Systematics with 1 Special Reference to Molecular of

Swapnendu Pattanaik

1. Bamboo Systematics – A Historical Perspective have always been a taxonomically challenging group of because while the classification of flowering plants depends largely on the characteristics of reproductive organs, flowering is rare in many bamboo . Some bamboo species flower at intervals as long as 120 years and for some there is no report of flowering to date. The first classification of bamboos was attempted by Carl Sigismund Kunth (Kunth, 1815) who made the bamboos (Graminae Bambusaceae) one of 10 groups in his natural system of classification of grasses, thus, conceptualizing what is today subfamily Bambusoideae. Further progress in the classification of the Bambusoideae was provided by Christian Gottfried Daniel Nees von Esenbeck (Nees von Esenbeck, 1835) in his treatment of Brazilian bamboos, when he recognized two woody ( and Arundinariae) and one herbaceous (Streptochaeteae) group. This was soon followed by the first worldwide treatment of bamboos 'Bambuseas Monographic' by Frank Joseph Ruprecht (Ruprecht, 1839), describing 9 genera and 67 species. Thirty years later Munro (1868) more than doubled this coverage, describing over 170 species in 20 genera, in what remains one of the most useful references on bamboos (Soderstrom, 1985). Munro's system was based on the foundation that Nees had laid down earlier but expanded to include many more taxa. Later Bentham (1883) modified Munro's scheme and in the account of Gramineae prepared for 'Genera Plantarum' included four sub-tribes under Bambusoideae: Sub-tribe 1- (, Phyllostachys, ); Sub-tribe 2- Eubambuseae (, , , , , ); Sub-tribe 3- Dendrocalameae (Dendrocalamus, , , Teinostachyum, ); Sub-tribe 4- (, , , ). The end of the 19th century saw appearance of another 2 Swapnendu Pattanaik

significant monograph 'Bambuseae: The bamboos of British ' by James Sykes Gamble in 1896. Gamble adopted Bentham's scheme, covered 15 genera and 115 species mostly from India, , and Malaysia. By the beginning of the 20th century, the study of bamboos had progressed further. Notable works in the first half of the century included Rendle's (1904) treatment of 44 bamboos from , publication of Les Bambusees by Edmond Camus (1913) and a treatment of the bamboos of by Bor (1938). Treatments had followed Bentham's scheme until Aimee Camus (1935) proposed a new scheme in which all genera having staminal filaments united to form a tube were placed in a separate sub- tribe. Subsequently, however, Holttum (1956) disputing the schemes of both Bentham (1883) and Camus (1935), offered a new classification based on the structure of the ovary. Holttum's scheme suggested a close relationship between Bambusa and Dendrocalamus on the basis of ovary features and he placed both in an informal 'sub- tribe' - Bambusa-Dendrocalamus type. In all, Holttum's system of classification included four sub-tribes A. Schizostachyum type (Melocanna, Ochlandra, Schizostachyum), B. Oxytenanthera type (Oxytenanthera), C. Bambusa- Dendrocalamus type (Melocalamus, Dinochloa, Thyrsostachys, Bambusa, Guadua, Dendrocalamus, Gigantochloa, Racemobambos), and D. Arundinaria type (Arundinaria). The woody bamboos have always been the basis of the concept of the bamboo group even though Nees had envisaged herbaceous bamboos in his scheme of Bambusoideae. Indeed, herbaceous bamboos were neglected in the schemes of Munro (1868), Bentham (1883), Gamble (1896), Camus (1913) and even the relatively modern scheme of McClure (1961). In that year, however, a paper was published by Prof. Lorenzo R. Parodi (1961) which brought into focus the bambusoid affinities of certain gramineous genera. Parodi defined Bambusoideae in a system of classification for the grasses of Argentina in which all woody bamboos were included in a single tribe (Bambuseae), but three further tribes were established for herbaceous members: , Phareae, Streptochaeteae. As botanists began to look at plants more closely, from the evolutionary perspective, the significance of the herbaceous bamboos began to emerge and later authorities (Clayton and Renvoize, 1986; Soderstrom and Ellis, 1987; Watson and Dallwitz, 1992) all included herbaceous bamboos in a heterogeneous Bambusoideae (Clark et al., 1995). Among the modern traditional concepts of Bambusoideae, the circumscriptions of Watson and Dallwitz (1992) is considered to be the most inclusive, which contained 14 herbaceous tribes along with the woody bamboo tribe Bambuseae. In comparison, Soderstrom and Ellis (1987) separated the core Bambusoideae having five tribes (Anomochloeae, Buergersiochloeae, Olyreae, Streptochaeteae and Bambuseae) from those showing some relationships but lacking core Bambusoideae characters Bamboo Systematics with Special Reference to Molecular Taxonomy of Dendrocalamus 3

