Variation in susceptibility among macadamia genotypes and species to Phytophthora root decay caused by Phytophthora cinnamomi
Introduction
Four species of macadamia (Macadamia integrifolia, Macadamia tetraphylla, Macadamia ternifolia and Macadamia jansenii) originate in Eastern Australia and represent a significant resource for the macadamia industry, as potential sources of resistance to biotic and abiotic stress, and for improving yield and quality. The wild germplasm is vulnerable to extinction due to habitat loss and fragmentation (Pisanu et al., 2009, Neal et al., 2010, Powell et al., 2010). Under the Australian Environment Protection and Biodiversity Conservation Act, 1999, three species (M. integrifolia, M. tetraphylla and M. ternifolia) are listed as vulnerable while M. jansenii is listed as endangered (Shapcott and Powell, 2011). M. ternifolia and M. jansenii do not produce edible nuts and mostly exist in the wild ecosystem (Hardner et al., 2009). M. integrifolia and hybrids with M. tetraphylla constitute the current commercial macadamia production worldwide (Hardner et al., 2009). Genetic diversity that exists in the wild populations of Macadamia has not been explored for resistance to pathogens and pests, yield, quality or tolerance to abiotic stresses.
Macadamia trees in commercial orchards are propagated on grafted rootstocks derived from either vegetatively propagated clonal cuttings or germinated open-pollinated seeds (Hardner et al., 2009). Most rootstocks are selected based on ease of germination, propagation and grafting rather than their resistance to biotic or abiotic stress. In Australia, nearly all the grafted trees in commercial macadamia orchards are established on seedlings rootstocks of the cultivar ‘H2’, a M. integrifolia & M. tetraphylla hybrid. In South Africa, clonal cuttings of cultivar ‘Beaumont’ (HAES 695) a M. tetraphylla & M. integrifolia hybrid are preferred as rootstocks (Trochoulias, 1992, Huett, 2004, Hardner et al., 2009). Phenotypic characteristics of ‘H2’ are similar to the M. integrifolia characteristics, whereas, the ‘Beaumont’ characteristics are similar to M. tetraphylla. There is little information to support the choice of either genotype as rootstock in macadamia. The root systems of seedling populations are likely to have a high degree of variation in terms of root architecture and efficiencies of nutrient utilization (Stephenson and Cull, 1986), which may influence their performance with regard to impact on disease expression. The root systems of vegetatively propagated cutting-derived rootstocks of a particular variety are more likely to be very similar and equally susceptible to invading root pathogens since they are clonally propagated.
Phytophthora cinnamomi is an important soilborne pathogen in macadamia, and is considered a major constraint of macadamia production worldwide (Drenth et al., 2009, Akinsanmi and Drenth, 2013a). Since P. cinnamomi was introduced into Australia, it now occurs widely in all states and territories where it causes disease in a several plant species (Cahill et al., 2008, Hee et al., 2013). Information on the susceptibility of the Australian native Macadamia species is scanty. The diseases caused by P. cinnamomi are of significant economic importance in many horticultural crops including macadamia therefore research, focused on its control, continues to be a priority in many Australian horticultural and forestry industries.
P. cinnamomi can cause a range of symptoms in macadamias. At the early stage of P. cinnamomi infection, disease symptom expression is often misdiagnosed, or appears as general tree decline due to poor nutrition. Tree decline associated with P. cinnamomi is usually expressed as pale or yellow green leaves instead of dark green. Under conditions of moisture stress, in the advanced stages of infection, the leaves of infected trees rapidly wilt and readily abscise from the tree, giving rise to a sparse canopy appearance. The later stages of symptoms are more evident in macadamia following prolonged water-logging or drought conditions (Akinsanmi and Drenth, 2013b). Most times, fresh leaf flushes and shoot growth are absent or sparse and branches die back from the tip (Pegg, 1973). P. cinnamomi may directly infect macadamia stems or branches causing numerous small stem or trunk cankers. Infections of the stem are first characterized as gummosis or bleeding of the trunk and cracking of the bark which, in more advanced stages of the disease may develop in irregular areas of dead bark that extend from the soil line to several feet high. This often results in furrowed deep cankers on the trunk.
