Paper · 2024 · Phytobiomes Journal

Plant-Guided Microbiome Selection Produces Transient Effects on Insect Performance and Rhizosphere Community Assembly

Laramy Enders; Elizabeth French; MacKenzie Kjeldgaard; et al.

8
claims
16
verbatim quotes
8
citations
1
research areas
✓
Open access

Abstract

Microbial communities are essential for plant health, but using these relationships to enhance growth and pest protection is challenging. Leveraging the natural mechanisms plants employ to manage relationships with microbes is one promising means to selectively engineer whole microbial communities with beneficial properties. This approach, known as host-guided selection, has been successful in some model species targeting performance traits (e.g., biomass). However, few studies use crop plants or focus on defensive traits (e.g., pest resistance). Our goal was to naturally engineer tomato root-associated microbiomes that increase resistance to insect pests. First, we used an iterative soil microbial inoculation process to engineer insect-suppressive rhizosphere soil microbiomes that reduce damage from aphid feeding ( Macrosiphum euphorbiae) or caterpillar defoliation ( Manduca sexta, Spodoptera exigua). We then characterized the bacterial and fungal microbial communities of soils associated with differences in insect performance using metabarcoding approaches. Overall, soil microbiome selection produced transient differences in aphid performance, but caterpillar growth was unaffected. In four of nine generations, the aphid population growth rate was significantly lower on plants with rhizospheres selected for “low” insect performance, where abundance was reduced by up to 20%. Correspondingly minor shifts in fungal and bacterial relative abundance occurred in insect-suppressive communities. However, network analysis indicated that aphid feeding disrupted rhizosphere microbiome assembly, resulting in lower community complexity and connectivity and fewer structurally important taxa compared with uninfested controls. Overall, our results highlight critical factors for successful engineering of beneficial microbiomes, particularly insect feeding guild and microbial community stability.

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Claims 8

Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Soil microbiome selection produced transient differences in aphid performance.

Treatment
soil microbiome selectione0
Interactor
aphide0pest
Outcome
aphid performancee0
Qualifier
transient differencese0

Not reportedComparatorDirection

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Overall, soil microbiome selection produced transient differences in aphid performance, but caterpillar growth was unaffected.”

✓ located verbatim in the source · abstract, characters 1076–1202 · show in text ↑
e1

“tomato root-associated microbiomes”

✓ located verbatim in the source · abstract, characters 588–622 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Microbiome selection did not affect Manduca sexta caterpillar growth.

Taxon
Manduca sextaManduca sextae1
Treatment
soil microbiome selectione0
Outcome
caterpillar growthe0
Direction
unaffectede0

Not reportedComparator

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

Manduca sexta
Manduca sexta · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Overall, soil microbiome selection produced transient differences in aphid performance, but caterpillar growth was unaffected.”

✓ located verbatim in the source · abstract, characters 1076–1202 · show in text ↑
e1

“caterpillar defoliation ( Manduca sexta, Spodoptera exigua)”

✓ located verbatim in the source · abstract, characters 855–914 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Microbiome selection did not affect Spodoptera exigua caterpillar growth.

Taxon
Spodoptera exiguaSpodoptera exiguae1
Treatment
soil microbiome selectione0
Outcome
caterpillar growthe0
Direction
unaffectede0

Not reportedComparator

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

Spodoptera exigua
Spodoptera exigua · TaxonDumi · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Overall, soil microbiome selection produced transient differences in aphid performance, but caterpillar growth was unaffected.”

✓ located verbatim in the source · abstract, characters 1076–1202 · show in text ↑
e1

“caterpillar defoliation ( Manduca sexta, Spodoptera exigua)”

✓ located verbatim in the source · abstract, characters 855–914 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Aphid population growth rate was significantly lower on plants selected for low insect performance in four of nine generations.

Treatment
rhizospheres selected for “low” insect performancee0
Interactor
aphide0pest
Outcome
aphid population growth ratee0
Direction
lowere0
Qualifier
In four of nine generationse0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“In four of nine generations, the aphid population growth rate was significantly lower on plants with rhizospheres selected for “low” insect performance, where abundance was reduced by up to 20%.”

✓ located verbatim in the source · abstract, characters 1203–1397 · show in text ↑
e1

“tomato root-associated microbiomes”

✓ located verbatim in the source · abstract, characters 588–622 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Aphid abundance was reduced by up to 20% on plants with rhizospheres selected for low insect performance.

Treatment
rhizospheres selected for “low” insect performancee0
Interactor
aphide0pest
Outcome
abundancee0
Direction
reducede0
Value
up to 20%e0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“In four of nine generations, the aphid population growth rate was significantly lower on plants with rhizospheres selected for “low” insect performance, where abundance was reduced by up to 20%.”

✓ located verbatim in the source · abstract, characters 1203–1397 · show in text ↑
e1

“tomato root-associated microbiomes”

✓ located verbatim in the source · abstract, characters 588–622 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Minor shifts in fungal and bacterial relative abundance occurred in insect-suppressive communities.

Interactor
fungale0other
Second interactor
bacteriale0other
Outcome
fungal and bacterial relative abundancee0
Qualifier
minor shiftse0

Not reportedDirection

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Correspondingly minor shifts in fungal and bacterial relative abundance occurred in insect-suppressive communities.”

✓ located verbatim in the source · abstract, characters 1398–1513 · show in text ↑
e1

“tomato root-associated microbiomes”

✓ located verbatim in the source · abstract, characters 588–622 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Aphid feeding lowered rhizosphere community complexity and connectivity and reduced structurally important taxa relative to uninfested controls.

Treatment
aphid feedinge0
Interactor
aphide0pest
Outcome
community complexity and connectivitye0
Direction
lowere0
Comparator
uninfested controlse0

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“aphid feeding disrupted rhizosphere microbiome assembly, resulting in lower community complexity and connectivity and fewer structurally important taxa compared with uninfested controls.”

✓ located verbatim in the source · abstract, characters 1555–1741 · show in text ↑
e1

“tomato root-associated microbiomes”

✓ located verbatim in the source · abstract, characters 588–622 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Aphid feeding resulted in fewer structurally important rhizosphere taxa than in uninfested controls.

Treatment
aphid feedinge0
Interactor
aphide0pest
Outcome
structurally important taxae0
Direction
fewere0
Comparator
uninfested controlse0

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“aphid feeding disrupted rhizosphere microbiome assembly, resulting in lower community complexity and connectivity and fewer structurally important taxa compared with uninfested controls.”

✓ located verbatim in the source · abstract, characters 1555–1741 · show in text ↑
e1

“tomato root-associated microbiomes”

✓ located verbatim in the source · abstract, characters 588–622 · show in text ↑