Phosphite for the prevention of disease caused by Phytophthora species in six rare or threatened species. Will it kill or cure?

Introduction

The oomycete pathogen Phytophthora cinnamomi is a significant threat to Australia’s flora (McDougall and Liew 2024) and is accordingly recognised as such in the listing of the disease it causes as a key threatening process under Commonwealth (Environment Protection and Biodiversity Conservation Act 1999) and New South Wales (NSW) legislation (Biodiversity Conservation Act 2016). Preventing the introduction of Phytophthora species through quarantine and hygiene is the most effective management response for protecting biodiversity assets because, once introduced, the likelihood of eradication is minimal and options for control are few (Cahill et al. 2008).

The only chemical widely used in Australia to control the spread of P. cinnamomi in native vegetation is phosphite (salts of phosphonic acid, H₃PO₃; Hardy et al. 2001). It works directly on the pathogen by inhibiting growth (Jackson et al. 2000) but may also activate a host defence response (Dalio et al. 2014), both of which can slow the spread of infection and increase the likelihood of plant survival. Phosphite can be applied as a foliar spray or injected into the stems of plants, its effectiveness varying with the technique and target plants (Crane and Shearer 2014), which can take up phosphite at greatly different rates (Pilbeam et al. 2000), and even with the isolate of P. cinnamomi (Wilkinson et al. 2001a). Phosphite has been used effectively both in the protection of individual plants in threatened species populations and aerially to slow pathogen spread in vulnerable habitat, especially habitat containing large numbers of species in the family Proteaceae (Barrett and Rathbone 2018; Boulle et al. 2023). However, not all plant species are protected from P. cinnamomi by phosphite and the chemical can be phytotoxic, causing chlorosis of leaves or even plant death (Aberton et al. 1999; Pilbeam et al. 2000).

As the taxonomy of the genus Phytophthora becomes more clear (Burgess et al. 2021), other species are increasingly being regarded as a threat to Australia’s flora (e.g. Phytophthora gregata, McDougall et al. 2018; and Phytophthora multivora, Migliorini et al. 2019). While phosphite can provide protection to some plant species harmed by P. cinnamomi, its effectiveness against other Phytophthora species is variable (Hunter et al. 2022) but largely unknown.

In the case of rare plant species, the potential for either positive or negative effects from phosphite makes its use in the wild problematic. In vitro experimental trials can be used to evaluate efficacy because of the advantage of controlling for plant age and growing conditions (Wilkinson et al. 2001b; Barrett et al. 2003); they are also prudent where the risk to native vegetation is great. In this trial, we tested the effects of P. cinnamomi and P. gregata on six rare or threatened plant species in a glasshouse trial. Three species are susceptible to infection by P. cinnamomi: (1) Hibbertia circinata (critically endangered); (2) Nematolepis rhytidophylla (critically endangered); and (3) Phebalium squamulosum subsp. alpinum (rare) (McDougall and Liew 2024). Three species are susceptible to infection by P. gregata: (1) Boronia deanei (vulnerable); (2) Correa baeuerlenii (vulnerable); and (3) Pimelea bracteata (critically endangered) (Wan et al. 2020). For most of these species, producing large numbers of plants for a well-replicated trial is not possible. The current trial also aims to evaluate whether small pot trials can be informative for assessing negative or positive effects of phosphite on threatened species.

Materials and methods

Results

For the results of the experimental treatments, see Supplementary Table S1.

Phytotoxicity was greatest for C. baeuerlenii, where all sprayed, uninoculated plants died before the end of the trial, and least for N. rhytidophylla, where no plants died (Fig. 1a); for the other species, net mortality associated with phosphite ranged from 17% to 44% and damage to leaves was often visible soon after spraying. For C. baeuerlenii, there was at least some survival of inoculated plants to allow an assessment of phosphite effectiveness.

Fig. 1.

The effect and effectiveness of phosphite on six rare or threatened plant species. (a) Phytotoxicity, the net % of test plants that died after being sprayed with phosphite (equals % of plants that died after treatment with phosphite minus % of control plants that died). (b) Net % of test plants becoming infected (Infection) and that died (Mortality) after inoculation with Phytophthora cinnamomi or Phytophthora gregata (in comparison with control uninoculated plants). +p, plants were treated with phosphite.

