Lessons from the Incursion of Myrtle Rust in Australia

Abstract

Austropuccinia psidii (myrtle rust) is a globally invasive neotropical rust of the Myrtaceae that came into international prominence following extensive damage to exotic Eucalyptus plantations in Brazil in the 1970s and 1980s. In 2005, myrtle rust established in Hawaii (USA), and over the past 12 years has spread from the Americas into Asia, the Pacific, and South Africa. Myr-tle rust was detected in Australia in 2010, and the response and ultimately unsuccessful eradication attempt was a lesson to those concerned about the threat of exotic pests and diseases to Australia's environment. Seven years following establishment, we are already observing the decline of many myrtaceous species and severe impacts to native plant communities. However , the recently developed Myrtle rust in Australia draft action plan identified that there is no nationally coordinated response strategy for the environmental dimensions of this threat. Recent reviews have identified a greater need for involvement from environmental agencies in biosecurity preparedness , response, and resourcing, and we believe this approach needs to extend to the management of invasive environmental pathogens once they establish.

Full text

PY56CH21_Carnegie ARI 31 July 2018 10:32
Annual Review of Phytopathology
Lessons from the Incursion
of Myrtle Rust in Australia
Angus J. Carnegie1and Geoff S. Pegg2
1New South Wales Forest Science, New South Wales Department of Primary
Industries—Forestry, Parramatta, New South Wales 2150, Australia;
email: angus.carnegie@dpi.nsw.gov.au
2Department of Agriculture and Fisheries, Dutton Park, Queensland 4102, Australia
Annu. Rev. Phytopathol. 2018. 56:457–78
First published as a Review in Advance on
July 5, 2018
The Annual Review of Phytopathology is online at
phyto.annualreviews.org
https://doi.org/10.1146/annurev-phyto- 080516-
035256
Copyright c
2018 by Annual Reviews.
All rights reserved
Keywords
Austropuccinia psidii, invasive species, biosecurity, environmental impact,
Myrtaceae, native ecosystems
Abstract
Austropuccinia psidii (myrtle rust) is a globally invasive neotropical rust of
the Myrtaceae that came into international prominence following extensive
damage to exotic Eucalyptus plantations in Brazil in the 1970s and 1980s. In
2005, myrtle rust established in Hawaii (USA), and over the past 12 years
has spread from the Americas into Asia, the Pacific, and South Africa. Myr-
tle rust was detected in Australia in 2010, and the response and ultimately
unsuccessful eradication attempt was a lesson to those concerned about
the threat of exotic pests and diseases to Australia’s environment. Seven
years following establishment, we are already observing the decline of many
myrtaceous species and severe impacts to native plant communities. How-
ever, the recently developed Myrtle rust in Australia draft action plan iden-
tified that there is no nationally coordinated response strategy for the envi-
ronmental dimensions of this threat. Recent reviews have identified a greater
need for involvement from environmental agencies in biosecurity prepared-
ness, response, and resourcing, and we believe this approach needs to extend
to the management of invasive environmental pathogens once they establish.
457
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INTRODUCTION
Austropuccinia psidii (formerly Puccinia psidii ) (9) is a neotropical rust of Myrtaceae (27, 42). It
infects, impacts, and often kills newly expanding leaves and stems as well as fruit and flowers (27,
38, 42). Repeated infection and defoliation can result in tree mortality (21). A. psidii was described
from common guava (Psidium guajava) in Brazil (135), from which it gained its original common
name, guava rust. Sporadic outbreaks of A. psidii occur in guava plantations in Brazil (30, 102),
but major epidemics occur on the exotic rose apple Syzygium jambos (123). The invasive potential
of A. psidii was first realized when a new biotype invaded Jamaica in the early 1930s [A. psidii had
previously been identified from Jamaica (29)] and caused extensive damage to allspice (Pimenta
dioica) plantations (68, 114). Although identified from Eucalyptus (Corymbia citriodora) in 1912 in
Brazil (27, 53), it was not until serious outbreaks occurred in nurseries and young plantations in
Brazil that the true threat to Eucalyptus was realized (38).
Owing to the significant threat of A. psidii to the extensive Eucalyptus plantation estates in
Brazil, it gained another common name, eucalyptus rust (38), and many species of this genus
were shown to be susceptible (32). The international implications of this threat were realized
soon thereafter because of the extensive commercial plantations of Eucalyptus planted as non-
natives in many countries (27) and the eucalypt plantations and native Myrtaceae in Australia (24).
This led to an international project beginning in 2000 and funded by the Australian government
[Australian Centre for International Agricultural Research (ACIAR)] to test the susceptibility of a
comprehensive range of Australian Myrtaceae (127, 137), create disease risk maps (11, 12), prepare
pest risk analyses, and develop molecular diagnostic techniques for A. psidii (60).
In 1997, 20 years after A. psidii had first been detected in Florida, USA (70), a new biotype of A.
psidii invaded and caused extensive damage to exotic Australian broad-leaved paperbarks (Melaleuca
quinquenervia) that had initially been planted in Florida but later escaped and became an invasive
weed (100). When A. psidii was detected in Hawaii, USA (56), the subsequent epidemic resulted
in extensive damage to the exotic rose apple (129) and threatened Hawaii’s most common native
species, ‘¯
ohi‘a (Metrosideros polymorpha) (65). There it gained another common name, ‘¯
ohi‘a rust.
Viable spores of A. psidii on plastic-wrapped timber pallets from Brazil were detected in
Australia in 2004, leading to this pathway being closed to prevent further ingress of A. psidii
to Australia (49). The Australian government also developed a pest-specific contingency plan for
A. psidii (85), and A. psidii was identified as a high-priority pest by the forest industry (94) and the
nursery and garden industry (95). It appeared that Australia was prepared for A. psidii.
