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SCIENCE CHINA Life Sciences, Volume 62, Issue 4: 498-506(2019) https://doi.org/10.1007/s11427-018-9450-1

Complete loss of RNA editing from the plastid genome and most highly expressed mitochondrial genes of Welwitschia mirabilis

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  • ReceivedSep 10, 2018
  • AcceptedOct 2, 2018
  • PublishedMar 7, 2019

Abstract

Comparative genomics among gymnosperms suggested extensive loss of mitochondrial RNA editing sites from Welwitschia mirabilis based on predictive analysis. However, empirical or transcriptome data to confirm this massive loss event are lacking, and the potential mechanisms of RNA site loss are unclear. By comparing genomic sequences with transcriptomic and reverse-transcription PCR sequencing data, we performed a comprehensive analysis of the pattern of RNA editing in the mitochondrial and plastid genomes (mitogenome and plastome, respectively) of W. mirabilis and a second gymnosperm, Ginkgo biloba. For W. mirabilis, we found only 99 editing sites located in 13 protein-coding genes in the mitogenome and a complete loss of RNA editing from the plastome. The few genes having high editing frequency in the Welwitschia mitogenome showed a strong negative correlation with gene expression level. Comparative analyses with G. biloba, containing 1,405 mitochondrial and 345 plastid editing sites, revealed that the editing loss from W. mirabilis is mainly due to the substitution of editable cytidines to thymidines at the genomic level, which could be caused by retroprocessing. Our result is the first study to uncover massive editing loss from both the mitogenome and plastome in a single genus. Furthermore, our results suggest that gene expression level and retroprocessing both contributed to the evolution of RNA editing in plant organellar genomes.


Funded by

the National Natural Science Foundation of China(31801051,to,WF)

by the Large-scale Scientific Facilities of the Chinese Academy of Sciences(2017-LSF-GBOWS-02)

by CAS Pioneer Hundred Talents Program(to,AZ)


Acknowledgment

We thank Amy Hilske and Samantha Link for care of Welwitschia plants in the Beadle Center greenhouse. This research was supported by the National Natural Science Foundation of China (31801051 to WF), by the Large-scale Scientific Facilities of the Chinese Academy of Sciences (2017-LSF-GBOWS-02) and by CAS Pioneer Hundred Talents Program (to AZ).


Interest statement

The author(s) declare that they have no conflict of interest.


Supplement

SUPPORTING INFORMATION

Figure S1ƒRNA-Seq read coverages for mitogenome and plastome.

Figure S2ƒEditable site substitution pattern in the Welwitschia plastome.

Table S1ƒRNA editing sites distribution in Welwitschia mitogenome

Table S2ƒRT-PCR validation of Welwitschia mitogenes

Table S3ƒRNA editing sites distribution in Ginkgo mitogenome and plastome

Table S4ƒGene specific primers for Welwitschia mitochondrial genes

The supporting information is available online at http://life.scichina.com and http://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.


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  • Figure 1

    RNA editing site distribution in 29 shared protein-coding genes in Welwitschia and Ginkgo mitogenomes. Vertical lines indicate RNA editing sites and horizontal lines represent gene length. Selected gene names are shown on the right and the length bar shown at the bottom.

  • Figure 2

    Comparative evolutionary analysis of editing sites in Welwitschia and Ginkgo mitochondrial genes. A, Venn diagram depicts the numbers of conserved and unique editing sites. B, State of the unique Ginkgo editing sites in Welwitschia and the unique Welwitschia editing sites in Ginkgo. The relative frequency of retaining cytosine (C-C) and thymidine (C-T) and others (C-R, R=A, G) substitutions are shown.

  • Figure 3

    The relationship between gene expression level and editing frequency in the Welwitschia mitogenome. Triangles represent protein-coding genes. The shade area represents the 95% confidence interval.

