Plant Systematics and Evolution

, Volume 299, Issue 1, pp 239–257 | Cite as

Multi-gene region phylogenetic analyses suggest reticulate evolution and a clade of Australian origin among paleotropical woody bamboos (Poaceae: Bambusoideae: Bambuseae)

  • W. L. Goh
  • S. Chandran
  • D. C. Franklin
  • Y. Isagi
  • K. C. Koshy
  • S. Sungkaew
  • H. Q. Yang
  • N. H. Xia
  • K. M. Wong
Original Article

Abstract

The paleotropical woody bamboo subtribe Bambusinae has not been satisfactorily circumscribed and remains a major taxonomic problem. Genera such as Holttumochloa, Mullerochloa and Temburongia have not been confidently assigned to this subtribe. The phylogenetic relationships among genera hitherto placed in or near the Bambusinae, together with the related subtribes Racemobambosinae and Melocanninae, were investigated using three chloroplast DNA markers (rps16-trnQ, trnC-rpoB and trnD-T intergenic spacers) and a nuclear DNA marker (granule-bound starch synthase I, GBSSI) for a sample of 51 ingroup species and 2 outgroup species. Phylogenetic analyses revealed four distinct lineages among the members of the currently recognized Bambusinae: (1) the Bambusa-Dendrocalamus-Gigantochloa (BDG) complex, (2) the Holttumochloa-Kinabaluchloa clade, (3) the Dinochloa-Mullerochloa-Neololeba-Sphaerobambos (DMNS) clade and (4) Temburongia simplex. The BDG complex, which comprises the core of the Bambusinae, appears to have a complex evolutionary history as indicated by incongruence between the cpDNA and the nuclear gene topologies. Introgressive hybridization and incomplete lineage sorting are possible underlying causes for this complexity. The distinction of the climbing-scrambling bamboo lineages from the core Bambusinae and Racemobambosinae suggests directions for investigating the possible existence of further subtribes with increased taxon and geographical sampling. Possible biogeographic scenarios associated with the Holttumochloa-Kinabaluchloa clade and the DMNS clade are discussed.

Keywords

Australia Bambusinae Biogeography Paleotropical bamboos Racemobambosinae Reticulate evolution Incomplete lineage sorting Incongruent gene topologies Introgressive hybridization Southeast Asia 

Notes

Acknowledgments

This work would have been impossible without the generous help and interest of many who helped make available the diverse array of samples used: Forest Research Centre, Sabah; Rimba Ilmu Botanical Garden, University of Malaya; South China Botanical Garden; South West Forestry College, Kunming; the Kunming World Expo; Kinabalu Park, Sabah; Brunei Forestry Department; David Bowman, Nicholas Hogarth, Shingo Kaneko, Lin Rushun, Y.W. Low, Janna Nilsson, Joan Pereira, M. Sugumaran, Cliff Sussman, Tran Van Tien and Zheng Chaohan. We are likewise grateful for comments and constructive suggestions from Lynn G. Clark (Iowa State University), Koichi Kamiya (Ehime University) and Scot A. Kelchner (Idaho State University) during the preparation of this paper. WLG was supported by a Postgraduate Fellowship of the University of Malaya. This work received funding from University of Malaya research grants FS275/2008C, PS151/2008B and PS293/2009C, and the H.M. Burkill Research Fellowship of the Singapore Botanic Gardens. This paper is dedicated to Len Muller, whose huge enthusiasm for unraveling the many mysteries of Southeast Asian and Australian bamboos has been a constant encouragement.