In April 2010, A. psidii was detected on the central coast of New South Wales (NSW) in Australia
(20). Eradication was attempted but was ultimately unsuccessful (16). Myrtle rust is now prevalent
in native ecosystems along the east coast of Australia (10), where it has caused the decline of native
rainforest species (21), had a significant impact on native plant communities (92), and affected
the health and reproductive capacity of endangered tree species (122). Developing native oil
and food industries have also been impacted (https://landcareaustralia.org.au/project/myrtle-
rust-threat-australias-unique-biodiversity/) (35). There has been criticism of the emergency
response to the detection of myrtle rust in Australia (25, 72), and there is currently still no national
response to the ongoing threat in native ecosystems now that the pathogen has established. Here,
we review the emergency response to the detection of A. psidii, provide an update on the impact
of myrtle rust in Australia, and identify lessons from the response to the incursion of this invasive
pathogen and the impact it is now causing in the native environment.
MYRTLE RUST: A GLOBAL INVASIVE SPECIES
Although originally described in Brazil (135), it can be assumed that A. psidii is endemic to
neighboring countries. The detection of A. psidii in countries in South and Central America
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and the Caribbean can be tracked via publications (Table 1): Paraguay (117), Uruguay (118),
Ecuador (119), Cuba (3), Puerto Rico (3), Colombia (71), the Dominican Republic (55), Venezuela
(22), Jamaica (114), Trinidad and Tobago (113), Argentina (33), Dominica (6), Guatemala (110),
El Salvador (23), Costa Rica (34), and Panama (93). It is likely that A. psidii was present in El
Salvador and Costa Rica for some time prior to being reported, and it was known in Jamaica prior
to the 1930s (27).
Table 1 History of Austropuccinia psidii invasion events, defined as detection in a new country, significant range expansion
within a country, a new biotype record within a country, or a significant host-damage eventa
Year Invasion event Biotype References
1884 Brazil EU/SJ +103, 135
1884 Paraguay EU/SJ +103, 117
1889 Uruguay EU/SJ +103, 118
1891 Ecuador Unknown 119
1903 Cuba Unknown 3
1912 Puerto Rico Pandemic 3, 103
1913 Colombia EU/SJ +48, 71
1933 Dominican Republic Unknown 55
1934 Venezuela Unknown 22
1934 Jamaica Pandemic +114, 120
1945 Trinidad and Tobago Unknown 113
1946 Argentina Unknown 33
1948 Dominica Unknown 6
1968 Guatemala Unknown 110
1973 Brazil (Eucalyptus plantations) EU/SJ +38
1977 US, Florida Unknown 70
1981 Mexico Pandemic 63, 103
1987 El Salvador Unknown 23
1997 US, Florida (new strain) Pandemic 100, 120
1998 Costa Rica Pandemic 33, 103
2002 Panama Unknown 93
2005 US, Hawaii Pandemic 56, 103
2006 US, California Pandemic 46, 74
2007 Japan Unknown 54
2009 China Pandemic 67, 138
2010 Australia, New South Wales Pandemic 20, 67
2013 New Caledonia Pandemic 67, 115
2013 South Africa South African 105, 106
2015 Australia, Northern Territory Pandemic 67, 132
2016 Indonesia Pandemic 73
2016 Singapore Unknown 36
2017 New Zealand Pandemic 50, 75
2017 Colombia Pandemic 48
aWhere known, the biotype is identified (103, 120).
Abbreviation: EU/SJ, collections from Eucalyptus spp. and Syzygium jambos from Brazil, Paraguay and Uruguay.
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In North America, A. psidii was reported in Florida in 1977 (70), Mexico in 1981 (63), Hawaii
in 2005 (56), and California in 2006 (74), although it was likely present there prior to 2006.
The introduction into California is likely to have been from the live plant or foliage trade from
Florida, based on data on interceptions and nursery detections (136). The introduction to Hawaii
is also likely to have been from the live plant or foliage trade (65, 66), most likely from the
mainland United States. Currently, A. psidii is restricted to southeastern Florida, has a restricted
distribution in California, mainly in nurseries (P. Cannon, personal communication), and has
spread throughout the Hawaiian Islands (1).
In 2007, A. psidii was detected on rooted cuttings of M. polymorpha in Japan (54), again most
likely imported via the live plant trade. No further reference to its distribution in Japan has been
found. In 2011, A. psidii was reported from southern China based on collections from 2009 (138).
In 2010, A. psidii reached Australia (20) and is now widespread along the east coast (10). There is no
indication of the pathway of entry into Australia. In 2013, A. psidii was reported from both South
Africa—where its distribution was originally restricted (106) but is now considered widespread
(105)—and New Caledonia, where it has spread throughout the islands (115). More recent detec-
tions of A. psidii have been in Indonesia (73), Sumatra (where it impacted on Rhodomyrtus tomentosa
within its native range; M. Purcell, personal communication), Singapore (36), and New Zealand
(http://mpi.govt.nz/protection-and-response/responding/alerts/myrtle-rust/).
Since reaching Hawaii in 2005, A. psidii has expanded its global range exponentially. Figure 1
illustrates the cumulative increase in invasion events for A. psidii since it was first described.
We define an invasion event as the detection of A. psidii in a new country, a significant new
0
5
10
15
20
25
30
35
1880 1900 1920 1940 1960
Year
Austropuccinia psidii invasion events
1980 2000 2020
Described in Brazil
Eucalyptus in Brazil
Hawaii, USA
Australia
South Africa
New Zealand
Jamaica
Mexico
EU/SJ +
Unknown
S-Africa
Pandemic
Pandemic +
Biotypes
Figure 1
Cumulative history of Austropuccinia psidii invasion events, defined as detection in a new country, significant
range expansion within a country, a new biotype record within a country, or significant host-damage event.
Where known, the biotype is identified, based on Ross-Davis et al. (103) and Stewart et al. (120).
Abbreviations: EU/SJ, collections from Eucalyptus spp. and Syzygium jambos from Brazil, Paraguay, and
Uruguay; S-Africa, South Africa. Plus sign indicates that other biotypes are also known from this location.
