Phylogenomic proof of Recurrent Demipolyploidization and Evolutionary Stalling of the “Triploid Bridge” in Arundo (Poaceae)

Abstract

Polyploidization is a frequent phenomenon in plants, which entails the increase from one generation to the next by multiples of the haploid number of chromosomes. While tetraploidization is arguably the most common and stable outcome of polyploidization, over evolutionary time triploids often constitute only a transient phase, or a “triploid bridge”, between diploid and tetraploid levels. In this study, we reconstructed in a robust phylogenomic and statistical framework the evolutionary history of polyploidization in Arundo, a small genus from the Poaceae family with promising biomass, bioenergy and phytoremediation species. Through the obtainment of 10 novel leaf transcriptomes for Arundo and outgroup species, our results prove that recurrent demiduplication has likely been a major driver of evolution in this species-poor genus. Molecular dating further demonstrates that the species originating by demiduplication stalled in the “triploid bridge” for evolutionary times in the order of millions of years without undergoing tetratploidization. Nevertheless, we found signatures of molecular evolution highlighting some of the processes that accompanied the genus radiation. Our results clarify the complex nature of Arundo evolution and are valuable for future gene functional validation as well as reverse and comparative genomics efforts in the Arundo genus and other Arundinoideae.

Interspecific and intraspecific phenotypic diversity for drought adaptation in bioenergy Arundo species

“…plinii (2 n = 12 x = 76; Hardion et al, 2015) and A. donaciformis are phylogenetically sister species, being A. donaciformis likely derived from A . plinii following a demiploidization event (Jike et al, 2020). Under unstressed conditions, several of the traits analysed transgressed evolutionary relationship (i.e.…”

“…Despite the larger biomass of the species with higher ploidy level, large differences exist also between them, with A. donax being much more productive in unstressed conditions than A. donaciformis . As the extraordinary productivity of A. donax may be a consequence of the contribution of the Asian gene pool of species (Jike et al, 2020), further studies comparing eastern and western accessions of A. donax invasive clone will be required to disentangle the relative contribution to productivity of ploidy versus genotype of origin.…”

“…Other important factors to be taken into account are also the date of polyploidization and the possible presence of post-polyploidization adaptation (Soltis et al, 2016). Both polyploidization events in the Arundo considered in our study are relatively old, dating back more than 2 million years ago for A. donaciformis and even earlier for A. donax (Jike et al, 2020), leaving ample space to secondary evolution of the above-mentioned traits due to post-speciation adaptation.…”

“…Other species belonging to the same genus, for example, Arundo donaciformis and Arundo plinii, produce seed and display an elevated degree of drought tolerance (Danin, 2004). Despite A. donaciformis and A. plinii being phylogenetically sister species (Jike et al, 2020), A. donaciformis underwent the same number of demiploidization events as A. donax (Jike et al, 2020) and attains a larger size than A. plinii . Thus, a comparative assessment of A. donax, A. donaciformis and A. plinii could provide additional insights into the relationship between productivity, drought tolerance and polyploidization level.…”

“…Despite A. donaciformis and A . plinii being phylogenetically sister species (Jike et al, 2020), A. donaciformis underwent the same number of demiploidization events as A. donax (Jike et al, 2020) and attains a larger size than A . plinii (Hardion et al, 2014).…”