Argonaute 8 (AGO8) Mediates the Elicitation of Direct Defenses against Herbivory

Pradhan, Maitree; Pandey, Priyanka; Gase, Klaus; Sharaff, Murali; Singh, Ravi; Sethi, Avinash; Baldwin, Ian Thomas; Pandey, Sarvesh

doi:10.1104/pp.17.00702

Cited by 29 publications

(35 citation statements)

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“…In brief, DNA extracted from individual transgenic plants was used for NanoString to detect the content of inserted fragments according to the designed probes. To validate the single-copy-number insertions inferred from the segregation rates, a published single-copy insertion stably transformed line, ago8 (871-8-8), was used as a positive control [ 82 ]. The following three previously characterized transgenic lines were also used in this study: myb8 (A-07-810-2) plants silenced in the expression of MYB8 gene [ 47 ]; pmt (A-03-108-3) plants silenced in the expression of putrescine N-methyltransferase, a key nicotine biosynthetic enzyme [ 51 ]; and aoc (A-07-457-1) plants silenced in the expression of AOC, a single-copy key biosynthetic enzyme in JA biosynthesis [ 45 ].…”

Section: Methodsmentioning

confidence: 99%

Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores

Joo

Cao

et al. 2020

PLoS Biol

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Plants are attacked by herbivores, which often specialize on different tissues, and in response, have evolved sophisticated resistance strategies that involve different types of chemical defenses frequently targeted to different tissues. Most known phytohormones have been implicated in regulating these defenses, with jasmonates (JAs) playing a pivotal role in complex regulatory networks of signaling interactions, often generically referred to as "cross talk." The newly identified class of phytohormones, strigolactones (SLs), known to regulate the shoot architecture, remain unstudied with regard to plant-herbivore interactions. We explored the role of SL signaling in resistance to a specialist weevil (Trichobaris mucorea) herbivore of the native tobacco, Nicotiana attenuata, that attacks the root-shoot junction (RSJ), the part of the plant most strongly influenced by alterations in SL signaling (increased branching). As SL signaling shares molecular components, such as the core Fbox protein MORE AXILLARY GROWTH 2 (MAX2), with another new class of phytohormones, the karrikins (KARs), which promote seed germination and seedling growth, we generated transformed lines, individually silenced in the expression of NaMAX2, DWARF 14 (NaD14: the receptor for SL) and CAROTENOID CLEAVAGE DIOXYGENASE 7 (NaCCD7: a key enzyme in SL biosynthesis), and KARRIKIN INSENSITIVE 2 (NaKAI2: the KAR receptor). The mature stems of all transgenic lines impaired in the SL, but not the KAR signaling pathway, overaccumulated anthocyanins, as did the stems of plants attacked by the larvae of weevil, which burrow into the RSJs to feed on the pith of N. attenuata stems. T. mucorea larvae grew larger in the plants silenced in the SL pathway, but again, not in the KAI2-silenced plants. These phenotypes were associated with elevated JA and auxin (indole-3-acetic acid [IAA]) levels and significant changes in the accumulation of defensive compounds, including phenolamides and nicotine. The overaccumulation of phenolamides and anthocyanins in the SL pathway-silenced plants likely resulted from antagonism between the SL and JA pathway in N. attenuata. We show that the repressors of SL signaling, suppressor of max2-like (NaSMXL6/7), and JA signaling, jasmonate zim-domain

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Section: Methodsmentioning

confidence: 99%

Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores

Joo

Cao

et al. 2020

PLoS Biol

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“…Feeding by D. noxia on susceptible and resistant wheat induced similar responses in TaAGO5 regulation for susceptible plants, where a twofold induction was observed 1 h after the aphids were placed on the plants. This increased steadily and peaked at threefold induction at 48 h. Similarly, NaAGO5 was differentially regulated in N. tabacum by M. sexta larvae oral secretions (Pradhan et al, 2017). Oral secretions elicited a sixand threefold increase in NaAGO5 and 8 at 18 h. This differential regulation in response to M. sexta oral secretions was only observed for NaAGO5 and 8.…”

Section: Discussionmentioning

confidence: 82%

“…This role is similar to that observed for NaAGO8 in Nicotiana tabacum against Manduca sexta. Results from Pradhan et al (2017) suggested this holds true for NaAGO5. Knockdown of NaAGO8 directly affected phytohormone biosynthesis and the production of nicotine, diterpenoid glycosides, and phenolamides under MYB8 transcription factor regulation.…”

Section: Discussionmentioning

confidence: 90%

“…Taken together, this may point to a similar regulation of the phytohormone and secondary metabolite pathways in the wheat-D. noxia interaction when compared with NaAGO8 after arthropod feeding. The extent of the role that TaAGO5 plays in this is not clear; however, Pradhan et al (2017), proposes that AGO5 and AGO8 proteins may have overlapping targets based on similarity in their roles during arthropod herbivory. This may hold true for TaAGO5 and TaAGO8 proteins during the wheat defense response against the intimate feeding by D. noxia.…”

Section: Discussionmentioning

confidence: 99%

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Wheat Argonaute 5 Functions in Aphid–Plant Interaction

Sibisi

Venter

2020

Front. Plant Sci.

