TY - JOUR
AU1 - Leandro, Thales, D
AU2 - Scatena, Vera, L
AU3 - Clark, Lynn, G
AB - Abstract Leaf blade anatomical and micromorphological data have increasingly proved to be useful in the systematics and phylogeny of Bambusoideae. The presence of well-developed, asymmetrically strongly infolded mesophyll cells (arm cells) as seen in cross-section is regarded a synapomorphy for bamboos, whereas many well-known, widely used features for diagnosing groups remain to be formally tested in a comprehensive phylogenetic framework. In this review, we investigate the use of anatomical and micromorphological features in defining and delimiting minor and major groups in Bambusoideae. A general description of the leaf blade as seen in cross-section and surface view is provided for the subfamily, as well as features commonly found in the three currently recognized tribes (Arundinarieae, Bambuseae and Olyreae) and their subtribes. Some features, including midrib vasculature, fusoid cells and stomatal apparatus, are discussed in the light of systematic and phylogenetic perspectives, along with a clarification of terminology. Illustrations of relevant features are also provided. This review allowed us to elucidate anatomical and micromorphological features useful in defining and delimiting lineages but also to highlight some research priorities in Bambusoideae. bamboos, epidermis, grass anatomy, leaves, mesophyll Introduction Grass leaf blades as seen in cross-section were studied for their systematic value for the first time by Duval-Jouve in 1875. Since then, studies on this subject have become increasingly frequent, and for a long time diagnostic combinations of leaf blade anatomical and micromorphological features have been used to establish relationships and to define major groups in the family (e.g. Brown, 1958; Ellis, 1987; Soderstrom & Ellis, 1987). In the 15 years following the first International Symposium on Grass Systematics and Evolution, held at the Smithsonian Institution in Washington, DC, in July 1986, many studies were undertaken to address grass relationships based on phenetic and phylogenetic analyses (Hamby & Zimmer, 1988; Esen & Hilu, 1989; Doebley et al., 1990; Hilu & Johnson, 1991; Davis & Soreng, 1993; Nadot, Bajon & Lejeune, 1994; Verboom, Linder & Barker, 1994; Barker, Linder & Harley, 1995, 1999; Clark, Zhang & Wendel, 1995; Duvall & Morton, 1996; Liang & Hilu, 1996; Hsiao et al., 1998; Hilu, Alice & Liang, 1999; Mathews, Tsai & Kellogg, 2000; Zhang, 2000). Some of these included leaf blade anatomical and/or micromorphological data (Kellogg & Campbell, 1987; Watson & Dallwitz, 1992; Watson, Macfarlane & Dallwitz, 1992 onwards; Clark & Judziewicz, 1996; Soreng & Davis, 1998; Clark et al., 2000). These papers were the basis for the first broad and explicitly phylogenetic work on grass systematics and classification published in the early 2000s, undertaken by a large collaborative group, which was referred to as the Grass Phylogeny Working Group (GPWG, 2001). The GPWG (2001) included a large dataset based on anatomical evidence, but also micro- and macromorphological, biochemical, embryological and molecular data. Although going through a few changes in its subfamilial circumscriptions, since GPWG (2001) and even today, Poaceae are usually recognized as including 12 well-supported subfamilies (Soreng et al., 2015; 2017): (1) the early-diverging lineages Anomochlooideae, Pharoideae and Puelioideae; (2) the BOP clade comprising Bambusoideae, Oryzoideae and Pooideae; and (3) the PACMAD clade comprising Panicoideae, Aristidoideae, Chloridoideae, Micrairoideae, Arundinoideae and Danthonioideae. Bambusoideae (bamboos) are the third most diverse and one of the most economically important subfamilies of Poaceae (Clark, Londoño & Ruiz-Sanchez, 2015; Soreng et al., 2017) comprising c. 1680 species in 127 genera (Soreng et al., 2017, plus additional new species and genera published since their estimate). The use of anatomical and micromorphological data in bamboo systematics and phylogeny has remarkable importance, especially for woody bamboos. Growing vegetatively for long periods, the life cycle of woody bamboos usually ends after a single gregarious episode (Seifriz, 1950; Janzen, 1976; Judziewicz et al., 1999), which often makes establishing systematic relationships challenging because flowering material may not be readily available. In contrast, virtually all herbaceous bamboos exhibit seasonal flowering episodes (Clark et al., 2015), although there are a few reports of possible gregarious flowering (Judziewicz et al., 1999), but leaf blade anatomy and micromorphology in this group is currently being studied and the results are awaited with interest. Primarily diversified in association with forests (Clark et al., 2015; Kellogg, 2015), bamboo species have leaf blades anatomically characterized by the presence of well-developed, asymmetrically usually strongly infolded mesophyll cells (arm cells) as seen in cross-section (Clark et al., 2015; Leandro et al., 2016; Leandro, Scatena & Clark, 2017). With a few exceptions, most bamboos also exhibit a mesophyll with intercellular cavities flanking the vascular bundles, often referred to as fusoid cells (see Leandro et al., 2018, and references therein). In addition, micromorphologically, the occurrence of papillae has been recognized as a prominent feature of bamboo leaves (Judziewicz et al., 1999). Strongly invaginated arm cells have been considered a synapomorphy for bamboos (Clark et al., 2015; Kellogg, 2015), but anatomical and micromorphological features such as type of midrib vasculature, presence of intercostal sclerenchyma and refractive papillae, type of trichomes, and morphology of the stomatal apparatus and silica cells appear to be fairly useful in diagnosing and delimiting species or groups in Bambusoideae (e.g. Oliveira, Longhi-Wagner & Leite, 2008a; Viana, Filgueiras & Paiva, 2011; Jesus Junior et al., 2012; Guerreiro, Rúgolo de Agrasar & Rodríguez, 2013; Zhang, Zeng & Li, 2014; Gu et al., 2016; Jaén et al., 2016; Leandro et al., 2016, 2017; Fernández & Ely, 2017). Herein, we review and investigate the use of leaf blade anatomical and micromorphological data in bamboo systematics and phylogeny. The last review on this subject was published by Soderstrom & Ellis (1987), but there is now a more accurate phylogenetic framework in which to interpret these data. Accepting that the use of many features still requires further assessment and clarification, we explore the current knowledge of bamboo leaf blade anatomy and micromorphology, including a general description of the leaf blade as seen in cross-section and surface view, the use of some features in bamboo systematics and phylogeny and general comments on key features for establishing systematic relationships in Bambusoideae. Our primary goals are to (1) emphasize the importance of leaf blade anatomical and micromorphological data in bamboo systematics and phylogeny and the standardization of anatomical descriptions; (2) clarify the use and terminology of some leaf blade anatomical features; and (3) establish research priorities in Bambusoideae. GENERAL ANATOMICAL AND MICROMORPHOLOGICAL DESCRIPTION OF A BAMBOO LEAF BLADE The following general description was based on the most common anatomical and micromorphological features found in bamboo leaf blades (for further details see Metcalfe, 1960; Chen, Jin & Wu, 1993a; Judziewicz et al., 1999; Clark et al., 2015; Kellogg, 2015). Terminology for the leaf blade as seen in cross-section and surface view primarily follows Ellis (1976, 1979, respectively). For describing the leaf blade as seen in cross-section, the widely employed term ‘fusoid cells’ was used as a proxy for the intercellular cavities formed as a result of the collapse of one to several fusoid cells during their development (Leandro et al., 2018). A general view of bamboo leaf blade anatomy and micromorphology is provided in Figures 1, 2 and 3. Figure 1. Open in new tabDownload slide Cross-section of Aulonemia pumila L.G.Clark & Londoño (Londoño et al. 382, ISC) leaf blade (light microscopy), showing a simple midrib vasculature and other mesophyll features commonly found in Bambusoideae. Scale bar = 20 µm. Figure 1. Open in new tabDownload slide Cross-section of Aulonemia pumila L.G.Clark & Londoño (Londoño et al. 382, ISC) leaf blade (light microscopy), showing a simple midrib vasculature and other mesophyll features commonly found in Bambusoideae. Scale bar = 20 µm. Figure 2. Open in new tabDownload slide Cross (A, B) and longitudinal sections (C) of bamboo leaf blades (light microscopy). A, well-developed, asymmetrically strongly infolded arm cells of Chusquea longispiculata L.G.Clark (Kuhlmann 3141, ISC). B, intercostal sclerenchyma near and opposite to the bulliform cells of Aulonemia aristulata (Shirasuna 2860, SP). C, cavities and fusoid cell (arrow) of Aulonemia aristulata (Shirasuna 2860, SP). Abbreviations: ac, arm cell; bc, bulliform cell; cv, cavity; is, intercostal sclerenchyma. Scale