Domestication for Conservation of an Endangered Species: The Case of the Wollemi Pine

A small population of tall slender conifers was discovered in 1994 in a deep rainforest canyon of the Wollemi National Park, New SouthWales, Australia. The living trees closely resembled fossils that were more than 65 million years old, and this ‘living fossil’ was recognised as a third extant genus in the Araucariaceae (Araucaria, Agathis and now Wollemia). The species was named the Wollemi pine (W. nobilis). Extensive searches uncovered very few populations, with the total number of adult trees being less than 100. Ex situ collections were quickly established in Sydney as part of the Wollemi Pine Recovery Plan. The majority of the ex situ population was later transferred to our custom-built facility in Queensland for commercial multiplication. Domestication has relied very heavily on the species’ amenability to vegetative propagation because seed collection from the natural populations is dangerous, expensive, and undesirable for conservation reasons. Early propagation success was poor, with only about 25% of cuttings producing roots. However, small increases in propagation success have a very large impact on a domestication program because plant production can be modelled on an exponential curve where each rooted cutting develops into a mother plant that, in turn, provides more rooted cuttings. An extensive research program elevated rooting percentages to greater than 80% and also provided in vitro methods for plant multiplication. These successes have enabled international release of the Wollemi pine as a new and attractive species for ornamental horticulture

Myrtle Rust in Australia – a National Action Plan

Myrtle Rust, a plant disease caused by the introduced fungal pathogen Austropuccinia psidii, poses a serious and urgent threat to Australia’s native biodiversity. Myrtle Rust affects plant species in the family Myrtaceae (paperbarks, tea-trees, eucalypts, and lillipillies), which are key and often dominant species in many Australian ecosystems. To date it has proved capable of infecting 382 native species and this number is likely to grow. Serious declines towards extinction are underway in some species, and broader ecological consequences are expected. Myrtle Rust is likely to have a significant impact on matters of national environmental significance protected under national environment law, including listed threatened species and ecological communities, wetlands of international importance, world heritage properties, and national heritage places

Screening Eucalyptus cloeziana and E. argophloia populations for resistance to Puccinia psidii

Disease screening to determine the threat Puccinia psidii poses to plantation and native eucalypts in Australia was undertaken in half-sib families of two contrasting eucalypt species, Eucalyptus cloeziana and E. argophloia. Artificial inoculation with a single-lesion isolate of P. psidii was used to screen these species for resistance to the biotype of P. psidii established in Australia. The objective was to characterize resistance to P. psidii within these two distinct species: E. argophloia, a vulnerable species with a narrow distribution, and E. cloeziana, a species with a broad and extensive distribution in Queensland. Results for E. cloeziana indicate that inland provenances are more resistant to P. psidii infection than provenances from coastal regions. Heritability estimates for the two assessment systems used (resistance on a 1-to-5 ordinal scale verses resistance on a 0-to-1 binomial scale) were low to high (0.24 to 0.63) for E. argophloia and moderate to high (0.4 to 0.91) for E. cloeziana, indicating a significant level of additive genetic variance for rust resistance within the populations. This study demonstrates the potential to select resistant families within the tested populations and indicates that P. psidii could detrimentally affect these species in native forests, nurseries, and plantations. Disease screening to determine the threat Puccinia psidii poses to plantation and native eucalypts in Australia was undertaken in half-sib families of two contrasting eucalypt species, Eucalyptus cloeziana and E. argophloia. Artificial inoculation with a single-lesion isolate of P. psidii was used to screen these species for resistance to the biotype of P. psidii established in Australia. The objective was to characterize resistance to P. psidii within these two distinct species: E. argophloia, a vulnerable species with a narrow distribution, and E. cloeziana, a species with a broad and extensive distribution in Queensland. Results for E. cloeziana indicate that inland provenances are more resistant to P. psidii infection than provenances from coastal regions. Heritability estimates for the two assessment systems used (resistance on a 1-to-5 ordinal scale verses resistance on a 0-to-1 binomial scale) were low to high (0.24 to 0.63) for E. argophloia and moderate to high (0.4 to 0.91) for E. cloeziana, indicating a significant level of additive genetic variance for rust resistance within the populations. This study demonstrates the potential to select resistant families within the tested populations and indicates that P. psidii could detrimentally affect these species in native forests, nurseries, and plantations

Screening Eucalyptus cloeziana and E. argophloia populations for resistance to Puccinia psidii

