Field survival and growth of clonal, micropropagated Eucalyptus marginata selected for resistance to Phytophthora cinnamomi

doi:10.1016/j.foreco.2006.10.028

Forest Ecology and Management

Volume 238, Issues 1–3, 30 January 2007, Pages 330-334

https://doi.org/10.1016/j.foreco.2006.10.028 Get rights and content

Abstract

Clones of jarrah (Eucalyptus marginata), micropropagated from glasshouse-grown seedlings selected for resistance or susceptibility to Phytophthora cinnamomi, were planted in a former bauxite mine-site in the jarrah forest and inoculated with P. cinnamomi. Mortality after 13 years in resistant clones was 0–30%, while that of susceptible clones was 40–100%. Mean heights of resistant clones after 13 years were 7.8–13.6 m, while heights of surviving susceptible clones were 0.9–6.7 m. The resistance character of the seedling ortets was transmitted consistently to the clones. The field mortality of clones of some rare, apparently resistant seedlings selected from susceptible half-sib families was low after 1 year, but approached that of the susceptible clones after 2 years. The results show that Phytophthora-resistant jarrah ortets can be selected using stem-inoculation of glasshouse-grown seedlings; the resistance of the resulting clones has been validated in the field in an inoculation trial.

Introduction

Jarrah (Eucalyptus marginata Donn ex Sm.) is Western Australia's most important hardwood timber-producing species, and is endemic in the south-west region of the state. The “jarrah dieback” disease caused by the root-rotting water-mould Phytophthora cinnamomi Rands (Podger, 1972) has caused serious damage to the jarrah forest, with the most severely affected areas being located in the higher rainfall zone on the western edge of the Darling Scarp, and further south in the Donnybrook Sunklands (Shearer and Tippett, 1989).

The existence of genetically based resistance to P. cinnamomi in jarrah has been demonstrated in pot and field trials, using seedlings from open-pollinated mother trees selected in the forest (Stukely and Crane, 1994). There was wide variation in resistance levels between these “families” of half-sib seedlings, and also between individual seedlings within families. Narrow-sense heritability of the resistance was very high at both family (0.78–0.85) and individual tree (0.43 ± 0.18) levels, and this is believed to be under polygenic control (Stukely and Crane, 1994). Selected P. cinnamomi-resistant lines of jarrah could be useful in rehabilitation of degraded jarrah forest sites.

Jarrah can be propagated by tissue culture (McComb and Bennett, 1982), and resistance to P. cinnamomi has been shown to exist in some micropropagated clonal lines of jarrah (Bennett et al., 1993). The purpose of this study was to compare the field survival and growth of jarrah clones derived from seedlings that had been selected for resistance or susceptibility to P. cinnamomi in glasshouse screening trials, in order to validate the resistant selections for use in the restoration planting of dieback-affected jarrah forest sites. Some of the mortality results were included in preliminary reports (McComb et al., 1990, Stukely et al., 2001).

Section snippets

Selection of E. marginata lines

Half-sib families of 14-month-old pot-grown E. marginata seedlings were stem-inoculated with P. cinnamomi type A2 (IMI 264384) as described previously (Stukely and Crane, 1994). Necrotic lesions developing in the stems were measured for 14 days, after which the stems were pruned to remove infected tissue and to encourage healthy axillary growth from the basal regions of the plants for use in tissue culture.

The relative levels of “resistance” or “susceptibility” to P. cinnamomi of 16 seedling

Results

Survival of the clones from field planting to the time of inoculation was 98%; P. cinnamomi was not isolated from the roots of the three plants (of three different clones) which died prior to inoculation. P. cinnamomi was isolated from the roots of 94% of clones which died in the first 2 years after inoculation. Three months after inoculation (December 1988), P. cinnamomi was still readily isolated from the pine inoculum plugs excavated with dead plants. Recoveries from the plugs diminished as

Discussion

Clonal E. marginata, micropropagated from seedlings selected for their outstanding levels of resistance to P. cinnamomi (category RR) in glasshouse screening trials, exhibited very low (0–30%) mortality 13 years after planting in a field site inoculated with P. cinnamomi. In contrast, the mortality of clones of P. cinnamomi-susceptible seedlings (category SS) was high (40–100%). Furthermore, the heights of 2–13-year-old RR clones, and their mean annual increments of height, were consistently

Acknowledgements

We thank Alcoa World Alumina Australia for preparing the field site for planting, and for their continuing support of the Dieback Resistant Jarrah program. Matthew R. Williams advised and assisted with statistical analyses, and Edward L.K. Lim assisted with the later trial assessments and measurements.