bars: 6 µm (C); 10 µm (A, B). Figure 2. Open in new tabDownload slide Cross (A, B) and longitudinal sections (C) of bamboo leaf blades (light microscopy). A, well-developed, asymmetrically strongly infolded arm cells of Chusquea longispiculata L.G.Clark (Kuhlmann 3141, ISC). B, intercostal sclerenchyma near and opposite to the bulliform cells of Aulonemia aristulata (Shirasuna 2860, SP). C, cavities and fusoid cell (arrow) of Aulonemia aristulata (Shirasuna 2860, SP). Abbreviations: ac, arm cell; bc, bulliform cell; cv, cavity; is, intercostal sclerenchyma. Scale bars: 6 µm (C); 10 µm (A, B). Figure 3. Open in new tabDownload slide Leaf blade micromorphology showing features commonly found in Bambusoideae. A, from light microscopy; B–E, scanning electron micrographs. A, types of leaf blade epidermal cells and their arrangement based on Chusquea ramosissima (Clark and Windisch 849, ISC). B, adaxial surface showing papillae, silica cells and trichomes (prickles) of Chusquea tenella (Swallen 9004, US). C, abaxial surface showing papillae, stomata and trichomes (macrohairs) of Chusquea tenella (Swallen 9004, US). D, detail of prickle and stomata apparatus bearing two simple papillae per subsidiary cell of C. tenella (Klein and Bresolin 7766, US). E, detail of microhair and stomata apparatus bearing two branched papillae per subsidiary cell of C. ramosissima (Klein and Klein 11041, US). Abbreviations: cc, cork cell; clc, costal long cell; ilc, intercostal long cell; pa, papilla; ma, unicellular macrohair; mi, bicellular microhair; pr, prickle; sc, silica cell; st, stomatal apparatus. Scale bars = 13 µm (D, E); 45 µm (B, C). Figure 3. Open in new tabDownload slide Leaf blade micromorphology showing features commonly found in Bambusoideae. A, from light microscopy; B–E, scanning electron micrographs. A, types of leaf blade epidermal cells and their arrangement based on Chusquea ramosissima (Clark and Windisch 849, ISC). B, adaxial surface showing papillae, silica cells and trichomes (prickles) of Chusquea tenella (Swallen 9004, US). C, abaxial surface showing papillae, stomata and trichomes (macrohairs) of Chusquea tenella (Swallen 9004, US). D, detail of prickle and stomata apparatus bearing two simple papillae per subsidiary cell of C. tenella (Klein and Bresolin 7766, US). E, detail of microhair and stomata apparatus bearing two branched papillae per subsidiary cell of C. ramosissima (Klein and Klein 11041, US). Abbreviations: cc, cork cell; clc, costal long cell; ilc, intercostal long cell; pa, papilla; ma, unicellular macrohair; mi, bicellular microhair; pr, prickle; sc, silica cell; st, stomatal apparatus. Scale bars = 13 µm (D, E); 45 µm (B, C). Surface view Adaxial surface Long cells tabular with undulate anticlinal walls. Bulliform cells always present. Short cells present over the veins (costal zone) and usually scattered between the veins (intercostal zone); horizontally or vertically orientated. Silica bodies usually saddle-shaped in the woody bamboos; usually crenate (olyroid-type) in the intercostal zone and cross-shaped in the costal zone in herbaceous bamboos. Cork cells usually present, occurring in silico-suberose pairs in the intercostal zone. Papillae often present, often well developed at least on the long cells. Prickles often present, mainly in the costal zone. Microhairs often present, usually unicellular and silicified or bicellular and non-silicified. Macrohairs usually present; unicellular. Stomatal apparatuses often absent (except in Guaduinae); when present with dome-shaped, triangular or parallel-sided subsidiary cells, these usually lacking papillae (except in Chusqueinae and some Olyreae). Abaxial surface Long cells tabular with undulate anticlinal walls. Short cells present over the veins (costal zone) and usually scattered between the veins (intercostal zone); horizontally or vertically orientated. Silica bodies usually saddle-shaped in the woody bamboos; usually crenate (olyroid-type) in the intercostal zone and cross-shaped in the costal zone in herbaceous bamboos. Cork cells usually present, occurring in silico-suberose pairs in the intercostal zone. Papillae often present, often well developed at least on the long cells. Prickles often present, mainly in the costal zone. Microhairs often present, usually unicellular and silicified or bicellular and non-silicified. Macrohairs often present; unicellular. Stomatal apparatuses virtually always present, with dome-shaped, triangular, or parallel-sided subsidiary cells, these usually lacking papillae (except in Chusqueinae and some Olyreae). Cross-section Epidermis with a single layer of cells. Bulliform cells adaxially present, usually organized in fan-shaped arrays between vascular bundles. Mesophyll non-radiate, with usually two layers of arm cells adjacent to the adaxial surface and one layer adjacent to the abaxial surface. Kranz anatomy absent. Fusoid cells often present in the middle of the mesophyll, flanking the vascular bundles. Arm cells present; usually strongly asymmetrically infolded; adaxially of usually larger cells, with prominent, usually abaxial invaginations; abaxially usually of smaller cells, with less prominent and more irregular invaginations. Rosette cells present in the middle of the mesophyll, between the fusoid cells (when present); uniformly weakly infolded around the cell. Vascular bundles with a double sheath, the inner mestome and the outer parenchymatous. Midrib vasculature simple or complex. Sclerenchyma girders present; associated with vascular bundles. Margins usually acute or obtuse; sometimes exhibiting dimorphism. PHYLOGENETIC RELATIONSHIPS IN BAMBUSOIDEAE AND THE USE OF ANATOMICAL AND MICROMORPHOLOGICAL DATA Phylogenetic relationships in Bambusoideae are generally based on plastid or nuclear DNA evidence, in which three major lineages (tribes) are currently recognized and strongly supported as monophyletic (BPG, 2012; Kelchner & BPG, 2013; Saarela et al., 2018) (Fig. 4): (1) Arundinarieae, the temperate woody bamboos; (2) Bambuseae, the tropical woody bamboos; and (3) Olyreae, the herbaceous bamboos. In analyses based on plastid markers or whole plastomes, Bambuseae and Olyreae are strongly supported as sister to each other, with Arundinarieae as sister to that clade (Kelchner & BPG, 2013; Ma et al., 2014; Wysocki et al., 2015; Attigala et al., 2016; Zhang et al., 2016; Saarela et al., 2018). However, analyses based on nuclear data strongly support the monophyly of the woody bamboos (Arundinarieae + Bambuseae), with Olyreae sister to that clade (Triplett et al., 2014; Wysocki et al., 2016). Figure 4. Open in new tabDownload slide Phylogenetic relationships currently recognized in Bambusoideae based on multiple plastid markers (Zhang et al., 2016; Zhou et al., 2017) and whole plastomes (Wysocki et al., 2015; Saarela et al., 2018). Key leaf blade anatomical and micromorphological features are summarized on the phylogenetic tree. 1, well-developed, asymmetrically usually strongly infolded arm cells; 2, epidermis usually with cross-shaped silica bodies in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone; 3, stomatal apparatus bearing two papillae per subsidiary cell; 4, intercostal sclerenchyma; 5, simple, abaxially projecting midrib vasculature; 6, papillae usually abundant and well developed on the adaxial surface; 7, stomata usually well developed on the adaxial surface. NWB = Neotropical woody bamboos; PWB = Palaeotropical woody bamboos. Red circles = synapomorphies; brown circles = potential synapomorphies. Figure 4. Open in new tabDownload slide Phylogenetic relationships currently recognized in Bambusoideae based on multiple plastid markers (Zhang et al., 2016; Zhou et al., 2017) and whole plastomes (Wysocki et al., 2015; Saarela et al., 2018). Key leaf blade anatomical and micromorphological features are summarized on the phylogenetic tree. 1, well-developed, asymmetrically usually strongly infolded arm cells; 2, epidermis usually with cross-shaped silica bodies in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone; 3, stomatal apparatus bearing two papillae per subsidiary cell; 4, intercostal sclerenchyma; 5, simple, abaxially projecting midrib vasculature; 6, papillae usually abundant and well developed on the adaxial surface; 7, stomata usually well developed on the adaxial surface. NWB = Neotropical woody bamboos; PWB = Palaeotropical woody bamboos. Red circles = synapomorphies; brown circles = potential synapomorphies. A summary of the most informative leaf blade anatomical and micromorphological features useful in defining and delimiting each bamboo tribe and its subtribes (when possible) is provided in Table 1 and Figure 4. A list including all the taxa and main references used to build the descriptions in Table 1 is provided in the Supporting Information (S1). Table 1. Leaf blade anatomical and micromorphological features commonly found in Bambusoideae, including tribes and subtribes. Features recognized as synapomorphies or potential synapomorphies are in bold type Taxa . Features