PMC:4502367 / 31201-44755 JSONTXT

{"target":"http://pubannotation.org/docs/sourcedb/PMC/sourceid/4502367","sourcedb":"PMC","sourceid":"4502367","source_url":"https://www.ncbi.nlm.nih.gov/pmc/4502367","text":"Transposable element annotation\n\nTEs in Z. tritici:\nOf the 39.7-Mb genome assembly of Z. tritici IPO323, 7.4 Mb (18.6%) (Table 2) were found to be repetitive DNA, in agreement with the recently reported repeat content of IPO323 (\u003e17%) in Dhillon et al. (2014). Repeats were classified into TE families based on features such as terminal repeats, protein domains, and homology with known TE available in the Repbase Update database (Jurka et al. 2005). The fact that the assembled genome of Z. tritici consists of complete chromosomes allowed a high-quality repeat annotation with only few uncategorized families. TEs of class I (retrotransposons) are the most abundant in the IPO323 genome and represent 13.1% of the total genome size (5.2 Mb), whereas TEs of class II (DNA transposons) represent 4.2% (1.6 Mb) (Table 2). The remaining repetitive sequences represent 0.5 Mb and could not be associated with classified TEs. From the 111 consensus sequences obtained by our procedure (see Materials and Methods), we identified 101 families of TEs. The majority of these families belong to the class II (62 families), mainly represented by TIRs (44 families), MITEs (11 families), and Helitron (4 families). Although present in a lower number (32 families), class I elements represent 71% of the repetitive fraction of the genome. The most abundant group of class I elements is the LTR elements from the Gypsy superfamily (14 families), followed by those of the Copia superfamily (12 families) and LINEs (7 families) (Table 2). Interestingly, we also identified one family of a complete tyrosine-recombinase retrotransposon that belongs to the Ngaro superfamily and that otherwise has been described to be absent in Ascomycota (Muszewska et al. 2013). Distinguishing core and accessory chromosomes of Z. tritici, we find that repetitive DNA represents 16.6% of the core chromosomes and 33.6% of the accessory chromosomes (Figure 2A). However, the relative distribution of the major TE families on core and accessory chromosomes does not differ significantly (Wilcoxon test, P = 0.3692) (Figure 2B).\nTable 2 Transposable element content in genomes of the Zymoseptoria species complex\nZ. tritici Z. pseudotritici Z. ardabiliae Z. brevis\nFamily No. DNA Amount (kb) % of Genome Family No. DNA Amount (kb) % of Genome Family No. DNA Amount (kb) % of Genome Family No. DNA Amount (kb) % of Genome\nClass I (retrotransposons)\nLTR RLC 12 1017 2.56 6 90 0.23 5 232 0.62 7 827 2.08\nRLG 14 2649 6.67 17 2906 7.50 16 1074 2.88 18 3616 9.09\nLINE RII 4 737 1.86 0 0 0.00 3 76 0.20 4 547 1.38\nRIL 2 747 1.88 0 0 0.00 1 32 0.09 0 0 0.00\nRIX 1 5 0.01 1 83 0.22 1 67 0.18 1 193 0.48\nDIRS RYN 1 23 0.06 0 0 0.00 0 0 0.00 0 0 0.00\nSINE RSX 1 1 0.00 0 0 0.00 0 0 0.00 0 0 0.00\nTRIM RLX-TRIM 4 35 0.09 0 0 0.00 0 0 0.00 1 4 0.01\nSub-total class I 39 5214 13.14 24 3080 7.94 26 1481 3.97 31 5186 13.04\nClass II (DNA transposons)\nTIR DTT 14 246 0.62 3 51 0.13 4 29 0.08 9 254 0.64\nDTA 7 150 0.38 1 35 0.09 1 4 0.01 5 175 0.44\nDTH 10 184 0.46 0 0 0.00 0 0 0.00 11 292 0.74\nDTM 7 145 0.36 1 44 0.11 0 0 0.00 4 213 0.54\nDTX 6 364 