichous to glumes, lemma and palea (Fig. 4E). All spikelets mature basipetally with respect to their branch axis at all developmental stages of the inflorescence (Fig. 4A, D, E).

Anatomy of branch/main axis vestiges and sterile florets of Bouteloua

Transverse sections of the branch below the distal vestiges of mature branches of B. chondrosioides and B. arizonica show multiple vasculature strands at the centre of the branch and two well-defined lateral vascular bundles (aligned at 180° from each other) (Fig. 5A, B, C, J). Each vascular bundle forms, on their lateral side, an arc of two adjacent rows of outer chlorenchyma cells (Fig. 5A, B, C, J) that resembles the anatomy of the B. arizonica main axis distal vestige (Fig. 3N, O). This arrangement of vascular bundles endures throughout the extension of branches, and for B. chondrosioides each lateral bundle exceeds the extension of the branch distally, forming two lateral vestiges (Figs 1A and 5D). In B. arizonica, the two lateral bundles fuse at the apex of the branch forming a single vestige (Figs 1B and 5J, K).

Fig. 5.

Fig. 5.

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Anatomy of Bouteloua branch vestiges and a Bouteloua chondrosioides sterile floret. (A–I) Bouteloua chondrosioides. (A) Transverse section of a branch tip showing lateral bundles with arcs of chlorenchyma cells. (B) Magnification of the upper square portion from (A). (C) Magnification of the lower square portion from (A). (D) Transverse section of branch distal vestiges, each one with an arc of chlorenchyma cells. (E) Longitudinal section of the awn column and medial awn of a sterile floret. (F) Magnification of the square in (E) showing a vertical row of chlorenchyma cells at the medial awn. (G) Transverse section of the medial awn at the location indicated by the dashed line in (F). (H) Transverse section of the awn column at the location indicated by the lower dashed line in (E). (I) Transverse section of the awn column at the location indicated by the upper dashed line in (E). (J) Transverse branch section below the apical portion of a B. arizonica branch vestige showing lateral bundles partially fused. (K) Transverse section at the apical portion of a B. arizonica branch vestige showing lateral bundles fused into a single bundle. Numbers in (H) and (I) indicate provascular bundles. Red arrows, indicate chlorenchyma cells. Scale bars = 50 μm.

The sterile floret awn column and medial awn of B. chondrosioides show a distinct vascular anatomy (Fig. 5E). The medial awn has a central vascular bundle with two adjacent adaxial rows of chlorenchyma cells (Fig. 5E–G). The base of the awn column forms a central vascular bundle surrounded by parenchyma cells which asynchronously branches, producing two lateral vascular bundles (Fig. 5H, I). Transverse anatomical sections of the mature medial awn of B. arizonica sterile floret show a girder of sclerenchyma cells that is significantly thickened on its adaxial side, surrounded by layers of parenchymatous cells (Fig. 4C).

DISCUSSION

Inflorescence transition and branch initiation

The first morphological sign of the grass SAM transition from a VM into an IM is a rapid increase in meristem size, associated with a shift in phyllotaxy (Hoshikawa, 1989; Taguchi-Shiobara et al., 2001; Kellogg, 2015). Although phyllotaxy transitions from distichous to spiral in most species (Kellogg, 2015), other phyllotactic patterns characterize large clades of grasses. Such is the case of almost the entire Pooideae subfamily, where a distichous inflorescence phyllotaxy prevails (Kellogg et al., 2013). However, in Brachyelytrum erectum the distichous phyllotaxy of the inflorescence seems to follow a shift in orientation at the inflorescence transition since vegetative leaves are perpendicular to the first developed branches (Kellogg et al., 2013).

During its vegetative phase, the SAM of B. arizonica forms vegetative structures distichously. After the shift into an IM, three structures are apparent, two of them placed at 180°, and the third one medial from the other two at about 90° (Fig. 3A–C). The medial structure follows the distichous phyllotaxy of the VM (i.e. it is distichous to the last sheathing leaf primordia of the vegetative phase) (Fig. 3A–C, J) and remains vestigial (Fig. 3A–C, F, I–N). The other two structures develop into branches. Subsequent branches initiate distichously and basipetally along the inflorescence main axis (Fig. 3A–K). Bouteloua arizonica branch phyllotaxis resembles that seen in most Pooideae species where a distichous phyllotaxy prevails. However, the presence of the B. arizonica main axis vestige marks the end of the vegetative phase and a 90° change in the distichous phyllotaxy pattern of organogenesis in the SAM at its transition from a VM to an IM as suggested by Kellogg et al. (2013).