commonly found . Main references . Bambusoideae Papillae usually well developed and common on the abaxial surface; usually well developed if present adaxially; stomata usually common on the abaxial surface; mesophyll with non-radiate chlorenchyma cells, of well-developed, arm cells, rosette cells, and often fusoid cells; C3; simple or complex midrib vasculature, often with abaxially projecting midrib. Brandis (1907); Calderón & Soderstrom (1980); Soderstrom (1981); Soderstrom, Ellis & Judziewicz (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a, 2017, 2018). ArundinarieaeTemperate woody bamboos Papillae usually well-developed at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex (often) midrib vasculature, with flat to adaxially or abaxially projecting midrib. Brown (1958); Metcalfe (1960); Jacques-Félix (1962); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); BPG (2012); Wu et al. (2014); Zhang et al. (2014); Nie et al. (2018). BambuseaeTropical woody bamboos Comprising approximately 58% of the total species of bamboos, this is a fairly heterogeneous tribe in terms of anatomical and micromorphological features. Palaeotropical woody bamboos Melocanninae Papillae well developed on both surfaces (at least on some long cells); stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); Yang et al. (2014); Tien et al. (2014); BPG (2012); Clark et al. (2015). Bambusinae + Holttumochloinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and usually a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Palmer & Gerbeth-Jones (1988); Soderstrom & Ellis (1988); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); BPG (2012); Clark et al. (2015). Dinochloiinae + Greslaniinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Clark et al. (2015). Racemobambosinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; Yang et al. (2008); Clark et al. (2015). Hickeliinae Papillae usually well developed at least on the abaxial surface, on some long cells; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma and fibre-like epidermal cells sometimes present; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Temburongiinae Leaf blade anatomy and micromorphology unknown. Neotropical woody bamboos Arthrostylidiinae + Guaduinae Refractive papillae usually present. Ruiz-Sanchez et al. (2008), but further investigation is needed. Arthrostylidiinae Papillae usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomata usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma always present; simple midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Santos-Gonçalves (2005); Gomes & Neves (2009); Viana (2010); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a). Guaduinae Papillae usually abundant and well developed on the adaxial surface and absent to well developed on the abaxial surface; stomata usually well developed on the adaxial surface and abundant on the abaxial surface (except Apoclada); stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and an often complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); BPG (2012); Lizarazu, (2012); Clark et al. (2015); Kellogg (2015); Santana (2017). Chusqueinae Papillae lacking to infrequent or poorly developed on the adaxial surface and usually well developed on the abaxial surface (at least on some long cells); stomata lacking to infrequent or poorly developed on the adaxial surface and usually abundant on the abaxial surface; stomatal apparatus bearing two papillae per subsidiary cell, often overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Clark (1986, 1989); Watson et al. (1992) onwards; Judziewicz et al. (1999); Montti et al. (2008); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Mota (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2017). OlyreaeHerbaceous bamboos Buergersiochloinae Epidermis without cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone; papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with approximately equally protruding midrib. Soderstrom & Ellis (1987); Renvoize (1985); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Parianinae + Olyrinae Epidermis usually with cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone. Calderón & Soderstrom (1967); Soderstrom & Ellis (1987); Judziewicz et al. (1999); BPG (2012); Clark et al. (2015); Kellogg (2015). Parianinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Tateoka (1961); Renvoize (1985); Watson et al. (1992) onwards; Vieira (2002); Oliveira et al. (2008b); Clark et al. (2015). Olyrinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Calderón & Soderstrom (1973); Renvoize (1985); Watson et al. (1992) onwards; Zuloaga et al. (1993); Vieira et al. (2002); Oliveira et al. (2008a); Jesus Junior et al. (2012); Clark et al. (2015); Jaén et al. (2016); Leandro et al. (2016a). Taxa . Features commonly found . Main references . Bambusoideae Papillae usually well developed and common on the abaxial surface; usually well developed if present adaxially; stomata usually common on the abaxial surface; mesophyll with non-radiate chlorenchyma cells, of well-developed, arm cells, rosette cells, and often fusoid cells; C3; simple or complex midrib vasculature, often with abaxially projecting midrib. Brandis (1907); Calderón & Soderstrom (1980); Soderstrom (1981); Soderstrom, Ellis & Judziewicz (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a, 2017, 2018). ArundinarieaeTemperate woody bamboos Papillae usually well-developed at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex (often) midrib vasculature, with flat to adaxially or abaxially projecting midrib. Brown (1958); Metcalfe (1960); Jacques-Félix (1962); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); BPG (2012); Wu et al. (2014); Zhang et al. (2014); Nie et al. (2018). BambuseaeTropical woody bamboos Comprising approximately 58% of the total species of bamboos, this is a fairly heterogeneous tribe in terms of anatomical and micromorphological features. Palaeotropical woody bamboos Melocanninae Papillae well developed on both surfaces (at least on some long cells); stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); Yang et al. (2014); Tien et al. (2014); BPG (2012); Clark et al. (2015). Bambusinae + Holttumochloinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and usually a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Palmer & Gerbeth-Jones (1988); Soderstrom & Ellis (1988); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); BPG (2012); Clark et al. (2015). Dinochloiinae + Greslaniinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Clark et al. (2015). Racemobambosinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; Yang et al. (2008); Clark et al. (2015). Hickeliinae Papillae usually well developed at least on the abaxial surface, on some long cells; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma and fibre-like epidermal cells sometimes present; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Temburongiinae Leaf blade anatomy and micromorphology unknown. Neotropical woody bamboos Arthrostylidiinae + Guaduinae Refractive papillae usually present. Ruiz-Sanchez et al. (2008), but further investigation is needed. Arthrostylidiinae Papillae usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomata usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma always present; simple midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Santos-Gonçalves (2005); Gomes & Neves (2009); Viana (2010); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a). Guaduinae Papillae usually abundant and well developed on the adaxial surface and absent to well developed on the abaxial surface; stomata usually well developed on the adaxial surface and abundant on the abaxial surface (except Apoclada); stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and an often complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); BPG (2012); Lizarazu, (2012); Clark et al. (2015); Kellogg (2015); Santana (2017). Chusqueinae Papillae lacking to infrequent or poorly developed on the adaxial surface and usually well developed on the abaxial surface (at least on some long cells); stomata lacking to infrequent or poorly developed on the adaxial surface and usually abundant on the abaxial surface; stomatal apparatus bearing two papillae per subsidiary cell, often overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Clark (1986, 1989); Watson et al. (1992) onwards; Judziewicz et al. (1999); Montti et al. (2008); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Mota (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2017). OlyreaeHerbaceous bamboos Buergersiochloinae Epidermis without cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone; papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with approximately equally protruding midrib. Soderstrom & Ellis (1987); Renvoize (1985); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Parianinae + Olyrinae Epidermis usually with cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone. Calderón & Soderstrom (1967); Soderstrom & Ellis (1987); Judziewicz et al. (1999); BPG (2012); Clark et al. (2015); Kellogg (2015). Parianinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Tateoka (1961); Renvoize (1985); Watson et al. (1992) onwards; Vieira (2002); Oliveira et al. (2008b); Clark et al. (2015). Olyrinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Calderón & Soderstrom (1973); Renvoize (1985); Watson et al. (1992) onwards; Zuloaga et al. (1993); Vieira et al. (2002); Oliveira et al. (2008a); Jesus Junior et al. (2012); Clark et al. (2015); Jaén et al. (2016); Leandro et al. (2016a). Open in new tab Table 1. Leaf blade anatomical and micromorphological features commonly found in Bambusoideae, including tribes and subtribes. Features recognized as synapomorphies or potential synapomorphies are in bold type Taxa . Features commonly found . Main references . Bambusoideae Papillae usually well developed and common on the abaxial surface; usually well developed if present adaxially; stomata usually common on the abaxial surface; mesophyll with non-radiate chlorenchyma cells, of well-developed, arm cells, rosette cells, and often fusoid cells; C3; simple or complex midrib vasculature, often with abaxially projecting midrib. Brandis (1907); Calderón & Soderstrom (1980); Soderstrom (1981); Soderstrom, Ellis & Judziewicz (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a, 2017, 2018). ArundinarieaeTemperate woody bamboos Papillae usually well-developed at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex (often) midrib vasculature, with flat to adaxially or abaxially projecting midrib. Brown (1958); Metcalfe (1960); Jacques-Félix (1962); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); BPG (2012); Wu et al. (2014); Zhang et al. (2014); Nie et al. (2018). BambuseaeTropical woody bamboos Comprising approximately 58% of the total species of bamboos, this is a fairly heterogeneous tribe in terms of anatomical and micromorphological features. Palaeotropical woody bamboos Melocanninae Papillae well developed on both surfaces (at least on some long cells); stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); Yang et al. (2014); Tien et al. (2014); BPG (2012); Clark et al. (2015). Bambusinae + Holttumochloinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and usually a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Palmer & Gerbeth-Jones (1988); Soderstrom & Ellis (1988); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); BPG (2012); Clark et al. (2015). Dinochloiinae + Greslaniinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Clark et al. (2015). Racemobambosinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; Yang et al. (2008); Clark et al. (2015). Hickeliinae Papillae usually well developed at least on the abaxial surface, on some long cells; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma and fibre-like epidermal cells sometimes present; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Temburongiinae Leaf blade anatomy and micromorphology unknown. Neotropical woody bamboos Arthrostylidiinae + Guaduinae Refractive papillae usually present. Ruiz-Sanchez et al. (2008), but further investigation is needed. Arthrostylidiinae Papillae usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomata usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma always present; simple midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Santos-Gonçalves (2005); Gomes & Neves (2009); Viana (2010); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a). Guaduinae Papillae usually abundant and well developed on the adaxial surface and absent to well developed on the abaxial surface; stomata usually well developed on the adaxial surface and abundant on the abaxial surface (except Apoclada); stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and an often complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); BPG (2012); Lizarazu, (2012); Clark et al. (2015); Kellogg (2015); Santana (2017). Chusqueinae Papillae lacking to infrequent or poorly developed on the adaxial surface and usually well developed on the abaxial surface (at least on some long cells); stomata lacking to infrequent or poorly developed on the adaxial surface and usually abundant on the abaxial surface; stomatal apparatus bearing two papillae per subsidiary cell, often overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Clark (1986, 1989); Watson et al. (1992) onwards; Judziewicz et al. (1999); Montti et al. (2008); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Mota (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2017). OlyreaeHerbaceous bamboos Buergersiochloinae Epidermis without cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone; papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with approximately equally protruding midrib. Soderstrom & Ellis (1987); Renvoize (1985); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Parianinae + Olyrinae Epidermis usually with cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone. Calderón & Soderstrom (1967); Soderstrom & Ellis (1987); Judziewicz et al. (1999); BPG (2012); Clark et al. (2015); Kellogg (2015). Parianinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Tateoka (1961); Renvoize (1985); Watson et al. (1992) onwards; Vieira (2002); Oliveira et al. (2008b); Clark et al. (2015). Olyrinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Calderón & Soderstrom (1973); Renvoize (1985); Watson et al. (1992) onwards; Zuloaga et al. (1993); Vieira et al. (2002); Oliveira et al. (2008a); Jesus Junior et al. (2012); Clark et al. (2015); Jaén et al. (2016); Leandro et al. (2016a). Taxa . Features commonly found . Main references . Bambusoideae Papillae usually well developed and common on the abaxial surface; usually well developed if present adaxially; stomata usually common on the abaxial surface; mesophyll with non-radiate chlorenchyma cells, of well-developed, arm cells, rosette cells, and often fusoid cells; C3; simple or complex midrib vasculature, often with abaxially projecting midrib. Brandis (1907); Calderón & Soderstrom (1980); Soderstrom (1981); Soderstrom, Ellis & Judziewicz (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a, 2017, 2018). ArundinarieaeTemperate woody bamboos Papillae usually well-developed at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex (often) midrib vasculature, with flat to adaxially or abaxially projecting midrib. Brown (1958); Metcalfe (1960); Jacques-Félix (1962); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); BPG (2012); Wu et al. (2014); Zhang et al. (2014); Nie et al. (2018). BambuseaeTropical woody bamboos Comprising approximately 58% of the total species of bamboos, this is a fairly heterogeneous tribe in terms of anatomical and micromorphological features. Palaeotropical woody bamboos Melocanninae Papillae well developed on both surfaces (at least on some long cells); stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); Yang et al. (2014); Tien et al. (2014); BPG (2012); Clark et al. (2015). Bambusinae + Holttumochloinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and usually a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Palmer & Gerbeth-Jones (1988); Soderstrom & Ellis (1988); Watson et al. (1992) onwards; Chen et al. (1993); Yang et al. (2008); BPG (2012); Clark et al. (2015). Dinochloiinae + Greslaniinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with abaxially projecting midrib. Metcalfe (1960); Renvoize (1987); Watson et al. (1992) onwards; Clark et al. (2015). Racemobambosinae Papillae usually well developed at least on the abaxial surface; stomata abundant at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; Yang et al. (2008); Clark et al. (2015). Hickeliinae Papillae usually well developed at least on the abaxial surface, on some long cells; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma and fibre-like epidermal cells sometimes present; and a simple midrib vasculature, with usually adaxially projecting midrib. Renvoize (1987); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Temburongiinae Leaf blade anatomy and micromorphology unknown. Neotropical woody bamboos Arthrostylidiinae + Guaduinae Refractive papillae usually present. Ruiz-Sanchez et al. (2008), but further investigation is needed. Arthrostylidiinae Papillae usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomata usually infrequent or poorly developed on the adaxial surface and often well developed on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma always present; simple midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); Santos-Gonçalves (2005); Gomes & Neves (2009); Viana (2010); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2016a). Guaduinae Papillae usually abundant and well developed on the adaxial surface and absent to well developed on the abaxial surface; stomata usually well developed on the adaxial surface and abundant on the abaxial surface (except Apoclada); stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and an often complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Watson et al. (1992) onwards; Judziewicz et al. (1999); BPG (2012); Lizarazu, (2012); Clark et al. (2015); Kellogg (2015); Santana (2017). Chusqueinae Papillae lacking to infrequent or poorly developed on the adaxial surface and usually well developed on the abaxial surface (at least on some long cells); stomata lacking to infrequent or poorly developed on the adaxial surface and usually abundant on the abaxial surface; stomatal apparatus bearing two papillae per subsidiary cell, often overarched by papillae from adjacent long cells; intercostal sclerenchyma absent; and a complex midrib vasculature, with abaxially projecting midrib. Renvoize (1987); Soderstrom & Ellis (1987); Clark (1986, 1989); Watson et al. (1992) onwards; Judziewicz et al. (1999); Montti et al. (2008); BPG (2012); Lizarazu (2012); Guerreiro et al. (2013); Mota (2013); Clark et al. (2015); Kellogg (2015); Leandro et al. (2017). OlyreaeHerbaceous bamboos Buergersiochloinae Epidermis without cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone; papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple midrib vasculature, with approximately equally protruding midrib. Soderstrom & Ellis (1987); Renvoize (1985); Watson et al. (1992) onwards; BPG (2012); Clark et al. (2015). Parianinae + Olyrinae Epidermis usually with cross-shaped silica cells in the costal zone and crenate (olyroid-type) silica bodies in the intercostal zone. Calderón & Soderstrom (1967); Soderstrom & Ellis (1987); Judziewicz et al. (1999); BPG (2012); Clark et al. (2015); Kellogg (2015). Parianinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Tateoka (1961); Renvoize (1985); Watson et al. (1992) onwards; Vieira (2002); Oliveira et al. (2008b); Clark et al. (2015). Olyrinae Papillae occurring at least on the abaxial surface; stomata common at least on the abaxial surface; stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells; and a simple or complex midrib vasculature, with usually adaxially projecting midrib. Metcalfe (1960); Calderón & Soderstrom (1973); Renvoize (1985); Watson et al. (1992) onwards; Zuloaga et al. (1993); Vieira et al. (2002); Oliveira et al. (2008a); Jesus Junior et al. (2012); Clark et al. (2015); Jaén et al. (2016); Leandro et al. (2016a). Open in new tab Tribe Arundinarieae: temperate woody bamboos Arundinarieae currently comprise 12 lineages (I–XII), with still unclear relationships and no formally recognized subtribes (Clark et al., 2015; Attigala et al., 2016) (Fig. 4). Basipetal branch development is the prominent morphological feature of this group (BPG, 2012; Clark et al., 2015); however, no defining leaf blade anatomical or micromorphological features for the tribe have been identified to date. Although the presence of papillae has been recognized as a characteristic feature of bamboo leaves (Judziewicz et al., 1999), their arrangement on the leaf blade epidermis and association with the stomatal apparatus have proved to be consistent in delimiting closely related groups of species in Arundinarieae, such as those included in the polyphyletic Gelidocalamus T.H.Wen (Wu et al., 2014; Nie et al., 2018) and Chimonobambusa Makino (Chen et al., 1993b) and Phyllostachys Siebold & Zucc. (Chen et al., 1986, 1993a). Studying the leaf blade micromorphology of 94 species in 24 genera of Arundinarieae, Zhang et al. (2014) reported seven types (I–VII) of papilla arrangements surrounding the stomatal apparatus, with the caveat that such recognized types have little taxonomic value but may be useful when combined with other epidermal features (e.g. type of trichomes and morphology of silica bodies). In their work, the authors also included a mini-review of the occurrence of each type within the tribe, with types III (four to eight non-overarched, elongated or short papillae surrounding the stomatal apparatus) and IV (four to ten overarched, elongated papillae surrounding the stomatal apparatus) being the most common ones found, but further investigation in a phylogenetic framework is needed. In addition, the leaf blade micromorphological data of 11 genera and 49 species of Arundinarieae were also examined by Chen et al. (1993a), but the taxonomic significance of features was not discussed by the authors. Leaf blade anatomy in this tribe is poorly known, although abundant stomata and papillae at least on the abaxial surface and a usually complex midrib vasculature have been reported in this group (Soderstrom & Ellis, 1987) (Table 1). Studying 16 arundinarioid species in eight genera, Soderstrom & Ellis (1982) concluded that there were no diagnostic features for each studied genus or species due to the homogeneity of leaf blade anatomy and micromorphology in this group. The authors pointed out, however, that the presence of large microhairs and dumbbell-shaped silica bodies would be useful for recognizing the genus Thamnocalamus Munro and its allies. Tribe Bambuseae: tropical woody bamboos In Bambuseae, two major lineages are recognized based on molecular evidence (Sungkaew et al., 2009; Kelchner & BPG, 2013; Wysocki et al., 2015; Saarela et al., 2018) (Fig. 4): (1) the Palaeotropical woody bamboos (PWB) and (2) the Neotropical woody bamboos (NWB). Acropetal branch development is the notable shared morphological feature of Bambuseae, although there is some variation (Clark et al., 2015); however, no defining leaf blade anatomical or micromorphological feature has been identified for the whole tribe. Nonetheless, some features have proved to be useful at some taxonomic levels in the NWB (Table 1; Fig. 4). Palaeotropical woody bamboos The PWB currently comprise the early-diverging lineage Melocanninae, plus two clades (Holttumochloinae + Bambusinae) and (Dinochloiinae + Greslaniinae) (the latter formerly the DGMNS assemblage) forming a polytomy with Racemobambosinae, Hickeliinae and Temburongiinae (Zhou et al., 2017) (Fig. 4). In terms of leaf blade anatomy and micromorphology, the PWB are fairly heterogeneous (Table 1), in general characterized by: the presence of a complex or simple midrib vasculature (sometimes both present in Bambusinae); an S-shaped or asymmetrical keel; absence of intercostal sclerenchyma (sometimes present in Hickeliinae); stomata on the adaxial surface usually absent or poorly developed to abundant; papillae on the adaxial surface usually present, but sometimes absent or poorly developed; stomata on the abaxial surface usually abundant; papillae on the abaxial surface often well developed at least on some long cells; and the stomatal apparatus with papillae absent from the subsidiary cells but usually overarched by papillae from adjacent long cells. Although these anatomical and micromorphological descriptors may be useful in recognizing members of the PWB, they are mostly not exclusive features for this group (or Bambusoideae), and thus a combined morphological analysis would assist in their correct identification. Studying 35 PWB species in 11 genera, Yang, Wang & Li (2008) concluded that the shape and arrangement of papillae surrounding the stomatal apparatus on the abaxial surface of the leaf blade have great value for systematics at specific and generic levels, although these features were not useful for delimiting subtribes in the PWB. Based on the most recent phylogenetic analysis by Zhou et al. (2017), further anatomical and micromorphological studies should be carried out to assist in the resolution of the polytomies in the PWB. Neotropical woody bamboos The NWB comprise the Arthrostylidiinae + Guaduinae lineage with Chusqueinae sister to it, with good support (Ruiz-Sanchez, 2011; Tyrrell et al., 2012; Kelchner & BPG, 2013; Wysocki et al., 2015; Saarela et al., 2018) (Fig. 4). Leaf blade anatomy and micromorphology of the NWB have been intensively studied, but no defining features have been recognized for the whole group to date. Sister to each other, Arthrostylidiinae and Guaduinae are each well supported based on morphological and molecular evidence (Ruiz-Sanchez, Sosa & Mejía-Saules, 2008, 2011; Fisher et al., 2009; Sungkaew et al., 2009; Ruiz-Sanchez, 2011; Tyrrell et al., 2012; Kelchner & BPG, 2013). The presence of refractive papillae on the leaf epidermis has been considered a putative diagnostic feature supporting the sister relationship of these subtribes (Kelchner & Clark, 1997; Guala et al., 2000; Ruiz-Sanchez et al., 2008; Sungkaew et al., 2009; Zhang & Clark, 2000) (Table 1) [Note the comment in the following main section regarding refractive papillae.] Intercostal sclerenchyma, often referred to as ‘intercostal fibres’, has been reported as a diagnostic feature of Arthrostylidiinae (Soderstrom & Ellis, 1987) and, more recently, assumed to be taxonomically consistent in defining and delimiting this subtribe (Tyrrell et al., 2012; Clark et al., 2015; Leandro et al., 2016). The presence of intercostal sclerenchyma in Arthrostylidiinae appears to be an anatomical synapomorphy for this subtribe, although this needs to be formally tested in a phylogenetic framework. The unique