0.92 6 432 1.11 5 76 0.20 3 315 0.79\nUnknown DXX 2 40 0.10 0 0 0.00 0 0 0.00 0 0 0.00\nCrypton DYX 1 6 0.02 0 0 0.00 0 0 0.00 0 0 0.00\nHelitron DHH 4 470 1.18 7 357 0.92 1 39 0.10 5 391 0.98\nMaverick DMM 0 0 0.00 2 476 1.23 0 0 0.00 0 0 0.00\nMITE DTX-MITE 11 48 0.12 1 2 0.01 1 5 0.01 3 11 0.03\nSub-total class II 62 1653 4.17 21 1399 3.61 12 153 0.41 40 1652 4.15\nUncategorized repeats\nNoCat NoCat 10 516 1.30 60 1518 3.92 79 1303 3.49 93 2634 6.62\nTotal 111 7383 18.60 105 5997 15.47 117 2937 7.87 164 9472 23.87\nFigure 2 Transposable elements (TEs) characteristics along the 21 chromosomes of Zymoseptoria tritici. (A) Proportions of TEs in the chromosomes of Z. tritici. The red dashed lines show the mean values of TEs on core (1–13) and accessory chromosomes (14–21). (B) The distribution of five major TE classes across core and accessory chromosomes in Z. tritici show a more or less similar distribution and frequency on the two types of chromosomes. As already described by Goodwin et al. (2011), repetitive sequences are highly affected by the fungal-specific repeat inactivation mechanism known as repeat-induced point mutations (RIP) (Galagan and Selker 2004). Multiple alignments of several family copies analyzed by RIPCAL (Hane and Oliver 2008) showed an excess of CpA→TpA and TpG→TpA mutations. As hypothesized by Goodwin et al. (2011), these mutations should prevent TEs from expressing their own machinery. However, it appears that 98 predicted gene models overlap TE sequences with at least 50% of their length, including 75 genes models that are completely embedded in repetitive DNA. Of the 98 corresponding proteins, 33 harbor domains associated with TEs such as reverse-transcriptase, transposase, or integrase (Table 3). These domains belong to 22 distinct TE families, including 12 TIR, eight LTR, one LINE, and one uncategorized element. Comparison of these gene models with the reconstructed transcripts showed that 48% have RNA-seq support; this suggests that TE families (mainly class II DNA transposons) are still active in the Z. tritici genome despite the RIP machinery.\nTable 3 Gene models with protein domains associated with transposable elements\nProtein ID Length (aa) Domain Name Domain Description Interpro or Pfam Accession No. Overlapping Repeat Family RNA-seq Support\nZt09_chr_1_00001 143 RVT_1 Reverse-transcriptase (RNA-dependent DNA polymerase) PF00078 RIL_element2_ZTIPO323 —\nZt09_chr_1_00017 272 DDE_Tnp_4 DDE superfamily endonuclease PF13359 DTH_element5_ZTIPO323 —\nZt09_chr_1_01076 477 DDE_3 DDE superfamily endonuclease PF13358 DTT_element10_ZTIPO323 Yes\nZt09_chr_2_00093 477 DDE_3 DDE superfamily endonuclease PF13358 DTT_element10_ZTIPO323 —\nZt09_chr_2_00258 409 DDE_Tnp_1_7 Transposase IS4 PF13843 DTX_element1_ZPST04IR55 Yes\nZt09_chr_2_00383 648 DDE_1 DDE superfamily endonuclease PF03184 DTT_element1_ZTIPO323 Yes\nZt09_chr_2_00481 532 Chromo Chromo (CHRromatin Organization MOdifier) domain PF00385 RLG_element5_ZPST04IR55 —\nZt09_chr_2_00619 272 RVT_2 Reverse-transcriptase (RNA-dependent DNA polymerase) PF07727 RLC_element3_ZTIPO323 —\nZt09_chr_2_00906 219 DDE_1 DDE superfamily endonuclease PF03184 DTT_element5_ZTIPO323 Yes\nZt09_chr_2_00907 269 DDE_1 DDE superfamily endonuclease PF03184 DTT_element5_ZTIPO323 Yes\nZt09_chr_3_00204 734 RNaseH-like_dom Ribonuclease