(1. embryo formula F+PP or F-PP, 2. a linear hilum, 3. smaller embryo in comparison to endosperm, 4. three lodicules, 5. first blade is horizontal in a seedling and preceded by one or more bladeless sheaths, 6. rod like bicellular micro hairs, 7. a nonradiate mesophyll and C3 photosynthetic pathway, 8. a mesophyll with both fusoid and arm cells present, 9. vascular bundles usually more than one and superposed in the midrib and 10. vertical orientation of silica bodies to the long cells) which were considered as part of Bambusoideae sensu lato. While the most recent taxonomic treatment 'The Bamboos of the World' by Ohrnberger (1999) provided a more restrictive view of Bambusoideae (Fig. 1.1.). Ohrnberger limited the tribal assignments to Bambuseae (woody bamboos) and five other herbaceous tribes including and , though the inclusion of Puelia and Guaduella in Bambusoideae was tentative and later study (Clark et al., 2000) confirmed they should be excluded from the subfamily. They retained four of the core Bambusoideae described by Soderstrom and Ellis (1987) but moved , , Phareae and other herbaceous tribes (as of Clayton and Renvoize, 1986; Soderstrom and Ellis, 1987; Watson and Dallwitz, 1992) out of Bambusoideae. Clayton and Renvoize (1986) provided a provisional classification of the woody bamboo tribe Bambuseae based on the ovary appendage as the primary criterion. By taking the genera in a wide sense and ignoring aberrant species, they referred the woody bamboos to three subtribes, viz., Arundinariinae, and Melocanninae. The subsequent schemes of Soderstrom and Ellis (1987) and Ohrnberger (1999) were more explicit and similar to a large extent. Soderstrom and Ellis (1987) delimited nine subtribes under Bambuseae and expressed uncertainty about the placement of a few genera, viz., Apoclada, Glaziophyton, Hitchcockella, Oligostachyum and Racemobambos. Whereas, Ohrnberger's scheme included 10 subtribes. He merged the Nastinae and Neurolepidinae of Soderstrom and Ellis (1987) in his subtribes Hickeliinae and Chusqueinae respectively, and placed the uncertain genera Apoclada and Glaziophyton in subtribe Arthrostylidiinae, Hitchcockella in Hickeliinae, Oligostachyum in Arundinariinae, and Racemobambos in Racemobambosinae. The Old World tropical subtribe 'Bambusinae' has been variously circumscribed by the modern sytematists. Clayton and Renvoize's (1986) scheme included 25 genera based on type of inflorescence, culm sheath characters and ovary characters. Later, Soderstrom and Ellis (1987) narrowed down the subtribe to six genera based on floral and vegetative key characters as other anatomical characters were found unhelpful at this level. He also placed ten other genera as congeners with Bambusa and Dendrocalamus. The circumscription of Wong (1995) was limited to the taxa available in Peninsular Malaysia. Besides retaining five genera of Clayton and Renvoize (1986), Wong (1995) described three new genera, which were initially included in Bambusa 4 Swapnendu Pattanaik