  • Table 1   Summary of and mitogene editing sites

    Gene

    Ginkgo

    Welwitschia

    Length

    Editing number

    Frequency

    Length

    Editing number

    Frequency

    ATP synthase F1subunits

    atp1

    1,527

    23

    0.0151

    1,569

    0

    0

    atp4

    594

    27

    0.0455

    594

    0

    0

    atp6

    768

    63

    0.0820

    768

    0

    0

    atp8

    489

    19

    0.0389

    510

    0

    0

    atp9

    225

    21

    0.0933

    225

    0

    0

    Subtotal

    3,603

    153

    0.0425

    3,666

    0

    0

    Cytochrome cbiogenesis

    ccmB

    639

    21

    0.0329

    636

    19

    0.0299

    ccmC

    711

    45

    0.0633

    741

    3

    0.0040

    ccmFc

    1,386

    14

    0.0101

    1,566

    11

    0.0070

    ccmFn

    1,815

    35

    0.0193

    1,893

    0

    0

    Subtotal

    4,551

    115

    0.0253

    4,836

    33

    0.0068

    Cytochrome b

    cob

    1,197

    3

    0.0025

    1,143

    0

    0

    Subtotal

    1,197

    3

    0.0025

    1,143

    0

    0

    Cytochrome c oxidase subunits

    cox1

    1,563

    3

    0.0019

    1,572

    0

    0

    cox2

    765

    27

    0.0353

    801

    0

    0

    cox3

    798

    46

    0.0576

    801

    0

    0

    Subtotal

    3,126

    76

    0.0243

    3,174

    0

    0

    Other proteins

    matR

    2,034

    31

    0.0152

    2,676

    14

    0.0052

    mttB

    780

    37

    0.0474

    798

    10

    0.0125

    Subtotal

    2,814

    68

    0.0242

    3,474

    24

    0.0069

    NADH dehydrogenase subunits

    nad1

    978

    38

    0.0389

    981

    2

    0.0020

    nad2

    1,473

    57

    0.0387

    1,479

    0

    0

    nad3

    357

    7

    0.0196

    351

    0

    0

    nad4

    1,488

    103

    0.0692

    1,488

    1

    0.0007

    nad4L

    303

    20

    0.0660

    372

    0

    0

    nad5

    2,004

    114

    0.0569

    2,070

    2

    0.0010

    nad6

    606

    47

    0.0776

    636

    22

    0.0346

    nad7

    1,185

    45

    0.0380

    1,185

    9

    0.0076

    nad9

    594

    25

    0.0421

    612

    0

    0

    Subtotal

    8,988

    456

    0.0507

    9,174

    36

    0.0039

    Large ribosomal proteins

    rpl2

    1,440

    13

    0.0090

    rpl5

    570

    17

    0.0298

    rpl10

    483

    12

    0.0248

    549

    1

    0.0018

    rpl16

    411

    11

    0.0268

    Subtotal

    2,904

    53

    0.0183

    549

    1

    0.0018

    Small ribosomal proteins

    rps1

    594

    27

    0.0455

    rps2

    696

    9

    0.0129

    rps3

    1,737

    33

    0.0190

    1,704

    1

    0.0006

    rps4

    1,041

    47

    0.0451

    615

    4

    0.0065

    rps7

    621

    18

    0.0290

    rps10

    324

    2

    0.0062

    rps11

    519

    19

    0.0366

    rps12

    372

    18

    0.0484

    369

    0

    0

    rps13

    381

    2

    0.0052

    rps14

    303

    11

    0.0363

    rps19

    282

    13

    0.0461

    Subtotal

    6,870

    199

    0.0290

    2,688

    5

    0.0019

    Complex II

    sdh3

    402

    23

    0.0572

    sdh4

    396

    16

    0.0404

    426

    0

    0

    Subtotal

    798

    39

    0.0489

    426

    0

    0

    Total

     

    34,851

    1,162

    0.0333

    29,130

    99

    0.0034

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