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Aphids feeding on plants experience similar responses to pathogens due to the prolonged and intimate contact with the plant. Diuraphis noxia is an economically important aphid pest on wheat that exhibits such an interaction. Studies on small RNA (sRNA) that regulate genes imparting resistance to wheat against D. noxia have predicted an Argonaute 5 (TaAGO5) gene as possible role player in the resistance response. Functional characterization revealed that TaAGO5 is crucial in regulating the response to infestation by D. noxia. Knockdown of TaAGO5 by 22% in D. noxia resistant wheat resulted in a completely susceptible phenotype. The fecundity and stress levels of D. noxia feeding on these silenced plants were similar to aphids feeding on the susceptible controls. Thus, TaAGO5 is crucial in the defense response by wheat plants during aphid feeding and this is similar to Nicotiana benthaminia plants experiencing arthropod herbivory. Additionally, TaAGO5 was differentially regulated by the Barley mosaic virus (BMV) used in the functional characterization. This provides evidence that TaAGO5 could play a role during virus infection of wheat. The role of AGO5 proteins in plant responses to arthropod herbivory and virus infection is known for dicotyledonous plants. Here, we present data that indicate that this role of TaAGO5 is conserved in wheat and possibly for monocotyledonous plants. These observations extend our knowledge on the roles of AGO proteins in plant resistance.

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“…The genome of N. attenuata harbors three RDRs [44–46], four DCLs [47] and 11 AGOs [48]. RdR1, DCL3 and DCL4 and AGO8 were shown to contribute to N. attenuata’s herbivore resistance [44, 47, 49]. Furthermore, the context-dependent importance of AMF on N. attenuata’s growth and fitness has been shown.…”

Section: Introductionmentioning

confidence: 99%

Complex regulation of microRNAs in roots of competitively-grown isogenic Nicotiana attenuata plants with different capacities to interact with arbuscular mycorrhizal fungi

et al. 2018

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BackgroundNicotiana attenuata is an ecological model plant whose 2.57 Gb genome has recently been sequenced and assembled and for which miRNAs and their genomic locations have been identified. To understand how this plant’s miRNAs are reconfigured during plant-arbuscular mycorrhizal fungal (AMF) interactions and whether hostplant calcium- and calmodulin dependent protein kinase (CCaMK) expression which regulates the AMF interaction also modulates miRNAs levels and regulation, we performed a large-scale miRNA analysis of this plant-AMF interaction.ResultsNext generation sequencing of miRNAs in roots of empty vector (EV) N. attenuata plants and an isogenic line silenced in CCaMK expression (irCCaMK) impaired in AMF-interactions grown under competitive conditions with and without AMF inoculum revealed a total of 149 unique miRNAs: 67 conserved and 82 novel ones. The majority of the miRNAs had a length of 21 nucleotides. MiRNA abundances were highly variable ranging from 400 to more than 25,000 reads per million. The miRNA profile of irCCaMK plants impaired in AMF colonization was distinct from fully AMF-functional EV plants grown in the same pot. Six conserved miRNAs were present in all conditions and accumulated differentially depending on treatment and genotype; five (miR6153, miR403a-3p, miR7122a, miR167-5p and miR482d, but not miR399a-3p) showed the highest accumulation in AMF inoculated EV plants compared to inoculated irCCaMK plants. Furthermore, the accumulation patterns of sequence variants of selected conserved miRNAs showed a very distinct pattern related to AMF colonization - one variant of miR473-5p specifically accumulated in AMF-inoculated plants. Also abundances of miR403a-3p, miR171a-3p and one of the sequence variants of miR172a-3p increased in AMF-inoculated EV compared to inoculated irCCaMK plants and to non-inoculated EV plants, while miR399a-3p was most strongly enriched in AMF inoculated irCCaMK plants grown in competition with EV. The analysis of putative targets of selected miRNAs revealed an involvement in P starvation (miR399), phytohormone signaling (Nat-R-PN59, miR172, miR393) and defense (e.g. miR482, miR8667, Nat-R-PN-47).ConclusionsOur study demonstrates (1) a large-scale reprograming of miRNAs induced by AMF colonization and (2) that the impaired AMF signaling due to CCaMK silencing and the resulting reduced competitive ability of irCCaMK plants play a role in modulating signal-dependent miRNA accumulation.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5338-x) contains supplementary material, which is available to authorized users.

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Argonaute 8 (AGO8) Mediates the Elicitation of Direct Defenses against Herbivory

Cited by 29 publications

References 83 publications

Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores

Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores

Wheat Argonaute 5 Functions in Aphid–Plant Interaction

Complex regulation of microRNAs in roots of competitively-grown isogenic Nicotiana attenuata plants with different capacities to interact with arbuscular mycorrhizal fungi

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