Supplementary material

606_2012_718_MOESM1_ESM.doc (28 kb)
Supplementary material 1. (DOC 27 kb)
606_2012_718_MOESM2_ESM.jpg (463 kb)
Supplementary material 2. Phylogram of the 50% majority-rule consensus tree from the Bayesian analyses based on the cpDNA (rps16-trnQ+trnC-rpoB+trnD-T) data (JPEG 463 kb)
606_2012_718_MOESM3_ESM.jpg (515 kb)
Supplementary material 3. Phylogram of the 50% majority-rule consensus tree from the Bayesian analyses based on the partial GBSSI data (JPEG 514 kb)

References

  1. Armstrong KC (1991) Chromosome evolution of Bromus. In: Armstrong KC, Tsuchiya T, Gupta P (eds) Chromosome engineering in plants: genetics, breeding, evolution, part B. Elsevier Science Publ, The Netherlands, pp 366–377Google Scholar
  2. Avise JC, Arnold J, Ball RM, Birmingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann Rev Ecol Syst 18:489–522Google Scholar
  3. Bahadur KN, Jain SS (1981) Rare bamboos of India. Indian J For 4:280–286Google Scholar
  4. Bamboo Phylogeny Group (2005) L.G. Clark Lab: sequencing primers and PCR protocols. http://www.eeob.iastate.edu/research/bamboo/pdf/PCR_protocols.pdf
  5. Bamboo Phylogeny Group (2012) An updated tribal classification for the Bambusoideae (Poaceae). In: Proceedings of the 9th World Bamboo Congress, Antwerp, Belgium, 10−12 April 2012Google Scholar
  6. Bänfer G, Moog U, Fiala B, Mohamed M, Weising K, Blattner FR (2006) A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridization, vicariance and long-distance dispersal. Mol Ecol 15:4409–4424PubMedCrossRefGoogle Scholar
  7. Batchelor BC (1979) Discontinuously rising Late Cainozoic eustatic sea-levels, with special reference to Sundaland, southeast Asia. Geologie en Mijnbouw 58:1–20Google Scholar
  8. Borchsenius F (2009) FastGap 1.1. Department of Biological Sciences, University of Aarthus, Denmark, http://www.aubot.dk/fb/FastGap_home.htm
  9. Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, Bank M, Chase MW, Hodkinson TR (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol Phylogenet Evol 47:488–505PubMedCrossRefGoogle Scholar
  10. Bouchenak-Khelladi Y, Verboom A, Savolainen V, Hodkinson TR (2010) Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Bot J Linn Soc 162:543–557CrossRefGoogle Scholar
  11. Bowden WM (1959) Chromosome numbers and taxonomic notes on northern grasses: I Tribe Triticeae. Can J Bot 37:1143–1145CrossRefGoogle Scholar
  12. Bowden WM (1960a) Chromosome numbers and taxonomic notes on northern grasses: II Tribe Festuceae. Can J Bot 38:117–131CrossRefGoogle Scholar
  13. Bowden WM (1960b) Chromosome numbers and taxonomic notes on northern grasses: III Twenty-five genera. Can J Bot 38:541–557CrossRefGoogle Scholar
  14. Bowden WM (1961) Chromosome numbers and taxonomic notes on northern grasses: IV. Tribe Festuceae: Poa and Puccinellia. Can J Bot 39:123–138CrossRefGoogle Scholar
  15. Bremer K (2002) Gondwanan evolution of the grass alliance of families (Poales). Evolution 56:1374–1387PubMedGoogle Scholar
  16. Cannon CH, Manos PS (2003) Phylogeography of the Southeast Asian stone oaks (Lithocarpus). J Biogeogr 30:211–226CrossRefGoogle Scholar
  17. Chen R, Li X, Song W, Liang G, Zhang P, Lin R, Zong W, Chen C, Fung H (2004) Chromosome atlas of major economic plants genome in China (Tomus IV). Chromosome atlas of various bamboo species. Science Press, BeijingGoogle Scholar
