Relocation of genes generates non-conserved chromosomal segments in Fusarium graminearumthat show distinct and co-regulated gene expression patterns
© Zhao et al.; licensee BioMed Central Ltd. 2014
Received: 16 December 2013
Accepted: 7 March 2014
Published: 13 March 2014
Genome comparisons between closely related species often show non-conserved regions across chromosomes. Some of them are located in specific regions of chromosomes and some are even confined to one or more entire chromosomes. The origin and biological relevance of these non-conserved regions are still largely unknown. Here we used the genome of Fusarium graminearum to elucidate the significance of non-conserved regions.
The genome of F. graminearum harbours thirteen non-conserved regions dispersed over all of the four chromosomes. Using RNA-Seq data from the mycelium of F. graminearum, we found weakly expressed regions on all of the four chromosomes that exactly matched with non-conserved regions. Comparison of gene expression between two different developmental stages (conidia and mycelium) showed that the expression of genes in conserved regions is stable, while gene expression in non-conserved regions is much more influenced by developmental stage. In addition, genes involved in the production of secondary metabolites and secreted proteins are enriched in non-conserved regions, suggesting that these regions could also be important for adaptations to new environments, including adaptation to new hosts. Finally, we found evidence that non-conserved regions are generated by sequestration of genes from multiple locations. Gene relocations may lead to clustering of genes with similar expression patterns or similar biological functions, which was clearly exemplified by the PKS2 gene cluster.
Our results showed that chromosomes can be functionally divided into conserved and non-conserved regions, and both could have specific and distinct roles in genome evolution and regulation of gene expression.
KeywordsGene expression Non-conserved region Gene relocation Secondary metabolite gene cluster Fusarium graminearum
The genus Fusarium includes a large group of phytopathogenic fungi, each having a different or partially overlapping host range. F. graminearum is an important pathogen on wheat, barley and maize, causing Fusarium head blight [1, 2], while F. verticillioides mainly infects maize, causing rot and wilting . In contrast, F. oxysporum causes disease on more than 100 different plant species, but specific strains usually infect only a single host species . This has led to the introduction of the forma specialis concept in F. oxysporum, where strains are categorized according to the host plant they infect, such as tomato or banana . In addition, some strains of F. oxysporum may also cause infections in humans . Genomic sequences of several Fusarium species have been generated, including F. graminearum (strain PH-1), F. verticillioides (strain FGSC 7600), F. pseudograminearum (strain CS3096), F. solani (strain FGSC 9596), F. fujikuroi (strain IMI58289) and F. oxysporum f. sp. lycopersici strain 4287. In addition, 11 different F. oxysporum strains, including pathogens from different hosts as well as a biocontrol strain have been sequenced [7–11]. Genome comparisons showed that chromosome XII of F. fujikuroi is absent in the genome sequence of related species F. verticillioides, while 285 and 820 kb genome sequences at both ends of chromosome IV of F. verticillioides are absent in F. fujikuroi . Comparing the genome of F. pseudograminearum with F. graminearum showed that 89.8% of genomic sequence could be aligned at >70% nucleotide identity . Strikingly, F. oxysporum 4287 includes 11 core chromosomes and four lineage-specific (LS) chromosomes. LS chromosomes are specific to F. oxysporum strain 4287 and have no collinear chromosomes in either F. graminearum, F. verticillioides or other F. oxysporum strains. The LS chromosomes in F. oxysporum 4287 are suggested to have resulted from horizontal transfer from unknown sources . On LS chromosome 14, several effector-encoding genes have been identified that facilitate infection of its host plant [12–14].
In contrast to the high number of chromosomes present in F. verticillioides (11), F. oxysporum (15) and F. fujikuroi (12), F. graminearum has only four chromosomes, which probably resulted from fusions of ancestral chromosomes . Comparing the genome of F. graminearum isolate PH-1 with F. graminearum isolate GZ3639 revealed several regions with high SNP density . In addition, comparison of the genome of F. graminearum with the closely related species F. verticillioides and F. oxysporum revealed several non-conserved regions . Further analysis showed that high SNP density regions match with non-conserved regions. Although many of the genes specifically expressed during plant infection are enriched in non-conserved regions , the origin and the biological relevance for these non-conserved regions are still largely unknown. In this study, we explored RNA-Seq data from both conidia and mycelium of F. graminearum to investigate the putative effect of gene locations (in conserved or non-conserved regions) on their expression patterns. In addition, by comparing the genome of F. graminearum with those of F. verticillioides and F. oxysporum, we show a possible mechanism for the generation of non-conserved regions.