Pilatti et al. (2019) mention that branches in B. aristidoides are formed acropetally and mature basipetally. Our results show that B. arizonica primary branches originate and mature basipetally (Fig. 3A–I, K). Ontogenetic studies of Panicoideae species of Urochloa and Brachiaria decumbens were the first descriptions of primary grass branches not subtended by bracts that initiate basipetally (Stür, 1986; Reinheimer et al., 2005, 2009). The B. arizonica inflorescence forms primary branches only (the same as B. aristidoides). Moreover, initiation of subtending bracts of branching events as described for acropetal branch initiation in grasses (Reinheimer et al., 2009) was not observed in this study (Fig. 3A–I, K). Our evidence suggests basipetal initiation of branches in B. arizonica, in contrast to the description for B. aristidoides. It seems unlikely that sister species B. arizonica and B. aristodoides would differ in this fundamental trait. An interpretation that could amend these discrepancies is the hypothesis of Reinheimer et al. (2009) which suggests that the meristem cells responsible for the eventual formation of branch meristems are formed in an acropetal direction along the main axis and then later activation of those meristems is basipetal, which determins the basipetal initiation of primary branches. This interpretation could explain the acropetal structures displayed in the earliest developmental stages of the B. aristidoides main axis (Pilatti et al., 2019) as arrested meristems that later initiate branches basipetally. Unfortunately, our study did not find evidence for B. arizonica that could corroborate such an interpretation. Future analyses that could specifically test this hypothesis of Reinheimer et al. (2009) are encouraged.

The distal main axis vestiges (Figs 1, 2A and 3A–C, F, I–N) are characteristic of Bouteloua and many Chloridoideae species (Griffiths, 1912; Gould, 1979; Wipff, 2003; Herrera Arrieta et al., 2004; Pilatti et al., 2019; Muchut et al., 2021). Pilatti et al. (2019) and Muchut et al. (2021) interpret this structure as part of the aborted distal portion of the inflorescence main axis of chloridoids. Evidence in this study indicates that this structure in B. arizonica also includes an independent vegetative organ which emerged from the main axis. Chloridoid vestiges may be a combination of the aborted shoot apex as stated by Pilatti et al. (2019) and Muchut et al. (2021) plus a highly reduced structure that is produced by the VM as a last vegetative structure before it transitions into an IM.

The identity of the distal main axis vestige is not immediately clear. It is known that the grass IM can initiate bracts (inflorescence leaves) subtending branching events (Whipple et al., 2010; Whipple, 2017) along with BMs and SMs after it shifts phyllotaxy from its vegetative state (Pautler et al., 2013, Kellogg, 2015). However, these bracts are suppressed early in development (Evans and Grover, 1940; Latting, 1972; Fraser and Kokko, 1993; Whipple et al., 2010) by a genetic mechanism that inhibits the outgrowth of bracts that subtend inflorescence branching events before the production of spikelets (Chuck et al., 2010; Whipple et al., 2010; Whipple, 2017). The main axis vestige of B. arizonica marks a change in phyllotaxis between leaves and branches (Figs 2A and 3A–C). Although the phyllotaxy is the same for both branches and leaves (distichous), branches formed in the main axis do not share the same orthostichies as vegetative leaves (i.e. they are formed in a 90° disposition from leaves) (Figs 2A and 3A–C, J). This indicates a change in phyllotaxy orientation. Moreover, this vestige follows the orthostichies of vegetative leaves (i.e. opposite to the last vegetative leaf) (Fig. 3B, C) which is consistent with a vegetative origin. However, these vestiges do not subtend any branching events, which also suggests that they are novel modified leaf structures in Bouteloua distinct from suppressed bracts.

Bouteloua arizonica main axis/branch vestiges and B. chondrosioides branch vestiges share a similar vascular anatomy (Figs 3M, N and 5A–D, J, K). That is, all vestiges share Kranz anatomy as expected for vascular bundles of C4Bouteloua species (Columbus, 1998). This is the first study that presents the anatomy of these structures in both species.