Diseases caused by P. cinnamomi from root infections are difficult to control (Ali et al., 2000). In macadamia, chemical applications with phosphonates and metalaxyl have been reported to be effective against diseases caused by P. cinnamomi (Akinsanmi and Drenth, 2013b). Selection for resistance to Phytophthora in macadamia may offer additional advantages and may be an effective means of controlling Phytophthora-incited diseases compared with chemical control in macadamia. The resistance system in macadamia genotypes to P. cinnamomi is not well understood.
Although early reports suggested that macadamia roots are resistant to P. cinnamomi (Zentmyer, 1960), subsequent studies have reported that P. cinnamomi is able to infect macadamia roots. These studies suggested that symptoms of root infection may be expressed as root necrosis and soft root rot (Ko and Kunimoto, 1976, Serfontein, 2008, Mbaka et al., 2009). Black to dark necrotic lesions observed on macadamia fine roots are associated with P. cinnamomi infection, but there has been no clear or consistent re-isolation of P. cinnamomi from roots showing black root symptoms. Although several varieties are affected by P. cinnamomi under orchard conditions, there is still confusion as to whether P. cinnamomi causes soft root rot or necrosis. Although a preliminary study by Zentmyer and Storey (1961) suggested differences between M. integrifolia and M. tetraphylla to P. cinnamomi infection and variation is observed among varieties of grafted trees in orchard conditions, there is little information on the relative susceptibility of different Macadamia species and selections to P. cinnamomi.
Selection of P. cinnamomi resistant rootstocks depends on the presence and variability in susceptibility to P. cinnamomi among different macadamia selections and species. Material with genetic resistance to P. cinnamomi may be used directly as rootstocks or as parents in breeding programmes. This will provide a more long-term and economical approach to managing diseases caused by P. cinnamomi in macadamia than the current application of agrochemicals as the main control method (Akinsanmi and Drenth, 2013b). In this study, we hypothesize that the non-cultivated species (M. ternifolia and M. jansenii) are more tolerant to P. cinnamomi than the two species (M. integrifolia and M. tetraphylla) or their hybrids that are cultivated in commercial production systems. We also evaluated the range of susceptibility among the four species of macadamia and their interspecific hybrids to root infections by P. cinnamomi. This study provides a more definitive description of symptoms of root infection by P. cinnamomi in macadamia. For the purpose of this study, we defined root necrotic lesions as any localized area of root tissue with extended spot, canker or scab, while root rot refers to the softness or decay of the root tissue that compromise its structural integrity.
Section snippets
Plant materials and inoculation
Plants of four Macadamia species (M. integrifolia, M. tetraphylla, M. ternifolia and M. jansenii), two accessions of reverse crosses of M. ternifolia × M. jansenii, three accessions (ITH-1425, ITH-4323, ITH-679) of M. integrifolia & M. tetraphylla hybrids and one accession (ITH-Beau) of M. tetraphylla & M. integrifolia hybrid that represent a range of genotypes were selected. A total of 132 plants were established in the glasshouse, propagated as own-rooted cuttings (clonal) or seedlings as
Relative susceptibility of Macadamia species and hybrids to P. cinnamomi
The consistency between the trials is shown in Table 1. Results of the accumulated analysis of variance showed similar (P > 0.05) results between the repeat runs, whereas, disease severity levels were significantly (P < 0.001) different among the macadamia germplasm of the four Macadamia species and their hybrids (Table 1). Varying degrees of root decay were observed in roots infected with P. cinnamomi among the macadamia germplasm, from darkening of the primary and secondary feeder roots to
Discussion
This study revealed the relative susceptibility of the four Macadamia species to root infections by P. cinnamomi and showed that cultivated species are more tolerant than the non-edible species. M. tetraphylla was the most tolerant species while M. ternifolia was the most susceptible species to P. cinnamomi root infection. The relative tolerance of M. tetraphylla compared with M. integrifolia may support its use as a preferred rootstock for protection against the soilborne P. cinnamomi pathogen
Acknowledgements
The research was funded by Horticulture Innovation Australia Limited with levy funds from the Australian macadamia industry (Project MC12007).
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