combination of intercostal sclerenchyma plus a simple midrib vasculature has been useful in defining and delimiting Arthrostylidiinae (Soderstrom & Ellis, 1987; Clark et al., 2015; Kellogg, 2015; Leandro et al., 2016) (Table 1; Fig. 4). Although sharing refractive papillae with Arthrostylidiinae, Guaduinae may be distinguished from arthrostylidioid bamboos by the presence of a complex midrib vasculature, the adaxial surface usually with abundant stomata and well-developed papillae (rarely lacking or poorly developed) and the absence of intercostal sclerenchyma (Judziewicz et al., 1999; Clark et al., 2015; Kellogg, 2015) (Table 1; Fig. 4). The abundance of stomata on both surfaces (except in Apoclada McClure) and papillae (sometimes absent on the abaxial surface), although helpful in recognizing the subtribe, are generally not informative at the species level with some exceptions (e.g. Lizarazu, 2012); the use of a combination of anatomical and micromorphological features for delimiting species is therefore recommended. With regard to midrib vasculature, to the best of our knowledge, the occurrence of a simple midrib in this subtribe has been reported only in Guadua paniculata Munro (Santana, 2017). A stomatal apparatus bearing two papillae per subsidiary cell has been proposed as a synapormophy for Chusqueinae, which includes the single, well-supported genus Chusquea Kunth (Fisher et al., 2009; Fisher, Clark & Kelchner, 2014; Kelchner & BPG, 2013). The presence of two papillae is also known in a few herbaceous bamboos (Calderón & Soderstrom, 1973; Judziewicz et al., 1999), these sometimes bearing more than two papillae per subsidiary cell. Regardless of their occurrence in Olyreae, a pair of papillae on each subsidiary cell is regarded as highly informative in defining and delimiting Chusquea spp., and the morphology of these papillae can be useful in delimiting its species (Clark et al., 2015; Kellogg, 2015; Leandro et al., 2016, 2017) (Table 1; Fig. 4). Tribe Olyreae: herbaceous bamboos The herbaceous bamboo tribe Olyreae comprise Buergersiochloinae as sister to the Parianinae + Olyrinae clade (Kelchner & BPG, 2013; Oliveira et al., 2014; Saarela et al., 2018) (Fig. 4). An epidermis usually with cross-shaped silica bodies in the costal zone and crenate silica bodies in the intercostal zone (more evident on the adaxial surface) is the prominent leaf blade micromorphological feature of Parianinae + Olyrinae (Clark et al., 2015) (Table 1; Fig. 4); these are absent in Buergersiochloinae, comprising the single genus Buergersiochloa Pilg. Crenate silica bodies are also referred to as olyroid silica bodies (Tateoka, 1961). Most species of Olyreae exhibit an adaxiallly projecting midrib (e.g. Oliveira et al., 2008a; Jesus Junior et al., 2012), which is an unusual feature in bamboos and Poaceae in general (Soderstrom & Ellis, 1987). Although the olyroid-type silica body has been helpful in supporting the monophyly of Parianinae + Olyrinae, data on leaf blade anatomy and micromorphology of herbaceous bamboos are still needed, even though a better sampling in the tribe is currently in progress (J. F. Lima, pers. comm.). Revisiting and clarifying the use of some bamboo leaf blade features Historically, bamboo leaf blade anatomical and micromorphological data have been shown to be highly informative in defining major groups but many of these also show significant variation and some features are not well defined or understood, thus indicating research priorities in Bambusoideae. Since the first and only broad review on this subject for grasses (Ellis, 1987), many new structural concepts as well as evidence for environmental influence on these features were introduced to grass anatomy and micromorphology. Therefore, some terminology needs to be introduced or standardized in descriptions, but the use of some leaf blade features in bamboo systematics and phylogeny needs to be re-evaluated. In this section, some anatomical and micromorphological features are structurally defined and discussed with reference to their character states, occurrence and usefulness in delimiting bamboo taxa. Some general comments for the grass family and an illustration of each character state currently known to be useful for anatomical studies are provided (Figs 1, 2, 3); these are merely illustrative and not necessarily related to a specific taxon. Illustrations included here were obtained from several bamboo species, including living and dried plants, with the aid of light microscopy (LM) and scanning electron microscopy (SEM). For LM, living or dried mature branch leaves were taken and sampled (0.5 cm2) from the middle portion of the leaf blade. For living samples, each piece was fixed in FAA50 for 48 h (Johansen, 1940), and then stored in 70% ethanol. Living and dried samples were embedded in polyethylene glycol 1.500 solution and kept in an incubator at 60 °C for 15 days (adapted from Richter, 1985), dried, sectioned using a Leica RM 2145 rotary microtome, and stained with Astra Blue and Safranin (Roeser, 1972); semi-permanent slides were then mounted in glycerin and distilled water (1:1). For SEM, pieces (0.5 cm2) of the middle portion of dried, mature branch leaves were sampled and attached to a cylindrical sample holder (stub) and coated with a thin sample of gold (Denton vacuum Desk III). Some samples were submerged in xylene for ~10 min to eliminate epicuticular wax in order to provide a better view of micromorphological features (Dávila & Clark, 1990). Observation were made and images were obtained with the aid of a Leica DM4000B microscope through the Leica Application Suite LASV4.0 (LM), and JEOL JSM-5800LV (SEM). Observations were made in the Departamento de Botânica at the Universidade Estadual Paulista – UNESP, Rio Claro, Brazil, and in the Roy J. Carver High Resolution Microscopy Facility (HRMF) at Iowa State University, USA. Herbarium acronyms are in accordance with Thiers (2019, continuously updated). Plicate mesophyll parenchyma: arm and rosette cells Arm cells are thin-walled, photosynthetic mesophyll cells that exhibit cell wall invaginations (lobes) extending to different depths from one or both sides of the leaf blade as seen in cross-section (Figs 1, 2A). Complementary images may be found in Judziewicz et al. (1999), Montti, Graciano-Ribeiro & Goldstein (2008), Viana (2010), Viana et al. (2011), Jesus Junior et al. (2012), Lizarazu (2012), Mota (2013) and Leandro et al. (2016, 2017). Arm cells were originally reported in bamboos and species currently regarded as early-diverging grasses (e.g. Metcalfe, 1956, 1960; Ellis, 1987; Soderstrom & Ellis, 1987), but today the occurrence of strongly invaginated arm cells has been recognized as a synapomorphy for Bambusoideae, with weakly invaginated arm cells being characteristic of the early-diverging grasses (Judziewicz et al., 1999; GPWG, 2001; BPG, 2012; Clark et al., 2015; Kellogg, 2015). Arm cells occur closely appressed and vertically orientated, forming layers above and below the cavities resulting from the collapse of fusoid cells (when present), and adjacent to the epidermis (Figs 1, 2A). One or two (rarely more) layers of arm cells with vertically orientated lobes may occur below the adaxial surface, usually just one layer in Olyreae (Zuloaga, Morrone & Judziewicz, 1993) and some of the temperate woody bamboos (Arundinarieae) (L. G. Clark, pers. obs.). As noted above, well-developed, asymmetrically strongly arm-like lobes from both sides or just from the abaxial side of the leaf blade are commonly found in bamboo leaves (Figs 1, 2A). Weakly lobed arm cells have been reported in a few Bambusoideae (Bambuseae and Olyreae), which have apparently reverted to this putatively ancestral state (Zhang, 1996). The type of lobed arm cells, along with the number of layers directly below the adaxial surface, may be taxonomically informative in delimiting species (e.g. Leandro et al., 2017) and thus should be incorporated in anatomical descriptions. Rosette cells are thin-walled photosynthetic mesophyll cells that exhibit weak cell-wall invaginations (lobes) around the entire cell as seen in cross-section (Fig. 1). Complementary images may be found in Viana (2010), Viana et al. (2011), Lizarazu (2012), Mota (2013) and Leandro et al. (2016, 2017). Formerly treated as arm cells, rosette cells are as closely appressed as arm cells, but are distinguished by having their lobes around the entire cell and thus as a whole are more or less symmetric. Evidence also suggests that rosette cells are typically elongated proximo-distally, whereas arm cells are not (T. J. Gallaher, pers. comm.). Although the presence of rosette cells has been proposed as a putative synapomorphy for the bistigmatic clade (Puelioideae + (BOP + PACMAD)), these cells occur mainly in Oryzoideae and Bambusoideae, and their presence in a few Pooideae and in the PACMAD clade may be the result of ancestral retention or independent evolution (L. G. Clark, pers. obs.). Rosette cells often vary in number and extent of development in the