Jasmonic and salicylic acid response in the fern Azolla filiculoides and its cyanobiont

Abstract

Plants sense and respond to microbes utilizing a multilayered signalling cascade. In seed plants, the phytohormones jasmonic and salicylic acid (JA and SA) are key denominators of how plants respond to certain microbes. Their interplay is especially well-known for tipping the scales in plants' strategies of dealing with phytopathogens. In non-angiosperm lineages, the interplay is less well understood, but current data indicate that it is intertwined to a lesser extent and the canonical JA/SA antagonism appears to be absent. Here, we used the water fern Azolla filiculoides to gain insights into the fern's JA/SA signalling and the molecular communication with its unique nitrogen fixing cyanobiont Nostoc azollae, which the fern inherits both during sexual and vegetative reproduction. By mining large-scale sequencing data, we demonstrate that Azolla has most of the genetic repertoire to produce and sense JA and SA. Using qRT-PCR on the identified biosynthesis and signalling marker genes, we show that Azolla is responsive to exogenously applied SA. Furthermore, exogenous SA application influenced the abundance and gene expression of Azolla's cyanobiont. Our data provide a framework for JA/SA signalling in ferns and suggest that SA might be involved in Azolla's communication with its vertically inherited cyanobiont.

On plant defense signaling networks and early land plant evolution

“…However, other lycophytes including another species from the genus Selaginella did not produce measurable levels of JA [127], supporting the notion of a high species-specificity in JA biosynthesis. Similarly, some species of ferns show pronounced JA responses, while others do not [134-136]; likewise, the production of JA was shown to be species-specific in ferns [127]. This distribution of JA biosynthesis becomes less patchy in gymnosperms and angiosperms, as shown in the dataset by Gachet and colleagues [127], where only one species in each of these two lineages was identified that did not produce a detectable amount of JA.…”

“…Indeed, Thaler et al [141] and Han [125] suggested that the JA/SA-antagonism arose at the earliest in seed plants. Along these lines, it was hypothesized that in the fern Azolla some JA-orchestrated signaling responses may be initiated via SA instead of JA because MeSA application induced the expression of Plant Defensin 1.4 ( AfPDF1.4 [136]); in Arabidopsis, PDFs are JA-responsive [142]. These results, together with the data from mosses, speak in favor of a reduced antagonism – or perhaps complete lack thereof – between JA and SA in mosses and ferns.…”

Volatile emissions of six New Zealand fern species in response to physical damage and herbivory

“…There are two possible explanations for this outcome: (1) JA is not involved in anti-herbivore responses in all ferns, (2) all ferns use JA but differ in their thresholds or the time needed to trigger anti-herbivore-responses. Recent studies indicate that the water fern Azolla filiculoides has genes for the production and sensing of jasmonic and salicylic acids, indicating that JA signalling can be a highly conservative mechanism (de Vries et al 2018). More studies are needed to establish if JA is a universal molecule mediating anti-herbivore responses in plants, and if so, the threshold levels and response times required by different fern species.…”

Hormonal complex of gametophytes of Dryopteris filix-mas (Dryopteridaceae) in in vitro culture

“…Відомо лише, що екзогенне використання СК при культивуванні водної папороті Azolla filiculoides Lam., яка утворює симбіоз з азотфіксуючою ціанобактерією Trichormus azollae (Strasburger) Komárek & Anagnostidis (Nostoc azollae), виявило присутність у папороті СК-генів, відповідальних за експресію та сигналінг. Крім того, екзогенна СК впливала на активність генів ціанобіонта (De Vries et al, 2018).…”