Abstract
Plants produce chemical defenses that poison insect herbivores or deter their feeding, but herbivores are also accompanied by microbial endosymbionts crucial for their nutrition, reproduction, and fitness. Hence, plant defenses could target a herbivore’s beneficial endosymbionts, but this has not yet been demonstrated. Here, we studied flavonoids that are induced when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH), which harbors beneficial yeast-like symbionts (YLS) essential for insect nutrition, such as by remedying deficiencies in sterols. BPH attack dramatically increased sakuranetin accumulations in leaf sheaths and phloem exudates. Sakuranetin is an antifungal phytoalexin derived from the antibacterial precursor, naringenin, via catalysis of naringenin- O -methyltransferase (NOMT). When added to artificial diets, sakuranetin decreased BPH survivorship, suggesting that it functions as an induced defense. Mutation of NOMT abolished sakuranetin accumulation and increased BPH oviposition and hatching rates. High-throughput amplicon sequencing revealed that BPH fed on sakuranetin-deficient nomt lines were enriched in YLS with only minor changes in the bacterial endosymbionts, compared to those feeding on sakuranetin-rich wild-type (WT) plants. In-vitro feeding of sakuranetin suggested that this flavonoid directly inhibited the growth of YLS. BPH feeding on nomt lines accumulated higher cholesterol levels, which might be attributed to increases in the supply of sterol precursors from the YLS, while nomt lines suffered more damage than WT plants did from BPH herbivory. BPH-elicited accumulation of sakuranetin requires intact jasmonate (JA) signaling. This study reveals that rice uses a JA-induced antifungal flavonoid phytoalexin in defense against BPH by inhibiting its beneficial endosymbionts.
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Claims 11
Claim · model-written summary
Brown planthopper attack dramatically increased sakuranetin accumulation in rice leaf sheaths and phloem exudates.
- Taxon
- rice
Oryza sativae1 - Organ / stage
- leaf sheathse0
- Treatment
- BPH attacke0
- Interactor
- brown planthopper
Nilaparvata lugense1pest - Outcome
- sakuranetin accumulations in leaf sheaths and phloem exudatese0
- Direction
- increasede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“BPH attack dramatically increased sakuranetin accumulations in leaf sheaths and phloem exudates”
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
Claim · model-written summary
Sakuranetin added to artificial diets decreased brown planthopper survivorship.
- Taxon
- riceOryza sativae1
- Treatment
- added to artificial dietse2
- Interactor
- BPHe2pest
- Compound
- sakuranetine2
- Outcome
- BPH survivorshipe2
- Direction
- decreasede2
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e2“When added to artificial diets, sakuranetin decreased BPH survivorship, suggesting that it functions as an induced defense”
Claim · model-written summary
Mutation of NOMT abolished sakuranetin accumulation in rice.
- Taxon
- riceOryza sativae1
- Treatment
- Mutation of NOMTe3
- Gene
- NOMTe3
- Outcome
- sakuranetin accumulatione3
- Direction
- abolishede3
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e3“Mutation of NOMT abolished sakuranetin accumulation and increased BPH oviposition and hatching rates”
Claim · model-written summary
Mutation of NOMT increased brown planthopper oviposition and hatching rates.
- Taxon
- riceOryza sativae1
- Treatment
- Mutation of NOMTe3
- Interactor
- BPHe3pest
- Gene
- NOMTe3
- Outcome
- BPH oviposition and hatching ratese3
- Direction
- increasede3
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e3“Mutation of NOMT abolished sakuranetin accumulation and increased BPH oviposition and hatching rates”
Claim · model-written summary
Brown planthopper fed on sakuranetin-deficient nomt lines was enriched in yeast-like symbionts compared with wild-type plants.
- Taxon
- riceOryza sativae1
- Material
- nomt linese4
- Treatment
- BPH fed on sakuranetin-deficient nomt linese4
- Interactor
- YLSe4symbiont
- Second interactor
- BPHe4pest
- Outcome
- YLSe4
- Direction
- enrichede4
- Comparator
- sakuranetin-rich wild-type (WT) plantse4
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e4“BPH fed on sakuranetin-deficient nomt lines were enriched in YLS with only minor changes in the bacterial endosymbionts, compared to those feeding on sakuranetin-rich wild-type (WT) plants”
e5“which harbors beneficial yeast-like symbionts (YLS) essential for insect nutrition”
Claim · model-written summary
Brown planthopper fed on sakuranetin-deficient nomt lines shows no appreciable change in bacterial endosymbionts compared with wild-type plants.
- Taxon
- riceOryza sativae1
- Treatment
- BPH fed on sakuranetin-deficient nomt linese4
- Interactor
- bacterial endosymbiontse4symbiont
- Second interactor
- BPHe4pest
- Outcome
- bacterial endosymbiontse4
- Direction
- no_changeinferrede4
- Comparator
- sakuranetin-rich wild-type (WT) plantse4
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e4“BPH fed on sakuranetin-deficient nomt lines were enriched in YLS with only minor changes in the bacterial endosymbionts, compared to those feeding on sakuranetin-rich wild-type (WT) plants”
Claim · model-written summary
In-vitro feeding of sakuranetin directly inhibited the growth of yeast-like symbionts.
- Taxon
- riceOryza sativae1
- Treatment
- In-vitro feeding of sakuranetine6
- Interactor
- YLSe6symbiont
- Compound
- sakuranetine6
- Outcome
- growth of YLSe6
- Direction
- inhibitede6
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e6“In-vitro feeding of sakuranetin suggested that this flavonoid directly inhibited the growth of YLS”
Claim · model-written summary
Brown planthopper feeding on nomt lines accumulated higher cholesterol levels, possibly from increased sterol precursor supply by the symbionts.
- Taxon
- riceOryza sativae1
- Treatment
- BPH feeding on nomt linese7
- Interactor
- BPHe7pest
- Second interactor
- YLSe7symbiont
- Compound
- sterol precursorse7
- Outcome
- cholesterol levelse7
- Direction
- highere7
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e7“BPH feeding on nomt lines accumulated higher cholesterol levels, which might be attributed to increases in the supply of sterol precursors from the YLS”
Claim · model-written summary
Nomt lines suffered more damage from brown planthopper herbivory than wild-type plants did.
- Taxon
- riceOryza sativae1
- Material
- nomt linese7
- Treatment
- BPH herbivorye7
- Interactor
- BPHe7pest
- Outcome
- damagee7
- Direction
- moree7
- Comparator
- WT plantse7
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e7“while nomt lines suffered more damage than WT plants did from BPH herbivory”
Claim · model-written summary
BPH-elicited accumulation of sakuranetin requires intact jasmonate signaling.
- Taxon
- riceOryza sativae1
- Interactor
- BPHe6pest
- Compound
- jasmonate (JA)e6
- Outcome
- accumulation of sakuranetine6
- Qualifier
- requires intact jasmonate (JA) signalinge6
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH)”
e6“BPH-elicited accumulation of sakuranetin requires intact jasmonate (JA) signaling”
Claim · model-written summary
Rice uses a JA-induced antifungal flavonoid phytoalexin in defense against brown planthopper by inhibiting its beneficial endosymbionts.
- Taxon
- riceOryza sativae7
- Interactor
- beneficial endosymbiontse7symbiont
- Second interactor
- BPHe7pest
- Compound
- antifungal flavonoid phytoalexine7
- Outcome
- defense against BPHe7
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e7“This study reveals that rice uses a JA-induced antifungal flavonoid phytoalexin in defense against BPH by inhibiting its beneficial endosymbionts”
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