Cytonuclear Variation of Rubisco in Synthesized Rice Hybrids and Allotetraploids

Abstract

The allopolyploid speciation process faces the genomic challenge of stoichiometric disruption caused by merging biparental nuclear genomes with only one (usually maternal) of the two sets of progenitor cytoplasmic genomes. The photosynthetic protein 1,5-bisphosphate carboxylase/oxygenase (Rubisco) is composed of nuclear-encoded small subunits (SSUs) and plastome-encoded large subunits (LSUs), making it an ideal enzyme to explore the evolution process of cytonuclear accommodation. We investigated the variation of SSUs and their encoding rbcS genes in synthetic nascent rice (Oryza sativa L.) allotetraploid lineages, formed from the parental subspecies japonica and indica of Asian rice. The evolution of rbcS genes in rice subspecies involves both mutation and concerted homogenization. Within reciprocal rice hybrids and allopolyploids, there was no consistent pattern of biased expression of rbcS alleles or homeologs, nor was there biased gene conversion favoring the maternal gene copies. Instead, we observed an apparently stochastic pattern of rbcS intergenomic gene conversions and biased expression of rbcS homeologs. We conclude that in young rice allopolyploids, cytonuclear coordination either is not selectively favored because of high parental sequence similarity or because there has been insufficient time for subtle selective effects to become observable. P olyploidy, involving the combining of two or more sets of diploid parental nuclear genomes, recursively occurs during plant evolution, generating modern plant lineages that are considered to be paleopolyploid (having • This study characterized the evolutionary features of rbcS genes in diploid rice subspecies and investigated the cytonuclear coevolution of Rubisco genes (biparentally inherited nuclear rbcS and unimaternal plastid rbcL genes encoding small subunits and large subunits, respectively) in synthesized rice hybrids (9N and N9) and allotetraploids (99NN and NN99).

Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole‐genome duplications in Brassica

“…Differential evolution of maternal and paternal Rubisco genes was also reported between homoeologous genomes of Arabidopsis suecica , Arachis hypogaea and Nicotiana tabacum allopolyploids (Gong et al ., ). This scenario was not observed in the young allopolyploid Tragopogon miscellus or in resynthesized allotetraploid Oryza sativa , despite non‐synonymous substitutions observed in the Rubisco plastid‐encoded parental sequences of these species (Sehrish et al ., ; Wang et al ., ).…”

Robust Cytonuclear Coordination of Transcription in Nascent Arabidopsis thaliana Autopolyploids

“…It has often been speculated that WGD disrupts the coordinated functioning of nuclear and cytoplasmic genomes, both by disrupting co-evolved complexes (particularly in allopolyploids), and by disrupting inter-genome dosage balance. Several lines of evidence support the conclusion that the genes encoding chimeric protein complexes in organelles have co-evolved [33], and that hybridization can produce incompatibilities that disrupt their function [9,[13][14][15][16]. However, surprisingly little experimental evidence has been gathered to test if WGD, in the absence of hybridization (autopolyploidy) disrupts dosage balance between the nucleus and organelles.…”

“…Allopolyploidy, which involves the merger of two or more differentiated nuclear genomes, also brings together novel combinations of nuclear and cytoplasmic genomes, potentially creating cytonuclear incompatibilities. These incompatibilities have been the major focus of research on cytonuclear interactions in polyploids [9,[12][13][14][15][16].…”

The Intertwined Chloroplast and Nuclear Genome Coevolution in Plants

“…In contrast, the allotetraploid Brassica napus showed no sign of homoeologous exchanges or bias expression probably because of either recent (compared to the other models) divergence time between diploid parental species (only 4 MYA). In the same way, resynthesized reciprocal hybrids and allotetraploids formed between Oryza sativa indica and japonica (that diverged around 9000 yr. ago) did not exhibit biased expression of rbcS alleles or homoeologs and also no biased gene conversion toward maternal gene copies [112]. In Tragopogon miscellus, a very recent neoallopolyploid formed only 80 years ago, homoeolog gene loss and biased expression were limited, occurring only in 12 and 16% of individuals coming from two naturally and repeatedly formed polyploid populations [113].…”