Disease screening to determine the threat Puccinia psidii poses to plantation and native eucalypts in Australia was undertaken in half-sib families of two contrasting eucalypt species, Eucalyptus cloeziana and E. argophloia. Artificial inoculation with a single-lesion isolate of P. psidii was used to screen these species for resistance to the biotype of P. psidii established in Australia. The objective was to characterize resistance to P. psidii within these two distinct species: E. argophloia, a vulnerable species with a narrow distribution, and E. cloeziana, a species with a broad and extensive distribution in Queensland. Results for E. cloeziana indicate that inland provenances are more resistant to P. psidii infection than provenances from coastal regions. Heritability estimates for the two assessment systems used (resistance on a 1-to-5 ordinal scale verses resistance on a 0-to-1 binomial scale) were low to high (0.24 to 0.63) for E. argophloia and moderate to high (0.4 to 0.91) for E. cloeziana, indicating a significant level of additive genetic variance for rust resistance within the populations. This study demonstrates the potential to select resistant families within the tested populations and indicates that P. psidii could detrimentally affect these species in native forests, nurseries, and plantations. Disease screening to determine the threat Puccinia psidii poses to plantation and native eucalypts in Australia was undertaken in half-sib families of two contrasting eucalypt species, Eucalyptus cloeziana and E. argophloia. Artificial inoculation with a single-lesion isolate of P. psidii was used to screen these species for resistance to the biotype of P. psidii established in Australia. The objective was to characterize resistance to P. psidii within these two distinct species: E. argophloia, a vulnerable species with a narrow distribution, and E. cloeziana, a species with a broad and extensive distribution in Queensland. Results for E. cloeziana indicate that inland provenances are more resistant to P. psidii infection than provenances from coastal regions. Heritability estimates for the two assessment systems used (resistance on a 1-to-5 ordinal scale verses resistance on a 0-to-1 binomial scale) were low to high (0.24 to 0.63) for E. argophloia and moderate to high (0.4 to 0.91) for E. cloeziana, indicating a significant level of additive genetic variance for rust resistance within the populations. This study demonstrates the potential to select resistant families within the tested populations and indicates that P. psidii could detrimentally affect these species in native forests, nurseries, and plantations

Impacts of Myrtle Rust Induced Tree Mortality on Species and Functional Richness within Seedling Communities of a Wet Sclerophyll Forest in Eastern Australia

Austropuccinia psidii is an introduced plant pathogen known to have caused significant declines in populations of several Australian native Myrtaceae species. However, limited research has focused on the impacts of the pathogen on plant communities in the aftermath of its invasion. This study investigated the relationship between disease impact level, plant species diversity, and functional richness in seedling communities in a wet sclerophyll forest in southeast Queensland. A clear shift was found from early colonizer Myrtaceae species in the mid- and understory to a more diverse non-Myrtaceae seedling community indicative of secondary succession. Comparisons of key Myrtaceae species and the seedling community suggest that there may also be a shift towards species that produce drupes and larger seeds, and overall, a current reduction in fruit availability due to the dramatic loss of previously dominant species. Seedling diversity showed no significant correlation with tree mortality, possibly due to favorable rainfall conditions during the study period. The more subtle changes in forest composition, such as changes in fruit type and availability due to myrtle rust, however, could affect the visitation of local bird species in the short term and certainly reduce the store of early colonizing native shrub and tree species

Known or potential threats from pests and diseases to prospective tree species for high value timber plantings in northern Australia

The development of a high value timber industry in northern Australia requires high-level, long-term investment. To secure such a commitment, potential investors and growers must be confident of achieving high productivity and/or high quality end product. Pests and diseases, and their effect on tree health, can be major limiting factors to tree establishment and performance. This is especially true where native or endemic species are to be grown. Timber plantings in northern Australia are likely to be at risk from a number of pests and diseases. This includes both native and exotic species already present within the region, and species not yet present but which have potential to cause problems should they arrive. Existing and potential threats are listed and the more serious problems reviewed

Epidemic spread of smut fungi (Quambalaria) by sexual reproduction in a native pathosystem

Quambalaria are fungal pathogens of Corymbia, Eucalyptus and related genera of Myrtaceae. They are smut fungi (Ustilaginomycota) described from structures that resemble conidia and conidiophores. Whether these spore forms have asexual or sexual roles in life cycles of Quambalaria is unknown. An epidemic of Q. pitereka destroyed plantations of Corymbia in New South Wales and Queensland (Australia) in 2008. We sampled 177 individuals from three plantations of C. variegata and used AFLPs to test hypotheses that the epidemic was spread by asexual reproduction and dominated by a single genotype. There was high genotypic diversity across ≥600 AFLP loci in the pathogen populations at each plantation, and evidence of sexual reproduction based on neighbour-net analyses and rejection of linkage disequilibrium. The populations were not structured by host or location. Our data did not support a hypothesis of asexual reproduction but instead that Q. pitereka spreads exclusively by sexual reproduction, similar to life cycles of other smut fungi. Epidemics were exacerbated by monocultures of Corymbia established from seed collected from a single provenance. This study showcases an example of an endemic pathogen, Q. pitereka, with a strictly outbreeding life cycle that has caused epidemics when susceptible hosts were planted in large monoculture plantations

Impact of the invasive rust Puccinia psidii (myrtle rust) on native Myrtaceae in natural ecosystems in Australia