  18. Clark LG, Davidse G, Ellis RP (1989) Natural hybridization in bamboos: evidence from Chusquea sect. Swallenochloa (Poaceae: Bambusoideae). Nat Geo Res 5:459–476Google Scholar
  19. Clark LG, Zhang W, Wendel JF (1995) A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Syst Bot 20:436–460CrossRefGoogle Scholar
  20. Clark LG, Dransfield S, Triplett J, Sánchez-Ken JG (2007) Phylogenetic relationships among the one-flowered, determinate genera of Bambuseae (Poaceae: Bambusoideae). Aliso 23:315–332Google Scholar
  21. Cotton R, Stace CA (1976) Taxonomy of the genus Vulpia (Gramineae). I Chromosome numbers and geographical distribution of the old world species. Genetica 46:235–255CrossRefGoogle Scholar
  22. Devos KM et al (2010) Grass genome organization and evolution. Curr Opin Plant Biol 13:139–145PubMedCrossRefGoogle Scholar
  23. Döring E, Schneider J, Hilu KW, Röser M (2007) Phylogenetic relationships in the Aveneae/Poaceae complex (Pooideae, Poaceae). Kew Bull 62:407–424Google Scholar
  24. Dransfield S (1981) The genus Dinochloa (Gramineae–Bambusoideae) in Sabah. Kew Bull 36:613–633CrossRefGoogle Scholar
  25. Dransfield S (1983) The genus Racemobambos (Gramineae–Bambusoideae). Kew Bull 37:661–679CrossRefGoogle Scholar
  26. Dransfield S (1989) Sphaerobambos, a new genus of bamboo (Gramineae–Bambusoideae) from Malesia. Kew Bull 44:425–434CrossRefGoogle Scholar
  27. Dransfield S (1992) The bamboos of Sabah. Sabah Forest Records, No. 14. Sabah Forestry Department, MalaysiaGoogle Scholar
  28. Dransfield S, Widjaja EA (1995) Plant resources of South-East Asia No. 7: Bamboos. Backhuys Publishers, LeidenGoogle Scholar
  29. Dransfield S, Wong KM (1996) Temburongia, a new genus of bamboo (Gramineae: Bambusoideae) from Brunei. Sandakania 7:49–58Google Scholar
  30. Franklin DC (2003) Morphology and taxonomy of the Top End Bamboo Bambusa arnhemica F. Muell., a little-known bamboo from northern Australia. Bamboo Sci Cult 17:44–54Google Scholar
  31. Franklin DC (2008) Taxonomic interpretations of Australian native bamboos (Poaceae: Bambuseae) and their biogeographic implications. Telopea 12:179–191Google Scholar
  32. Goh WL, Chandran S, Xia NH, Lin RS, Wong KM (2010) Phylogenetic relationships among Southeast Asian climbing bamboos (Poaceae: Bambusoideae) and the Bambusa complex. Biochem Syst Ecol 38:764–773CrossRefGoogle Scholar
  33. Goh WL, Chandran S, Kamiya K, Wong KM (2011) A natural hybrid between Dendrocalamus pendulus and Gigantochloa scortechinii (Poaceae: Bambsoideae: Bambuseae) in Peninsular Malaysia. Gard Bull Sing 62:223–238Google Scholar
  34. GPWG (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann. Missouri Bot Gard 88:373–457CrossRefGoogle Scholar
  35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  36. Hall R (2009) Southeast Asia’s changing palaeogeography. Blumea 54:148–161CrossRefGoogle Scholar
  37. Harlan JR, deWet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev 41:361–390CrossRefGoogle Scholar
  38. Heaney LR (1991) A synopsis of climatic and vegetational change in Southeast Asia. Climate Change 19:53–61CrossRefGoogle Scholar
  39. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192Google Scholar
  40. Hilu KW (1985) Trends of variation and systematics of Poaceae. Taxon 34:102–114CrossRefGoogle Scholar