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distribution record within a country (e.g., Hawaii, USA; Darwin, Australia), a new biotype record
within a country (e.g., Pandemic biotype in Colombia), or a significant new host-damage event
(e.g., impact on Eucalyptus plantations in Brazil). The majority of new invasions over this period
(2005–2017) have been of the Pandemic biotype (as defined in References 103 and 120). The
biotype in Japan and Singapore is currently unknown; the biotype present in South Africa is to
date globally unique (106).
TAXONOMY AND PATHOGEN VARIATION
A. psidii was first described (as P. psidii ) in 1884 on guava (P. guajava) in Brazil (135) and has
at least 25 synonyms, many named following detection of the rust on a new host (42). A review
of rust fungi associated with Myrtaceae by Simpson et al. (113) introduced Uredo psidii, a name
considered superfluous for the uredinial stage of A. psidii (89) given there had already been several
validly published anamorphic names (Uredo subneurophila Speg. and Uredo neurophila Speg.). Also
introduced was the name Uredo rangelii for two specimens on Myrtus communis and S. jambos,
respectively. The presence of a tonsure on the lower half of the urediniospores, the shape and wall
thickness of the urediniospores, the size of the uredinia, and the symptoms, including a lack of
infection on stems or petioles of these specimens, were considered different from those found in
A. psidii by Simpson et al. (113). However, morphological variation had already been identified
within A. psidii (131), and several authors have not accepted U. rangelii as a distinct species,
considering it a synonym of A. psidii (42, 44, 99). Interesting to note, the name myrtle rust
stems from the common name for the host of the type specimen of U. rangelii, common myrtle
(M. communis), not for the family Myrtaceae.
When first detected in Australia, the original sample examined was identified as U. rangelii
(20) based on morphology (including a tonsure on the uredospore) and the taxonomy of Simpson
et al. (113). However, based on molecular analysis, Carnegie & Cooper (16) suggested the rust
in Australia was A. psidii, and Pegg et al. (89) later supported this based on molecular analysis of
two gene regions, morphological examination of two life-cycle stages, and host studies. Machado
et al. (67) and Sandhu et al. (108) have confirmed that a single genotype of A. psidii is present in
Australia.
Several previous studies had suggested that A. psidii did not have a well-supported relationship
with any described rust family and its taxonomic position was unclear (64, 89, 130). Beenken (9)
identified that A. psidii, although morphologically indistinguishable from the genus Puccinia, was
distinct genetically and did not fit to any valid genera. It was identified that this rust fungus was
more closely related to the genera Dayspora,Puccorchidium,Sphenorchidium,andSphaerophragmium
than to Puccinia. As a consequence, Beenken (9) created a new genus of Austropuccinia within the
family Sphaerophragmiaceae.
The diversity that exists within A. psidii has been known for many years and has been demon-
strated through cross-inoculation studies. Marlatt & Kimbrough (70) identified variation in
pathogenicity between isolates taken from P. dioica and S. jambos. Similarly, other studies identified
that isolates taken from P. guajava could not infect S. jambos or Eucalyptus spp. (38). Rayachhetry
et al. (101) also found that isolates collected from M. quinquenervia and P. dioica would not infect
S. jambos.
Using microsatellite markers, studies of A. psidii populations have identified that variability
exists within the species with different multilocus genotypes occurring within one strain (46, 103).
At least four biotypes (strains) of A. psidii have been identified (103, 120). Stewart et al. (120),
when studying isolates of A. psidii collected from Brazil, Costa Rica, Jamaica, Mexico, Puerto
Rico, Uruguay, and the United States, identified twenty-three unique multilocus genotypes.
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They identified nine genetic clusters (C1–C9), comparing relationships between geographic ori-
gin and host species. When comparing bioclimatic models for the different clusters, Stewart
et al. (120) identified differences that could influence their invasiveness potential in different ge-
ographic regions. The most diverse population was C1, identified as the Pandemic biotype (103,
120), a biotype with the widest geographic and host range, including many hosts in Australia,
collected from a range of host species in Costa Rica, Jamaica, Mexico, Puerto Rico, and Hawaii
(67, 108). Stewart et al. (120) concluded that the origin or source of the Pandemic biotype is
still unknown and is quite distinct from the biotype (C2/C3) associated with eucalypt and rose
apple in Brazil and Uruguay and the biotype (C6) in Brazil associated with guava and Brazilian
guava.
The Pandemic biotype is the most broadly distributed biotype globally, reported from Hawaii
(120), California (45), Australia and China (67), New Caledonia (115), Indonesia (73), and New
Zealand (50). This biotype has not been reported in Brazil but has recently been identified in
Columbia (48). Grac¸a et al. (47) suggest that this biotype did not originate from populations of A.
psidii on Eucalyptus,S. jambos,orP. guajava from Brazil. Although Granados et al. (48) hypothesize
that Columbia may be the center of origin of the Pandemic biotype, they also suggest it is plausible
that this genotype is a recent introduction and that many other host-associated genotypes of A.
psidii will be detected with further study, one of which may reveal the source of the Pandemic
biotype. The highest degree of variability within A. psidii populations has been identified in Brazil
(120). Host-associated lineages of A. psidii in Brazil have been demonstrated on (a)Psidium,(b)
Eucalyptus and S. jambos,and(c)Eugenia,Myrciaria,andSyzygium (47). The potential impacts of
the different strains have also been demonstrated when five Brazilian strains were tested against
M. polymorpha from Hawaii with three strains found to be highly virulent and two strains only
mildly virulent (112).
Stewart et al. (120) revealed geographic variation in predicted global distribution of the main
biotypes of A. psidii, with quite striking differences for both Hawaii and Australia between the
Pandemic biotype and the C2/C3 and C6 biotypes. Bioclimatic studies have utilized this informa-
tion to overlap current and future distributions of myrtle rust with the distribution of Myrtaceae
in Australia (10) and Mexico (37) to assist in management of this disease.