by Holttum (1956). In the most recent scheme of Ohrnberger (1999), the subtribe Bambusinae embraced seventeen genera and 297 species. He retained seven genera of Clayton and Renvoize (1986) and the four additional genera described by Wong (1995) in his scheme of Bambusinae. He placed six other genera in Bambusinae taking total number of genera to 17. Many genera included in the scheme of Clayton and Renvoize (1986) were moved to subtribes Arthrostylidiinae, Hickeliinae, Shibataeinae and Racemobambosinae and some of the genera (, Gigantochloa, and Oxytenanthera) placed as congeners in Soderstrom and Ellis's (1987) scheme were given generic status. The fluctuating size of the subtribe Bambusinae over the years reflect the problem whether to combine taxa based on character similarities or to delimit taxa into subgroups based on key character differences which is not easy in bamboos as the boundaries of many bamboo genera are not well defined (Soderstrom and Ellis, 1987). As such, there are differences of opinion with regard to the placement of Dinochloa, Melocalamus, Oxytenanthera and Holttumochloa, in Bambusinae.

2. Molecular Taxonomy of Bamboos – The Modern Approach The bamboo taxonomists have long been trying different sources of taxonomically informative data for the classification because of apparent paucity of morphological characters in bamboos, The availability of molecular data in the final decade of the 20th century enabled taxonomists to review phylogenetic concepts of the more objectively. Initially DNA products, viz., isozymes and secondary compounds like phenolics were used in exploring phylogenetic relationship among taxa (Chou and Hwang, 1985), species identification (Alam et al., 1997) and assessment of infraspecific polymorphism (Biswas, 1998). Later on, variation in DNA structure itself was the subject of investigations generating two different kinds of data, viz., restriction fragment data and gene sequence data. Data so generated was analyzed using numerical concepts like maximum parsimony and maximum likelihood. DNA fragment-based studies in bamboos include the use of restriction fragment length polymorphism (RFLP) in Phyllostachys (Friar and Kochert, 1991; Taguchi-Shiobara et al., 1998) and chloroplast DNA in Asian bamboos (Watanabe et al., 1994) and world bamboos (Kobayashi, 1997). Random amplified polymorphic DNA (RAPD) markers have been used in Phyllostachys (Gielis et al., 1997) and amplified fragment length polymorphism (AFLP) markers in other bamboo studies (Loh et al., 2000; Suyama et al., 2000; Pattanaik, 2008). DNA sequence-based studies in bamboos include the use of chloroplast rpl16 intron sequences in reconstructing phylogenetic relationships within Chusquea (Kelchner and Clark, 1997), the use of an internal transcribed spacer (ITS) and the GBSSI gene sequence in the group and its allies (Guo et Bamboo Systematics with Special Reference to Molecular Taxonomy of Dendrocalamus 5

al., 2001; 2002; Guo and Li, 2004), and the use of an ITS sequence in the Bambusa group (Sun et al., 2005). There are also studies, simultaneously involving both approaches as in Phyllostachys where AFLP and ITS sequences were used to reconstruct phylogeny (Hodkinson et al., 2000). The Bamboo Phylogeny Group has been working since 2005 to address the need for a robust, global phylogeny of Bambusoideae and an updated tribal, subtribal and generic classification based on molecular phylogenetic results. The Bambusoideae is one of 12 currently recognized subfamilies of Poaceae, receiving strong bootstrap support in comprehensive molecular analysis of the family (Fig. 2.1.) (BPG, 2012). It is the only major lineage of grasses to diversify in forests (Zhang and Clark, 2000). The complex morphology and unusual flowering behaviour of most bamboos are likely the result of adaptations to forest habitat or the retention of ancestral states like their broad, pseudopetiolate leaves with fusoid cells in the mesophyll (Clark, 1997; Judziewicz et al., 1999). Molecular data have provided convincing evidence for recircumscription of Bambusoideae to include only three tribes, viz., Bambuseae, Arundinarieae and Olyreae, reflecting three main lineages of Bambusoideae (Sungkaew et al., 2009).The tribe Bambuseae consists of about 784 tropical woody bamboos; the tribe Arundinarieae represents 533 temperate woody bamboos and the tribe Olyreae represents about 122 herbaceous bamboo species. Traditionally, Arundinarieae was classified in three subtribes, viz., the Arundinariinae, Shibateinae and Thamnocalaminae, based on the presence or absence of

FAMILY

SUBFAMILY

TRIBE

SUBTRIBE

GENERA

SPECIES D. HAMILTONII 50 OTHER SPECIES

Fig. 1.1. Traditional circumscription of bamboos.