Synteny block analysis between the genomes of Fusarium graminearum, F. verticillioides and F. oxysporum.
Gene expression analysis on individual chromosomes of F. graminearum
Detailed analysis of chromosome regions with weakly expressed genes in F. graminearum
Low-expression regions coincide with non-conserved regions
Detailed inspection showed that regions with low levels of expression correspond to non-conserved regions of F. graminearum (confer lines B and C in Figure 3). This was further analyzed by comparing genes predicted in the genome of F. graminearum to all the genes in F. verticillioides using BLASTn (Additional file 4). For 9297 genes in F. graminearum, conserved genes were found in F. verticillioides (p value ≤ 1E-5), while for 4024 genes in F. graminearum, no conserved ortholog in F. verticillioides was identified (p value > 1E-5). When calculating the number of non-conserved genes in each 20 kb window, we found that non-conserved genes are more abundant in chromosomal regions, where genes are weakly expressed (Lines C in Figure 3). This indicates that the regions with weakly expressed genes coincide with the non-conserved regions in F. graminearum. In addition, genes that are not expressed in nutrient-rich medium are enriched in non-conserved regions (Lines D in Figure 3).
Expression of genes in non-conserved regions is highly variable in different developmental stages
Non-conserved regions are enriched for genes encoding secreted proteins and enzymes required for the production of secondary metabolites
Non-conserved regions are enriched for relocated genes
Number of genes on each chromosome of Fusarium graminearum that have orthologs on each chromosome of F. verticillioides
To understand whether genes that are relocated to non-conserved regions are also affected in expression, we compared the expression levels of relocated genes with non-relocated genes. This analysis indicated that expression of relocated genes was significantly lower than non-relocated genes under the conditions examined (confer A and B in Additional file 7).
Secondary metabolite gene clusters are assembled in non-conserved regions by gene relocations
Analysis of PKS2 secondary metabolite gene cluster
Orthologs in Fusarium verticillioides
Putative bile acid 7-alpha protein
Integral membrane protein PTH11
MFS monosaccharide transporter
NAD binding oxidoreductase
Cytochrome P450 family protein
RTA1 like protein
RTA1 domain-containing protein
C6 transcription factor
The origin of lineage-specific chromosomes in F. oxysporum
F. oxysporum f. sp. lycopercisi isolate 4287 contains eleven core chromosomes and four lineage-specific (LS) chromosomes . Comparison of core chromosomes of F. oxysporum with those of F. verticillioides through synteny analysis revealed several non-conserved regions (Additional file 1), especially at the end of chromosomes 1 and 2. To determine whether the four LS chromosomes and non-conserved regions on core chromosomes of F. oxysporum are enriched for gene relocations, we selected all genes of F. oxysporum with homologs on a non-collinear chromosome of F. verticillioides and assigned these genes to each chromosome of F. oxysporum. The four LS chromosomes appear to be enriched for genes that have relocated from core chromosomes (Additional file 8). Gene relocations were also supported by the observation that multiple groups of adjacent genes on LS chromosomes showed collinearity with their homologs on the chromosomes of F. verticillioides (Additional file 9). In addition, relocation of genes was also observed in non-conserved regions of core chromosomes of F. oxysporum, especially in one telomere proximal region of chromosomes 1 and 2. In addition, synteny block analysis of chromosomes in F. oxysporum was performed and we found that most of the genes present on LS chromosomes 3 and 6 are duplicated, which is consistent with previous findings . Some genes on LS chromosome 14 might originate from LS chromosomes 3 or 6. Interestingly, genes on LS chromosome 15 are duplicated from core chromosome 1 (Additional file 10), suggesting that LS chromosome 15 originally arose from core chromosome.