From an Australian perspective, the identification of multiple biotypes of A. psidii should war-
rant extreme concern over new introductions, particularly from South America and South Africa,
where biotypes other than the Pandemic have been identified. Although importation of plant
material is controlled within Australia, including seed for sowing, other high-risk pathways re-
main open. Natural spread is likely to have been the pathway of A. psidii to New Caledonia and
New Zealand. The discovery in 2004 of viable spores of A. psidii on kiln-dried Eucalyptus sawn
timber imports from Brazil led to the suspension of trade in Eucalyptus timber from countries
with A. psidii (49). Thus, the recent relaxation of timber imports from South America, allow-
ing import of Eucalyptus timber following treatment within 90 days prior to the date of export
(https://bicon.agriculture.gov.au/BiconWeb4.0/), seems puzzling. This relaxation of condi-
tions appears to be based not on evidence of the existence of multiple biotypes but on studies
originating from Brazil that suggest spores would not remain viable during the transport of cargo
(59). Lana et al. (59) argue that their results do not support the earlier findings from Australia
by Grgurinovic et al. (49). The results from Grgurinovic et al. (49) suggest that this will pose a
significant risk of further incursions, including other biotypes not yet present in Australia. One
of those biotypes has been associated with a significant impact on eucalypt plantations in Brazil
(137). If any of these different biotypes become established in Australia, it would have a potential
additive impact on the Pandemic biotype that is already present.
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RESPONSE TO THE DETECTION OF MYRTLE RUST IN AUSTRALIA
Australia’s Biosecurity System
Australia has a robust and comprehensive biosecurity system focused on activities pre-border,
at the border, and post-border (2). However, much of the focus is on protecting agricultural
industries because of their economic benefits to Australia as well as the agricentric nature of
plant biosecurity agencies in Australia (18, 128). Several reviews have highlighted serious gaps in
Australia’s biosecurity system in relation to environmental biosecurity (25, 28) and forest pests (5,
18, 76, 128).
Prior to 2005, response activities to the detection of an exotic plant pest were relatively infor-
mal, fairly ad hoc, and conducted on a case-by-case manner, unlike the formal procedures in place
for animal health (8, 82). In 2005, all government and some industry parties became signatories
to the Emergency Plant Pest Response Deed (EPPRD), which outlines the basis for considering
all exotic plant pest detections, including plant industries’ participation in decision making and
funding of responses (97). Response actions to an exotic plant pest are guided by PLANTPLAN,
an operational manual under the EPPRD that describes Australia’s technical response to exotic
plant pest incursions (96). Response actions in PLANTPLAN include (a) initiation of the pro-
cess of pest identification and notification of relevant organizations and people; (b) activation of a
national committee [the Consultative Committee on Emergency Plant Pests (CCEPP)] to deter-
mine whether containment or eradication is technically feasible and economically justifiable; and
(c) implementation of the response plan. The CCEPP consists of representatives of the Australian
Government’s agricultural agency (Department of Agriculture and Water Resources), each of the
state’s primary industries agencies, and representatives from the affected parties. If relevant, a
scientific advisory panel (SAP) is convened to evaluate the technical aspects of the response.
In 2012, the Australian and state governments signed the National Environmental Biose-
curity Preparedness Agreement (NEBRA) to establish national emergency response arrange-
ments for pests and diseases of environmental and/or social amenity value (26). An example
of a response under this agreement is the current red imported fire ant eradication campaign
in Queensland (https://www.daf.qld.gov.au/plants/weeds-pest-animals-ants/invasive-ants/
fire-ants/national-red-imported-eradication-program/fire-ant-eradication). The EPPRD is
used when eradication of an exotic pest would benefit plant industries, whereas the NEBRA is used
when eradication of an exotic pest would benefit the public good, i.e., social amenity value (human
health) or the native environment. A response under the EPPRD is co-funded by government and
industry, whereas any response under the NEBRA is funded solely by government.
National Response to the Detection of Myrtle Rust
At the time that A. psidii was detected in Australia, the forest industry was not a signatory to the
EPPRD and therefore was not classed as an affected industry. Moreover, there were no senior
representatives from the environmental sector on the CCEPP, although the nursery and garden
industry was represented as an affected party. As such, the CCEPP was strongly influenced by
agricultural expertise because of the agricentric nature of Australia’s primary industry and biose-
curity agencies, although technical input was provided by forest health specialists. The NEBRA
had not come into effect when A. psidii was detected, so the response to A. psidii was conducted
under the EPPRD.
Myrtle rust was detected in April 2010 on the Central Coast of NSW, just north of Sydney
(20). A cut-flower grower had noticed an unusual symptom on his Agonis flexuosa ‘Afterdark’ plants
and brought a specimen into the local NSW Department of Primary Industries office on April 21.
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Fortuitously, the sample ended up on the desk of a researcher with access to a pest and disease field
guide for eucalypts, including information about eucalyptus rust (17). The sample was positively
identified as U. rangelii by a retired rust expert ( John Walker) on April 23, 2010 (20), and an
emergency response under the EPPRD began (16).
The initial identification of the rust as U. rangelii caused confusion at the beginning and
throughout the response, although it was recognized at the outset that this was an exotic disease and
within the guava rust complex (16, 20). Within one day of identification and three days of the sample
being provided by the grower, surveillance was conducted of the affected property, including a
wide range of Myrtaceae within the property and surrounding native forest. Approximately 1,100
A. flexuosa plants were identified as infected with myrtle rust on the initial property, as were a
row of turpentine trees (Syncarpia glomulifera) in a windbreak and a single bottlebrush [Melaleuca
(Callistemon)viminalis] shrub within the property. Surveillance in the surrounding area, including
of native forest, identified two small saplings of S. glomulifera with myrtle rust on the entry road
to the property but no other evidence of rust outside the property. A meeting of the CCEPP was
convened on April 27, and it was agreed more surveillance was needed to determine the extent of
spread of the rust and whether it was technically feasible to eradicate.