  41. Hilu KW (2004) Phylogenetics and chromosomal evolution in the Poaceae (grasses). Aust J Bot 52:13–22CrossRefGoogle Scholar
  42. Holttum RE (1956) The classification of bamboos. Phytomorphology 6:73–90Google Scholar
  43. Holttum RE (1958) The bamboos of the Malay Peninsula. Gard Bull Sing 16:1–135Google Scholar
  44. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  45. Hunziker JH, Wulff AF, Soderstrom TR (1982) Chromosome studies on the Bambusoideae (Gramineae). Brittonia 34:30–35CrossRefGoogle Scholar
  46. Ishiyama H, Inomata N, Yamazaki T, Shukor NAA, Szmidt AE (2008) Demographic history and interspecific hybridization of four Shorea species (Dipterocarpaceae) from Peninsular Malaysia inferred from nucleotide polymorphism in nuclear gene regions. Can J For Res 38:996–1007CrossRefGoogle Scholar
  47. Kamiya K, Gan YY, Lum SKY, Khoo MS, Chua SC, Faizu NNH (2011a) Morphological and molecular evidence of natural hybridization in Shorea (Dipterocarpaceae). Tree Genet Genomes 7:297–306CrossRefGoogle Scholar
  48. Kamiya K, Nanami S, Kenzo T, Yoneda R, Diway B, Chong L, Azani MA, Majid NM, Lum SKY, Wong KM, Harada K (2011b) Demographic history of Shorea curtisii (Dipterocarpaceae) inferred from chloroplast DNA sequence variations. Biotropica. doi: 10.1111/j.1744-7429.2011.00834.x Google Scholar
  49. Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application plant systematics. Ann Missouri Bot Gard 87:482–498CrossRefGoogle Scholar
  50. Kelchner SA, Clark LG (1997) Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (Poaceae). Mol Phylogenet Evol 8:385–397PubMedCrossRefGoogle Scholar
  51. Kelchner SA, Wendel JF (1996) Hairpins create minute inversions in non-coding regions of chloroplast DNA. Curr Genet 30:259–262PubMedCrossRefGoogle Scholar
  52. Kellogg EA (2009) The evolutionary history of Ehrhartoideae, Oryzeae, and Oryza. Rice 2:1–14CrossRefGoogle Scholar
  53. Kellogg EA, Appels R, Mason-Gamer RJ (1996) When genes tell different stories: the diploid genera of Triticeae (Gramineae). Syst Bot 21:321–347CrossRefGoogle Scholar
  54. Koshy KC, Jee G (2001) Studies on the absence of seed set in Bambusa vulgaris. Curr Sci 8:375–378Google Scholar
  55. Levin RA, Watson K, Bohs L (2005) A four-gene study of evolutionary relationships in Solanum section Acanthophora. Am J Bot 92:603–612PubMedCrossRefGoogle Scholar
  56. Li XL, Lin RS, Fung HL, Qi ZX, Song WQ, Chen RY (2001) Chromosome numbers of some bamboos native in or introduced to China. Acta Phytotax Sinica 39:433–442 (in Chinese)Google Scholar
  57. Maruyama I, Okamura H, Murata G (1979) On a new hybrid genus Hibanobambusa. Acta Phytotax Geobot 30:148–152 (in Japanese)Google Scholar
  58. Mason-Gamer RJ (2004) Reticulate evolution, introgression and intertribal gene capture in an allohexaploid grass. Syst Biol 53:25–37PubMedCrossRefGoogle Scholar
  59. Mason-Gamer RJ, Weil CF, Kellogg EA (1998) Granule-bound starch synthase: structure, function, and phylogenetic utility. Mol Biol Evol 15:1658–1673PubMedCrossRefGoogle Scholar
  60. Mason-Gamer RJ, Burns MM, Naum M (2010) Phylogenetic relationships and reticulation among Asian Elymus (Poaceae) allotetraploids: analyses of three nuclear gene trees. Mol Phylogenet Evol 54:10–22PubMedCrossRefGoogle Scholar
  61. McClure FA (1966) The Bamboos: A fresh perspective. Harvard University Press, Cambridge, pp 1–347Google Scholar