same species and even across the leaf blade and thus are useless for taxonomic purposes. Their occurrence in bamboos and other grasses, however, should be incorporated in anatomical descriptions. Fusoid cells These are thin-walled, apparently non-photosynthetic mesophyll cells that often collapse as a result of their development (Figs 1, 2A, C). Complementary images may be found in Yang et al. (2014), Vega, Castro & Guerreiro (2016), Wang et al. (2016) and Leandro et al. (2018). Fusoid cells have been reported in the three early-diverging lineages, unevenly in the BOP clade (virtually all Bambusoideae, some Oryzoideae and Pooideae) and in a few Panicoideae (for more details see Leandro et al., 2018, and references therein). They are recognized as plesiomorphic for the grass family (GPWG, 2001). A recent developmental study has shown that, in mature leaves, fusoid cells are observed only in longitudinal and paradermal sections (Fig. 2C), as cross-sections actually show intercellular cavities resulting from the collapse of one or more fusoid cells (Leandro et al., 2018) (Figs 1, 2C, D). Each cavity is delimited by successive collapsed (rarely not collapsed) fusoid cells arranged perpendicularly to the proximo-distal axis of the leaf blade (Vega et al., 2016; Leandro et al., 2018) (Fig. 2C). The presence or absence of intercellular cavities, and thus of fusoid cells, was traditionally considered useful in delimiting species in Bambusoideae (e.g. Metcalfe, 1960; Soderstrom & Ellis, 1982; Watson, Clifford & Dallwitz, 1985; Clayton & Renvoize, 1986; Guala, 1995; Santos-Gonçalves, 2005; Oliveira & Longhi-Wagner, 2007: in all these works ‘cavities’ were referred to as ‘fusoid cells’). It is also not uncommon to find studies using the shape of the cavities for delimiting bamboo species (e.g. Soderstrom & Ellis, 1987; Oliveira et al., 2008a, b). Many studies have suggested, however, that the development (or not) of fusoid cells and the shape of the cavities are environmentally influenced (Metcalfe, 1956; Wu, 1962; Pearson, Pearson & Gomez, 1994; March & Clark, 2011; Yang et al., 2014; Leandro et al., 2018), and thus this feature is not useful as an anatomical descriptor in distinguishing bamboos or any other species of grass. As a final remark on this subject, we emphasize that the presence of fusoid cells, although not taxonomically informative, is relevant in establishing subfamilial phylogenetic relationships in Poaceae. Therefore, it is necessary to report on their occurrence in anatomical studies. Intercostal sclerenchyma This refers to sclerenchymatous cells occurring in the intercostal zone adjacent to the adaxial and/or abaxial surface, associated with bulliform cells or opposite to them (Fig. 2B). Complementary images may be found in Silva-Filho (2006), Viana (2010), Viana et al. (2011) and Leandro et al. (2016). As previously mentioned, intercostal sclerenchyma has been traditionally referred to as ‘intercostal fibres’ and recognized as a diagnostic feature of Arthrostylidiinae (Soderstrom & Ellis, 1987) but also present in Hickeliinae (Bambuseae, PWB). Because there is no work addressing the development of intercostal sclerenchymatous cells, we emphasize that these cells are only assumed to be fibres. In this sense, we consider ‘intercostal sclerenchyma’ to be the appropriate term and strongly suggest its adoption in anatomical descriptions, at least until their development can be elucidated. The occurrence of intercostal sclerenchyma near and/or opposite to the adaxial bulliform cells has been shown to be taxonomically informative (e.g. Clark & Londoño, 1991; Viana, 2010), and thus a description of the topography of these cells in the mesophyll should be addressed in anatomical studies. A broader anatomical sampling of Arthrostylidiinae and a formal character optimization of the presence of intercostal sclerenchyma using a comprehensive phylogenetic tree for the tribe are needed to determine the value of this feature. Midrib vasculature This refers to the number of vascular bundles comprising the midrib (Fig. 1). Complementary images may be found in Viana (2010), Viana et al. (2011), Jesus Junior et al. (2012), Lizarazu (2012), Mota (2013), Viana, Filgueiras & Clark (2013a), Viana, Filgueiras & Graciano-Ribeiro (2013b) and Leandro et al. (2016, 2017). Most grass species exhibit an abaxially projecting midrib usually consisting of several vascular bundles equidistantly arranged forming an arc (keel) (Metcalfe, 1960; Soderstrom & Ellis, 1987). Although there are variations in the pattern of distribution of the vascular bundles (for more details see Metcalfe, 1960), the number comprising the midrib may be taxonomically informative. The midrib vasculature can be classified into two types: (1) simple, comprising only one central vascular bundle; and (2) complex, comprising two or more vascular bundles, with one central and additional ones forming an arc or superposing the central one. Many woody and a few herbaceous bamboos exhibit a complex midrib, even though a simple midrib vasculature is the expected condition in herbaceous species (Judziewicz et al., 1999). As previously mentioned, a simple midrib vasculature has been reported in Arthrostylidiinae, with this feature being useful in delimiting and distinguishing this subtribe from Chusqueinae and Guaduinae, because these two usually exhibit a complex midrib vasculature. In Chusqueinae, the complex midrib vasculature can be of three arrangements (Clark, 1986; Mota, 2013; Leandro et al., 2017): (1) comprising two opposing vascular bundles, with several adjacent ones, each with its own bundle sheath; (2) comprising two superposed vascular bundles sharing the same bundle sheath; and (3) comprising three vascular bundles, two smaller ones opposing the major one, all three sharing the same bundle sheath. Although all three are classified as complex midribs, those differences have been shown to be informative in distinguishing Chusquea spp. (Mota, 2013; Leandro et al., 2017). Midrib vasculature appears to be taxonomically relevant for Bambusoideae as a whole, and thus we strongly recommend its inclusion in anatomical descriptions. Refractive papillae These are, in general, tiny outgrowths developed on leaf blade epidermal cells, and they typically appear to ‘glow’ under SEM. Complementary images may be found in Santos-Gonçalves (2005), Viana (2010), Viana et al. (2011, 2013a, b) and Leandro et al. (2016). The occurrence of papillae in grass species is fairly variable, but is characteristic of bamboo leaves (Judziewicz et al., 1999). As previously mentioned, the presence of refractive papillae supports the sister relationship between Arthrostylidiinae and Guaduinae, although they may be also be observed in some species of Melocanninae (L. G. Clark, pers. obs.). The term ‘refractive papillae’ was originally assigned by Soderstrom & Ellis (1987) with no reference to a structural definition for this putative type of papilla. Although a refractive papilla is apparently smaller than a regular papilla, further comparative developmental and experimental studies are needed to verify their putative differences and the value of refractive papillae in defining the Arthrostylidiinae + Guaduinae (or other) clade in Bambuseae. Stomatal apparatus bearing papillae on the subsidiary cells These are illustrated in Figure 3(D, E). Complementary images may be found in Clark (1986), Judziewicz et al. (1999), Yang et al. (2008), Lizarazu (2012), Guerreiro et al. (2013), Mota (2013), Tien, Nghia & Xia (2014), Zhang et al. (2014) and Leandro et al. (2016, 2017). As previously mentioned, a stomatal apparatus bearing two papillae per subsidiary cell is regarded a synapomorphy for the NWB genus Chusquea (Fisher et al., 2009, 2014) and has proved to be highly informative in defining and delimiting species in the genus (e.g. Lizarazu, 2012; Leandro et al., 2016). The presence of two (or more) papillae on each subsidiary cell has been also reported in a few herbaceous bamboos (Calderón & Soderstrom, 1973; Zuloaga et al., 1993; Judziewicz et al., 1999; J. F. Lima, pers. obs.), and it is noteworthy that, in the BOP clade, some species of Oryza L. (Oryzoideae) also exhibit this feature (Prasad et al., 2011; T. D. Leandro, pers. obs.). In Chusquea (Chusqueinae), papillae from subsidiary cells can be simple or branched. Characterization of the type of papillae is sufficiently distinctive to be used for diagnostic and taxonomic purposes (e.g. Lizarazu, 2012; Guerreiro et al., 2013; Leandro et al., 2017), and thus we strongly recommend its inclusion in micromorphological descriptions. The shape of subsidiary cells, often dome-shaped or low-triangular-shaped in bamboos (Judziewicz et al., 1999), is another relevant feature that should be described because it may also assist in the delimitation of species (e.g. Leandro et al., 2016, 2017). Silica cells In grass leaves, these are short epidermal cells that incorporate silica into their lumen, forming a silica body and often occurring in association with cork cells