Surveys from April 28 to April 30, 2010, concentrated on nurseries and cut-flower growers,
native forest, road-side plantings, and residential gardens of known hosts and other Myrtaceae in
the immediate area of the first infected site (Somersby Plateau). This area has many small (hobby)
farms and nurseries but is also densely vegetated with native forest. A second infected property was
identified on April 28—a wholesale nursery 8.5 km south of the first infected property, with several
M. (Callistemon)viminalis plants showing light infection. At that stage, more than 25 sites had been
surveyed and found free of myrtle rust. With this information, the CCEPP convened on April 30
and determined that myrtle rust was not technically feasible to eradicate because it was thought
likely that a large spore load had already emanated from the first infected property, the efficacy
of tools to eradicate the rust in native forest was limited, and there were likely more unidentified
infected properties (16). Notably, only one week had passed from the initial identification of an
exotic plant pest to the cessation of the emergency response.
The following week, NSW state government agencies (NSW Department of Primary Indus-
tries, Forestry Corporation of NSW, and the Office of Environment and Heritage) agreed to
continue surveillance and containment operations on infected premises, including fungicide ap-
plication and quarantine but outside the EPPRD (as a state-based response funded by the state,
not a national response funded by all affected parties). Three more infected properties, situated up
to 35 km from the initial infected property, were identified by the end of June 2010, but with many
sites surveyed and negative for myrtle rust in the area. Infected properties were quarantined, and
infected plants treated with fungicide. More than 55 sites were surveyed by the end of July 2010,
under this program, with multiple visits to some high-risk sites (adjacent to infected properties or
those with large numbers of known hosts). Surveillance and other operations were carried out by
a small core (fewer than 10 staff members) of personnel for this period.
Observations gained during this period indicated that myrtle rust had not behaved as originally
expected: There was limited spread from infected properties, it had not been found in the native
environment, and there was a limited number of hosts. Furthermore, there was good control on
the five properties that had been identified as infected. There was also mounting pressure from key
groups (e.g., Plant Health Australia, Nursery and Garden Industry Australia, and the Australasian
Plant Pathology Society) on the CCEPP to restart the emergency response. Subsequently, on
July 2, 2010, the CCEPP agreed to reinstate the emergency response under the EPPRD. This
resulted in a significant increase in resourcing under the EPPRD and PLANTPLAN, with up to
380 staff involved to the end of December 2010 (16).
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A local disease control center was established, and teams of staff enlisted for planning, surveil-
lance, tracing, quarantine, treatment, plant destruction and communications (16). The two local
government areas on the Central Coast of NSW were gazetted as a Quarantine Area under the
Plant Diseases Act of 1924 No. 38, which restricted plant movement to and from the area unless
specific conditions were met. This also allowed for the destruction of infected plant material.
During the response, more than 16,000 infected plants were destroyed on nurseries and more
than 5,000 at native forest sites. Surveillance activities increased significantly from August, with
more than 1,600 inspections of over 1,300 properties by the end of December 2010, including 600
nurseries and 250 native forest sites. Systematic tracing identified more than 40 nurseries found to
be positive for myrtle rust, including some more than 350 km from the initial infected property.
The inadvertent transport of infected plant material was found to be the most significant agent
of movement of A. psidii during the response. By December 22, 2010, 201 infected premises had
been identified in NSW.
Several key events, or turning points, occurred during the myrtle rust emergency response
(16). The main one was the increase in resources provided by the EPPRD funding model, which
allowed for substantially enhanced surveillance, tracing, quarantine, and plant destruction as well
as a community engagement plan. The recoverable cost of the myrtle rust emergency response
under the EPPRD was AU$3.55 million, with another AU$1.5 million contributed as in-kind. In
August, Austromyrtus (Gossia)inophloia became a primary focus of tracing and surveillance following
its identification as a significant host, with many new detections of myrtle rust being on this host
in nurseries. On October 28, 2010, myrtle rust was found for the first time in native vegetation,
on Rhodamnia rubescens, and this became a primary focus from November. As the Australian
spring continued, it appeared that optimum conditions for the rust prevailed, and in combination
with highly susceptible hosts (e.g., A. inophloia and R. rubescens) the number of infected premises
escalated (16). On December 2, 2010, the CCEPP determined that it was no longer technically
feasible to eradicate myrtle rust, and the eradication response ceased on December 22.
The Australian government then funded a AU$1.5 million transition to management program
from 2011–2013 to develop knowledge and information to assist industries to manage the impacts
of the disease in urban, production, and natural environments (http://myrtlerust.net.au/). Re-
search projects included investigations into the A. psidii genome (121), life cycle (78), chemical
control (51), host screening (77, 109), identification of rust resistance genes in several genera (58,
124), and comparative genomics and phylogenetic analysis of A. psidii (43, 64). Although all these
were fundamentally important, there was no project to establish baseline data, or a monitoring
system and data repository, for tracking environmental and biodiversity impacts. The transition
to management program was mainly focused on primary industries, and no parallel environmental
agency initiative emerged.
Once funding for the transition to a management program was completed, industry and affected
land managers had to deal with this now-established pathogen on their own. Subsequently, the
Rural Industries Research and Development Corporation (RIRDC, now AgriFutures; https://
agrifutures.infoservices.com.au/items/12-098) and the Plant Biosecurity Cooperative Re-
search Centre (PBCRC) (http://www.pbcrc.com.au/news/2016/pbcrc/myrtle-rust-threat-
australian-landscape-and-plant-industries) funded research into the impact of myrtle rust and
management options on lemon myrtle plantations and other industries. Moreover, the PBCRC
funded several projects investigating impacts in the native environment, including assessment
protocols and quantifying impact (http://www.pbcrc.com.au/news/2016/pbcrc/myrtle-rust-
threat-australian-landscape-and-plant-industries), and, more recently, the NSW Environ-
mental Trust (http://www.environment.nsw.gov.au/grants/2014RDmajor.htm) funded a
project investigating the impact on the native environment. However, there has been no
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nationally coordinated program to deal with the short-, medium-, or long-term impact of myrtle
rust now that it has established in native ecosystems in Australia.
