Independent allopolyploidization events preceded speciation in the temperate and tropical woody bamboos

Abstract

SummaryThe objectives of the current study were to investigate the origin of polyploidy in the woody bamboos and examine putative hybrid relationships in one major lineage (the temperate woody bamboos, tribe Arundinarieae).Phylogenetic analyses were based on sequence data from three nuclear loci and 38 species in 27 genera.We identify six ancestral genome donors for contemporary bamboo lineages: temperate woody bamboos (tribe Arundinarieae) contain genomes A and B, tropical woody bamboos (tribe Bambuseae) contain genomes C and D, and herbaceous bamboos (tribe Olyreae) contain genome H; some hexaploid paleotropical bamboos contain genome E in addition to C and D. Molecular data indicate that allopolyploidy arose independently in temperate (AABB) and tropical woody lineages (CCDD and CCDDEE), and speciation occurred subsequent to polyploidization. Moreover, hybridization has played a surprising and recurrent role in bamboo evolution, generating allohexaploid species in the paleotropical clade and intergeneric hybrids among the allotetraploid temperate bamboos.We suggest this complex history of reticulate evolution is at least partially responsible for the taxonomic difficulty associated with the woody bamboos. This newly-resolved phylogenetic framework reflects a major step forward in our understanding of bamboo biodiversity and has important implications for the interpretation of bamboo phylogenomics.

A worldwide phylogenetic classification of the Poaceae (Gramineae) II: An update and a comparison of two 2015 classifications

“…Molecular data have confirmed that the Bambusoideae, especially the two woody tribes, exhibit a complex history of hybridization and allopolyploidy (Fisher et al, 2009Triplett et al, , 2014Goh et al, 2013;Yang et al, 2013;Attigala et al, 2014;Oliveira et al, 2014). Within Arundinarieae, the three traditionally recognized subtribes are polyphyletic and have been abandoned in favor of numbered lineages or clades (now twelve) based on molecular support (cited in Kellogg, 2015 but not in Soreng et al, 2015b), and a number of genera, including Ampelocalamus, Indocalamus, Pleioblastus and Pseudosasa among others, are demonstrably nonmonophyletic Zeng et al, 2010;Yang et al, 2013;Zhang et al, 2016).…”

V. Subfamily Bambusoideae Luerss. (1893)

“…Such characters include rhizome structure, presence or absence of pseudospikelets, numbers and arrangement of culm buds and branches, and inflorescence architecture. In addition, homoploid hybridization has been documented and appears to be far more common than previously thought possible (Takahashi et al 1994;Triplett et al , 2014. Several common "genera" appear to be simply early-generation (possibly F1) hybrids that combine the characters of their parent genera.…”

“…Thus, even very well sampled molecular phylogenies such as those of and Zeng et al (2010) often provide only weak hints of phylogenetic history. Finally, all woody bamboos appear to be polyploid (e.g., Stebbins 1971Stebbins , 1985Triplett et al 2014). Not surprisingly, the first genome sequence of a woody bamboo shows a whole genome duplication event, estimated to have occurred 7-12 mya (Peng et al 2013), although it is unclear if the methods used account for the very slow mutation rate.…”

“…Chloroplast data place Olyreae sister to Bambuseae (Bouchenak-Khelladi et al 2008;Burke et al 2012;Kelchner and Bamboo Phylogeny Group 2013;Kelchner and Clark 1997;Sungkaew et al 2009), although monophyly of the woody bamboos cannot be rejected statistically (Kelchner and Bamboo Phylogeny Group 2013). The data of Triplett et al (2014) indicate that woodiness is derived within Bambusoideae, but it is unclear if it evolved once or if each independent polyploidization event correlates with an independent origin of woodiness.…”

“…Not surprisingly, the first genome sequence of a woody bamboo shows a whole genome duplication event, estimated to have occurred 7-12 mya (Peng et al 2013), although it is unclear if the methods used account for the very slow mutation rate. More studies like that of Triplett et al (2014) will be needed to address the effects of hybridization and polyploidy on bamboo evolution and hybridization.…”