Lateral inflorescence development

Bouteloua arizonica is capable of developing two consecutive inflorescences in close proximity (Figs 2 and 3A, B, O). In order to achieve this, the vegetative SAM transitions into the apical IM while the lateral inflorescence is generated by an AM with a transient vegetative stage that quickly transitions into a reproductive stage. In Figs 2A and 3B, O, we can see evidence of the rapid transition as the lateral inflorescence of B. arizonica is enveloped by a prophyll produced as the first leaf of this lateral structure.

After the B. arizonica axillary VM shifts into an IM and produces primary branch primordia, the lateral inflorescence arrests development while the terminal inflorescence continues to develop to full maturity (Fig. 2). This developmental arrest could be due to axillary bud dormancy, a common and well-studied phenomenon that controls lateral bud growth across diverse grasses (Pautler et al., 2013). Axillary bud dormancy involves two factors: antagonistic action of plant hormones such as auxins, cytokinins (McSteen and Leyser, 2005) and strigolactones (Gomez-Roldan et al., 2008; Umehara et al., 2008); and the shade-sensitive genes TEOSINTE BRANCHED1 (Doebley et al., 1997) and GRASSY TILLERS1 (Whipple et al., 2011). Future analyses could assess the contribution of orthologues of these genes along with phytohormones in B. arizonica’s lateral inflorescence dormancy.

Spikelet development

Our results show a basipetal initiation and maturation of spikelets along the branch axis (Figs 3D, F–K and 4A), in agreement with the reported B. aristidoides spikelet development (Pilatti et al., 2019). Pilatti et al. (2019) describe the initiation of all B. aristidoides spikelet organs as acropetal. Our study confirms acropetal initiation and maturation of glumes (Fig. 4A). We also see that the SFM initiates lemma awns of the upper sterile floret before the rachilla elongates and before the FFM (lower floret) forms any primordia (Fig. 4D, E), which suggests a basipetal maturation of florets. Lateral organs produced by the FFM undergo acropetal initiation and maturation (Fig. 4D, E). Having different orders of maturation in different components of a single inflorescence is not a novel feature in grasses since this condition has been described in different species of the subfamily Panicoideae and Andropogoneae (Le Roux and Kellogg, 1999; Reinheimer et al., 2009).

The common primordium from which adjacent SMs of B. arizonica originate is atypical for a meristem because it lacks a spherical morphology characteristic of meristems. Rather than a simple meristem, this primordium resembles the common primordium described as a ‘spikelet pair meristem’ in maize and other Andropogoneae (Le Roux and Kellogg, 1999; Chuck et al., 2002). However, the centre of the B. arizonica common primordium does not align with the orthostichies of other inflorescence structures, and the spikelet meristems it produces are fully separated into distichous orthostichies shortly after initiation (Figs 3D and 4A). Moreover, odd numbers of spikelets per branch for B. arizonica are very common (Cuellar-Garrido and Siqueiros-Delgado, 2021). Hence, we suggest that instead of a common meristem which either branches laterally or bifurcates to produce two SMs, this structure results from the slightly asynchronous development of two distichous SMs that are initiated in close proximity to each other, appearing partially fused but separating shortly after initiation (Figs 3D and 4A). The larger size of the apical region of this common primordium is consistent with basipetal initiation of distichous SMs.

The number of sterile florets produced by different Bouteloua species can range from one to many, and they are always formed above the lowermost fertile floret. In very rare cases, two consecutive fertile florets are found (e.g. B. repens). Moreover, the descriptions of many species of this genus treat the lowermost sterile floret (above the fertile one) as a lemma with an atypical morphology (e.g. B. annua, B. curtipendula, B. chondrosioides and B. kayi) (Griffiths, 1912; Gould, 1979; Wipff, 2003; Herrera Arrieta et al., 2004). This morphology in its extreme form includes an awn column with three diverging awns that may or may not have a basal leaf blade in between that in most cases is reduced and restricted to the medial awn (Fig. 4B) (Griffiths, 1912; Gould, 1979; Wipff, 2003; Herrera Arrieta et al., 2004).