H-like domain IPR012337 DTA_element2_ZTIPO323 Yes\nZt09_chr_3_00229 349 DDE_3 DDE superfamily endonuclease PF13358 DTT_element14_ZTIPO323 Yes\nZt09_chr_4_00051 195 DDE_3 DDE superfamily endonuclease PF13358 DTT_element4_ZB163 —\nZt09_chr_4_00288 371 RNaseH-like_dom Ribonuclease H-like domain IPR012337 DTA_element3_ZTIPO323 Yes\nZt09_chr_5_00137 477 DDE_3 DDE superfamily endonuclease PF13358 DTT_element10_ZTIPO323 Yes\nZt09_chr_7_00478 338 RNaseH-like_dom Ribonuclease H-like domain IPR012337 DTA_element6_ZTIPO323 Yes\nZt09_chr_7_00479 108 RNaseH-like_dom Ribonuclease H-like domain IPR012337 DTA_element6_ZTIPO323 Yes\nZt09_chr_9_00003 1506 RVT_1 Reverse-transcriptase (RNA-dependent DNA polymerase) PF00078 RIL_element2_ZTIPO323 —\nZt09_chr_9_00154 621 DDE_1 DDE superfamily endonuclease PF03184 DTT_element1_ZTIPO323 Yes\nZt09_chr_9_00557 1061 rve Integrase core domain PF00665 RLC_element7_ZTIPO323 Yes\nZt09_chr_9_00615 458 DDE_Tnp_1_7 Transposase IS4 PF13843 DTX_element1_ZAST11IR611 Yes\nZt09_chr_10_00001 218 RVT_2 Reverse-transcriptase (RNA-dependent DNA polymerase) PF07727 RLC_element7_ZTIPO323 —\nZt09_chr_11_00364 162 Chromo Chromo (CHRromatin Organization MOdifier) domain PF00385 RLG_element7_ZPST04IR55 —\nZt09_chr_13_00054 869 DDE_3 DDE superfamily endonuclease PF13358 DTT_element10_ZTIPO323 Yes\nZt09_chr_13_00057 150 RVT_2 Reverse-transcriptase (RNA-dependent DNA polymerase) PF07727 RLC_element2_ZTIPO323 —\nZt09_chr_13_00271 480 RNaseH-like_dom Ribonuclease H-like domain IPR012337 DTA_element1_ZTIPO323 Yes\nZt09_chr_17_00004 876 RVT_1 Reverse-transcriptase (RNA-dependent DNA polymerase) PF00078 RIL_element2_ZTIPO323 —\nZt09_chr_17_00088 523 RVT_1 Reverse-transcriptase (RNA-dependent DNA polymerase) PF00078 RIL_element2_ZTIPO323 —\nZt09_chr_18_00008 750 RNaseH-like_dom Ribonuclease H-like domain IPR012337 NoCat_element60_ZAST11IR611 —\nZt09_chr_19_00003 169 RVT_2 Reverse-transcriptase (RNA-dependent DNA polymerase) PF07727 RLC_element5_ZTIPO323 —\nZt09_chr_19_00040 947 RVT_2 Reverse-transcriptase (RNA-dependent DNA polymerase) PF07727 RLC_element9_ZTIPO323 —\nZt09_chr_19_00041 107 UBN2_3 gag-polypeptide of LTR copia-type PF14244 RLC_element9_ZTIPO323 —\nZt09_chr_21_00003 1609 RVT_1 Reverse-transcriptase (RNA-dependent DNA polymerase) PF00078 RLG_element9_ZTIPO323 —\n\nTEs in Z. pseudotritici, Z. ardabiliae, and Z. brevis:\nTo improve the repeat annotation of Z. pseudotritici, Z. ardabiliae, and Z. brevis, we generated improved assemblies of Illumina-sequenced genomes of the isolates: ST04IR55 of Z. pseudotritici, ST11IR611 of Z. ardabiliae, and Zb163 of Z. brevis. The assembly sizes were 38.8 Mb, 37.3 Mb, and 39.8 Mb, respectively, compared to the 39.7 Mb genome assembly of Z. tritici.\nThe three genomes reflect different extents of repeat invasion: repetitive DNA comprises 7.9% of the Z. ardabiliae genome, 15.5% of the Z. pseudotritici genome, and 23.9% of the Z. brevis genome, including a total of 117, 105, and 164 repeat families identified in the genomes, respectively (Table 2). As a result of the fragmented assemblies, the number of uncategorized repeat families in the Z. pseudotritici, Z. ardabiliae, and Z. brevis genomes represent more than 50% of all the families and between 25% and 44% of the repetitive fraction. In contrast, the number of uncategorized families