References (14)

I.J. Bennett et al.
Inoculation of Eucalyptus marginata Donn ex Sm. (jarrah) clones with Phytophthora cinnamomi Rands in vitro and under glasshouse conditions
For. Ecol. Manage.
(1993)
T.B. Butcher et al.
Genetic variation in resistance of Pinus radiata to Phytophthora cinnamomi
For. Ecol. Manage.
(1984)
D.M. Cahill et al.
A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi
Physiol. Mol. Plant Pathol.
(1992)
J. Bartle et al.
Mining and rehabilitation
T.B. Butcher et al.
Field response of Pinus radiata selected for resistance to Phytophthora cinnamomi
D.M. Cahill et al.
Resistance of micropropagated Eucalyptus marginata to Phytophthora cinnamomi
Plant Dis.
(1992)
D.M. Cahill et al.
Mechanisms of resistance to Phytophthora cinnamomi in clonal, micropropagated Eucalyptus marginata
Plant Pathol.
(1993)

There are more references available in the full text version of this article.

Cited by (19)

Current practices and emerging possibilities for reducing the spread of oomycete pathogens in terrestrial and aquatic production systems in the European Union
2022, Fungal Biology Reviews
Citation Excerpt :
A successful long-term breeding programme for Port Orford cedar (Chamaecyparis lawsoniana) resulted in commercial production of host genotypes resistant to P. lateralis infection (Hayden et al., 2013). Likewise, the occurrence of heritable variation in resistance to oomycetes species has been demonstrated on other tree species, e.g., in Castanea spp. to P. cinnamomi and Phytophthora × cambivora, in Alnus glutinosa to Phytophthora × alni, Eucalyptus marginata to P. cinnamomi, in Pinus radiata to P. cinnamomi, and in Lithocarpus densiflorus to P. ramorum, indicating potential for resistance breeding programmes (Robin et al., 2006; Miranda-Fontaíña et al., 2007; Stukely et al., 2007; Hayden et al., 2013; Shearer et al., 2014; Santos et al., 2015; Chandelier et al., 2016; Jung et al., 2018). In contrast to plants, there are no data available on breeding for oomycete resistance in fish farming (OIE, 2019b).
Diseases caused by oomycete pathogens are a global threat to forestry, agriculture and aquaculture. Because of their complex life cycles, characterised by dormant resting structures that enable their survival for years under hostile environmental conditions, reducing the spread of oomycetes is a challenging task. In this review, we present an overview of this challenge, starting from the need to understand the natural and anthropogenic dispersal pathways of these pathogens. Focusing on the European Union, we explore current legislation that forms a backbone for biosecurity protocols against the spread of oomycetes through trade and transport. We discuss the options for prevention, containment and long-term management of oomycetes in different production settings, emphasising the importance of prevention as the most cost-efficient strategy to reduce the spread of these pathogens. Finally, we highlight some of the new and emerging technologies and strategies as potential tools in the integrated pest management of animal and plant diseases caused by oomycetes. We emphasise the urgency of actions to halt the global spread of these pathogens.
Phytophthora cinnamomi as a driver of forest change: Implications for conservation and management
2018, Forest Ecology and Management
Citation Excerpt :
Screening of jarrah suggests that jarrah susceptibility to Pc is variable, and that genetic resistance to Pc is present to varying degrees in natural populations (Stukely & Crane, 1994). Jarrah seedlings can be screened for resistance at an early growth stage as resistance in seedlings is correlated with in-field survival and growth (Stukely et al., 2007). Continued research elucidating genetic mechanisms for resistance to Pc in jarrah and other susceptible species in this ecosystem will inform development of varieties with improved resistance, useful for ecosystem restoration.
Phytophthora cinnamomi is a soil-borne plant pathogen of global significance, threatening many forest tree species around the world. In contrast to other well-known tree pathogens, P. cinnamomi is a generalist pathogen that, in many cases, causes less immediately obvious symptoms, making P. cinnamomi more difficult to diagnose. This creates special challenges for those trying to assess and manage diseases caused by P. cinnanmomi. P. cinnamomi affects a wide range of tree species across the world including chestnuts, particularly American and European chestnuts, Eucalyptus and Banksia species in Australia, and oaks in Mediterranean Europe. We believe that forest professionals should incorporate an understanding of the diseases caused by P. cinnamomi in conservation, management, and restoration of threatened ecosystems dominated by P. cinnamomi-affected tree species. Here we review the impact of P. cinnamomi on forest ecosystems internationally and suggest three major strategies for improving forest resilience to P. cinnamomi: (1) Improving site quality to reduce risk of P. cinnamomi-related disease, (2) Genetically improving threatened species to improve resistance to P. cinnamomi, and (3) Restricting further spread (especially by nursery trade) of P. cinnamomi.
Developing a taxonomic identification system of Phytophthora species based on microsatellites
2013, Revista Iberoamericana de Micologia
Phytophthora is the most important genus of the Oomycete plant pathogens. Nowadays, there are 117 described species in this genus, most of them being primary invaders of plant tissues. The different species are causal agents of diseases in a wide range of crops and plants in natural environments. In order to develop control strategies against Phytophthoraspecies, it is important to know the biology, ecology and evolutionary processes of these important pathogens.
The aim of this study was to propose and validate a low cost identification system for Phytophthora species based on a set of polymorphic microsatellite (SSRs) markers.
Thirty-three isolates representing Phytophthora infestans, Phytophthora andina, Phytophthora sojae, Phytophthora cryptogea, Phytophthora nicotianae, Phytophthora capsici and Phytophthora cinnamomi species were obtained, and 13 SSRs were selected as potentially transferable markers between these species. Amplification conditions, including annealing temperatures, were standardized for several markers.
A subset of these markers amplified in all species, showing species-specific alleles.
The adaptability and impact of the identification system in Colombia, an Andean agricultural country where different Phytophthora species co-exist in the same or in several hosts grown together, are discussed.
