Seagrass–pathogen interactions: ‘pseudo-induction’ of turtlegrass phenolics near wasting disease lesions

Abstract

Marine protists of the genus Labyrinthula cause the seagrass wasting disease, which is associated with regional die-offs of eelgrass Zostera marina and also infects turtlegrass Thalassia testudinum. The ability of seagrasses to resist pathogen attack is determined by multiple factors, which are poorly understood. One factor hypothesized to influence seagrass disease resistance is the presence of (poly)phenolic natural products such as caffeic acid, which inhibits the growth of L. zosterae in in vitro laboratory bioassays. This hypothesis has been supported by reports of pathogen-induced phenolic accumulations in eelgrass Z. marina. To test the response of T. testudinum to inoculation with Labyrinthula sp., we conducted a series of culture experiments wherein plants were inoculated with Labyrinthula sp. isolated from turtlegrass beds in Perdido Bay, Florida (USA). Concentrations of phenolic acids and condensed tannins were quantified in diseased leaves as well as those treated with 5 mM salicylic acid, a signaling molecule associated with pathogen-induced responses in plants.In infection experiments, increases in the concentrations of several phenolic acids, but not condensed tannins, were observed in tissues above, but not below, microbial lesions. Salicylic acid (SA) treatments did not induce any phenolic compound, either when applied alone or in concert with the pathogen. The induction of phenolic acids above, but not below, infection sites suggests that T. testudinum leaves did not respond to the pathogen specifically. Instead, the pattern is consistent with the predictions of the sink/source model of plant defense, which predicts increased phenolic contents in cases where wounds disrupt plant resource allocation and cause a local overabundance of carbonbased resources. Thus, we suggest that the emergence of Labyrinthula sp. lesions on turtlegrass blades causes a 'pseudo-induction' of specific phenolics as carbon resources over-accumulate in tissues located above wound sites.

Seagrass wasting disease varies with salinity and depth in natural Zostera marina populations

“…In addition, trans-cinnamate 4-monooxygenase, an enzyme for phenol synthesis, is upregulated in L. zosteraeinoculated shoots (Brakel et al 2014). However, increased phenolic acid production in turtlegrass T. testudinum is only found in infected leaves above the lesions, not below (Steele et al 2005). Those authors therefore suggest that the production of phenolic acids is not a response to L. zosterae infection, but is a pseudo-induction caused by a disruption in carbohydrate allocation within a leaf leading to higher abundance of carbon above the lesions and thereby an accumulation of phenolic acids.…”

Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica

“…Steele et al 2005 and references therein). Moreover, some authors have suggested that phenolics may be storage products when organic carbon is present in excess of that which can be metabolised, or as a result of changing patterns of carbon-based resource allocation (Steele et al 2005). However, the only experimentally demonstrated ecological role of specific seagrass phenolics is that of chemical defence against fouling microorganisms (e.g.…”

“…Harrison 1982) and with the occurrence of pathogen infection (e.g. Steele et al 2005 and references therein). Moreover, some authors have suggested that phenolics may be storage products when organic carbon is present in excess of that which can be metabolised, or as a result of changing patterns of carbon-based resource allocation (Steele et al 2005).…”

Functional, Phylogenetic and Host-Geographic Signatures of Labyrinthula spp. Provide for Putative Species Delimitation and a Global-Scale View of Seagrass Wasting Disease

“…These encompassed 41 separate treatments, including re-testing of several isolates. Protocols generally followed those of Renn (1936) and Muehlstein et al (1988), using the same seagrass culture system as Steele et al (2005), and a Bcommon garden^approach to testing the various isolates and hosts. Briefly, plants were collected as single shoots and acclimated for one week as bare-root cultures while submerged singly within 38 L tanks of natural seawater (≈25-30°C and salinity of ≈ 25-30), with a 12:12 h light:dark cycle and a saturating irradiance of 200 μmol PAR m −2 s −1…”