forming silico-suberose pairs. Silica bodies are known as phytoliths when isolated from the plant tissue (Fig. 3A, B). Complementary images may be found in Jesus Junior et al. (2012), Mota (2013), Baldini & Ortiz (2015) and Leandro et al. (2016, 2017). Short cells developing silica bodies are characteristic of grass leaves (GPWG, 2001; Kellogg, 2015). Silica bodies exhibit a large number of shapes and they may be horizontally or vertically orientated on the leaf epidermis (for more details, see Metcalfe, 1960; Ellis, 1979; Piperno & Pearsall, 1998). Silica bodies are reported as horizontally elongated and saddle-, rondel-, bilobate- or cross-shaped in most of the grasses (Metcalfe, 1960; Ellis, 1979; Piperno & Pearsall, 1998; Stevens, 2001 onwards), but a distinctive crenate shape (olyroid-type) can be observed in Olyreae, and saddle-shaped silica bodies can be observed in Guaduinae and Chusqueinae (Piperno & Pearsall, 1998; Leandro et al., 2017). It is likely that Bambusoideae are one of the most diverse subfamilies in terms of morphology of silica bodies, which, in turn, usually contribute to diagnosing tribes, subtribes and genera in the subfamily (Piperno & Pearsall, 1998; Clark et al., 2015). It appears that attributes such as shape and orientation of silica bodies are not greatly environmentally influenced, but rather are genetically controlled (Prychid, Rudall & Gregory, 2003) and thus may be useful for delimiting bamboo species (e.g. Leandro et al., 2017). Besides the systematic value of silica bodies, information about their morphology has proven to be highly informative in establishing estimates of divergence times for lineages in the grass family (e.g. Prasad et al., 2005, 2011; Wu, You & Li, 2018), reinforcing the need for a careful analysis and description of silica bodies in anatomical and micromorphological studies. Trichomes In general, a trichome is an outgrowth developed from leaf blade epidermal cells (Fig. 3B–E). Complementary images may be found in Judziewicz et al. (1999), Vieira et al. (2002), Montiel, Jiménez & Guevara (2006a), Montiel, Guevara & Jiménez (2006b), Gomes & Neves (2009), Viana (2011), Lizarazu (2012), Jesus Junior et al. (2012), Guerreiro et al. (2013), Mota (2013), Leandro et al. (2016, 2017) and Zhang et al. (2017). In grasses, trichomes can be of three main types (Ellis, 1979): (1) large, unicellular trichomes, usually termed macrohairs (Fig. 3C); (2) microhairs, usually termed bicellular trichomes (Fig. 3E), although one- or three-celled structures may occur (D. Graciano-Ribeiro, pers. comm.); and (3) pointed, often thick-walled and silicified structures, with swollen bases arising directly from the epidermis (including hooks), termed prickles (Fig. 3D). All three types of trichomes often occur at the same time on bamboo leaf blades, but some variations may be observed among closely related species (see previous references cited). Although traditionally used for delimiting grass species, and some distinctive patterns actually may be observed in some groups (e.g. Chloridoideae: Peterson, Romaschenko & Johnson, 2010; Ingram et al., 2010), the use of macrohairs, microhairs and prickles in defining and delimiting groups or species should be evaluated taking into account any possible intraspecific variation, which could easily modify the description of the occurrence and distribution of trichomes, and also stomata and papillae, on both leaf surfaces. CONCLUSIONS This review describes the anatomical and micromorphological features diagnostic in defining and delimiting taxa: (1) well-developed, asymmetrically strongly infolded mesophyll cells (arm cells) as seen in cross-section are regarded a synapomorphy for Bambusoideae; (2) intercostal sclerenchyma has been recognized in defining Arthrostylidiinae; (3) a stomatal apparatus bearing two papillae per subsidiary cell is regarded a synapomorphy for Chusqueinae; (4) refractive papillae have been recognized as a putative feature supporting the sister relationship of Arthrostylidiinae + Guaduinae, in the NWB; and (5) crenate (olyroid-type) silica bodies define the Olyrinae + Parianinae clade, in the herbaceous bamboos. A unique combination of features has been considered useful in defining two subtribes in the NWB: (1) Arthrostylidiinae based on the presence of intercostal sclerenchyma and a simple midrib vasculature, whereas (2) Guaduinae is defined by the presence of a complex midrib vasculature, the adaxial surface usually with abundant stomata and well-developed papillae, and the absence of intercostal sclerenchyma. Although exhibiting a phylogenetic signal at the family level, fusoid cells (or the cavities resulting from their collapse) should not be used for taxonomic purposes given the increasing evidence of environmental influences on their development. Moreover, the occurrence and abundance of papillae stomata, and trichomes are also likely to be environmentally influenced, and thus addressing intraspecific variation is mandatory in comparative grass anatomical and micromorphological studies. Further developmental studies are needed to clarify putative differences between common papillae and refractive papillae, as well as the type of cell originating from the differentiation of intercostal sclerenchyma. Here, we propose the use of ‘intercostal sclerenchyma’ when referring to ‘intercostal fibres’. The morphology and orientation of silica bodies in the leaf blade have been shown to be helpful in delimiting species, but also in defining relationships in Bambusoideae. Furthermore, the utility of phytoliths in establishing estimates of divergence times in Poaceae increases the importance of describing this feature properly. The temperate woody bamboos (Arundinarieae) and the PWB (Bambuseae) are the main research priorities in terms of anatomical and micromorphological studies in Bambusoideae. Seeking these data could assist in establishing well-supported relationships among the lineages of Arundinarieae (I–XII) and in the resolution of polytomies in the PWB. However, many NWB (Bambuseae) remain to be characterized anatomically or micromorphologically, and little is known about general evolutionary patterns of anatomical or micromorphological characters in this clade or the three tribes of Bambusoideae. As a final remark, many studies employing leaf blade anatomical and micromorphological descriptions have been published in the last few decades. Although most of them were performed by anatomists, some were carried out by taxonomists or physiologists, or even anatomists who did not have grass anatomy as their primary research focus. Taxonomists usually carefully describe structures as seen in cross-section and surface view, providing good sources of information in defining and delimiting taxa (e.g. Oliveira et al., 2008a; Guglieri, Longhi-Wagner & Zuloaga, 2008; Pelegrin, Longhi-Wagner & Oliveira, 2009; Viana, 2011; Mota, 2013). Physiologists, although not focused on descriptions, also provide useful information; functional anatomy, for example, has revealed patterns of mesophyll cell shape and arrangement in rice (Oryzoideae) (Sage & Sage, 2009). Advances in phylogenetics and microscopy methods place anatomists, taxonomists and physiologists in an unprecedented position to dissect and understand grass relationships and the functional importance of anatomical and micromorphological adaptive strategies. Such studies have become increasingly common, but a terminological standardization is probably the largest challenge in grass anatomy and micromorphology. For descriptive purposes, we strongly recommend use of the studies by Ellis (1976, 1979), which provide a procedure for standardizing descriptions of leaf blade as seen in cross-section and surface view. ACKNOWLEDGEMENTS This research was completed as a partial fulfilment for the first author’s scholarship funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (PDSE grant number 99999.003340/2015-05) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (GD grant number 163550/2012-3). V.L.S. was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (grant number 302397/2016-7). SEM was supported by National Science Foundation grants DEB-1120750 and DEB-1342787 to L.G.C. The first author is especially indebted to Maurício Miguel Fragali Pane for his invaluable support and encouragement. The authors are grateful to Dr Harry T. Horner and Tracey Stewart for their assistance and for access to the Roy J. Carver High Resolution Microscopy Facility (HRMF) at Iowa State University. References Attigala , LR , Wysocki WP , Duvall MR , Clark LG . 2016 . 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TI - Comparative leaf blade anatomy and micromorphology in the systematics and phylogeny of Bambusoideae (Poaceae: Poales)
JF - Botanical Journal of the Linnean Society
DO - 10.1093/botlinnean/boz074
DA - 2020-01-01
UR - https://www.deepdyve.com/lp/oxford-university-press/comparative-leaf-blade-anatomy-and-micromorphology-in-the-systematics-4Zw40KyBjH
SP - 165
VL - 192
IS - 1
DP - DeepDyve
ER -