Review of the Myrtle Rust Emergency Response
There have been several reviews of the myrtle rust emergency response. All have identified the
haste with which the initial decision that eradication was not feasible was made and the confusion
surrounding the taxonomy (name) as key deficiencies in the program. McAllister et al. (72) in-
terviewed key members of the emergency response (e.g., CCEPP, National Management Group,
SAP, and industry stakeholders) as well as participants in workshops and meetings during the
transition to the management phase following the establishment of myrtle rust. More than 250
stakeholders were involved in the often hotly debated eradication attempt. Industry representa-
tives highlighted the delay in declaring the myrtle rust outbreak an emergency as an indication of
a lack of commitment by the government to share the cost of the response. They also indicated
that the shift from eradication to containment/management and then back to eradication added
to industry mistrust. A major debate surrounded the naming of the rust. Some said that calling it
U. rangelii—a little-known name—instead of the commonly known P. psidii was done to deliber-
ately downplay the incursion of this dangerous rust. These actions were identified as a breach of
trust (72) by some industry stakeholders and science advisors.
A subsequent Senate inquiry into environmental biosecurity in Australia received several sub-
missions relating to the response to myrtle rust, including from the Invasive Species Council, the
PBCRC and the Australian Network for Plant Conservation (25). These groups criticized the
adequacy of the surveillance and early detection, decision-making in the initial response period,
confusion regarding the name of the disease, and resourcing. The haste in the decision to abandon
the initial response seemed to be compounded by the fact that published resources on response
procedures in biosecurity plans did not appear to have been fully utilized, thus hindering the
opportunity to respond appropriately. In fact, the response appeared to be “inconsistent with the
process outlined in the (threat-specific) contingency plan” for A. psidii, according to the Invasive
Species Council (52, p. 17). The forest industry (85) and the nursery and garden industry (95)
both had threat-specific contingency plans for guava/eucalyptus rust that identified U. rangelii as
a synonym of A. psidii, and there was little doubt the term myrtle rust caused confusion among
industry and government officials alike. Despite the well-known potential environmental threat
of A. psidii (27, 42, 85), environmental risks were not given sufficient weight in decision-making.
IMPACT OF MYRTLE RUST IN AUSTRALIA
Ecology and Importance of Myrtaceae
The Myrtaceae family is filled with dominant, iconic, and ecologically important plant species in
Australia (81), with approximately 2,250 native species occurring within 88 genera. They represent
more than half the global number of Myrtaceae (69), with more species than any other plant family
in Australia (7). Species of Myrtaceae occur in 11 out of the 13 major vegetation formations in
Australia (116). Eucalypt forests make up 74% of Australia’s total forested area (4). Aside from
providing essential habitat, Myrtaceae provide nectar and pollen for vertebrates and invertebrates,
and fleshy-fruited species provide a food source for birds and mammals (81).
In addition to their environmental significance, a range of Myrtaceae, including species in
Eucalyptus and Corymbia, have significant commercial value for timber production, and a different
suite of species, including tea tree (Melaleuca alternifolia) and lemon myrtle (Backhousia citriodora),
have significant commercial value for the native oil and food industries. Species of Myrtaceae,
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including Geraldton wax (Chamalaucium uncinatum), are also important for the cut-flower industry
(126). Many other species (e.g., Syzygium luehmannii ) are being used for developing native food
(125) and honey-based industries.
Distribution of Myrtle Rust in Australia
The current distribution of myrtle rust in Australia has been presented by Berthon et al. (10),
including maps of detections from nurseries, gardens, and native environments. Within 12 months
of the cessation of the emergency response, A. psidii had become established in gardens and native
forest along the east coast of Australia from Batemans Bay in southern NSW to Gympie in southern
Queensland. By the end of 2012, the distribution had extended north to Cairns in Queensland,
with A. psidii more recently found in Cape York on the northern tip of Queensland. Despite
detections in urban parks and gardens in Victoria (from 2011) and Tasmania (from 2014), A. psidii
has not been reported from native ecosystems in those two states (10). The reason the disease
has not been identified from native environments in these states is unknown, particularly given
that modeling (10, 57, 120) suggests climatic conditions are favorable for disease development
in these regions. In 2015, detections were made in the Northern Territory, on Melville Island
and in urban areas of Darwin (132), with more recent reports identifying infected trees in native
environments of eastern Arnhem Land (133). More recently, A. psidii was detected on Norfolk
Island and Lorde Howe Island off the east coast of Australia, with eradication attempts on Lorde
Howe Island reportedly successful (H. Bower, personal communication) and focused around the
removal of highly susceptible S. jambos, a non-native species. A. psidii has not been reported in
South Australia or Western Australia.
Host Range of Myrtle Rust in Australia
The host range of A. psidii in Australia now exceeds 347 species from 57 genera, of which 232 species
have been identified from observations under field conditions and 115 from artificial inoculation
only (10, 19, 40, 77, 89). Unfortunately, species susceptibility assessments have often been limited
to specimens within botanical garden collections and in some cases limited to a single tree or limited
collections of species (e.g., single provenance) under artificial inoculation. Although these assess-
ments are useful as an indicator of potential impact across native populations, extensive studies are
required to properly examine the potential and actual impact and to determine whether variability
in susceptibility occurs within a species and what impact multiple infection events have on a species.
A number of studies have examined susceptibility levels in more detail within species popu-
lations, particularly those of commercial significance such as eucalypts (62, 87, 88, 98, 104) and
Melaleuca (90, 111). These studies identified inter- and intraspecific variability in rust resistance.
Some results suggest climate at the origin as an influencing factor on resistance, with provenances
from lower rainfall areas generally having higher levels of resistance (62). When studying popula-
tions of M. alternifolia (tea tree), Shephard et al. (111) identified pronounced region-, provenance-,
and family-level effects. Upland plants, which are in areas of lower rainfall, had lower levels of
susceptibility in comparison to coastal plants from higher rainfall regions. When examining pop-
ulations of three broad-leaved Melaleuca species (M. quinquenervia,Melaleuca leucadendra,and
Melaleuca viridiflora), Pegg et al. (90) found variability in susceptibility at the provenance level.
