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Aversion and attraction to harmful plant secondary compounds jointly shape the foraging ecology of a specialist herbivore.

Humphrey PT, Gloss AD, Alexandre NM, Villalobos MM, Fremgen MR, Groen SC, Meihls LN, Jander G, Whiteman NK - Ecol Evol (2016)

Bottom Line: In contrast to many mustard specialists, S. nigrita does not prevent formation of toxic breakdown products (mustard oils) arising from glucosinolates (GLS), the primary defensive compounds in mustard plants.Therefore, it is an appealing model for dissecting the early stages of host specialization.Here, we report that jasmonic acid (JA) treatment increased GLS biosynthesis in bittercress, repelled adult female flies, and reduced larval growth.

View Article: PubMed Central - PubMed

Affiliation: Ecology and Evolutionary BiologyUniversity of ArizonaTucsonArizona85721; Rocky Mountain Biological LaboratoryGothicColorado81224; Present address: Organismic and Evolutionary BiologyHarvard UniversityCambridgeMassachusetts02138.

ABSTRACT
Most herbivorous insect species are restricted to a narrow taxonomic range of host plant species. Herbivore species that feed on mustard plants and their relatives in the Brassicales have evolved highly efficient detoxification mechanisms that actually prevent toxic mustard oils from forming in the bodies of the animals. However, these mechanisms likely were not present during the initial stages of specialization on mustard plants ~100 million years ago. The herbivorous fly Scaptomyza nigrita (Drosophilidae) is a specialist on a single mustard species, bittercress (Cardamine cordifolia; Brassicaceae) and is in a fly lineage that evolved to feed on mustards only in the past 10-20 million years. In contrast to many mustard specialists, S. nigrita does not prevent formation of toxic breakdown products (mustard oils) arising from glucosinolates (GLS), the primary defensive compounds in mustard plants. Therefore, it is an appealing model for dissecting the early stages of host specialization. Because mustard oils actually form in the bodies of S. nigrita, we hypothesized that in lieu of a specialized detoxification mechanism, S. nigrita may mitigate exposure to high GLS levels within plant tissues using behavioral avoidance. Here, we report that jasmonic acid (JA) treatment increased GLS biosynthesis in bittercress, repelled adult female flies, and reduced larval growth. S. nigrita larval damage also induced foliar GLS, especially in apical leaves, which correspondingly displayed the least S. nigrita damage in controlled feeding trials and field surveys. Paradoxically, flies preferred to feed and oviposit on GLS-producing Arabidopsis thaliana despite larvae performing worse in these plants versus non-GLS-producing mutants. GLS may be feeding cues for S. nigrita despite their deterrent and defensive properties, which underscores the diverse relationship a mustard specialist has with its host when lacking a specialized means of mustard oil detoxification.

No MeSH data available.


Related in: MedlinePlus

Individual and total glucosinolates (GLS) are induced across leaves in field‐collected bittercress stems 72 h post S. nigrita infestation. Data represent single measurements of pools of leaf discs from 15 leaves per leaf position per condition (S. nigrita‐infested vs. mock; see Materials and Methods). (A) Absolute GLS concentration (nmol/mg leaf dry mass) following S. nigrita implantation in bittercress leaf disc pools summed across leaf positions 1–7. (B) Relative GLS induction (log2 difference between treatment and mock) locally (implanted leaves; positions 3 and 4, indicated by arrows) and systemically in leaves along bittercress stem. Color key indicates magnitude of log2 difference between treatment and mock. “na” indicates none of the indicated GLS were detected in one or both of the leaf pools.
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ece32082-fig-0003: Individual and total glucosinolates (GLS) are induced across leaves in field‐collected bittercress stems 72 h post S. nigrita infestation. Data represent single measurements of pools of leaf discs from 15 leaves per leaf position per condition (S. nigrita‐infested vs. mock; see Materials and Methods). (A) Absolute GLS concentration (nmol/mg leaf dry mass) following S. nigrita implantation in bittercress leaf disc pools summed across leaf positions 1–7. (B) Relative GLS induction (log2 difference between treatment and mock) locally (implanted leaves; positions 3 and 4, indicated by arrows) and systemically in leaves along bittercress stem. Color key indicates magnitude of log2 difference between treatment and mock. “na” indicates none of the indicated GLS were detected in one or both of the leaf pools.

Mentions: In parallel, we tested if leaf mining by S. nigrita larvae induced foliar GLS accumulation locally and systemically within bittercress ramets. S. nigrita larvae feeding in a basal leaf was sufficient to increase GLS concentration both locally (i.e., in damaged local leaves at positions 3 and 4, Fig. 3B) and in apical leaf positions (i.e., in undamaged and younger leaves at positions 6 and 7, Fig. 3B). All six detected GLS increased following S. nigrita treatment, (P = 0.031, Wilcoxon signed‐rank test, two‐sided), constituting a 3.73‐fold net increase in total GLS concentration across all leaf positions (mock: 32.36 vs. S. nigrita larva: 145.01 nmol/mg dry leaf mass, Fig. 3A). Level of induction varied by type of GLS, with 1‐methylethyl‐GLS and indole‐3‐ylmethyl‐GLS increasing the most in apical leaves as well as plant‐wide (Fig. 3A). Although plant‐wide GLS concentration increased, leaf position 5 experienced a decrease in concentration of all individual foliar GLS (Fig. 3A) following S. nigrita damage. Leaf pools from each leaf positions from S. nigrita‐infested plants generally displayed an increase in GLS content versus mock‐treated leaf pools, with the highest inductions occurring in the position that received S. nigrita damage followed by the two most apical leaf positions.


