A New Double-Stranded RNA Mycovirus in Cryphonectria naterciae Is Able to Cross the Species Barrier and Is Deleterious to a New Host
<p>Collection sites and <span class="html-italic">in plant</span> habit of <span class="html-italic">Cryphonectria naterciae</span>. (<b>A</b>) Map section of western–central Europe (framed) and magnification of Portugal (gray). Shown are the collection sites of the three specimens analyzed by RNA-seq. (<b>B</b>) Removal of the cork bark (asterisk) revealed beneath the yellow to orange mycelium of <span class="html-italic">C. naterciae</span>. (<b>C</b>) Small stem segment of the European chestnut inoculated with an agar plug of <span class="html-italic">C. naterciae</span>, showing yellow mycelium breaking through the bark.</p> "> Figure 2
<p>Characterization of dsRNA extracted from <span class="html-italic">Cryphonectria naterciae</span>. (<b>A</b>) Agarose gel electrophoresis of dsRNA used for RNA-seq before (left) and after (right) DNase and S1 nuclease treatment. ZR1: 10, 5, 3 kb; ZR2: 20, 7, 4, 2.5 kb, Thermo Scientific ZipRuler Express DNA Ladder Set (SM1373). (<b>B</b>) Unrooted neighbor joining tree of a 958 nt alignment including concatenated sequences of ORF1 and ORF2. Bold labels highlight strains associated with <span class="html-italic">C. naterciae</span> from <span class="html-italic">Quercus suber</span>; others are from <span class="html-italic">Castanea sativa</span>. Numbers represent bootstrapping rate of 1000 replicates.</p> "> Figure 3
<p>Best matches of BLASTp searches (UniProt) and schematic genome organization of the new mycovirus Cryphonectria naterciae fusagravirus 1 (CnFGV1) found in the Portuguese isolate M10544 of <span class="html-italic">Cryphonectria naterciae</span>. The genome of CnFGV1 contains two predicted open reading frames (ORFs; green boxes). A putative shifting heptamer sequence located at site 6061 nt upstream of the stop codon of the hypothetical protein ORF1 is shown in blue.</p> "> Figure 4
<p>Phylogenetic analyses of amino-acid alignments resulting from ORF1 and ORF2 BLASTp searches of the new mycovirus Cryphonectria naterciae fusagravirus 1 (CnFGV1). Blue letters highlight the phylogenetic position of CnFGV1 in both neighbor joining trees. Names and UniProt accession numbers of related fusagraviruses included in the analyses are indicated in the trees. The numbers at nodes are values of >50% of 1000 bootstrap replicates.</p> "> Figure 5
<p>Pairwise co-cultivation of CnFGV1-positive (+) and CnFGV1-free (−) strains of <span class="html-italic">C. naterciae</span>. (<b>A</b>) After incubation for 10–15 days at 25 °C, two inocula from the recipient side (I and II) and one from the donor side (III) were sub-cultivated for 4–5 days. (<b>B</b>) Gel electrophoresis of Cn-Vir-ORF1 fragments used to verify the virus presence. Negative controls of pairing tests are virus-free strains labeled with asterisks. M: Thermo Scientific GeneRuler 1 kb Plus DNA Ladder (SM1334).</p> "> Figure 6
<p>Pairwise co-cultivation of CnFGV1-positive (+) <span class="html-italic">Cryphonectria naterciae</span> and CnFGV1-free (−) <span class="html-italic">Cryphonectria</span> spp. (<b>A</b>) Donor strain in co-culture with replicate M2270-C of <span class="html-italic">C. radicalis</span>. (<b>B</b>) Donor strain in co-culture with replicate M9290-C and M9290-H of <span class="html-italic">C. carpinicola</span>. Agarose gels below show Cn-Vir-ORF1 fragments of five (A–E) or 10 (A–J) replicates to verify the virus transmission. The position III is from the donor side and always CnFGV1-positive. Yellow letters highlight the positive CnFGV1-transmission to the recipient.</p> "> Figure 7