No population could be identified as totally resistant, and a lack of any resistance was identified
in some populations of M. leucadendra and M. viridiflora. Tobias et al. (126) found no resistance
to A. psidii among provenances of Chamelaucium uncinatum, a species native to Western Australia
used for cut flowers.
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Impact of Myrtle Rust in Australia
A. psidii is now identified from a range of native forest ecosystems in Australia. Impact on different
species has been recorded in coastal heath, littoral, subtropical and tropical rainforest, wet and
dry sclerophyll, and sand island ecosystems, including some World Heritage areas of Gondwana
Rainforest, Fraser Island (K’gari), and the wet tropics in northern Australia (88, 89). Although
susceptibility levels have been determined for a number of host species (89), assessments of sus-
ceptibility across the native range have been limited to only a few species. Impact on plant species
ranges from minor leaf spotting to varying levels of defoliation and dieback and death of trees in
all life stages, including seedlings, saplings, and mature trees (21, 88, 89, 92). On the basis of field
assessments, 48 myrtaceous species of the 163 species identified as susceptible in Queensland were
determined to be highly or extremely susceptible to A. psidii with evidence of severe leaf blight-
ing and infection on shoots and juvenile stems resulting in dieback (89). Infection of epicormic
regrowth has been recorded for a range of species (88, 92).
Indirect and direct impacts on flowering and fruit production have been recorded. Thirty-
two species in Queensland have been recorded with infection on flowers or fruit, which impacts
directly on maturation (88, 89). Reduced flowering has also been reported as a result of re-
peated infection causing dieback on species such as Melaleuca nodosa and Leptospermum liversidgei,
particularly on epicormic regrowth following wildfire (88). When assessing Melaleuca nodosa re-
generation following a wildfire event in coastal heath in northern NSW, it was found that trees
showing high levels of dieback produced lower numbers of seed capsules. Similarly, lower flow-
ering rates were observed on Baeckea frutescens and L. liversidgei with dieback in comparison to
individuals of the same species with no symptoms of rust infection. Pegg et al. (91) reported the
effects of A. psidii infection on juvenile stems and shoots of M. quinquenervia, with flowering re-
stricted to trees showing resistance or minor infection on foliage only; stem infection and dieback
affected flower production. Further research examining direct and indirect effects of repeated
A. psidii infection on species fecundity is required on a range of species. Trials using fungicides
to eliminate or limit A. psidii infection would be required to effectively study these impacts. The
effects of reduced plant density or fragmentation of populations and flowering rates on pollina-
tors, both mammals and invertebrates, and any long-term implications on genetic diversity are
unknown.
Studies conducted by Carnegie et al. (21) looking at the impact of repeated infection on
R. rubescens in NSW showed that repeated, severe infection by A. psidii resulted in a reduction in
foliage production and that this severely affected crown health, eventually leading to tree death. It
was also revealed that A. psidii is capable of killing some trees in a native forest ecosystem in fewer
than four years. Severe and repeated infections resulting in crown loss, dieback, and tree mortality
were reported across the native range of R. rubescens as well as for the native guava Rhodomyrtus
psidioides (21). Although both species are now in decline, impact on R. psidioides is particularly severe
with deaths of more than half the trees in many stands, including mature trees up to 12 m tall. Pegg
et al. (92) reported localized extinction of R. psidioides from study sites in southeastern Queensland,
with no evidence of regeneration and with the emergence of weed species such as lantana on those
same sites. In the seven years after the detection of A. psidii in Australia, both R. rubescens and
R. psidioides went from being considered common and widespread to being preliminarily listed as
Critically Endangered in NSW because of A. psidii (84).
Impacts of A. psidii are pushing already threatened species closer to extinction. Gossia gonoclada
is one of these species, only found in dry rainforest and riverine scrubs in southern Queensland and
listed as endangered under the Environment Protection and Biodiversity Conservation Act 1999 (122).
A. psidii has been reported causing dieback along with infection of flowers and fruit, reducing
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PY56CH21_Carnegie ARI 31 July 2018 10:32
fecundity. Although there is some evidence of disease tolerance within the small population, the
impact of A. psidii will further reduce the population size (122). Pegg et al. (89) reported on
the susceptibility of Rhodamnia angustifolia, a species in which only twelve trees remain in wild
populations because of land clearing and natural rarity. The impact of A. psidii on cultivated plants
was significant, with tree decline, including branch death and dieback, occurring within 18 months
of initial symptom observation. Additionally, production of flowers was adversely impacted both
directly and indirectly.
The impact that A. psidii might have on regeneration following disturbance such as fire has long
been considered a risk this pathogen posed prior to arrival in Australia, with consequences for forest
structure and survival of dependent fauna and understory plants (49). Pegg et al. (88) examined
the impact on regeneration following wildfire in coastal heath environments in northern NSW in
which a range of Myrtaceae were common. Although fire is considered an important selection agent
in the development of Australia’s native flora (41), the development of new epicormic regrowth
and young seedlings en masse following fire creates ideal conditions for the development and rapid
spread of A. psidii because juvenile leaf and stem tissues are much more susceptible to the rust than
older suberized tissues. A. psidii infection was identified within a month of epicormic regrowth
first being detected and was later found on all ten species of regenerating Myrtaceae in the coastal
heath environment (88). M. nodosa and M. quinquenervia were both significantly impacted, with
repeated A. psidii infection causing severe dieback and, in some cases, death of epicormic regrowth
within 18 months of symptoms first appearing. However, for M. quinquenervia, approximately
30% of trees were resistant to A. psidii. This was not the case for M. nodosa, where all trees assessed
showed some level of infection and dieback, although some individuals appeared more tolerant
to disease by producing flowers and seedpods. The viability of the seed produced under these
circumstances was not determined.