Source: Ohrnberger, 1999. 6 Swapnendu Pattanaik

FAMILY

SUBFAMILY

TRIBE

SUBTRIBE

GENERA

SPECIES 41 SPECIES

Fig. 2.1. Current circumscription of Bambusoideae. Source: BPG, 2012.

pseudospikelets and rhizome structure. The evident polyphyly among these subtribes has led them to be abandoned in favour of 10 current lineages whose branching order is unresolved. Within the Bambuseae, the three Neotropical subtribes, viz., Arthrostylidiinae, Chusqueinae and , as delimited by Judziewicz et al. (1999) are supported by molecular phylogenetic analysis. Among paleotropical subtribes, the Melocanninae, Hickeliinae and Bambusinae remain largely as circumscribed by Soderstrom and Ellis (1987). A number of recently described genera has been added in Bambusinae and Hickeliinae. The Racemobambosinae has been restricted to Racemobambos, as molecular results indicated and to fall within Bambusinae. Bambusinae is a paleotropical subtribe with its centre of diversity in southeast . It contains 28 genera (BPG, 2012), having no phylogenetic relationships. In the study of Pattanaik (2008), was placed within Dendrocalamus sensu lato supporting the closeness, or even inseparability of these two genera. Melocalamus and Thyrsostachys were recovered as sister lineages to Dendrocalamus and Bambusa. Watanabe et al. (1994), the first to study phylogenetic relationships among Asian bamboos using restriction fragment length polymorphism of chloroplast DNA, recovered a clade representing subtribe Bambusinae sensu Ohrnberger (1999), containing Bambusa, Dendrocalamus, Gigantochloa and Thyrsostachys. Bamboo Systematics with Special Reference to Molecular Taxonomy of Dendrocalamus 7

Internally, however, Watanabe's clade was poorly resolved among Bambusa, Gigantochloa and Dendrocalamus, suggesting close relationships among these genera. Thyrsostachys had emerged as a sister lineage to the other genera included in Watanabe's study. The study of Loh et al. (2000), using AFLPs and RAPDs, respectively also indicated a close relationship between Bambusa and Gigantochloa. The combined evidence from these molecular studies suggested that the taxa belonging to Bambusa, Dendrocalamus, Dinochloa and Gigantochloa form a close complex but are relatively distant from Melocalamus, Thyrsostachys and Oxytenanthera.

3. Dendrocalamus before the Availability of Molecular Tools

3.1.Generic Circumscription Since Dendrocalamus was separated from Bambusa by Nees von Esenbeck in 1834, over 70 species names have been assigned to the genus, although Ohrnberger (1999) retains only 51 of them. Most of the species that were not being maintained by Ohrnberger have been reduced to synonymy or to infraspecific rank. A few are transferred to, or sunk into, other genera, e.g., (subtribe Thamnocalaminae); Gigantochloa and (Bambusinae). After the genus was established, over 30 years passed before Munro (1868) consolidated its utility in his famous bamboo monograph. Subsequently, additional species were steadily distinguished, bringing the genus size to about 15 species by 1900 and to nearly 30 species by 1950. Post-World War II, there was little change until the 1980s when many more species, particularly from China, were described. The following description of Dendrocalamus is based on the accounts of Gamble (1896), Seethalakshmi and Muktesh Kumar (1998) and Li and Stapleton (2006). Species of Dendrocalamus are characterized by their sympodial rhizomes and large- sized dense clumps. Culms are unicaespitose, erect or occasionally scrambling and usually having a pendulous apex. In all cases several branches are found, up to three of which may be dominant. Culm sheaths are deciduous, ligules conspicuous, auricles small and often absent, blade usually recurved or erect. Foliage leaf blades are usually large, with conspicuous ligules and usually lacking auricles. The venation is not tessellate. The inflorescence is iterauctant and fully bracteate, subtended by a narrow single-keeled prophyll. The pseudospikelets are clustered in a soft or spiky globose mass at the nodes of leafless flowering branches. The pseudospikelets are prophyllate, with two to eight florets, with or without a rachilla extension. The fertile glumes are preceded by one or more bracts and up to two empty glumes. The prophyll is narrow and single-keeled. The rachilla internodes are usually abbreviated and not disarticulating. The lemma is broad, many veined 8 Swapnendu Pattanaik

