scholarly journals Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms

2021 ◽  
Author(s):  
Evan S Forsythe ◽  
Alissa M Williams ◽  
Daniel B Sloan

Abstract Nuclear and plastid (chloroplast) genomes experience different mutation rates, levels of selection, and transmission modes, yet key cellular functions depend on their coordinated interactions. Functionally related proteins often show correlated changes in rates of sequence evolution across a phylogeny (evolutionary rate covariation or ERC), offering a means to detect previously unidentified suites of coevolving and cofunctional genes. We performed phylogenomic analyses across angiosperm diversity, scanning the nuclear genome for genes that exhibit ERC with plastid genes. As expected, the strongest hits were highly enriched for genes encoding plastid-targeted proteins, providing evidence that cytonuclear interactions affect rates of molecular evolution at genome-wide scales. Many identified nuclear genes functioned in post-transcriptional regulation and the maintenance of protein homeostasis (proteostasis), including protein translation (in both the plastid and cytosol), import, quality control and turnover. We also identified nuclear genes that exhibit strong signatures of coevolution with the plastid genome, but their encoded proteins lack organellar-targeting annotations, making them candidates for having previously undescribed roles in plastids. In sum, our genome-wide analyses reveal that plastid-nuclear coevolution extends beyond the intimate molecular interactions within chloroplast enzyme complexes and may be driven by frequent rewiring of the machinery responsible for maintenance of plastid proteostasis in angiosperms.

2020 ◽  
Author(s):  
Evan S. Forsythe ◽  
Alissa M. Williams ◽  
Daniel B. Sloan

AbstractNuclear and plastid (chloroplast) genomes experience different mutation rates, levels of selection, and transmission modes, yet key cellular functions depend on coordinated interactions between proteins encoded in both genomes. Functionally related proteins often show correlated changes in rates of sequence evolution across a phylogeny (evolutionary rate covariation or ERC), offering a means to detect previously unidentified suites of coevolving and cofunctional genes. We performed phylogenomic analyses across angiosperm diversity, scanning the nuclear genome for genes that exhibit ERC with plastid genes. As expected, the strongest hits are highly enriched for plastid-targeted proteins, providing evidence that cytonuclear interactions affect rates of molecular evolution at genome-wide scales. Many identified nuclear genes function in post-transcriptional regulation and the maintenance of protein homeostasis (proteostasis), including protein translation (in both the plastid and cytosol), import, quality control and turnover. We also identified nuclear genes that exhibit strong signatures of coevolution with the plastid genome but lack organellar-targeting annotations, making them candidates for having previously undescribed roles in plastids. In sum, our genome-wide analyses reveal that plastid- nuclear coevolution extends beyond the intimate molecular interactions within chloroplast enzyme complexes and may be driven by frequent rewiring of the machinery responsible for maintenance of plastid proteostasis in angiosperms.


2017 ◽  
Author(s):  
M.I. Schelkunov ◽  
A.A. Penin ◽  
M.D. Logacheva

Summary• While photosynthesis is the most notable trait of plants, several lineages of plants (so-called holo-heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic levels.• Here, we characterize the transcriptomes of three species representing two lineages of mycoheterotrophic plants: orchids (Epipogium aphyllum and Epipogium roseum) and Ericaceae (Hypopitys monotropa). Comparative analysis is used to highlight the parallelism between distantly related holo-heterotrophic plants.• In both lineages, we observed genome-wide elimination of nuclear genes that encode proteins related to photosynthesis, while systems associated with protein import to plastids as well as plastid transcription and translation remain active. Genes encoding components of plastid ribosomes that have been lost from the plastid genomes have not been transferred to the nuclear genomes; instead, some of the encoded proteins have been substituted by homologs. The nuclear genes of both Epipogium species accumulated mutations twice as rapidly as their photosynthetic relatives; in contrast, no increase in the substitution rate was observed in H.monotropa.• Holo-heterotrophy leads to profound changes in nuclear gene content. The observed increase in the rate of nucleotide substitutions is lineage specific, rather than a universal phenomenon among non-photosynthetic plants.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Zhiqiang Du ◽  
Jeniece Regan ◽  
Elizabeth Bartom ◽  
Wei-Sheng Wu ◽  
Li Zhang ◽  
...  

