Paper · 2018 · Molecular Plant-Microbe Interactions

Secretome Analysis and In Planta Expression of Salivary Proteins Identify Candidate Effectors from the Brown Planthopper Nilaparvata lugens

Weiwei Rao; Xiaohong Zheng; Bingfang Liu; et al.

12
claims
24
verbatim quotes
74
citations
3
research areas
✓
Open access

Abstract

The brown planthopper (BPH), Nilaparvata lugens (Stål), is a phloem sap-feeding insect. During feeding on rice plants, BPH secretes salivary proteins with potential effector functions, which may play a critical role in the plant-insect interactions. However, a limited number of BPH effector proteins have been identified to date. Here, we sequenced the salivary gland transcriptomes of five BPH populations and subsequently established a N. lugens secretome consisting of 1,140 protein-encoding genes. Secretome analysis revealed the presence of both conserved and rapidly evolving salivary proteins. A screen for potential effectors that elicit responses in the plant was performed via the transient expression analysis of 64 BPH salivary proteins in Nicotiana benthamiana leaves and rice protoplasts. The salivary proteins Nl12, Nl16, Nl28, and Nl43 induced cell death, whereas Nl40 induced chlorosis and Nl32 induced a dwarf phenotype in N. benthamiana, indicating effector properties of these proteins. Ectopic expression of the six salivary proteins in N. benthamiana upregulated expression of defense-related genes and callose deposition. Tissue expression analysis showed a higher expression level of the six candidate effectors in salivary glands than in other tissues. Subcellular localization and analysis of the domain required for cell death showed a diverse structure of the six effectors. Nl28, Nl40, and Nl43 are N. lugens specific; in contrast, Nl12, Nl16, and Nl32 are conserved among insects. The Nl40 family has numerous isoforms produced by alternative splicing, exemplifying rapid evolution and expansion of effector proteins in the BPH. Our results suggest a potential large effector repertoire in BPH and a higher level of effector conservation exist in BPH compared with that in plant pathogens.

Abstract from the paper’s OpenAlex record, shown for indexing and research. Copyright remains with the authors or the publisher. Read at the source ↗

The text the model read, with the source record’s inline markup (italics, sub- and superscripts) rendered and its character entities decoded; quote offsets refer to the raw text.

Claims 12

Method / resourceobservedoriginal resultmeasured

Claim · model-written summary

Sequencing yielded a N. lugens secretome of 1,140 protein-encoding genes.

Interactor
N. lugensNilaparvata lugense1pest
Outcome
secretomee1
Value
1,140 protein-encoding genese1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Nilaparvata lugens
Nilaparvata lugens · InteractorNatasha Wright, Florida Department of Agriculture and Consumer Services, Bugwood.org - See more at: http://www.forestryimages.org/browse/detail.cfm?imgnum=51900 · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“established a N. lugens secretome consisting of 1,140 protein-encoding genes”

✓ located verbatim in the source · abstract, characters 425–501 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Secretome analysis found conserved and rapidly evolving salivary proteins.

Interactor
BPHe0pest
Outcome
conserved and rapidly evolving salivary proteinse1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“Secretome analysis revealed the presence of both conserved and rapidly evolving salivary proteins”

✓ located verbatim in the source · abstract, characters 503–600 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Nl12, Nl16, Nl28 and Nl43 induced cell death in N. benthamiana.

Taxon
N. benthamianaNicotiana benthamianae1
Treatment
Nl12, Nl16, Nl28, and Nl43e1
Interactor
BPHe0pest
Outcome
cell deathe1

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The brown planthopper (BPH), Nilaparvata lugens (Stål)”

✓ located verbatim in the source · abstract, characters 0–54 · show in text ↑
e1

“The salivary proteins Nl12, Nl16, Nl28, and Nl43 induced cell death, whereas Nl40 induced chlorosis and Nl32 induced a dwarf phenotype in N. benthamiana”

✓ located verbatim in the source · abstract, characters 804–956 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Nl40 induced chlorosis in N. benthamiana.