The invasive rust Puccinia psidii (myrtle rust) was detected in Australia in 2010 and is now established along the east coast from southern New South Wales to far north Queensland. Prior to reaching Australia, severe damage from P. psidii was mainly restricted to exotic eucalypt plantations in South America, guava plantations in Brazil, allspice plantations in Jamaica, and exotic Myrtaceous tree species in the USA; the only previous record of widespread damage in native environments is of endangered Eugenia koolauensis in Hawai’i. Using two rainforest tree species as indicators of the impact of P. psidii, we report for the first time severe damage to endemic Myrtaceae in native forests in Australia, after only 4 years’ exposure to P. psidii. A 3-year disease exclusion trial in a natural stand of Rhodamnia rubescens unequivocally showed that repeated, severe infection leads to gradual crown loss and ultimately tree mortality; trees were killed in less than 4 years. Significant (p < 0.001) correlations were found between both incidence (r = 0.36) and severity (r = 0.38) of P. psidii and subsequent crown loss (crown transparency). This provided supporting evidence to conclude a causal association between P. psidii and crown loss and tree mortality in our field assessments of R. rubescens and Rhodomyrtus psidioides across their native range. Assessments revealed high levels of damage by P. psidii to immature leaves, shoots and tree crowns—averaging 76 % (R. rubescens) and 95 % (R. psidioides) crown transparency—as well as tree mortality. For R. psidioides, we saw exceptionally high levels of tree mortality, with over half the trees surveyed dead and 40 % of stands with greater than 50 % tree mortality, including two stands where all trees were dead. Tree mortality was less prevalent for R. rubescens, with only 12 % of trees surveyed dead and two sites with greater than 50 % mortality. Any alternative causal agents for this tree mortality have been discounted. The ecological implications of this are unclear, but our work clearly illustrates the potential for P. psidii to negatively affect Australia’s biodiversity

Both Constitutive and Infection‐Responsive Secondary Metabolites Linked to Resistance against Austropuccinia psidii (Myrtle Rust) in Melaleuca quinquenervia

Austropuccinia psidii is a fungal plant pathogen that infects species within the Myrtaceae, causing the disease myrtle rust. Myrtle rust is causing declines in populations within natural and managed ecosystems and is expected to result in species extinctions. Despite this, variation in response to A. psidii exist within some species, from complete susceptibility to resistance that prevents or limits infection by the pathogen. Untargeted metabolomics using Ultra Performance Liquid Chromatography with Ion Mobility followed by analysis using MetaboAnalyst 3.0, was used to ex-plore the chemical defence profiles of resistant, hypersensitive and susceptible phenotypes within Melaleuca quinquenervia during the early stages of A. psidii infection. We were able to identify three separate pools of secondary metabolites: (i) metabolites classified structurally as flavonoids that were naturally higher in the leaves of resistant individuals prior to infection, (ii) organoheterocyclic and carbohydrate‐related metabolites that varied with the level of host resistance post‐infection, and (iii) metabolites from the terpenoid pathways that were responsive to disease progression re-gardless of resistance phenotype suggesting that these play a minimal role in disease resistance during the early stages of colonization of this species. Based on the classes of these secondary me-tabolites, our results provide an improved understanding of key pathways that could be linked more generally to rust resistance with particular application within Melaleuca. © 2022 by the authors. Licensee MDPI, Basel, Switzerland

Phylogeny of the Quambalariaceae fam. nov., including important Eucalyptus pathogens in South Africa and Australia

The genus Quambalaria consists of plant-pathogenic fungi causing disease on leaves and shoots of species of Eucalyptus and its close relative, Corymbia. The phylogenetic relationship of Quambalaria spp., previously classified in genera such as Sporothrix and Ramularia, has never been addressed. It has, however, been suggested that they belong to the basidiomycete orders Exobasidiales or Ustilaginales. The aim of this study was thus to consider the ordinal relationships of Q. eucalypti and Q. pitereka using ribosomal LSU sequences. Sequence data from the ITS nrDNA were used to determine the phylogenetic relationship of the two Quambalaria species together with Fugomyces (= Cerinosterus) cyanescens. In addition to sequence data, the ultrastructure of the septal pores of the species in question was compared. From the LSU sequence data it was concluded that Quambalaria spp. and F. cyanescens form a monophyletic clade in the Microstromatales, an order of the Ustilaginomycetes. Sequences from the ITS region confirmed that Q. pitereka and Q. eucalypti are distinct species. The ex-type isolate of F. cyanescens, together with another isolate from Eucalyptus in Australia, constitute a third species of Quambalaria, Q. cyanescens (de Hoog & G.A. de Vries) Z.W. de Beer, Begerow & R. Bauer comb. nov. Transmission electron-microscopic studies of the septal pores confirm that all three Quambalaria spp. have dolipores with swollen lips, which differ from other members of the Microstromatales (i.e. the Microstromataceae and Volvocisporiaceae) that have simple pores with more or less rounded pore lips. Based on their unique ultrastructural features and the monophyly of the three Quambalaria spp. in the Microstromatales, a new family, Quambalariaceae Z.W. de Beer, Begerow & R. Bauer fam. nov., is described