Argonaute 8 (AGO8) Mediates the Elicitation of Direct Defenses against Herbivory1

• Published in: Plant physiology (Bethesda) Vol. 175; no. 2; pp. 927 - 946
• Main Authors: Pradhan, Maitree, Pandey, Priyanka, Gase, Klaus, Sharaff, Murali, Singh, Ravi K., Sethi, Avinash, Baldwin, Ian T., Pandey, Shree P.
• Format: Journal Article
• Language: English
• Published: American Society of Plant Biologists 15-08-2017
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.17.00702

AGO8 forms an important component of induced direct defense machinery as it modulates several regulatory nodes in signaling and response networks during herbivore attack in wild tobacco.
In
Nicotiana attenuata
, specific RNA-directed RNA polymerase (RdR1) and the Dicer-like (DCL3 and DCL4) proteins are recruited during herbivore attack to mediate the regulation of defense responses. However, the identity and role(s) of Argonautes (AGOs) involved in herbivory remain unknown. Of the 11 AGOs in the
N. attenuata
genome, we silenced the expression of 10. Plants silenced in
NaAGO8
expression grew normally but were highly susceptible to herbivore attack. Larvae of
Manduca sexta
grew faster when consuming inverted-repeat stable transformants (ir
AGO8
) plants but did not differ from the wild type when consuming plants silenced in
AGO1
(
a
,
b
, and
c
),
AGO2
,
AGO4
(
a
and
b
),
AGO7
, or
AGO10
expression. ir
AGO8
plants were significantly compromised in herbivore-induced levels of defense metabolites such as nicotine, phenolamides, and diterpenoid glycosides. Time-course analyses revealed extensively altered microRNA profiles and the reduced accumulation of
MYB8
transcripts and of the associated genes of the phenolamide and phenylpropanoid pathways as well as the nicotine biosynthetic pathway. A possible AGO8-modulated microRNA-messenger RNA target network was inferred. Furthermore, comparative analysis of domains revealed the diversity of AGO conformations, particularly in the small RNA-binding pocket, which may influence substrate recognition/binding and functional specificity. We infer that AGO8 plays a central role in the induction of direct defenses by modulating several regulatory nodes in the defense signaling network during herbivore response. Thus, our study identifies the effector AGO of the herbivore-induced small RNA machinery, which in
N. attenuata
now comprises RdR1, DCL3/4, and AGO8.