Phytophthora es el género más importante de los oomicetos, que son patógenos vegetales. Actualmente se han descrito 117 especies de este género, siendo la mayoría invasivas primarias de los tejidos vegetales. Las diferentes especies son agentes causales de enfermedades en una amplia variedad de cultivos y plantas en su medio natural. Con el objetivo de formular estrategias eficientes de control frente a especies de Phytophthora, es primordial conocer la biología, ecología y procesos evolutivos de estos importantes patógenos.
El objetivo de este estudio fue proponer y validar un sistema de identificación de bajo coste de especies de Phytophthora con una serie de marcadores microsatélites polimórficos (SSR).
Se obtuvo un total de 33 aislamientos de diferentes especies del género, incluidas Phytophthora infestans, Phytophthora andina, Phytophthora sojae, Phytophthora cryptogea, Phytophthora nicotianae, Phytophthora capsici y Phytophthora cinnamomi. Como marcadores potencialmente transferibles entre estas especies del género Phytophthora se seleccionaron 13 microsatélites, y las condiciones de amplificación, incluidas las temperaturas de alineamiento, se estandarizaron para varios marcadores.
Un subgrupo de estos marcadores microsatélites se amplificó en todas las especies mostrando alelos específicos de especie.
Se describen la adaptabilidad e influencia del sistema de identificación en un país agrícola andino como Colombia, donde coexisten diferentes especies de Phytophthora en el mismo huésped o en diversos huéspedes cultivados al mismo tiempo.
A forest pathogen drives change in plant functional trait composition in the Southwest Australian Floristic Region
2011, Agriculture, Ecosystems and Environment
Citation Excerpt :
Although the pathogen will persist in the landscape, maintenance of species diversity may allow some regeneration of key species (and hence function) through persistence of susceptible species tolerant or more resistant to the pathogen (e.g. Stukely and Crane, 1994; Stukely et al., 2007) However, we anticipate that pathogen-infested Banksia woodlands are unlikely to regain the functional properties characteristic of uninfested vegetation due to the substantial reduction in species cover and associated structural and compositional changes.
Plant functional traits weighted by cover-abundance have been used to measure change across a wide range of temperature, moisture and grazing gradients. We use this approach along a chronosequence of disease infestation (Phytophthora cinnamomi) in the species-diverse Banksia woodlands of the Southwest Australian Floristic Region (SWAFR). We compare the use of absolute (community-weighted totals-CWT) and relative cover data (community-weighted means-CWM) to demonstrate the importance of total cover change in reference to the Mass Ratio Hypothesis.
Plant species cover-abundance was recorded along a space-for-time disease chronosequence, and functional trait data collected for the 48 dominant species from healthy vegetation. Six traits with deduced links to key ecosystem functions were measured for each species and values for two indices (CWT and CWM) compared along the disease chronosequence. Trait data was collected on plant height, growth form, specific leaf area, leaf dry matter content, root pattern and carbohydrate storage.
Despite substantial shifts in individual species cover and a reduction in total species cover, the majority of CWM values did not change significantly following disease infestation. The use of relative cover-abundance data disregards important changes in total species cover, apparent from our comparative analysis. In contrast to CWMs, all CWT values were reduced following disease infestation, suggesting a potential reduction in productivity, reduced capacity as a carbon sink and altered site water balance. Verification of these potential changes in ecosystem functions is required using fine-scale quantitative techniques. The CWT index is complementary to traditional CWMs and useful when analysing changes in plant trait data where total species cover changes have been detected. In relation to P. cinnamomi infestation, shifts in CWT trait values indicate the ability of an introduced plant pathogen to have substantial indirect impacts beyond substantial floristic change.
Will all the trees fall? Variable resistance to an introduced forest disease in a highly susceptible host
2011, Forest Ecology and Management
Citation Excerpt :
Plant populations and communities can be dramatically altered by disease epidemics (reviewed by Burdon et al., 2006; Gilbert, 2002); in particular, introduced forest pathogens have significantly and irreversibly altered the North American landscape (Loo, 2009). In some instances, populations of forest trees have been found to have some degree of resistance to invasive pathogens (reviewed by Sniezko, 2006), as in the cases of white pine blister rust (Cronartium ribicola) (Kinloch, 1992) and jarrah dieback (Phytophthora cinnamomi) (Stukely and Crane, 1994; Stukely et al., 2007). In other cases, well exemplified by the chestnut blight (Cryphonectria parasitica) epidemic, trees have lacked significant resistance to a newly introduced microbe.
Although tanoak (Notholithocarpus densiflorus syn. Lithocarpus densiflorus) is the species most affected by the introduced pathogen Phytophthora ramorum, with demonstrable risk of extirpation, little is known about the origin, range or structuring of the tree's susceptibility. We examined variation in resistance to P. ramorum using a wound inoculation assay of detached leaves from trees at five geographically separated sites, and a non-wound inoculation assay on twigs from trees at two sites. The structure of variation in resistance was compared to the structure at nine nuclear microsatellite markers.
Resistance varied quantitatively, with 23% and 12% of the variation among individuals and populations, respectively. There was a significant correlation between resistance in detached leaves and lesion size in non-wounding twig inoculations. Among-population genetic diversity at nine microsatellite loci was weakly structured but significantly non-zero, with 9.5% of variation among populations. Within-population neutral genetic diversity was a poor predictor of resistance, and estimates of phenotypic distances for resistance were no greater than neutral genetic distances.
The limited phenotypic and genetic structure we found indicates that tanoaks at all study sites are susceptible, and there is no evidence of prior selection for disease resistance. We conclude that tanoak populations across the species’ range are at risk, but local disease dynamics will depend on both host genetics and environmental conditions.
Screening native pepper, Tasmannia lanceolata (Poir.) A.C. Smith, for resistance against Phytophthora cinnamomi dieback
2023, Australasian Plant Pathology