in the Z. tritici genome represents only 9% of the families and 7% of the repetitive fraction. Nevertheless, it was possible to classify some TE families of Z. pseudotritici, Z. ardabiliae, and Z. brevis and to record general patterns of TE distribution among the three genomes. As in the Z. tritici genome, class I TEs that are mainly represented by LTR-Gypsy elements are most abundant and account for 51–55% of the total repetitive fraction (Table 2). LINE elements are hardly represented in the Z. pseudotritici, Z. ardabiliae, and Z. brevis assemblies; however, this may be an artifact of the fragmented assemblies. In Z. pseudotritici and Z. brevis, class II TEs are mainly composed of TIRs that represent approximately 20% of the repetitive fraction similar to class II TEs in Z. tritici. Helitron elements were also identified in Z. pseudotritici, Z. ardabiliae, and Z. brevis; however, they accounted for only 1–6% of the repetitive fraction compared to 6.4% in Z. tritici. Maverick elements (Pritham et al. 2007) were only identified in Z. pseudotritici and were the third most represented TE family in the genome (Table 2). The unique presence and distribution of Maverick elements in Z. pseudotritici could result from a recent invasion of the genome followed by massive waves of transposition of these elements.\n\nThe complete repertoire of repeats in Zymoseptoria spp:\nIn total, we found 497 repeat families in the four Zymoseptoria species, including 120 families of class I TEs (24.1%), 135 families of class II TEs (27.2%), and 242 uncategorized families (48.7%). We could improve the TE annotation using the complete Zymoseptoria TE library generated here. We found 19.9% of repeats (+1.3%) in the genome of Z. tritici, 17.6% (+2.2%) in the genome of Z. pseudotritici, 12.7% (+4.8%) in the genome of Z. ardabiliae, and 25.2% (+1.3%) in the genome of Z. brevis.\nAddressing TE evolution in the Zymoseptoria genomes, we found that some families identified independently in each species were derived from a common ancestral TE family. An analysis of the 497 families was performed using Blastclust (Altschul et al. 1990) with a coverage cut-off of 50% and an identity percentage cut-off of 80%; this resulted in the clustering of 76 families into 34 larger groups (Table S2). Fourteen of these groups were composed of TIR elements, eight groups of LTR-Gypsy elements, six groups of uncategorized elements, three groups of LTR-Copia elements, two groups of Helitrons, and one group of LINE elements. Only one of these groups included TE families present in each of the four species; this suggests that this element, an LTR-Gypsy element, was present in the genome of the common ancestor of the four species (Table S2). Interestingly, this element may have expanded prior to the divergence of species because we observed a comparable size expansion in the four species comprising between 120 and 180 kb in each genome. Given the phylogenetic tree of the four Zymoseptoria species, as shown in Stukenbrock et al. (2012), the other TE groups were distributed in either two or three species with eight different ancestral relationships (Table S2). This analysis mainly showed that these species have undergone events of invasion and expansion of distinct TEs after their 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