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Viral Small Interfering RNAs Target Host Genes to Mediate Disease
Symptoms in Plants


The Cucumber mosaic virus (CMV) Y-satellite RNA (Y-Sat) has a

small non-protein-coding RNA genome that induces yellowing symptoms in infected

Nicotiana tabacum (tobacco). How this RNA pathogen induces

such symptoms has been a longstanding question. We show that the yellowing

symptoms are a result of small interfering RNA (siRNA)-directed RNA silencing of

the chlorophyll biosynthetic gene, CHLI. The CHLI mRNA contains a 22-nucleotide

(nt) complementary sequence to the Y-Sat genome, and in Y-Sat-infected plants,

CHLI expression is dramatically down-regulated. Small RNA sequencing and

5′ RACE analyses confirmed that this 22-nt sequence was targeted for mRNA

cleavage by Y-Sat-derived siRNAs. Transformation of tobacco with a RNA

interference (RNAi) vector targeting CHLI induced Y-Sat-like symptoms. In

addition, the symptoms of Y-Sat infection can be completely prevented by

transforming tobacco with a silencing-resistant variant of the CHLI gene. These

results suggest that siRNA-directed silencing of CHLI is solely responsible for

the Y-Sat-induced symptoms. Furthermore, we demonstrate that two

Nicotiana species, which do not develop yellowing symptoms

upon Y-Sat infection, contain a single nucleotide polymorphism within the

siRNA-targeted CHLI sequence. This suggests that the previously observed species

specificity of Y-Sat-induced symptoms is due to natural sequence variation in

the CHLI gene, preventing CHLI silencing in species with a mismatch to the Y-Sat

siRNA. Taken together, these findings provide the first demonstration of small

RNA-mediated viral disease symptom production and offer an explanation of the

species specificity of the viral disease.


Vyšlo v časopise: Viral Small Interfering RNAs Target Host Genes to Mediate Disease Symptoms in Plants. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1002022
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002022

Souhrn

The Cucumber mosaic virus (CMV) Y-satellite RNA (Y-Sat) has a

small non-protein-coding RNA genome that induces yellowing symptoms in infected

Nicotiana tabacum (tobacco). How this RNA pathogen induces

such symptoms has been a longstanding question. We show that the yellowing

symptoms are a result of small interfering RNA (siRNA)-directed RNA silencing of

the chlorophyll biosynthetic gene, CHLI. The CHLI mRNA contains a 22-nucleotide

(nt) complementary sequence to the Y-Sat genome, and in Y-Sat-infected plants,

CHLI expression is dramatically down-regulated. Small RNA sequencing and

5′ RACE analyses confirmed that this 22-nt sequence was targeted for mRNA

cleavage by Y-Sat-derived siRNAs. Transformation of tobacco with a RNA

interference (RNAi) vector targeting CHLI induced Y-Sat-like symptoms. In

addition, the symptoms of Y-Sat infection can be completely prevented by

transforming tobacco with a silencing-resistant variant of the CHLI gene. These

results suggest that siRNA-directed silencing of CHLI is solely responsible for

the Y-Sat-induced symptoms. Furthermore, we demonstrate that two

Nicotiana species, which do not develop yellowing symptoms

upon Y-Sat infection, contain a single nucleotide polymorphism within the

siRNA-targeted CHLI sequence. This suggests that the previously observed species

specificity of Y-Sat-induced symptoms is due to natural sequence variation in

the CHLI gene, preventing CHLI silencing in species with a mismatch to the Y-Sat

siRNA. Taken together, these findings provide the first demonstration of small

RNA-mediated viral disease symptom production and offer an explanation of the

species specificity of the viral disease.


Zdroje

1. HuCCHsuYHLinNS

2009

Satellite RNAs and satellite viruses of plants.

Viruses

1

1325

1350

2. Garcia-ArenalFPalukaitisP

1999

Structure and functional relationship of satellite RNAs of

cucumber mosaic virus.

Curr Top Microbiol Immunol

239

37

63

3. PalukaitisPRoossinckMJ

1996

Spontaneous change of a benign satellite RNA of cucumber mosaic

virus to a pathogenic variant.

Nat Biotechnol

14

1264

1268

4. DevicMJaegleMBaulcombeD

1990

Cucumber mosaic virus satellite RNA (strain Y): analysis of

sequences which affect systemic necrosis on tomato.

J Gen Virol

71

1443

1449

5. SleatDEPalukaitisP

1992

A single nucleotide change within a plant virus satellite RNA

alters the host specificity of disease induction.

Plant J

2

43

49

6. ZhangLKimCHPalukaitisP

1994

The chlorosis-induction domain of the satellite RNA of cucumber

mosaic virus: identifying sequences that affect accumulation and the degree

of chlorosis.

Mol Plant Microbe Interact

7

208

213

7. WangMBWesleySVFinneganEJSmithNAWaterhousePM

2001

Replicating satellite RNA induces sequence-specific DNA

methylation and truncated transcripts in plants.

RNA

7

16

28

8. GhildiyalMZamorePD

2009

Small silencing RNAs: an expanding universe.

Nat Rev Genet

10

94

108

9. WirthSCrespiM

2009

Non-protein coding RNAs, a diverse class of gene regulators, and

their action in plants.