Genome comparison between closely related species may help us to understand the mechanism of genome evolution and apprehend how species evolve to adapt to new environments [18–20]. Comparing the genome of Homo sapiens with the closely related species chimpanzee showed that 98.76% of the genomic sequences are similar , but 1,576 putative inversions were identified on the chromosomes of H. sapiens  that are likely to be involved in genome evolution. Large-scale translocations and inversions appear to have also occurred in the ascomycete Saccharomyces cerevisiae [23, 24]. Here, we compared the genome of F. graminearum with that of two closely related species F. verticillioides and F. oxysporum. Again, a large number of translocations and inversions were identified. Next to these translocations and inversions of large chromosomal segments, non-conserved regions are commonly discovered in closely related species. For instance, synteny analysis of the genome of Aspergillus nidulans with related species A. fumigatus and A. oryzae showed that around 78% of the genome could be mapped to conserved syntenic blocks, while the remaining genomic sequences lack significant syntenic blocks . In addition, syntenic analysis of 12 sequenced Drosophila species showed that on average 66% of each genome was covered by syntenic blocks , indicating that the location of the remaining 34% of the genome is not conserved. Comparing the genome of F. graminearum with those of F. verticillioides and F. oxysporum, thirteen non-conserved regions were identified. The presence of these non-conserved regions suggests that genome evolution has occurred unevenly across the chromosomes. Although non-conserved regions frequently occur in the genomes of many species, their origin and biological relevance are still largely unknown.
The development of RNA-Seq technology  allowed us to evaluate the global gene expression patterns along chromosomes [28, 29]. In this study, we used RNA-Seq data obtained from the mycelium of the sequenced isolate PH-1 of F. graminearum grown in nutrient-rich medium to investigate the gene expression pattern along whole chromosomes. Interestingly, we found two striking features in F. graminearum: (i) there is a strong correlation between the degree of gene conservation and gene expression level and (ii) genes in the non-conserved regions showed lower expression levels than genes in the conserved regions. In addition, comparing gene expression levels between conidia and mycelium, we found that the expression of genes in non-conserved regions is highly variable, while the expressions of genes in conserved regions is surprisingly stable. This indicates the expression of genes in conserved regions is less dependent on fungal development (e.g. in conidia vs. mycelium), while the expression of genes in non-conserved regions seems more developmentally regulated. Furthermore, house-keeping genes are more abundant in conserved regions, while genes required in specific developmental stages or environmental conditions are found more often in non-conserved regions. This conclusion was supported by the fact that genes encoding secreted proteins or involved in the production of secondary metabolites, which are induced under specific conditions [8, 30–32], are more abundant in non-conserved regions, while ribosomal genes are mainly located in conserved regions.
Gene enrichment in specific chromosomal regions has also been studied in other species. For instance, secondary metabolite genes are enriched in subtelomeric regions of Aspergillus species. The rapid rearrangement of subtelomeric regions may promote the rapid evolution of these genes to become species-specific attributes [25, 33]. In the plant pathogenic fungus Verticillium dahliae, in planta-expressed genes are enriched in lineage-specific genomic regions that have developed by extensive chromosomal reshuffling, which was suggested to drive evolution of virulence . In F. oxysporum, genes encoding secreted effectors and virulence factors are more abundant in LS chromosomes, while few house-keeping genes are identified on LS chromosomes . The drivers and biological relevance of gene enrichment in specific chromosome regions are still not fully understood. One possible reason could be that clustering of genes with similar expression patterns may facilitate co-regulation of specific sets of genes under specific conditions or developmental stages. This phenomenon has been observed in many species, such as yeast, mouse and human [35–38]. Secondly, changes in gene expression levels have also been shown to be important in adaptive evolution [39, 40], so perhaps enrichment of genes in non-conserved regions could facilitate them to rapidly change their expression pattern.
Our data indicate that genes in non-conserved regions are weakly expressed, but how the expression of these genes is suppressed is still unknown. Previous studies have shown that gene position in the nucleus is associated with their transcriptional regulation, for instance, the nuclear periphery was considered as a zone for transcriptionally repressed genes . This type of organization could also occur in F. graminearum and non-conserved regions could form specific sub-compartments of the nucleus with repressed gene expression.