Our study shows that the B. arizonica SFM asynchronously forms three awns laterally while the awn column elongates directly below it (Fig. 4D, E). The lemma primordium from which awns arise is apparent as a subtle continuity of tissue between the medial and lateral awns formed as each awn originates (Fig. 4E). The rachilla is occasionally interpreted as a basal product of the SM that supports FMs that in turn produce lemmas as lateral structures. However, some authors have interpreted the lemma as a structure that arises directly from the rachilla (i.e. from the SM) instead of being generated by the FM, in which case the lemma should be regarded as a fertile spikelet bract that subtends an FM (Arber, 1934; Bell, 1991; Kellogg, 2001; Lombardo and Yoshida, 2015). The later interpretation can explain the formation of B. arizonica sterile florets insofar as the SFM would be regarded as a lateral meristem formed in the axis of a highly reduced lemma (reduced to three divergent awns) produced by the SM and the awn column as an extension of the rachilla (previously interpreted as highly reduced) (Fig. 4A, B, D, E).

In conclusion, this analysis presents inflorescence development in B. arizonica and the anatomy of branch vestiges and sterile lemmas in this species and B. chondrosoides. The data show a basipetal initiation of branches in B. arizonica which contrasts with current descriptions of its sister species B. aristidoides (Pilatti et al., 2019), but a hypothesis by Reinheimer et al. (2009) could reconcile these discrepancies. The anatomy of mature vestiges of Bouteloua species and early developmental stages of the B. arizonica terminal inflorescence vestige indicates a novel modified leaf structure formed in grasses. The anatomy of Bouteloua sterile floret awns is presented for the first time. This anatomy consists of chlorenchyma, parenchyma and girders of sclerenchyma cells disposed in a configuration similar to the anatomy of C4 grass leaves. Moreover, B. arizonica early development and anatomy suggest a basipetal maturation of florets, and the awn column as an extension of the rachilla rather than the base of the rudimentary lemma.

SUPPLEMENTARY DATA

Supplementary data are available online at https://academic.oup.com/aob and consist of Table S1: Sharman staining series schedule with modifications provided by J. Travis Columbus.

mcac104_suppl_Supplementary_Material
Click here for additional data file. (11.4KB, docx)

ACKNOWLEDGEMENTS

We thank Mahinda Martínez (Universidad de Querétaro), the California Botanic Garden and the LaniVeg of Querétaro and Guadalajara for providing the facilities, equipment and materials used in the realization of this project. Thanks to J. Travis Columbus (California Botanic Garden) for his guidance during the establishment of methods, and to Michael Powell (Sul Ross State University) for providing seeds of Bouteloua chondrosioides. Also, many thanks to Elizabeth A. Kellogg (Donald Danforth Plant Science Center) and the anonymous editors and reviewers for their constructive criticisms and useful suggestions.

Contributor Information

Luis Fernando Cuellar-Garrido, Doctorado en Ciencias en Biosistemática, Ecología y Manejo de Recursos Naturales y Agrícolas (BEMARENA), Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Zapopan, Jalisco 45200, México; Laboratorio Nacional de Identificación y Caracterización Vegetal, Instituto de Botánica, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Zapopan, Jalisco 45200, México.

Eduardo Ruiz-Sanchez, Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Zapopan, Jalisco 45200, México; Laboratorio Nacional de Identificación y Caracterización Vegetal, Instituto de Botánica, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Zapopan, Jalisco 45200, México.

Ofelia Vargas-Ponce, Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Zapopan, Jalisco 45200, México; Laboratorio Nacional de Identificación y Caracterización Vegetal, Instituto de Botánica, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Zapopan, Jalisco 45200, México.

Clinton J Whipple, Department of Biology, Brigham Young University, 4102 LSB, Provo, UT 84602, USA.

FUNDING

This work was supported by the Consejo Nacional de Ciencia y Tecnología (grant no. 615539) and the Instituto para el Desarrollo de la Sociedad del Conocimiento del Estado de Aguascalientes CONACYT-Gobierno del estado de Aguascalientes 2017 grant, both provided to L.F.C.-G.

CONFLICT OF INTEREST

L.F.C.-G. conceived the project, wrote the paper and performed all the anatomical and scanning electron microscope analyses. C.W., E.R.-S. and O.V.-P. edited the paper and contributed with ideas, literature references and concepts during interpretation of results. The authors have no conflict of interest.

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Supplementary Materials

mcac104_suppl_Supplementary_Material
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