RECONSTRUCTING THE COMPLEX EVOLUTIONARY ORIGIN OF WILD ALLOPOLYPLOID TOBACCOS (NICOTIANASECTIONSUAVEOLENTES)

Abstract

Nicotiana (Solanaceae) provides an ideal system for understanding polyploidization, a pervasive and powerful evolutionary force in plants, as this genus contains several groups of allotetraploids that formed at different times from different diploid progenitors.However, the parental lineages of the largest group of allotetraploids, Nicotiana section Suaveolentes, have been problematic to identify. Using data from four regions of three low-copy nuclear genes, nuclear ribosomal DNA, and regions of the plastid genome, we have reconstructed the evolutionary origin of sect. Suaveolentes and identified the most likely diploid progenitors by using a combination of gene trees and network approaches to uncover the most strongly supported evidence of species relationships. Our analyses best support a scenario where a member of the sect. Sylvestres lineage acted as the paternal progenitor and a member of either sect. Petunioides or sect. Noctiflorae that also contained introgressed DNA from the other, or a hypothetical hybrid species between these two sections, was the maternal progenitor. Nicotiana exemplifies many of the factors that can complicate the reconstruction of polyploid evolutionary history and highlights how reticulate evolution at the diploid level can add even greater complexity to allopolyploid genomes.

Time-calibrated phylogenetic trees establish a lag between polyploidisation and diversification in Nicotiana (Solanaceae)

“…Close relatives of the diploid progenitors are known for all these allotetraploids with the exception of the maternal progenitor of Suaveolentes Kelly et al 2013). Some allopolyploids are recent and have no close polyploid relatives, whereas others appear to be much older and numerous, the result of speciation at the polyploid level.…”

“…Some allopolyploids are recent and have no close polyploid relatives, whereas others appear to be much older and numerous, the result of speciation at the polyploid level. Polyploidy and diploidisation have been the subject of study in the genus for around two decades: chromosome arm translocations (Lim et al 2004), homoploid hybridisation , intergenic recombination , concerted evolution , long-term diploidisation of genomic repeats (Clarkson et al 2005;Dodsworth et al 2016a), progenitor determination (Kelly et al 2013), maternal genome donors , elimination of genomic repeats (Renny-Byfield et al 2011), the phylogenetic signal in repeats (Dodsworth et al 2015(Dodsworth et al , 2016b, floral evolution (McCarthy et al 2015), morphological character evolution (Marks et al 2011a;McCarthy et al 2016), biogeography (Ladiges et al 2011) and genome size changes (Leitch et al 2008). An earlier paper (Clarkson et al 2005) focused on the timing of polyploid events for a subset of polyploids in Nicotiana, using nonparametric rate smoothing (NPRS), but recent advances in molecular clock analysis make another study of this subject in the genus as a whole timely.…”

“…However, dates within Nicotiana are problematic and unreliable in that study due to the low levels of variation and potential incongruence of the loci combined [see tree in Supplementary Data File two of Särkinen et al (2013)]. The current study is based on three of our previously published DNA sequence datasets Kelly et al 2013). Our intention is to produce time-calibrated phylogenetic trees using both maternally (plastid DNA) and biparentally inherited (low copy nuclear) loci.…”

“…In order to produce a robust, well-resolved and well-supported nuclear phylogenetic analysis, the sequences from two previous datasets, nuclear-encoded plastid-expressed glutamine synthetase (GS) from Clarkson et al (2010) and leafy/floricaula (LFY) from Kelly et al (2013), were combined. The DNA sequences used in both studies were produced from the same accession, thus reducing sampling error.…”

“…The origin of the maternal progenitor of N. section Suaveolentes is complex (Kelly et al 2013). Breaking GS into the two pieces indicated by recombination break points results in the maternal progenitor of N. sect.…”