and sometimes long mucronate. The paleae of the lower florets are two-keeled, but in the terminal floret rounded or imperfectly keeled. Lodicules are usually absent but sometimes one to three are present. There are six stamens, with free (usually) filaments, rarely united into a loose tube. The ovary is stalked with a hairy thickened apex, and a very short, solid style. The long plumose stigmas number varies from one to three. The caryopsis is characterized by a hairy apex and a slightly thickened pericarp. The original description of Dendrocalamus was based on the type species D. strictus. Subsequently, the description was expanded to include pericarp characters which were used to distinguish between Dendrocalamus and Bambusa (Munro, 1868; Bentham, 1883; Gamble, 1896). However, while, at present, it is taxonomically convenient for Dendrocalamus to be recognized in a broad sense (its species being distinguished by the presence of single-keeled prophylls throughout the inflorescence Stapleton, 1991), the limits between Bambusa and Dendrocalamus are not satisfactorily defined and there are intermediate species. As long ago as Holttum (1956) recognized the close relationship between the two genera by analyzing ovaries placing the two genera in a unit he called Bambusa-Dendrocalamus type. Evidence from culm anatomy (Grosser and Liese, 1973) and embryology (Gopal and Mohan Ram, 1985) has supported this point of view.

3.2.Infrageneric Proposals for Dendrocalamus Various infrageneric classifications of Dendrocalamus have been proposed by Chinese botanists. Hsueh and Li (1988) proposed the first infrageneric classification of Dendrocalamus by recognizing two subgenera and five sections in it, limiting the assignments to only those species reported from China. In this classification, subgenera were recognized based on reproductive and vegetative characters, whereas sections were segregated by reproductive characters. Species were delimited mainly by vegetative characters like culm sheath, nodes and internodes. Ohrnberger (1999) transferred D. patellares and D. mianningensis out of Bambusinae into genus Ampelocalamus (Thamnocalaminae) and assigned species only to sections Dendrocalamus, Bambusoidetes, Sinocalamus and Draconicalamus. Out of the 51 taxa recognized by Ohrnberger, 22 were assigned to particular sections while 29 taxa were unplaced. A more recent taxonomic revision of Chinese Dendrocalamus (Li and Stapleton, 2006) retains the subgenera proposed by Hsueh and Li (1988) but disregards sectional assignments, merging sections Dendrocalamus and Bambusoidetes as subgenus Dendrocalamus, and sections Sinocalamus and Draconicalamus as subgenus Sinocalamus. Li and Stapleton (2006) transferred 11 taxa previously referred to subgenus Sinocalamus to subgenus Dendrocalamus. The major problem in the infrageneric classification of Dendrocalamus is the paucity of published morphological character information for many of the species. Twenty- Bamboo Systematics with Special Reference to Molecular Taxonomy of Dendrocalamus 9 seven species do not appear to have been referred to any subgenus or section under any of the proposed schemes.