The non-conserved regions occur widely, but how they are generated is still unclear. In this study, many gene relocations were identified in non-conserved regions of F. graminearum, in contrast to conserved regions. Gene relocations have been described previously in S. cerevisiae where the DAL gene cluster, including six genes, was formed by gene relocations from six different loci . In F. graminearum and F. sporotrichioides, trichothecene biosynthesis requires genes at three loci: the 12-gene TRI cluster, a second locus with two genes (TR1 and TRI16), and a third locus with one gene (TRI101). However, in the more distantly related species F. equiseti, both TRI1 and TRI101 are located within the TRI core cluster suggesting that the latter two genes have been relocated during evolution of F. equiseti . We also showed that four successive genes were relocated to a non-conserved region in F. graminearum. However, how these genes are marked for relocation is still obscure. Based on our findings that genes with low similarity to their homologs have low expression levels (refer to Figure 4C), we hypothesize that the relocated genes in non-conserved chromosome regions already had a low expression level before they were relocated. Possibly, in the three dimensional organization of chromosomes in the interphase these weakly expressed genes are in close proximity with the likewise weakly expressed non-conserved regions. Such a close proximity might facilitate targeted relocation of weakly expressed genes to one of these non-conserved regions.
In F. oxysporum, four LS chromosomes and 11 core chromosomes were identified. It was suggested that these four LS chromosomes were generated by horizontal transfer from a yet unknown fungal source . Also for the dispensable chromosomes in Zymoseptoria tritici horizontal gene transfer was hypothesized . Although horizontal gene transfer is one of the reasonable explanations for the origin of LS chromosomes in F. oxysporum , other mechanisms or events could also contribute to the formation of LS regions. In this study, the frequent gene relocations identified in non-conserved regions of F. graminearum drove us to hypothesize that the generation of LS chromosomes in F. oxysporum could also have included extensive gene relocations. This hypothesis was supported by the fact that around 700 genes on LS chromosomes have a homolog in F. verticillioides, and in 22 cases, two or more adjacent genes are collinear with their homologs. In addition, large part of LS chromosome 15 represents a duplication of the telomere proximal region of core chromosome 1, suggesting that it might originate from the core chromosome. Based on the studies by us and others , we proposed that most likely horizontal gene transfer from other fungal species and gene relocations within the species both occurred in F. oxysporum.
Taken together, our data demonstrate that chromosomes of F. graminearum show distinct conserved and non-conserved regions. Subsequent gene expression analysis showed that genes in these regions exhibit different expression patterns. Genes showing high and stable expression levels are more abundant in conserved regions, while genes that are induced or repressed in specific developmental stages or under different environmental conditions (mung bean medium versus liquid CM) are significantly abundant in non-conserved regions. This type of genome arrangement may not only facilitate the co-regulation of specific sets of genes, but could also enable fungi to maintain on the one hand the required conservation of house-keeping genes and on the other to accelerate the evolution of species-specific genes to rapidly adapt to new environments or new hosts. Moreover, due to the selective transcription of genes in non-conserved regions, this could prevent organisms spending too much energy in transcription and translation of evolving genes that do not have acquired full functionality yet.
RNA isolation and RNA-Seq
Fusarium graminearum wild-type isolate PH-1 was used in this study. To prepare conidia and mycelium for RNA isolation, PH-1 was grown in 400 ml liquid mung bean medium for 3 days to produce conidia (25°C, 200 rpm). The conidia were collected by centrifugation. 10e5 conidia of PH-1 were transferred to 400 ml liquid complete medium and subsequently incubated for 30 h to produce mycelium (25°C, 200 rpm). Mycelium was harvested from liquid CM medium by filtration and grounded in liquid nitrogen using a mortar and pestle. The conidia and mycelium were used for RNA extraction using TRIzol reagent (Invitrogen, Cat. No. 15596–018) according to manufacturer’s instructions. The quality of RNA was analyzed by Agilent 2100. RNA-Seq was performed according to protocols described previously .