<p>Morphology of isogenic strains of <span class="html-italic">Cryphonectria naterciae</span> after 7 days incubation, shown here by way of example using the recipient strain M10562. (<b>A</b>) Infected from the donor M10535 with some sectoring at left side. (<b>B</b>) Infected from the donor M10544 showing an extreme sectoring with densely interwoven mycelium. (<b>C</b>) Infected from the donor M10545 with regular morphology.</p> "> Figure 8
<p>Growth rate of CnFGV1-positive and virus-free isogenic strains of <span class="html-italic">Cryphonectria naterciae</span>. Compared are isogenic virus-free strains (= vf) with experimentally infected recipients M10452, M10547, M10550, and M10562 of <span class="html-italic">C. naterciae</span>. Donors are a = M10535, b = M10544, and c = M10545. Gray columns show the growth of donor strains. Column height represents growth after 7 days of incubation. Vertical black lines indicate the standard deviation of three culture replicates, and vertical yellow <span class="html-italic">p</span>-numbers highlight significant growth differences between the virus-free and each infected strain. White <span class="html-italic">p</span>-numbers are nonsignificant considering a critical value of <span class="html-italic">p</span> < 0.05.</p> "> Figure 9
<p>Growth rate of CnFGV1-positive and virus-free isogenic strains of <span class="html-italic">Cryphonectria</span> spp. Column height represents the growth of isogenic virus-free strains (green) or infected recipient strains (dark and light blue) of <span class="html-italic">C. radicalis</span> (M2270, M4733) and <span class="html-italic">C. carpinicola</span> (M9290). Donor strains are <span class="html-italic">C. naterciae</span> M10544 and M10545. Column height represents growth after 7 days incubation. Vertical black lines indicate the standard deviation of three culture replicates, and vertical yellow <span class="html-italic">p</span>-numbers highlight significant growth differences between the virus-free and each infected strain. White <span class="html-italic">p</span>-numbers are nonsignificant considering a critical value of <span class="html-italic">p</span> < 0.05.</p> "> Figure 10
<p>Morphology of isogenic strain M9290 of <span class="html-italic">Cryphonectria carpinicola</span> after cross-species infection with CnFGV1. (<b>A</b>) Mycelium of the virus-free isolate M9290 formed numerous dark-orange pycnidia, which developed in concentric rings due to light/dark growth conditions (arrows). (<b>B</b>) Mycelium of the isogenic CnFGV1-infected strain M9290-HII that lacks visible pycnidia. (<b>A</b>,<b>B</b>) In each upper right box, magnification of the mycelium surface with pycnidia in (<b>A</b>) and without pycnidia in (<b>B</b>). Scale bar = 1 cm.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungal Isolates
2.2. Viral Detection and RNA-Seq
2.3. Specific Viral Primer and RT-PCR
2.4. Genome Terminal Sequences and Phylogeny
2.5. SSR-PCR of Cryphonectria naterciae
2.6. Horizontal CnFGV1 Transmission and Isogenic Strains
2.7. Effects on the Fungal Fitness
2.8. Effect of CnFGV1 Infection on the Fungus–Plant Interaction
3. Results
3.1. dsRNA Represents a Non-Segmented Genome of a Novel Virus Encoding the Conserved RdRp Domain
3.2. ORFs Were Phylogenetically Placed within the Proposed Family Fusagraviridae
3.3. CnFGV1 Was Able to Infect New Hosts beyond the Incompatibility and Species Barrier
3.4. CnFGV1 Reduced the Growth Rate of Newly Infected Hosts
3.5. CnFGV1 Was Vertically Transmitted at 100% to the Next Generation through Asexual Spores, but Not So in New Host Species
3.6. In Planta Tests Show That CnFGV1 Has No Major Effect on the C. naterciae–Tree Interaction
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Species/Host | Collection ID 1 | Country | Year | CnFGV1 Detection 2 | Reference |
---|---|---|---|---|---|
C. naterciae | |||||
Quercus suber | M10535 | Portugal | 1960 | Positive | [21] |
Q. suber | M10536 | Portugal | 2010 | Positive | This study |
Q. suber | M10537 | Portugal | 2001 | Negative | [21] |
Q. suber | M10538 | Portugal | 2001 | Negative | [21] |
