The Cytonuclear Dimension of Allopolyploid Evolution: An Example from Cotton Using Rubisco

Abstract

During allopolyploid speciation, two divergent nuclear genomes merge, yet only one (usually the maternal) of the two sets of progenitor organellar genomes is maintained. Rubisco (1,5-bisphosphate carboxylase/oxygenase) is composed of nuclear-encoded small subunits (SSUs) and plastome-encoded large subunits (LSUs), providing an ideal system to explore the evolutionary process of cytonuclear accommodation. Here, we take initial steps in this direction, using Gossypium allopolyploids as our model. SSU copies from divergent (5-10 My) progenitor diploids ("A" and "D" genomes) were combined at the time of polyploid formation 1-2 Ma, with the LSU encoded by the maternal A-genome parent. LSU genes from A- and D-genome diploids and AD-genome allopolyploids were sequenced, revealing several nonsynonymous substitutions and suggesting the possibility of differential selection on the nuclear-encoded rbcS partner following allopolyploid formation. Sequence data for the rbcS gene family revealed nonreciprocal homoeologous recombination between A- and D-rbcS homoeologs in all polyploid species but not in a synthetic intergenomic F1 hybrid, demonstrating "gene conversion" during allopolyploid evolution. All progenitor rbcS genes are retained and expressed in the five extant allopolyploid species, but analysis of the leaf transcriptome showed that A-homoeologs are preferentially expressed in both the allopolyploid and hybrid, consistent with the maternal origin of rbcL. Although rbcS genes from both progenitor genomes are expressed, some appear to have experienced mutations that may represent cytonuclear coevolution.

Cytonuclear Evolution of Rubisco in Four Allopolyploid Lineages

“…In Brassica , no amino acid differences exist between the parental diploid species (table 1). Similar to observations for rbcL genes in diploid cottons (Gong et al 2012), diverged amino acid residues cluster in the C-terminal α/β- barrel domain and/or N-terminal domains of LSU subunits (table 1), which together form the active sites for rubisco (Spreitzer and Salvucci 2002). Notably, amino acid substitutions are also observed in the middle regions following the C-terminal domains, where the LSUs interact with the SSUs (Spreitzer and Salvucci 2002; Spreitzer et al 2005).…”

“…To date, though, the special circumstances surrounding cytonuclear evolution in polyploids remains largely unexplored. Previously, we investigated how homoeologous nuclear genes of Gossypium allopolyploids encoding subunits of one protein complex evolved in a new context where they need to interact with a subunit encoded by a gene from the plastome, inherited (in cotton) from only one of the two progenitor diploids (Gong et al 2012). The model protein complex we utilized is Rubisco (Ribulose 1,5-bisphosphate carboxylase/oxygenase), an essential enzyme in carbon fixation during photosynthesis, which functions as octamer holoenzymes of small subunits (SSUs) encoded by a nuclear rbcS multigene family and large subunits (LSUs) encoded by a single plastid rbcL gene (Rodermel et al 1996).…”

“…The model protein complex we utilized is Rubisco (Ribulose 1,5-bisphosphate carboxylase/oxygenase), an essential enzyme in carbon fixation during photosynthesis, which functions as octamer holoenzymes of small subunits (SSUs) encoded by a nuclear rbcS multigene family and large subunits (LSUs) encoded by a single plastid rbcL gene (Rodermel et al 1996). After characterizing rbcS and rbcL genic compositions in Gossypium , we explored their cytonuclear coordination at the genomic level, showing postpolyploidy, intergenomic, maternal-to-paternal gene conversion between nuclear homoeologs (Gong et al 2012), in the direction opposite to that exhibited overall in Gossypium polyploids (Salmon et al 2010; Flagel et al 2012; Paterson et al 2012; Guo et al 2014). At the transcriptional level, biased maternal rbcS homoeolog expression was also demonstrated.…”

Quantitative Analysis of the Mitochondrial and Plastid Proteomes of the Moss Physcomitrella patens Reveals Protein Macrocompartmentation and Microcompartmentation

“…S10) is substantially expanded in P. patens and shows evidence of regulatory subfunctionalization, as we identified members of one clade to be less abundant than members of a second clade. Thus, the repeated duplication of rbcs genes resulted in dissimilar protein abundances of the paralogs in moss, indicating either subfunctionalization resulting in a differential spatiotemporal expression pattern or to balance gene dosage effects, as reported for rbcs homologs in cotton (Gossypium hirsutum; Gong et al, 2012). Similarly, our data suggest regulatory diversification of members of the mitochondrial isocitrate dehydrogenase and plastid ATPase b-chain families (Supplemental Table S2, worksheet 11).…”

Nonadditive Gene Expression in Polyploids

“…Because organellar genomes are typically maternally inherited in plants (with paternal inheritance of plastids in conifers a notable exception), greater compatibility is observed between the nuclear and maternal, rather than paternal, genomes, at least in angiosperms. Certainly, genes that encode proteins assembled from nuclear and plastid genome components must undergo coordinated expression, and this cytonuclear balance is observed for rbcS and rbcL, the nuclear and plastid genes responsible for the small and large subunits, respectively, of RUBISCO (61,159). However, reports attributing large-scale expression differences to maternal effects are rare, most likely because so few data sets have been explored.…”