4. Genus Dendrocalamus and Related Genera in Biochemical and Molecular Studies In a study involving five Dendrocalamus taxa and naibunensis W.C. Lin and quadrangularis Makino, a Dendrocalamus cluster could be differentiated from the other two genera using phenolic compounds and isozyme patterns of esterase and peroxidase. Within Dendrocalamus two clusters were recognized: Dendrocalamus asper associated with D. giganteus, while D. latiflorus associated with its variety D. latiflorus var. mei-nung. However, was distant from these two clusters. The more pertinent studies involving Dendrocalamus taxa are those of Loh et al. (2000) Sun et al. (2005) and Pattanaik (2008). In the first study, two Dendrocalamus taxa were sampled, with D. brandisii clustering with taxa from Bambusa, and D. giganteus appearing phylogenetically distant from all other taxa included. In the second study, three Dendrocalamus taxa were sampled. These three taxa did not form a separate clade but clustered within Bambusa, which was split into two distinct clades. D. membranaceus showed close affinity to D. strictus and both were placed within one Bambusa clade, whereas D. latiflorus was associated with the other Bambusa clade. The study of Pattanaik (2008) included 10 Indian Dendrocalamus taxa and five outgroup taxa from subtribe Bambusinae. Neither the phenetic (Fig. 4.1.) nor the phylogenetic (Fig. 4.2.) analysis adopted in the investigation supported monophyly of the genus Dendrocalamus as circumscribed by Hsueh and Li (1988), Ohrnberger (1999) and Li and Stapleton (2006) based on morphological data. The placement of Bambusa balcooa and D. strictus suggested otherwise. Bambusa balcooa, instead of forming a separate lineage, was recovered in cluster two shared with Dendrocalamus hamiltonii and D. sikkimensis. This supports the findings of Stapleton (1994a, b, c) who had reported the closeness of B. balcooa to Dendrocalamus species on morphological grounds, stressing similarity in the profuse aerial roots at the culm nodes, the large rhizomatous branch bases and the culm wax. Further similarities between B. balcooa and D. hamiltonii can be found in the reproductive parts with both species having three stigmas each. The placement of D. strictus near the root of the tree away from rest of the Dendrocalamus sensu lato was not entirely unexpected considering the findings of Chou and Hwang (1985) who had reported the isolation of D. strictus from other Dendrocalamus taxa based on studies involving isozymes and phenolics. The limited number of taxa, included in the aforementioned studies, has not yielded any robust relationships or boundaries of Dendrocalamus. The Bamboo 10 Swapnendu Pattanaik

Fig. 4.1. Neighbour-joining phenogram depicting phenetic relationships among 15 OTUs sampled from subtribe Bambusinae. Numbers at the nodes indicate bootstrap (%) support for the respective clusters.

Fig. 4.2. Cladogram depicting strict consensus of the two parsimonious trees obtained in the maximum parsimony analysis of a character matrix of 470 AFLP markers. Length =1480 steps (character state changes), CI = 0.317, RI = 0.289, RC = 0.092. Values above segments indicate bootstrap support for the respective nodes. Bootstrap support for nodes with less than 50 per cent support and which collapse under the 50 per cent majority rule tree is not shown. Bamboo Systematics with Special Reference to Molecular Taxonomy of Dendrocalamus 11

Phylogeny Group (BPG) (2012) has recognized 41 taxa under Dendrocalamus, the phylogenetic relationships among which are yet to be established.

5. Conclusion On account of rare flowering events in bamboos, the traditional classification systems relied solely on vegetative characteristics. The earlier bamboo classifications proved artificial when molecular level information like DNA sequences were used by taxonomists to build more natural classification systems reflecting the evolutionary history of bamboos. Molecular taxonomy has opened up new possibilities in bamboo classification where vegetative characters, though useful for identification in these infrequently flowering plants, have not been very helpful. Analysis of similarities in molecules such as DNA sequences has helped enormously in interpreting the relationships and evolution of most plants including bamboos. As more and more taxa and molecules (plastid sequences) are included in phylogenetic analyses, the subtribal and generic circumscription of bamboos will become more robust.

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