AbstractTranscriptional regulators are prevalent among identified prions in Saccharomyces cerevisiae, however, it is unclear how prions affect genome-wide transcription. We show here that the prion ([SWI+]) and mutant (swi1∆) forms of Swi1, a subunit of the SWI/SNF chromatin-remodeling complex, confer dramatically distinct transcriptomic profiles. In [SWI+] cells, genes encoding for 34 transcription factors (TFs) and 24 Swi1-interacting proteins can undergo transcriptional modifications. Several TFs show enhanced aggregation in [SWI+] cells. Further analyses suggest that such alterations are key factors in specifying the transcriptomic signatures of [SWI+] cells. Interestingly, swi1∆ and [SWI+] impose distinct and oftentimes opposite effects on cellular functions. Translation-associated activities, in particular, are significantly reduced in swi1∆ cells. Although both swi1∆ and [SWI+] cells are similarly sensitive to thermal, osmotic and drought stresses, harmful, neutral or beneficial effects were observed for a panel of tested chemical stressors. Further analyses suggest that the environmental stress response (ESR) is mechanistically different between swi1∆ and [SWI+] cells—stress-inducible ESR (iESR) are repressed by [SWI+] but unchanged by swi1∆ while stress-repressible ESR (rESR) are induced by [SWI+] but repressed by swi1∆. Our work thus demonstrates primarily gain-of-function outcomes through transcriptomic modifications by [SWI+] and highlights a prion-mediated regulation of transcription and phenotypes in yeast.


2021 ◽  
Author(s):  
Mangaljeet Singh ◽  
Kirandeep Kaur ◽  
Avinash Sharma ◽  
Rajvir Kaur ◽  
Dimple Joshi ◽  
...  

Abstract Peptidyl-prolyl cis-trans isomerases (PPIases) are the only class of enzymes capable of cis-trans isomerization of the prolyl peptide bond. The PPIases, comprising of different families viz., cyclophilins, FK506-binding proteins (FKBPs), parvulins and protein phosphatase 2A phosphatase activators (PTPAs), play essential roles in different cellular processes. Though PPIase gene families have been characterized in different organisms, information regarding these proteins lacks in Penicillium species, which are commercially an important fungi group. In this study, we carried out genome-wide analysis of PPIases in different Penicillium spp. and investigated their regulation by salt stress in a halotolerant strain of Penicillium oxalicum. These analyses revealed that the number of genes encoding cyclophilins, FKBPs, parvulins and PTPAs in Penicillium spp. varies between 7-11, 2-5, 1-2, and 1-2, respectively. The halotolerant P. oxalicum depicted significant enhancement in the mycelial PPIase activity in the presence of 15% NaCl, thus, highlighting the role of these enzymes in salt stress adaptation. The PPIase activity in P. oxalicum was associated with the expression of PoxCYP18, PoxCYP23, PoxCYP41, PoxFKBP12-2, and PoxFKBP52 genes. Characterization of PPIases in Penicillium spp. will provide an important database for understanding their cellular functions and might facilitate their applications in industrial processes through biotechnological interventions.


2019 ◽  
Vol 20 (5) ◽  
pp. 1056 ◽  
Author(s):  
Pedro Robles ◽  
Víctor Quesada

Given their endosymbiotic origin, chloroplasts and mitochondria genomes harbor only between 100 and 200 genes that encode the proteins involved in organellar gene expression (OGE), photosynthesis, and the electron transport chain. However, as the activity of these organelles also needs a few thousand proteins encoded by the nuclear genome, a close coordination of the gene expression between the nucleus and organelles must exist. In line with this, OGE regulation is crucial for plant growth and development, and is achieved mainly through post-transcriptional mechanisms performed by nuclear genes. In this way, the nucleus controls the activity of organelles and these, in turn, transmit information about their functional state to the nucleus by modulating nuclear expression according to the organelles’ physiological requirements. This adjusts organelle function to plant physiological, developmental, or growth demands. Therefore, OGE must appropriately respond to both the endogenous signals and exogenous environmental cues that can jeopardize plant survival. As sessile organisms, plants have to respond to adverse conditions to acclimate and adapt to them. Salinity is a major abiotic stress that negatively affects plant development and growth, disrupts chloroplast and mitochondria function, and leads to reduced yields. Information on the effects that the disturbance of the OGE function has on plant tolerance to salinity is still quite fragmented. Nonetheless, many plant mutants which display altered responses to salinity have been characterized in recent years, and interestingly, several are affected in nuclear genes encoding organelle-localized proteins that regulate the expression of organelle genes. These results strongly support a link between OGE and plant salt tolerance, likely through retrograde signaling. Our review analyzes recent findings on the OGE functions required by plants to respond and tolerate salinity, and highlights the fundamental role that chloroplast and mitochondrion homeostasis plays in plant adaptation to salt stress.


