A temporal gradient of cytonuclear coordination of chaperonins and chaperones during RuBisCo biogenesis in allopolyploid plants

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo) has long been studied from many perspectives. As a multisubunit (large subunits [LSUs] and small subunits[SSUs]) protein encoded by genes residing in the chloroplast ( rbcL ) and nuclear ( rbcS ) genomes, RuBisCo also is a model for cytonuclear coevolution following allopolyploid speciation in plants. Here, we studied the genomic and transcriptional cytonuclear coordination of auxiliary chaperonin and chaperones that facilitate RuBisCo biogenesis across multiple natural and artificially synthesized plant allopolyploids. We found similar genomic and transcriptional cytonuclear responses, including respective paternal-to-maternal conversions and maternal homeologous biased expression, in chaperonin/chaperon-assisted folding and assembly of RuBisCo in different allopolyploids. One observation is about the temporally attenuated genomic and transcriptional cytonuclear evolutionary responses during early folding and later assembly process of RuBisCo biogenesis, which were established by long-term evolution and immediate onset of allopolyploidy, respectively. Our study not only points to the potential widespread and hitherto unrecognized features of cytonuclear evolution but also bears implications for the structural interaction interface between LSU and Cpn60 chaperonin and the functioning stage of the Raf2 chaperone.

Whole-Genome Evolutionary Analyses of Non-Endosymbiotic Organelle-Targeting Nuclear Genes Reveal Their Genetic Evolution in 12 Representative Poaceae Species

“…Notable exceptions include Z. mays and M. sinensis, which experienced separate ancient wholegenome duplications (aWGDs) after speciation. However, to maintain the cytonuclear dosage balance, since organelle-targeting genes are prone to restore to single copy within following diploidization after aWGD [48,49], the relatively lower but significant frequency of single-copy NE-ONGs in these cases still supports the general trend (Table 1). In addition, the specialized and non-overlapping functions of species-specific NE-ONGs (Figure 3A,B) could facilitate nuclear control, fine-tuning chloroplasts and mitochondria in photosynthesis, energy supply, stress responses and even metabolism [50][51][52][53][54].…”

Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex

“…Another intriguing feature of the process is the involvement of the nuclear‐encoded chaperonins and chaperones in the folding and assembly of the protein complexes encoded by nuclear and organelle genes. The most comprehensive overview was provided for RuBisCO (Li et al., 2022). In four different allopolyploids (wheat, cotton, tobacco, and Arabidopsis), chaperonins and chaperones of RuBisCO showed similar evolutionary genomic and transcriptomic patterns as the nuclear‐encoded gene ( rbcS ): a frequent paternal‐to‐maternal homoeologous gene conversion and maternal HEB.…”

“…Observations on RuBisCO, a single plastid-nuclear complex, provide insights into how parentspecific divergence in nuclear-encoded genes can result in preferential expression of the maternal allele, affecting its retention over time (Gong et al, 2014;Li et al, 2019Li et al, , 2020Sehrish et al, 2015). The entire process of the RuBisCO maturation involving folding and assembly stages is further complicated by the necessary involvement of nuclear-encoded chaperones and chaperonins (Li et al, 2022;Xia et al, 2020). A broad analysis of the cytonuclear accommodation in six allopolyploid lineages by Grover et al (2022) found cytonuclear genes in most lineages that are biased towards the homoeologue or the expression level from the donor of the cytoplasmic genome.…”

“…These challenges encompass chromosomal rearrangements, mitotic and meiotic abnormalities, and genome‐wide gene expression alterations affected by epigenetic responses to the novel genomic constitution (Glombik et al., 2021; Kopecky et al., 2009; Majka et al., 2023; Svačina et al., 2020). One of the challenges for newly arising polyploids is the disruption of stoichiometry between nuclear‐ and organelle‐encoded genes (Ceriotti et al., 2022; Fernandes Gyorfy et al., 2021; Ferreira de Carvalho et al., 2019; Gong et al., 2012, 2014; Li et al., 2020, 2022; Sehrish et al., 2015; Sharbrough et al., 2017; Wang et al., 2017; Zhai et al., 2019). Core functions in eukaryotes depend on the integration and coevolution of nuclear and organelle genomes, particularly within multi‐subunit enzyme complexes (Rand et al., 2004; Roux et al., 2016; Woodson & Chory, 2008).…”

Polyploid plants take cytonuclear perturbations in stride

“…For example, allohexaploid wheat experienced a paternal-to-maternal gene conversion event in the region of a nuclear RbcS gene that encodes the transit peptide required for protein targeting and import into the plastids (Li et al, 2020). In addition, paternal-tomaternal gene conversions and biased expression of maternal homoeologs has been documented for some of the nuclear-encoded chaperones that function in assembly of Rubisco enzyme complexes (Li et al, 2022). Whether examples like this are driven by selection against cytonuclear incompatibilities remains unclear, but they point to a relatively unexplored area in the stabilization of allopolyploid cytonuclear interactions that merits further investigation.…”