Down, then up: non-parallel genome size changes and a descending chromosome series in a recent radiation of the Australian allotetraploid plant species, Nicotiana section Suaveolentes (Solanaceae)

Abstract

Background and aims The extent to which genome size and chromosome numbers evolve in concert is little understood, particularly after polyploidy (whole-genome duplication), when a genome returns to a diploid-like condition (diploidisation). We study this phenomenon in 46 species of allotetraploid Nicotiana section Suaveolentes (Solanaceae), which formed less than six million years ago and radiated in the arid centre of Australia. Methods We analysed newly assessed genome sizes and chromosome numbers within the context of a restriction site-associated nuclear DNA (RADseq) phylogenetic framework. Key results RADseq generated a well-supported phylogenetic tree, in which multiple accessions from each species formed unique genetic clusters. Chromosome numbers and genome sizes vary from n = 2x = 15-24 and 2.7-5.8 pg/1 C nucleus, respectively. Decreases in both genome size and chromosome number occur, although neither consistently nor in parallel. Species with the lowest chromosome numbers (n = 15–18) do not possess the smallest genome sizes, and although N. heterantha has retained the ancestral chromosome complement, n = 2x = 24, it nonetheless has the smallest genome size, even smaller than that of the modern representatives of ancestral diploids. Conclusions The results indicate that decreases in genome size and chromosome number occur in parallel down to a chromosome number threshold, n = 20, below which genome size increases, a phenomenon potentially explained by decreasing rates of recombination over fewer chromosomes. We hypothesize that, more generally in plants, major decreases in genome size post-polyploidization take place while chromosome numbers are still high because in these stages elimination of retrotransposons and other repetitive elements is more efficient. Once such major genome size change has been accomplished, then dysploid chromosome reductions take place to reorganize these smaller genomes, producing species with small genomes and low chromosome numbers such as those observed in many annual angiosperms, including Arabidopsis.

Repeat Dynamics across Timescales: A Perspective from Sibling Allotetraploid Marsh Orchids (Dactylorhiza majalis s.l.)

“…Concerted evolution of rDNA alleles is well underway in these allopolyploids ( Pillon et al 2007 ), with D. majalis typically exhibiting only maternal copies. In multiple other established species a decrease of TE content rather than an increase compared to expected was evident over the long term (e.g., Ozkan et al 2003 ; Leitch and Bennett 2004 ; Eilam et al 2009 ; Chase et al 2022 ). Indeed, it is generally accepted that over broad evolutionary time scales polyploidy is not a major factor in genome size increase ( Wang et al 2021 ; Chase et al 2022 ).…”

“…Genome reorganizations after allopolyploidization have been investigated in different systems, from recent neoallopolyploids (e.g., 140 years old Mimulus peregrinus , Edger et al 2017 ) to old, well-established paleopolyploids (e.g., ∼2–4 Ma tetraploid and hexaploid Spartina , Giraud et al 2020 , and ∼6 Ma Nicotiana sect. Suaveolentes , Dodsworth et al 2020 ; Chase et al 2022 ), and from synthetic allopolyploids (e.g., Nicotiana , Mhiri et al 2019 ) to natural populations (e.g., Spartina anglica , Parisod et al 2009 ). However, to our knowledge, mobile element turnover after allopolyploidization has not been evaluated thus far in multiple allopolyploid species formed independently and unidirectionally by the same parental diploids.…”

“…In the long term, WGD is followed by diploidization, a repeating process that results in polyploidization–diploidization cycles ( Van de Peer et al 2009 ; Jiao et al 2011 ; Wendel 2015 ; Chase et al 2022 ). When distinct genomes are combined together, one of them can dominate the other during the diploidization process to ultimately result in “biased fractionation” ( Sankoff et al 2012 ).…”

“…However, in several other study systems this pattern was clearly not detected (e.g., Parisod et al 2009 ; Mhri et al 2019 ; Dodsworth et al 2020 ). Nonetheless, altogether post-WGD TE activation is often ( Kashkush et al 2003 ; Parisod et al 2010 ; Renny-Byfield et al 2011 ; Oliver et al 2013 ; Vicient and Casacuberta 2017 ; Chase et al 2022 ), but not always ( IWGSC et al 2018 ; Burns et al 2021 ) regarded as a key driver of adaptation to the polyploid state and of further evolution.…”

<em>Piper</em> species (Piperaceae) of Sri Lanka and the diversity of the economically important <em>Piper nigrum</em> (black pepper): An overview of what has been done and what is yet to be achieved

“…In Heliosperma pusillum, RADseq has been successfully used to examine parallel ecological divergence (Trucchi et al, 2017), whereas in radiating New Caledonia Diospyros this method could be used to evaluate substrate effects on speciation (Paun et al, 2016). In Nicotiana (Solanaceae), RADseq was employed to evaluate the possible interactions between chromosome number and genome size changes, which are both controlled by epigenetic mechanisms (Chase et al, 2022).…”