  62. McKenna MCC (1973) Sweepstakes, filters, corridors, Noah’s Arks, and beached Viking funeral ships in palaeogeography. In: Tarling DH, Runcorn SK (eds) Implications of continental drift to the earth sciences. Academic Press, London, pp 291–304Google Scholar
  63. Meijaard E, Groves CP (2006) The geography of mammals and rivers in mainland Southeast Asia. In: Lehman SM, Fleagle JG (eds) Primate biogeography. Springer, New York, pp 305–329CrossRefGoogle Scholar
  64. Morley RJ (2000) Origin and evolution of tropical rainforest. John Wiley & Sons, ChichesterGoogle Scholar
  65. Morley RJ (2003) Interplate dispersal paths for megathermal angiosperms. Persp Pl Ecol Evol Syst 6:5–20CrossRefGoogle Scholar
  66. Muller L (1998) Flowering and fruiting of a Gigantochloa ridleyi clone, seed germination and growth. Amer Bamboo Soc Newslett 19:8–11Google Scholar
  67. Munro W (1868) A monograph of the Bambusaceae, including descriptions of all species. Trans Linn Soc Lond 26:1–157CrossRefGoogle Scholar
  68. Muramatsu M (1981) Hybridization among Bambuseae species. In: Higuchi T (ed) Bamboo production and utilization. Proceedings of the 17th IUFRO World Congress, Kyoto, Sept 6–17, 1981Google Scholar
  69. Ní Chonghaile G (2002) Systematics of the woody bamboos (Tribe Bambuseae). PhD thesis, University of Dublin, Trinity College, IrelandGoogle Scholar
  70. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, UppsalaGoogle Scholar
  71. Ohrnberger D (1999) The bamboos of the world: annotated nomenclature and literature of the species and the higher and lower taxa. Elsevier Science, AmsterdamGoogle Scholar
  72. Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583PubMedGoogle Scholar
  73. Pohl RW, Clark LG (1992) New chromosome counts for Chusquea and Aulonemia (Poaceae: Bambusoideae). Am J Bot 79:478–480CrossRefGoogle Scholar
  74. Rieseberg LH, Brunsfield SJ (1992) Molecular evidence and plant introgression. In: Soltis DE, Soltis PS, Doyle JJ (eds) Plant molecular systematics. Chapman and Hall Inc., New York, pp 151–176CrossRefGoogle Scholar
  75. Rieseberg LH, Wendel JF (1993) Introgression and its consequences in plants. In: Harrison RG (ed) Hybrid zones and evolutionary process. Oxford University Press, New York, pp 70–109Google Scholar
  76. Roodt R, Spies JJ (2003) Chromosome studies in the grass subfamily Chloridoideae II. An analysis of polyploidy. Taxon 52:736–746CrossRefGoogle Scholar
  77. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogeny inference. Mol Biol Evol 16:1114–1116CrossRefGoogle Scholar
  78. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381PubMedCrossRefGoogle Scholar
  79. Soderstrom TR (1981) Some evolutionary trends in the Bambusoideae (Poaceae). Ann Missouri Bot Gard 68:15–47CrossRefGoogle Scholar
  80. Soderstrom TR, Ellis RP (1987) The position of bamboo genera and allies in a system of grass classification. In: Soderstrom TR, Hilu KW, Campbell CS, Barkworth ME (eds) Grass systematics and evolution. Smithsonian Institution, Washington DC, pp 225–238Google Scholar
  81. Soderstrom TR, Young SM (1983) A guide to collecting bamboos. Ann Missouri Bot Gard 70:128–136CrossRefGoogle Scholar
  82. Soreng RJ, Davis JI, Voionmaa MA (2007) A phylogenetic analysis of Poaceae tribe Poeae sensu lato based on morphological characters and sequence data from three plastid-encoded genes: evidence for reticulation, and a new classification for the tribe. Kew Bull 62:425–454Google Scholar