RNA Biol

6

161

164

10. WangMBBianXYWuLMLiuLXSmithNA

2004

On the role of RNA silencing in the pathogenicity and evolution

of viroids and viral satellites.

Proc Natl Acad Sci U S A

101

3275

3280

11. MasutaCTakanamiY

1989

Determination of sequence and structural requirements for

pathogenicity of a cucumber mosaic virus satellite RNA

(Y-satRNA).

Plant Cell

1

1165

1173

12. DevicMJaegleMBaulcombeD

1989

Symptom production on tobacco and tomato is determined by two

distinct domains of the satellite RNA of cucumber mosaic virus (strain

Y).

J Gen Virol

70

2765

2774

13. JaegleMDevicMLongstaffMBaulcombeD

1990

Cucumber mosaic virus satellite RNA (Y strain): analysis of

sequences which affect yellow mosaic symptoms on tobacco.

J Gen Virol

71

1905

1912

14. KuwataSMasutaCTakanamiY

1991

Reciprocal phenotype alterations between two satellite RNAs of

cucumber mosaic virus.

J Gen Virol

72

2385

2389

15. MasutaCSuzukiMKuwataSTakanamiYKoiwaiA

1993

Yellow mosaic induced by Y satellite RNA of cucumber mosaic virus

is regulated by a single incompletely dominant gene in wild

Nicotiana species.

Genetics

83

411

413

16. MasutaCSuzukiMMatsuzakiTHondaIKuwataS

1993

Bright yellow chlorosis by cucumber mosaic virus Y satellite RNA

is specifically induced without severe chloroplast damage.

Physiol Mol Plant Pathol

42

267

278

17. HaleyBZamorePD

2004

Kinetic analysis of the RNAi enzyme complex.

Nat Struct Mol Biol

11

599

606

18. YamaguchiKNishimuraM

2000

Reduction to below threshold levels of glycolate oxidase

activities in transgenic tobacco enhances photoinhibition during

irradiation.

Plant Cell Physiol

41

1397

1406

19. TsagrisEMMartínez de AlbaAEGozmanovaMKalantidisK

2008

Viroids.

Cell Microbiol

10

2168

2179

20. SchmitzARiesnerD

1998

Correlation between bending of the VM region and pathogenicity of

different Potato Spindle Tuber Viroid strains.

RNA

4

1295

1303

21. DingSWVoinnetO

2007

Antiviral immunity directed by small RNAs.

Cell

130

413

426

22. SleatDEPalukaitisP

1990

Induction of tobacco chlorosis by certain cucumber mosaic virus

satellite RNAs is specific to subgroup II helper strains.

Virol

176

292

295

23. YeJQuJZhangJFGengYFFangRX

2009

A critical domain of the Cucumber mosaic virus 2b protein for RNA

silencing suppressor activity.

FEBS Lett

583

101

6

24. ItayaAZhongXBundschuhRQiYWangY

2007

A structured viroid RNA serves as a substrate for dicer-like

cleavage to produce biologically active small RNAs but is resistant to

RNA-induced silencing complex-mediated degradation.

J Virol

81

2980

2984

25. GottweinECullenBR

2008

Viral and cellular microRNAs as determinants of viral

pathogenesis and immunity.

Cell Host Microbe

3

375

387

26. MoissiardGVoinnetO

2006

RNA silencing of host transcripts by cauliflower mosaic virus

requires coordinated action of the four Arabidopsis Dicer-like

proteins.

Proc Natl Acad Sci U S A

103

19593

19598

27. GreyFHookLNelsonJ

2008

The functions of herpesvirus-encoded microRNAs.

Med Microbiol Immunol

197

261

267

28. QiXBaoFSXieZ

2009

Small RNA deep sequencing reveals role for Arabidopsis thaliana

RNA-dependent RNA polymerases in viral siRNA biogenesis.

PLoS One

4

e4971

29. GreyFTirabassiRMeyersHWuGMcWeeneyS

2010

A viral microRNA down-regulates multiple cell cycle genes through

mRNA 5′ UTRs.

Plos Pathog

6

e1000967

30. LinKYChengCPChangBCWangWCHuangYW

2010

Global analyses of small interfering RNAs derived from Bamboo

mosaic virus and its associated satellite RNAs in different

plants.

PLoS One

5

e11928

31. SteinhauerDAHollandJJ

1987

Rapid evolution of RNA viruses.

Ann Rev Microbiol

41

409

433

32. SmithNAEamensALWangMB

2010

The presence of high-molecular-weight viral RNAs interferes with

the detection of viral small RNAs.

RNA

16

1062

1067

33. GleaveAP

1992

A versatile binary vector system with a T-DNA organisational

structure conducive to efficient integration of cloned DNA into the plant

genome.

Plant Mol Biol

20

1203

1207

34. HelliwellCAWaterhousePM

2005

Constructs and methods for hairpin RNA-mediated gene silencing in

plants.

Methods Enzymol

392

24

35

35. SmithNASinghSPWangMBStoutjesdijkPAGreenAG

2000

Total silencing by intron-spliced hairpin RNAs.

Nature

407

319

20

36. EllisJGLlewellynDJDennisESPeacockWJ

1987

Maize Adh1 promoter sequences control anaerobic regulation:

Addition of upstream promoter elements from constitutive genes is necessary

for expression in tobacco.

EMBO J

6

11

16

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


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