View all citing articles on Scopus

View full text

Article preview

Forest Ecology and Management

Abstract

Introduction

Section snippets

Selection of E. marginata lines

Results

Discussion

Acknowledgements

References (14)

Inoculation of Eucalyptus marginata Donn ex Sm. (jarrah) clones with Phytophthora cinnamomi Rands in vitro and under glasshouse conditions

For. Ecol. Manage.

Genetic variation in resistance of Pinus radiata to Phytophthora cinnamomi

For. Ecol. Manage.

A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi

Physiol. Mol. Plant Pathol.

Mining and rehabilitation

Field response of Pinus radiata selected for resistance to Phytophthora cinnamomi

Resistance of micropropagated Eucalyptus marginata to Phytophthora cinnamomi

Plant Dis.

Mechanisms of resistance to Phytophthora cinnamomi in clonal, micropropagated Eucalyptus marginata

Plant Pathol.

Cited by (19)

Current practices and emerging possibilities for reducing the spread of oomycete pathogens in terrestrial and aquatic production systems in the European Union

Phytophthora cinnamomi as a driver of forest change: Implications for conservation and management

Developing a taxonomic identification system of Phytophthora species based on microsatellites

A forest pathogen drives change in plant functional trait composition in the Southwest Australian Floristic Region

Will all the trees fall? Variable resistance to an introduced forest disease in a highly susceptible host

Screening native pepper, Tasmannia lanceolata (Poir.) A.C. Smith, for resistance against Phytophthora cinnamomi dieback