Q. suber | M10539 | Portugal | 2001 | Negative | [21] |
Q. suber | M10540 | Portugal | 2000 | Negative | [21] |
Q. suber | M10541 | Portugal | 2000 | Positive | [21] |
Q. suber | M10542 | Portugal | 2001 | Negative | [21] |
Q. suber | M10543 | Portugal | 2001 | Negative | [21] |
Q. suber | M10544 | Portugal | 2005 | Positive | [21] |
Q. suber | M10545 | Portugal | 2005 | Positive | [21] |
Q. suber | M10557 | Portugal | 2014 | Negative | This study |
Q. suber | M10558 | Portugal | 2014 | Negative | This study |
Q. suber | M10559 | Portugal | 2014 | Positive | This study |
Q. suber | M10560 | Portugal | 2014 | Positive | This study |
Q. suber | M10561 | Portugal | 2014 | Positive | This study |
Q. suber | M10562 | Portugal | 2015 | Negative | This study |
Q. suber | M10563 | Portugal | 2011 | Negative | This study |
Q. suber | M10564 | Portugal | 2014 | Positive | This study |
Q. suber | M10565 | Portugal | 2015 | Positive | This study |
Castanea sativa | M10546 | Portugal | 2001 | Negative | [21] |
C. sativa | M10547 | Portugal | 2001 | Negative | [21] |
C. sativa | M10548 | Portugal | 2001 | Positive | [21] |
C. sativa | M10549 | Portugal | 2001 | Positive | [21] |
C. sativa | M10550 | Portugal | 2001 | Negative | [21] |
C. sativa | M10551 | Portugal | 2001 | Positive | [21] |
C. sativa | M10552 | Portugal | 2001 | Negative | [21] |
C. sativa | M10553 | Portugal | 2001 | Negative | [21] |
C. sativa | M10554 | Portugal | 2001 | Negative | [21] |
C. sativa | M10555 | Portugal | 2001 | Negative | [21] |
C. sativa | M10556 | Portugal | 2001 | Negative | [21] |
C. carpinicola | |||||
Carpinus sp. | M9290 | Austria | 2009 | Negative | [20] |
Carpinus betulus | M9615 | Switzerland | 2019 | Negative | [20] |
C. parasitica | |||||
C. sativa | M2372 | Switzerland | 1992 | Negative | [40] |
C. sativa | M2671 | Switzerland | 1992 | Negative | [40] |
C. sativa | M4023 | Switzerland | 2000 | Negative | [41] |
C. radicalis | |||||
C. sativa | M2270 | Switzerland | 1996 | Negative | [42] |
C. sativa | M4733 | Switzerland | 2001 | Negative | This study |
Donor | |||||
---|---|---|---|---|---|
Cryphonectria naterciae | |||||
Recipient | Isolate-ID | M10535 | M10544 | M10545 | |
Within-species tests | C. naterciae | M10542 | 2/3 | 3/3 | 3/3 |
M10547 | 2/3 | 3/3 | 3/3 | ||
M10550 | 0/3 | 2/3 | 3/3 | ||
M10562 | 1/3 | 3/3 | 3/3 | ||
Cross-species tests | C. carpinicola | M9290 | 0/10 | 0/10 | 2/10 |
M9615 | 0/10 | 0/10 | 0/10 | ||
C. radicalis | M2270 | 0/10 | 1/10 | 1/10 | |
M4733 | 0/10 | 0/10 | 1/10 | ||
C. parasitica | M2372 | 0/10 | 0/10 | 0/10 | |
M2671 | 0/10 | 0/10 | 0/10 | ||
M4023 | 0/10 | 0/10 | 0/10 |
Strain Label (Rate of Vertical Transmission) | |||
---|---|---|---|
Species | Experiment I | Experiment II | |
Donor strain | C. naterciae | M10544 (50/50) | M10545 (50/50) |
Recipient, isogenic strain | C. radicalis | M2270-14II (1/50) | M2270-EI (44/48) 1 |
No transmission 2 | M4733-CII (44/50) | ||
C. carpinicola | No transmission 2 | M9290-CII (24/50) 3 M9290-HII (49/50) 4 |
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Cornejo, C.; Hisano, S.; Bragança, H.; Suzuki, N.; Rigling, D. A New Double-Stranded RNA Mycovirus in Cryphonectria naterciae Is Able to Cross the Species Barrier and Is Deleterious to a New Host. J. Fungi 2021, 7, 861. https://doi.org/10.3390/jof7100861
Cornejo C, Hisano S, Bragança H, Suzuki N, Rigling D. A New Double-Stranded RNA Mycovirus in Cryphonectria naterciae Is Able to Cross the Species Barrier and Is Deleterious to a New Host. Journal of Fungi. 2021; 7(10):861. https://doi.org/10.3390/jof7100861
Chicago/Turabian StyleCornejo, Carolina, Sakae Hisano, Helena Bragança, Nobuhiro Suzuki, and Daniel Rigling. 2021. "A New Double-Stranded RNA Mycovirus in Cryphonectria naterciae Is Able to Cross the Species Barrier and Is Deleterious to a New Host" Journal of Fungi 7, no. 10: 861. https://doi.org/10.3390/jof7100861