Analysis of gene homology
Gene homology was evaluated in CLC genomic workbench. The gene database of F. graminearum, F. verticillioides and F. oxysporum were downloaded from Broad Fusarium Comparative Database. The gene database (fasta file format) of each Fusarium species were imported into CLC, and “BLASTn” option was used to align the genes of F. graminearum against the genes of F. verticillioides or F. oxysporum using default settings. Genes of F. graminearum were grouped according to their p value after aligning with the genes of F. verticillioides by using BLASTn.
The identification of orthologs between Fusarium species was based on two criteria: (i) a cutoff of p value of 1E-5, and (ii) reciprocal best blast hits. For the genes in conserved chromosomal regions, synteny block analysis was also explored for the definition of orthologous relationship.
Synteny block analysis
Synteny block analysis was performed according to the program MCScanX with a small modification . The gene data sets (fasta format file) of F. graminearum, F. verticillioides and F. oxysporum were downloaded from the Broad Fusarium database. The local blast database pools of F. verticillioides and F. oxysporum were created by using program formatdb. All genes in F. graminearum were analyzed against the gene database pool of F. verticillioides and F. oxysporum, respectively, by using BLAST tool. The BLAST results were exported in m8 format. Besides, gff file containing the information of the chromosome number (e.g. Fg1), gene name (e.g. FGSG_00001), start position and stop position of each gene on each chromosome of Fusarium species was prepared. The BLAST file and gff file were imported for synteny block analysis according to the procedure described in the manual of MCScanX. The criteria for the synteny analysis are as follow: match score 50, match size > 5, gap_penalty −1, overlap_window 5, max gaps 25. Finally, two types of output (dual synteny plot and circle plot) were obtained by using two downstream programs.
Analysis of relocated genes
According to the BLASTn result, all F. graminearum genes with high similarity (p value ≤ 1E-5) in F. verticillioides or F. oxysporum were collected, from which we selected genes that have their putative orthologs on non-collinear chromosomes of F. verticillioides or F. oxysporum. The map of these genes to their orthologs was performed by using MCScanX software . Furthermore, the sequences of all these putative orthologs from either F. verticillioides or F. oxysporum were collected and matched with all predicated genes in F. graminearum using BLASTn tool to identify the best hits to show that they are the bidirectional best hits.
Gene expression analysis
To evaluate gene expression along chromosomes, RNA-Seq reads were mapped to chromosome sequences of F. graminearum using software available in the CLC Genomics Workbench. The RNA-Seq reads were mapped to each chromosome by using “RNA-Seq analysis” option with default settings. The number of reads matched to each chromosome was calculated and subsequently the expression level of each chromosome was evaluated by using RPKM (reads per kilobase per million mapped reads) values. Similarly, to evaluate the expression of each gene, the transcript database of F. graminearum were imported in CLC and the expression level of each gene was evaluated by RPKM value.
To draw the gene expression level along each chromosome, we divided the chromosomes into portions of 20 kb. The read coverage of each 20 kb window was calculated and log2-transformed reads coverage in each window was used to compare gene expression levels. To compare the gene expression level between conidia and mycelium, reads coverage of each window was compared and log2-transformed reads coverage fold change was used to evaluate gene expression differences. The total gene number and the number of non-conserved genes in each 20 kb window were calculated manually based on the criteria described above.
To analyze the expression levels of conserved and non-conserved genes, the transcript sequences of conserved and non-conserved genes were collected and assembled, respectively. Also in this case the PRKM value was used to evaluate the expression levels of conserved and non-conserved genes. Box plot analysis of gene expression was performed by using SPSS software.
Availability of supporting data
The data sets supporting the results of this article are included within the article and its additional files. Six Illumina sequence data used in this study are available in the NCBI GEO repository (accession number GSE55477, http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE55477).
Reads per kilobase per million mapped reads
Single nucleotide polymorphism.
This work was supported by grants from the National Basic Research Program of China (2011CB100700) and Chinese Academy of Sciences (SAJC201305). P. J. G. M. de Wit is supported by grants from the Royal Netherlands Academy of Arts and Sciences, the Centre for BioSystems Genomics. We would like to thank Dr. Jan-Peter Nap (Applied Bioinformatics PRT WUR) for stimulating discussion.
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