Phosphonate sensitivity of phytophthora nicotianae in South African citrus orchards and nurseries

Abstract

The first citrus trees introduced into South Africa were orange seedlings from St. Helena, brought to the Cape by the Dutch East India Company, and planted in the Company’s gardens in 1654. Seven years later, commander Jan van Riebeeck and his wife picked the first oranges from these original trees. By then, numerous other plantings had occurred, including that of 1162 citrus seedlings at Boschheuvel, van Riebeeck’s private estate. However, it was not until 1895 that citrus cultivation in South Africa grew to a commercial scale under the guidance of horticulturists from California, who brought with them the scientifically based methods of the time. In 1907, the first substantial volume of citrus, consisting of 3000 cases, was shipped to England. By, 2022, exports of fresh citrus had grown to 2.6 million tons, making South Africa a world leader and citrus an important asset to the agricultural economy. Citrus trees can have a lifespan of more than a century. During this time, they face a constant barrage of biotic and abiotic challenges. Among these are diseases caused by members of a genus named Phytophthora, which literally means the plant destroyer. Phytophthora species are the most important soil- and water-borne pathogens of citrus and cause a variety of diseases symptoms including, fibrous root rot, crown rot, gummosis, and brown rot of the fruit. The two most important citrus pathogens in this genus are Phytophthora nicotianae and Phytophthora citrophthora. They have been implicated in devastating epidemics on citrus in 19th century Europe. Phytophthora nicotianae is the predominant species in South Africa, with a country-wide distribution, while P. citrophthora is mainly found in the cooler production regions. The management of Phytophthora diseases of citrus involves the use of oomycide chemicals. Ever since the introduction of fosetyl-Al in 1977, phosphonates have formed an integral part of the chemical arsenal against Phytophthora. The name ‘phosphonate’ refers to the esters and salts of phosphonic acid. They have been described as the ideal oomycide due to their ambimobility, complex, multipronged mode of action, persistence in plants yet transient non-toxic nature in the environment, and affordability. It is because of this complex mode of action that phosphonates are considered to be at low risk to resistance development. Despite this, there have recently been reports of reduced phosphonate sensitivity in Phytophthora species, including P. nicotianae and P. citrophthora from citrus. In some instances, this translated into reduced disease control. This is a cause for concern. There is limited knowledge concerning the phosphonate sensitivity of Phytophthora isolates from South African citrus growing areas. To prolong the effective life of phosphonates, resistance management strategies guided by evolutionary principles should be considered. This includes accounting for fitness costs associated with resistance traits. Theoretically, a fitness cost can prevent or slow the development of pesticide resistance, given adequate time between pesticide treatments. Conversely, resistance without a fitness cost will persist, rendering the pesticide permanently ineffective. Therefore, fitness costs have implications for resistance management decisions. Information on fitness costs associated with reduced phosphonate sensitivity in Phytophthora is lacking. Accordingly, the literature review of Chapter 1 summarised the current knowledge on phosphonates as a treatment modality for Phytophthora diseases, with special emphasis placed on citrus and the most relevant Phytophthora species in South Africa. A deeper investigation was carried out into the mode of action of these chemicals and, most importantly, into their current efficacy. Recent reports of reduced phosphonate sensitivity in Phytophthora warranted a discussion of resistance management practices driven by evolutionary principles. Fitness costs associated with resistance and its relevance to resistance management were also discussed in depth. The first experimental work aimed to investigate the phosphonate sensitivity of P. nicotianae isolates from South African citrus production regions, to establish whether phosphonates are still effective at controlling citrus root rot caused by this pathogen. Following the collection and identification of P. nicotianae isolates from citrus growing areas across the country, they were screened for their in vitro sensitivity to potassium- and ammonium phosphite. None were found to be resistant although some had reduced sensitivity, albeit less than previously reported. Furthermore, previous phosphonate exposure did not appear to play a role in the isolate’s phosphonate sensitivity. Subsequently, the efficacy of foliar phosphonate applications against these isolates, was tested on rough lemon seedlings. The phosphonates failed to reduce root rot severity or P. nicotianae concentrations. Although these results could suggest that reduced phosphonate sensitivity has developed in the South African P. nicotianae citrus population, it is unlikely the case. Other factors, such as low root phosphite concentrations, could have led to the observed results. These findings are discussed in detail in Chapter 2. The second aim of the experimental work was to investigate whether reduced phosphonate sensitivity in P. nicotianae was associated with a fitness cost. To this end, the least- and most sensitive isolates from Chapter 2, were compared in vitro and in planta for various measures of fitness. This yielded very little evidence of a fitness cost. However, as these isolates were still comparatively sensitive to phosphonates, the possibility of fitness costs in less sensitive isolates cannot be excluded. Other factors could also have contributed to the observed results. This is discussed fully in Chapter 3. Finally, this thesis is concluded with a summary of the overall findings of this study and possible implications thereof. Suggestions are also made for bettering similar future studies.