  83. Stapleton CMA (1994) The bamboos of Nepal and Bhutan Part III: Drepanostachyum, Himalayacalamus, Ampelocalamus, Neomicrocalamus and Chimonobambusa (Gramineae: Poaceae, Bambusoideae). Edinburgh J Bot 51:301–330CrossRefGoogle Scholar
  84. Stapleton CMA (1997) The morphology of woody bamboos. In: Chapman GP (eds) The bamboos, vol 19. Linnean Soc Symposium Series, pp 251–267Google Scholar
  85. Stebbins GL (1981) Chromosomes and evolution in the Genus Bromus (Gramineae). Bot Jahrb Syst 102:359–379Google Scholar
  86. Stebbins GL (1983) Cytogenetics and phylogeny in the family Poacae. Am J Bot 70:96–97Google Scholar
  87. Sun Y, Xia NH, Lin RS (2005) Phylogenetic analysis of Bambusa (Poaceae: Bambusoideae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. Biochem Genet 43:603–612PubMedCrossRefGoogle Scholar
  88. Sun Y, Xia NH, Stapleton CMA (2006) Relationships between Bambusa species (Poaceae, Bambusoideae) revealed by random amplified polymorphic DNA. Biochem Syst Ecol 34:417–423CrossRefGoogle Scholar
  89. Sungkaew S, Stapleton CMA, Salamin N, Hodkinson TR (2009) Non-monophyly of the woody bamboos (Bambuseae; Poaceae): a multi-gene region phylogenetic analysis of Bambusoideae s.s. J Plant Res 122:95–108PubMedCrossRefGoogle Scholar
  90. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  91. Takahashi K, Watano Y, Shimizu T (1994) Allozyme evidence for intersectional and intergeneric hybridization in the genus Sasa and its related genera (Poaceae: Bambusoideae). J Phytogeogr Taxon 42:49–60Google Scholar
  92. Taylor DJ, Piel WH (2004) An assessment of accuracy, error, and conflict with support values from genome-scale phylogenetic data. Mol Biol Evol 21:1534–1537PubMedCrossRefGoogle Scholar
  93. Thompson JD (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  94. Tran VT, Xia N, Nguyen HN, Diep MH (2012) Kinabaluchloa wrayi (Poaceae: Bambusoideae), a new bamboo record for Vietnam and a new synonym. Nordic J Bot (in press)Google Scholar
  95. Triplett JK, Clark LG (2010) Phylogeny of the temperate bamboos (Poaceae: Bambusoideae: Bambuseae) with an emphasis on Arundinaria and allies. Syst Bot 35:102–120CrossRefGoogle Scholar
  96. Triplett JK, Oltrogge KA, Clark LG (2010) Phylogenetic relationships and natural hybridization among the North American woody bamboos (Poaceae: Bambusoideae: Arundinaria). Am J Bot 97:1–22CrossRefGoogle Scholar
  97. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167CrossRefGoogle Scholar
  98. Widjaja EA (1987) A revision of Malesian Gigantochloa (Poaceae-Bambusoideae). Reinwardtia 10:291–380Google Scholar
  99. Widjaja EA (1997) New taxa in Indonesian bamboos. Reinwardtia 11:57–152Google Scholar
  100. Wong KM (1993) Four new genera of bamboos (Gramineae: Bambusoideae) from Malesia. Kew Bull 48:517–532CrossRefGoogle Scholar
  101. Wong KM (1995) The morphology, anatomy, biology and classification of Peninsular Malaysian bamboos. University of Malaya botanical monographs No. 1. University of Malaya, Kuala LumpurGoogle Scholar
  102. Wong KM (2005) Mullerochloa, a new genus of bamboo (Poaceae: Bambusoideae) from north-east Australia and notes on the circumscription of Bambusa. Blumea 50:425–441CrossRefGoogle Scholar