2021 ◽  
Vol 9 (3) ◽  
pp. 485
Author(s):  
Ke Fan ◽  
Qiao Cao ◽  
Lefu Lan

BfmR is a response regulator that modulates diverse pathogenic phenotypes and induces an acute-to-chronic virulence switch in Pseudomonas aeruginosa, an important human pathogen causing serious nosocomial infections. However, the mechanisms of action of BfmR remain largely unknown. Here, using chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq), we showed that 174 chromosomal regions of P. aeruginosa MPAO1 genome were highly enriched by coimmunoprecipitation with a C-terminal Flag-tagged BfmR. Integration of these data with global transcriptome analyses revealed that 172 genes in 106 predicted transcription units are potential targets for BfmR. We determined that BfmR binds to and modulates the promoter activity of genes encoding transcriptional regulators CzcR, ExsA, and PhoB. Intriguingly, BfmR bound to the promoters of a number of genes belong to either CzcR or PhoB regulon, or both, indicating that CzcRS and PhoBR two-component systems (TCSs) deeply feed into the BfmR-mediated regulatory network. In addition, we demonstrated that phoB is required for BfmR to promote the biofilm formation by P. aeruginosa. These results delineate the direct BfmR regulon and exemplify the complexity of BfmR-mediated regulation of cellular functions in P. aeruginosa.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Mangaljeet Singh ◽  
Kirandeep Kaur ◽  
Avinash Sharma ◽  
Rajvir Kaur ◽  
Dimple Joshi ◽  
...  

AbstractPeptidyl-prolyl cis–trans isomerases (PPIases) are the only class of enzymes capable of cis–trans isomerization of the prolyl peptide bond. The PPIases, comprising of different families viz., cyclophilins, FK506-binding proteins (FKBPs), parvulins and protein phosphatase 2A phosphatase activators (PTPAs), play essential roles in different cellular processes. Though PPIase gene families have been characterized in different organisms, information regarding these proteins is lacking in Penicillium species, which are commercially an important fungi group. In this study, we carried out genome-wide analysis of PPIases in different Penicillium spp. and investigated their regulation by salt stress in a halotolerant strain of Penicillium oxalicum. These analyses revealed that the number of genes encoding cyclophilins, FKBPs, parvulins and PTPAs in Penicillium spp. varies between 7–11, 2–5, 1–2, and 1–2, respectively. The halotolerant P. oxalicum depicted significant enhancement in the mycelial PPIase activity in the presence of 15% NaCl, thus, highlighting the role of these enzymes in salt stress adaptation. The stress-induced increase in PPIase activity at 4 and 10 DAI in P. oxalicum was associated with higher expression of PoxCYP18. Characterization of PPIases in Penicillium spp. will provide an important database for understanding their cellular functions and might facilitate their applications in industrial processes through biotechnological interventions.


2021 ◽  
Vol 7 (12) ◽  
pp. eabe7520
Author(s):  
Priyanka Nandakumar ◽  
Chao Tian ◽  
Jared O’Connell ◽  
David Hinds ◽  
Andrew D. Paterson ◽  
...  

The role of the nuclear genome in maintaining the stability of the mitochondrial genome (mtDNA) is incompletely known. mtDNA sequence variants can exist in a state of heteroplasmy, which denotes the coexistence of organellar genomes with different sequences. Heteroplasmic variants that impair mitochondrial capacity cause disease, and the state of heteroplasmy itself is deleterious. However, mitochondrial heteroplasmy may provide an intermediate state in the emergence of novel mitochondrial haplogroups. We used genome-wide genotyping data from 982,072 European ancestry individuals to evaluate variation in mitochondrial heteroplasmy and to identify the regions of the nuclear genome that affect it. Age, sex, and mitochondrial haplogroup were associated with the extent of heteroplasmy. GWAS identified 20 loci for heteroplasmy that exceeded genome-wide significance. This included a region overlapping mitochondrial transcription factor A (TFAM), which has multiple roles in mtDNA packaging, replication, and transcription. These results show that mitochondrial heteroplasmy has a heritable nuclear component.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jiawei Zhou ◽  
Shuo Zhang ◽  
Jie Wang ◽  
Hongmei Shen ◽  
Bin Ai ◽  
...  

AbstractThe chloroplast is one of two organelles containing a separate genome that codes for essential and distinct cellular functions such as photosynthesis. Given the importance of chloroplasts in plant metabolism, the genomic architecture and gene content have been strongly conserved through long periods of time and as such are useful molecular tools for evolutionary inferences. At present, complete chloroplast genomes from over 4000 species have been deposited into publicly accessible databases. Despite the large number of complete chloroplast genomes, comprehensive analyses regarding genome architecture and gene content have not been conducted for many lineages with complete species sampling. In this study, we employed the genus Populus to assess how more comprehensively sampled chloroplast genome analyses can be used in understanding chloroplast evolution in a broadly studied lineage of angiosperms. We conducted comparative analyses across Populus in order to elucidate variation in key genome features such as genome size, gene number, gene content, repeat type and number, SSR (Simple Sequence Repeat) abundance, and boundary positioning between the four main units of the genome. We found that some genome annotations were variable across the genus owing in part from errors in assembly or data checking and from this provided corrected annotations. We also employed complete chloroplast genomes for phylogenetic analyses including the dating of divergence times throughout the genus. Lastly, we utilized re-sequencing data to describe the variations of pan-chloroplast genomes at the population level for P. euphratica. The analyses used in this paper provide a blueprint for the types of analyses that can be conducted with publicly available chloroplast genomes as well as methods for building upon existing datasets to improve evolutionary inference.


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