Taxon
N. benthamianaNicotiana benthamianae1
Treatment
Nl40e1
Interactor
BPHe0pest
Outcome
chlorosise1

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The brown planthopper (BPH), Nilaparvata lugens (Stål)”

✓ located verbatim in the source · abstract, characters 0–54 · show in text ↑
e1

“Nl40 induced chlorosis and Nl32 induced a dwarf phenotype in N. benthamiana”

✓ located verbatim in the source · abstract, characters 881–956 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Nl32 induced a dwarf phenotype in N. benthamiana.

Taxon
N. benthamianaNicotiana benthamianae1
Treatment
Nl32e1
Interactor
BPHe0pest
Outcome
dwarf phenotypee1

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The brown planthopper (BPH), Nilaparvata lugens (Stål)”

✓ located verbatim in the source · abstract, characters 0–54 · show in text ↑
e1

“Nl32 induced a dwarf phenotype in N. benthamiana”

✓ located verbatim in the source · abstract, characters 908–956 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Ectopic expression of six salivary proteins upregulated defense-related genes and callose deposition in N. benthamiana.

Taxon
N. benthamianaNicotiana benthamianae1
Treatment
Ectopic expression of the six salivary proteinse1
Interactor
BPHe0pest
Outcome
expression of defense-related genes and callose depositione1
Direction
upregulatede1

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The brown planthopper (BPH), Nilaparvata lugens (Stål)”

✓ located verbatim in the source · abstract, characters 0–54 · show in text ↑
e1

“Ectopic expression of the six salivary proteins in N. benthamiana upregulated expression of defense-related genes and callose deposition”

✓ located verbatim in the source · abstract, characters 1008–1144 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Six candidate effectors had higher expression in salivary glands than other tissues.

Organ / stage
salivary glandse1
Interactor
BPHe0pest
Outcome
expression level of the six candidate effectorse1
Direction
highere1
Comparator
other tissuese1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“Tissue expression analysis showed a higher expression level of the six candidate effectors in salivary glands than in other tissues”

✓ located verbatim in the source · abstract, characters 1146–1277 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The six effectors had diverse structures in localization and cell-death domain analyses.

Interactor
BPHe0pest
Outcome
diverse structure of the six effectorse1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“Subcellular localization and analysis of the domain required for cell death showed a diverse structure of the six effectors”

✓ located verbatim in the source · abstract, characters 1279–1402 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Nl28, Nl40 and Nl43 were N. lugens specific.

Interactor
N. lugensNilaparvata lugense1pest
Gene
Nl28, Nl40, and Nl43e1
Outcome
N. lugens specifice1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Nilaparvata lugens
Nilaparvata lugens · InteractorNatasha Wright, Florida Department of Agriculture and Consumer Services, Bugwood.org - See more at: http://www.forestryimages.org/browse/detail.cfm?imgnum=51900 · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“Nl28, Nl40, and Nl43 are N. lugens specific”

✓ located verbatim in the source · abstract, characters 1404–1447 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Nl12, Nl16 and Nl32 were conserved among insects.

Interactor
BPHe0pest
Gene
Nl12, Nl16, and Nl32e1
Outcome
conserved among insectse1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“Nl12, Nl16, and Nl32 are conserved among insects”

✓ located verbatim in the source · abstract, characters 1462–1510 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The Nl40 family had many alternatively spliced isoforms.

Interactor
BPHe0pest
Gene
Nl40e1
Outcome
numerous isoforms produced by alternative splicinge1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“The Nl40 family has numerous isoforms produced by alternative splicing”

✓ located verbatim in the source · abstract, characters 1512–1582 · show in text ↑
Observationauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors inferred a large effector repertoire and greater effector conservation in BPH than plant pathogens.

Interactor
BPHe1pest
Outcome
effector conservatione1
Direction
highere1
Qualifier
potential large effector repertoiree1
Comparator
plant pathogense1

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“During feeding on rice plants, BPH secretes salivary proteins”

✓ located verbatim in the source · abstract, characters 88–149 · show in text ↑
e1

“a potential large effector repertoire in BPH and a higher level of effector conservation exist in BPH compared with that in plant pathogens”

✓ located verbatim in the source · abstract, characters 1680–1819 · show in text ↑

overexpression · molecular: expression · Nicotiana benthamianaPositive and negative results

11 papers: 5 positive, 6 negative or no effect

4 papers in the same direction as this paper · 6 in the opposite direction

  1. negative
  2. negative
  3. negative

7 papers more in this group

See all 11 papers →

Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.