Global Patterns of Subgenome Evolution in Organelle-Targeted Genes of Six Allotetraploid Angiosperms

Abstract

Whole-genome duplications (WGDs) are a prominent process of diversification in eukaryotes. The genetic and evolutionary forces that WGD imposes upon cytoplasmic genomes are not well understood, despite the central role that cytonuclear interactions play in eukaryotic function and fitness. Cellular respiration and photosynthesis depend upon successful interaction between the 3000+ nuclear-encoded proteins destined for the mitochondria or plastids and the gene products of cytoplasmic genomes in multi-subunit complexes such as OXPHOS, organellar ribosomes, Photosystems I and II, and Rubisco. Allopolyploids are thus faced with the critical task of coordinating interactions between nuclear and cytoplasmic genes that were inherited from different species. Because cytoplasmic genomes share a more recent history of common descent with the maternal nuclear subgenome than the paternal subgenome, evolutionary “mismatches” between the paternal subgenome and the cytoplasmic genomes in allopolyploids might lead to accelerated rates of evolution in the paternal homoeologs of allopolyploids, either through relaxed purifying selection or strong directional selection to rectify these mismatches. We report evidence from six independently formed allotetraploids that subgenomes exhibit unequal rates of protein-sequence evolution, but we found no evidence that cytonuclear incompatibilities result in altered evolutionary trajectories of paternal homoeologs of organelle-targeted genes. Analyses of gene content revealed mixed evidence for whether organelle-targeted genes are lost more rapidly than non-organelle-targeted genes. Together, these global analyses provide insights into the complex evolutionary dynamics of allopolyploids, showing that allopolyploid subgenomes have separate evolutionary trajectories despite sharing the same nucleus, generation time, and ecological context.

Two divergent immune receptors of the allopolyploid Nicotiana benthamiana reinforce the recognition of a fungal microbe-associated molecular pattern VdEIX3

“…Polyploidy results in duplicated genes that play important roles in crop domestication and disease resistance ( Renny-Byfield and Wendel, 2014 ). A recent subgenome evolution analysis of allotetraploid angiosperms revealed that subgenomes of the allotetraploids exhibit unequal rates of protein evolution, showing separate evolutionary trajectories ( Sharbrough et al, 2022 ). Consistently, N. benthamiana obtained two EIX-responding loci with diverged functions from different ancestors.…”

Variation in cytonuclear expression accommodation among allopolyploid plants

“…We followed the methods of Sharbrough et al (2022) to identify orthologous genes arising from allopolyploidy (i.e. “quartets” consisting of one homolog from each diploid parent and 2 homoeologs from the allopolyploid).…”

“…We retained orthogroups containing 3 or more homologs, extracted coding sequences (CDS) for those proteins, and aligned each using the L-INS-i algorithm in MAFFT (v7.480) ( Katoh and Standley 2013 ). Model selection was done using jModelTest2 v2.1.10 ( Darriba et al 2012 ) and phylogenetic inference was performed in PhyML v3.3.20211021 ( Guindon and Gascuel 2003 ), as described previously ( Sharbrough et al 2022 ). Because these gene trees often contain multiple orthologous groups resulting from ancient duplications, we extracted subtrees containing potential quartets (i.e.…”

Comparison of ONT and CCS sequencing technologies on the polyploid genome of a medicinal plant showed that high error rate of ONT reads are not suitable for self-correction

“…1a), suggesting VDL was a tetraploid species, which may be more challenging for genome sequencing and assembly. A recent study reported that subgenome sequence divergence (measured in synonymous substitutions per synonymous site, Ks) since allopolyploidization of six allopolyploid angiosperms ranged from 0.026 to 0.105 [26], while sequence divergence between allelic chromosomes of autotetraploid alfalfa is much lower, peaked at ~ 0.01 [27]. We applied the WGDI pipeline (whole-genome duplication identification v0.4.7 [28]) to perform collinearity analysis of the The phylogenetic tree is consistent with the tree constructed by Pellicer, et al [25], and VDL is located in "2n = 4x = 32" clade, suggesting tetraploid.…”