Evidence for rapid adaptive evolution of tolerance to chemical treatments in Phytophthora species and its practical implications

Abstract

Chemical treatments are used widely in agricultural and natural settings to protect plants from diseases; however, they may exert an important selection pressure on plant pathogens, promoting the development of tolerant isolates through adaptive evolution. Phosphite is used to manage diseases caused by Phytophthora species which include a large number of the most economically damaging plant pathogens worldwide. Phosphite controls the growth of Phytophthora species in planta without killing it; as a result, isolates can develop tolerance to phosphite after prolonged exposure. We investigated the inter- and intra-specific variability in phosphite tolerance of eleven Phytophthora species, including P. ramorum, an internationally important, highly regulated pathogen. Phytophthora ramorum is a good model system because it is comprised of multiple genetically homogeneous lineages. Seven species were found to be consistently sensitive to phosphite based on the low Effective Concentration (EC) 50 values of all isolates tested (amount of phosphite required to inhibit mycelial growth by 50% relative to growth in the absence of phosphite). However, P. ramorum, P. lateralis, P. crassamura and P. cambivora showed intraspecific variability in sensitivity to phosphite, with at least one isolate showing significantly higher tolerance than the other isolates. Within the three P. ramorum evolutionarily divergent lineages tested, NA1 was the most susceptible to phosphite, the NA1 and EU1 lineages showed intralineage variability and the NA2 lineage showed a decreased sensitivity to phosphite overall as all isolates were relatively tolerant. This finding is relevant because NA1 is dominant in the wild and can be controlled using phosphite, while the EU1 lineage has recently been identified in the wild and is phosphite-tolerant, making the treatment approach potentially less effective. Phytophthora ramorum, P. lateralis and P. crassamura are either selfing, homothallic species, or are known to reproduce exclusively clonally, indicating tolerance to phosphite can emerge even in the absence of sexual recombination.

Phytophthora agathidicida: research progress, cultural perspectives and knowledge gaps in the control and management of kauri dieback in New Zealand

“…Although treatment is quick, easy and relatively cheap (a few minutes and less than a dollar for most trees, depending on size), repeated treatments over large areas may not be sustainable. In the long‐term, there is potential to develop resistance to phosphite, such as that observed in other Phytophthora pathosystems with intensive phosphite application (Dobrowolski et al , ; Hunter et al , ). Although to date there is no evidence for this with P. agathidicida , phosphite has not yet been used intensively at regular intervals over a long period of time.…”

Management Strategies for Conservation of Tanoak in California Forests Threatened by Sudden Oak Death: A Disease-Community Feedback Modelling Approach

“…While the model suggests that further field trials on phosphonate protection efficacy would inform stand-level disease management [41], there are some suggestions that recently introduced P. ramorum lineages could develop tolerance to this treatment [62]. Our assumption of transitory chemical protection (1 year), led inevitably to a requirement of long-term follow-up treatments in the model (at two year frequency); a commitment that seems unfeasible except in the most highly managed areas such as arboretums or for important individual trees.…”

Natural Biostimulants Elicit Plant Immune System in an Integrated Management Strategy of the Postharvest Green Mold of Orange Fruits Incited by Penicillium digitatum

“…and Phytophthora spp. ( Yogev et al, 2006 ; Garbelotto et al, 2007 ; Lobato et al, 2008 ; MacKenzie et al, 2009 ; Cerioni et al, 2013 ; Ogoshi et al, 2013 ; Hunter et al, 2018 ; Ramallo et al, 2019 ; Kasuga et al, 2021 ), proving that their use is a practical and effective alternative to conventional fungicides for the control of plant diseases.…”