Parental origin of the allotetraploid tobacco Nicotiana benthamiana.

Matteo Schiavinato,Heinz Himmelbauer,Juliane C. Dohm,Marina Marcet‐Houben,Toni Gabaldón

doi:10.1111/tpj.14648

Abstract

Summary Nicotiana section Suaveolentes is an almost all‐Australian clade of allopolyploid tobacco species including the important plant model Nicotiana benthamiana. The homology relationships of this clade and its formation are not completely understood. To address this gap, we assessed phylogenies of all individual genes of N. benthamiana and the well studied N. tabacum (section Nicotiana) and their homologues in six diploid Nicotiana species. We generated sets of 44 424 and 65 457 phylogenetic trees of N. benthamiana and N. tabacum genes, respectively, each collectively called a phylome. Members of Nicotiana sections Noctiflorae and Sylvestres were represented as the species closest to N. benthamiana in most of the gene trees. Analyzing the gene trees of the phylome we: (i) dated the hybridization event giving rise to N. benthamiana to 4–5 MyA, and (ii) separated the subgenomes. We assigned 1.42 Gbp of the genome sequence to section Noctiflorae and 0.97 Gbp to section Sylvestres based on phylome analysis. In contrast, read mapping of the donor species did not succeed in separating the subgenomes of N. benthamiana. We show that the maternal progenitor of N. benthamiana was a member of section Noctiflorae, and confirm a member of section Sylvestres as paternal subgenome donor. We also demonstrate that the advanced stage of long‐term genome diploidization in N. benthamiana is reflected in its subgenome organization. Taken together, our results underscore the usefulness of phylome analysis for subgenome characterization in hybrid species.

Highlights

Nicotiana benthamiana is an Australian tobacco species, mostly popular as a platform for recombinant protein production (van Herpen et al, 2010; Bally et al, 2018)
N. benthamiana belongs to the section Suaveolentes, an almost all-Australian clade with the exception of a few species that are native to Africa, New Caledonia or French Polynesia
Our study aimed to address the open questions on the maternal progenitor of N. benthamiana and the time of the interspecific hybridization event that gave rise to N. benthamiana

Summary

Introduction

Nicotiana benthamiana is an Australian tobacco species, mostly popular as a platform for recombinant protein production (van Herpen et al, 2010; Bally et al, 2018). The genus Nicotiana is organized into several sections, five of which contain polyploids formed by interspecific hybridization (Figure 1; Knapp et al, 2004; Leitch et al, 2008). It has repeatedly been shown that the paternal progenitor in the hybridization that resulted in the species of section Suaveolentes is affiliated with the section Sylvestres (Knapp et al, 2004; Leitch et al, 2008; Clarkson et al, 2010; Wang and Bennetzen, 2015; Bally et al, 2018). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd

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Discussion

Conclusion