Without phosphite application, the pathogen was detected in at least half the plants of all species inoculated and for all but B. deanei, at least half of the inoculated plants died before the end of the trial in comparison with the control treatment (Fig. 1b). With phosphite application, this was also true for all species except N. rhytidophylla, where only one plant (10%) died and P. cinnamomi was recovered from its roots. The percentage of detections of P. gregata in B. deanei plants treated with phosphite was lower than that without phosphite. For species other than B. deanei and N. rhytidophylla, there was no improvement in survival or protection from infection. Indeed, for H. circinata and C. baeuerlenii, there were more deaths of phosphite-treated inoculated plants than control inoculated plants.

Discussion

The level of replication for this trial was unlikely to be great enough to produce unequivocal results unless the effects were profound. However, even if there was no ‘significant difference’ in phytotoxicity between treated and control plants, would land managers tolerate any deaths in small populations of critically endangered species? From our limited study, we can suggest that it should be safe to conduct a field trial using phosphite on N. rhytidophylla because the risk of phytotoxicity appears to be very low and the benefits appear to be potentially substantial. P. cinnamomi is apparently not present in the single population of this species, which occurs in a very remote area rarely visited by humans. However, it is instructive to know that there is a tool to help with control, should the pathogen find its way to the population. We identified a possible benefit from phosphite in reducing infection in B. deanei, and deaths from phytotoxicity in that species were few. Lowering the chance of infection may buy time for this species should P. gregata become a substantial threat in populations. Field trials will then be worthwhile; fortunately, some populations of B. deanei are large enough to permit this.

In field situations, phytotoxic effects may be reduced through low volume application of phosphite, for example using aerial spraying (Barrett 2001). While this could be trialled for plants of C. baeuerlenii, P. bracteata, and P. squamulosum subsp. alpinum because they are numerous enough to localise the risk, our small glasshouse trial suggests that phosphite will have little or no value in control of Phytophthora for these species. However, the risk from aerial spraying to the single small population of H. circinata is likely to be too great because it faces extinction in the coming decades without protection against P. cinnamomi (McDougall et al. 2023). Phosphite gave no apparent benefit and indeed may have weakened inoculated plants, increasing the likelihood of infection and death. For this species, alternative methods for phosphite delivery should be trialled. For instance, phosphite can be delivered effectively as a stem paint (Nyoni et al. 2021), possibly avoiding the scorching effects of a foliar application.

Ultimately, other control options will be required for H. circinata if it is to persist in the wild, and for other threatened species not aided by phosphite such as C. baeuerlenii. This is especially important because disease resistance and the selection of tolerant isolates have been identified with repeated phosphite use (Dobrowolski et al. 2008; Hunter 2018); multiple control options are desirable to avoid this risk. New oomycete-specific chemicals have become available in the past decade but to our knowledge, none has been trialled on native plants in Australia. One of the new chemicals, oxathiapiprolin, has proven effective at controlling Phytophthora agathidicida in kauri trees (Agathis australis) in New Zealand (Lacey et al. 2021). Oxathiapiprolin can be very effective at low concentration and it works in multiple ways to negatively affect the oomycete life cycle (for example, inhibition of zoospore release and sporangial germination, and the prevention of mycelial growth; Cohen 2015). While oxathiapiprolin and related chemicals have been applied to soils as drenches against soil-born oomycetes (Adaskaveg et al. 2024) and as foliar sprays against aerial pathogens (e.g. Phytophthora infestans; Cohen et al. 2018), there is also recent evidence that foliar spraying with oxathiapiprolin can be effective against a root pathogen (Wang et al. 2023). Trials of chemicals such as oxathiapiprolin are urgently needed to broaden control options, and especially for species on the brink of extinction such as Hibbertia circinata.

Our trial of the effectiveness of phosphite for the protection of six rare or threatened species against two Phytophthora species provided useful management information, despite its low replication; the use of phosphite on C. baeuerlenii seems inadvisable because of phytotoxicity and the chemical may be an important future tool for N. rytidophylla conservation. However, phosphite is unlikely to be a panacea for some threatened species; new control options are needed.

Supplementary material

Supplementary material is available online.