  103. Wong KM (2011) A biogeographic history of Southeast Asian rainforests. In: Wickneswari R, Cannon C (eds) Managing the future of Southeast Asia’s valuable tropical rainforests, Advances in Asian human-environmental research 2. Springer, Dordrecht, pp 21–55CrossRefGoogle Scholar
  104. Xia NH, Jia LZ, Li DZ, Stapleton CMA (2007) Bambusa Schreber. In: Wu Z, Raven PH, Hong D (eds) Flora of China, vol 22. Science Press, Beijing & Missouri Botanical Garden Press, St. Louis, pp 9–38Google Scholar
  105. Yamane K, Kawahara T (2005) Intra- and interspecific phylogenetic relationships among diploid Triticum-Aegilops species (Poaceae) based on base-pair substitutions, indels and microsatellites in chloroplast noncoding sequences. Am J Bot 92:1887–1898PubMedCrossRefGoogle Scholar
  106. Yang HQ, Peng S, Li DZ (2007) Generic delimitations of Schizostachyum and its allies (Gramineae: Bambusoideae) inferred from GBSSI and trnL-F sequence phylogenies. Taxon 56:45–54CrossRefGoogle Scholar
  107. Yang HQ, Yang JB, Peng ZH, Gao J, Yang YM, Peng S, Li DZ (2008) A molecular phylogenetic and fruit evolutionary analysis of the major groups of the paleotropical woody bamboos (Gramineae: Bambusoideae) based on nuclear ITS, GBSSI gene and plastid trnL-F DNA sequences. Mol Phylogenet Evol 48:809–824PubMedCrossRefGoogle Scholar
  108. Yang JB, Yang HQ, Li DZ, Wong KM, Yang YM (2010) Phylogeny of Bambusa and its allies (Poaceae: Bambusoideae) inferred from nuclear GBSSI gene and plastid psbA-trnH, rpl32-trnL and rps16 intron DNA sequences. Taxon 59:1102–1110Google Scholar
  109. Zeng CX, Zhang YX, Triplett JK, Yang JB, Li DZ (2010) Large multi-locus plastid phylogeny of the tribe Arundinarieae (Poaceae: Bambusoideae) reveals ten major lineages and low rate of molecular divergence. Mol Phylogenet Evol 56:821–839PubMedCrossRefGoogle Scholar
  110. Zhang GZ (1985) Studies on chromosome number of some sympodial bamboos. Bamboo Research 2:1–7Google Scholar
  111. Zhang GC, Chen FS (1980) No. 1 of Chenmaqing, a good bamboo hybrid. Forest Sci Technol Gansu 16(Suppl 1):124–126 (in Chinese)Google Scholar
  112. Zhang YX, Zeng CX, Li DZ (2012) Complex evolution in Arundinarieae (Poaceae: Bambusoideae): incongruence between plastid and nuclear GBSSI gene phylogenies. Mol Phylogenet Evol 63:777–797PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2012

Authors and Affiliations

  • W. L. Goh
    • 1
  • S. Chandran
    • 1
  • D. C. Franklin
    • 2
  • Y. Isagi
    • 3
  • K. C. Koshy
    • 4
  • S. Sungkaew
    • 5
  • H. Q. Yang
    • 6
  • N. H. Xia
    • 7
  • K. M. Wong
    • 8
  1. 1.Center for Research in Biotechnology for Agriculture, Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  2. 2.Research Institute for the Environment and LivelihoodsCharles Darwin UniversityDarwinAustralia
  3. 3.Laboratory of Forest Biology, Division of Forest and Biomaterials Science, Graduate School of AgricultureKyoto UniversityKyotoJapan
  4. 4.Tropical Botanic Garden and Research InstituteThiruvananthapuramIndia
  5. 5.Department of Forest Biology, Faculty of ForestryKasetsart UniversityBangkokThailand
  6. 6.Research Institute of Resources InsectsChinese Academy of ForestryKunmingChina
  7. 7.South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  8. 8.Singapore Botanic GardensSingaporeSingapore

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