Aversion and attraction to harmful plant secondary compounds jointly shape the foraging ecology of a specialist herbivore.

Humphrey PT, Gloss AD, Alexandre NM, Villalobos MM, Fremgen MR, Groen SC, Meihls LN, Jander G, Whiteman NK - Ecol Evol (2016)

Individual and total glucosinolates (GLS) are induced across leaves in field‐collected bittercress stems 72 h post S. nigrita infestation. Data represent single measurements of pools of leaf discs from 15 leaves per leaf position per condition (S. nigrita‐infested vs. mock; see Materials and Methods). (A) Absolute GLS concentration (nmol/mg leaf dry mass) following S. nigrita implantation in bittercress leaf disc pools summed across leaf positions 1–7. (B) Relative GLS induction (log2 difference between treatment and mock) locally (implanted leaves; positions 3 and 4, indicated by arrows) and systemically in leaves along bittercress stem. Color key indicates magnitude of log2 difference between treatment and mock. “na” indicates none of the indicated GLS were detected in one or both of the leaf pools.
© Copyright Policy - creativeCommonsBy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4829532&req=5

ece32082-fig-0003: Individual and total glucosinolates (GLS) are induced across leaves in field‐collected bittercress stems 72 h post S. nigrita infestation. Data represent single measurements of pools of leaf discs from 15 leaves per leaf position per condition (S. nigrita‐infested vs. mock; see Materials and Methods). (A) Absolute GLS concentration (nmol/mg leaf dry mass) following S. nigrita implantation in bittercress leaf disc pools summed across leaf positions 1–7. (B) Relative GLS induction (log2 difference between treatment and mock) locally (implanted leaves; positions 3 and 4, indicated by arrows) and systemically in leaves along bittercress stem. Color key indicates magnitude of log2 difference between treatment and mock. “na” indicates none of the indicated GLS were detected in one or both of the leaf pools.
Mentions: In parallel, we tested if leaf mining by S. nigrita larvae induced foliar GLS accumulation locally and systemically within bittercress ramets. S. nigrita larvae feeding in a basal leaf was sufficient to increase GLS concentration both locally (i.e., in damaged local leaves at positions 3 and 4, Fig. 3B) and in apical leaf positions (i.e., in undamaged and younger leaves at positions 6 and 7, Fig. 3B). All six detected GLS increased following S. nigrita treatment, (P = 0.031, Wilcoxon signed‐rank test, two‐sided), constituting a 3.73‐fold net increase in total GLS concentration across all leaf positions (mock: 32.36 vs. S. nigrita larva: 145.01 nmol/mg dry leaf mass, Fig. 3A). Level of induction varied by type of GLS, with 1‐methylethyl‐GLS and indole‐3‐ylmethyl‐GLS increasing the most in apical leaves as well as plant‐wide (Fig. 3A). Although plant‐wide GLS concentration increased, leaf position 5 experienced a decrease in concentration of all individual foliar GLS (Fig. 3A) following S. nigrita damage. Leaf pools from each leaf positions from S. nigrita‐infested plants generally displayed an increase in GLS content versus mock‐treated leaf pools, with the highest inductions occurring in the position that received S. nigrita damage followed by the two most apical leaf positions.

Bottom Line: In contrast to many mustard specialists, S. nigrita does not prevent formation of toxic breakdown products (mustard oils) arising from glucosinolates (GLS), the primary defensive compounds in mustard plants.Therefore, it is an appealing model for dissecting the early stages of host specialization.Here, we report that jasmonic acid (JA) treatment increased GLS biosynthesis in bittercress, repelled adult female flies, and reduced larval growth.

View Article: PubMed Central - PubMed

Affiliation: Ecology and Evolutionary BiologyUniversity of ArizonaTucsonArizona85721; Rocky Mountain Biological LaboratoryGothicColorado81224; Present address: Organismic and Evolutionary BiologyHarvard UniversityCambridgeMassachusetts02138.

ABSTRACT
Most herbivorous insect species are restricted to a narrow taxonomic range of host plant species. Herbivore species that feed on mustard plants and their relatives in the Brassicales have evolved highly efficient detoxification mechanisms that actually prevent toxic mustard oils from forming in the bodies of the animals. However, these mechanisms likely were not present during the initial stages of specialization on mustard plants ~100 million years ago. The herbivorous fly Scaptomyza nigrita (Drosophilidae) is a specialist on a single mustard species, bittercress (Cardamine cordifolia; Brassicaceae) and is in a fly lineage that evolved to feed on mustards only in the past 10-20 million years. In contrast to many mustard specialists, S. nigrita does not prevent formation of toxic breakdown products (mustard oils) arising from glucosinolates (GLS), the primary defensive compounds in mustard plants. Therefore, it is an appealing model for dissecting the early stages of host specialization. Because mustard oils actually form in the bodies of S. nigrita, we hypothesized that in lieu of a specialized detoxification mechanism, S. nigrita may mitigate exposure to high GLS levels within plant tissues using behavioral avoidance. Here, we report that jasmonic acid (JA) treatment increased GLS biosynthesis in bittercress, repelled adult female flies, and reduced larval growth. S. nigrita larval damage also induced foliar GLS, especially in apical leaves, which correspondingly displayed the least S. nigrita damage in controlled feeding trials and field surveys. Paradoxically, flies preferred to feed and oviposit on GLS-producing Arabidopsis thaliana despite larvae performing worse in these plants versus non-GLS-producing mutants. GLS may be feeding cues for S. nigrita despite their deterrent and defensive properties, which underscores the diverse relationship a mustard specialist has with its host when lacking a specialized means of mustard oil detoxification.

No MeSH data available.


Related in: MedlinePlus