The ecological effects of plant community level impacts are likely to become more obvious
over time. Pegg et al. (92) identified significant changes in species composition within rainforest
understory of a wet sclerophyll ecosystem in southeastern Queensland. These environments are
unique to Australia, and A. psidii is causing a rapid decline of all but one of the mid- and understory
Myrtaceae at this site. The most severely affected species include the important rainforest pioneer
species Archirhodomyrtus psidioides,Gossia hillii,Decaspermum humile,andRhodamnia maideniana
(92). Although these species are being replaced by non-Myrtaceae, it is unclear whether the dis-
turbance caused by myrtle rust is significant enough to prevent the site transitioning to rainforest,
as is usually the case in this habitat unless fire intervenes. This has implications for the ecology
of the region. No other studies have been conducted looking at plant community level impacts,
and no studies have measured the impact of myrtle rust on biodiversity or ecosystem function in
affected environments.
So far there has been no impact of myrtle rust in eucalypt plantations in Australia (15). However,
this could change if a more virulent biotype were to establish. The tea tree (M. alternifolia) industry
has also not been significantly impacted (P. Entwistle, personal communication). In contrast, the
establishment of myrtle rust in eastern Australia resulted in a significant impact on the nursery
and garden industry, with growers ceasing to grow highly susceptible species—and needing to
find acceptable alternatives—and requiring increased fungicide applications. The introduction of
myrtle rust into Australia is jeopardizing the growth and success of the expanding lemon myrtle
(B. citriodora) industry, with yield losses estimated to be up to 70% in untreated plantations, and the
need to apply fungicides resulting in some growers abandoning plans to become certified organic
(http://www.pbcrc.com.au/news/2016/pbcrc/myrtle-rust-threat-australian-landscape-and-
plant-industries).
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RECOMMENDATIONS FOR FUTURE INVASIVE PATHOGEN
INCURSIONS
Greater Involvement from Environmental Agencies in Biosecurity Policy
and Emergency Response Activities
There have been several independent reviews of Australia’s biosecurity system (e.g., 8, 28, 82) as
well as a specific review of environmental biosecurity in Australia (25), and all have highlighted
the inadequacy of and lack of focus on environmental biosecurity. Nairn et al. (82) highlighted
that biosecurity decisions need to take greater account of environmental considerations and that
Australia’s forest resources and native plant communities are at risk from the ongoing decline in
forest entomology and pathology capacities in state departments. Beale et al. (8) identified sig-
nificant achievements in plant biosecurity in Australia since the Nairn et al. (82) review but con-
cluded that the current biosecurity framework is “not being effectively used or analyzed to manage
risks to the Australian environment” (8, p. 123). Furthermore, there is poor knowledge of the biose-
curity threats to the natural environment and Australia “lacks the national capacity to respond to
pest and disease threats to environmental biosecurity” (8, p. 144).
An Australian Government Senate Inquiry determined that the level of support, resourcing,
and policy for environmental biosecurity is inadequate in comparison to that available to agri-
cultural plant industries, which benefit from the readily identifiable economic benefits of plant
industry biosecurity (25). Moreover, the capacity of government environmental departments to
address biosecurity is not adequate, as most of the biosecurity operational capability is in the plant
industry sector. Tellingly, as concluded by the Commonwealth Scientific and Industrial Research
Organization (CSIRO), “there are currently few resourced institutional arrangements for envi-
ronmental biosecurity to underpin a timely, coordinated and collaborative approach to prevent
and reduce the adverse impacts of invasive species” (25, p. 31).
In 2012, Australian commonwealth and state governments signed the Intergovernmental
Agreement on Biosecurity (IGAB) to coordinate and identify priority areas of reform and ac-
tion to build a stronger and more effective biosecurity system (28). An independent review of the
IGAB determined that environmental agencies must play a more direct role in policy and emer-
gency response and argued that environmental and social amenity biosecurity should be given the
same priority as animal and plant biosecurity (28). The review once again highlighted the lack of
involvement of environmental agencies in biosecurity policy and emergency response.
There is a weight of evidence showing that there would be substantial value in environmental
agencies being involved in prioritization—and resourcing—of biosecurity actions in Australia,
including the development of surveillance and diagnostics protocols. This needs to extend to
on-the-ground action, such as early-detection surveillance and direct involvement in emergency
response activities of environmental pests and pathogens. Currently, governments are relying on
better-funded agricultural agencies, who have the technical expertise in biosecurity but not neces-
sarily the expertise in environmental management, to do this work. The EPPRD was developed to
allow greater input—and resourcing—of biosecurity activities by industries; the NEBRA has not
achieved the reciprocal for environmental agencies. Recently, the forest industry identified gaps in
the biosecurity system with respect to forest pests (18, 128) and has worked with the Australian and
state governments and Plant Health Australia to address them, including the areas of resourcing
preparedness and response activities (31).
Australia has remained free from many of the devastating pests and pathogens of forests found
elsewhere, such as the emerald ash borer (79), Dutch elm disease (39), and Phytophthora ramorum
(13). However, the risk of exotic forest pests and pathogens arriving in Australia is increasing
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(61). There are significant and emerging diseases of iconic Australian tree genera that have been
planted as exotics that threaten our native environment, such as Ceratocystis wilts of Acacia (134),
Eucalyptus (107), and Metrosideros (80). Environmental agencies need to take a greater role in
activities to reduce the chance of these new threats establishing in Australia. There has been some
movement in this space over the past 12 months, with several projects commencing to identify
potential exotic invasive species for environmental pests (28). However, there needs to be direct
involvement in selecting these pests by environmental agencies as well as direct involvement of
environmental agencies in future pest incursions that threaten Australia’s environment.
Management of Non-Native Invasive Pathogens in Native Ecosystems
in Australia
Myrtle rust is only the second significant non-native invasive plant pathogen of the native en-
vironment in Australia, after Phytophthora cinnamomi. Although there is a financial incentive for
plant industries to manage non-native invasive pests, including in forestry (e.g., 14), there is no
direct financial incentive for environmental agencies to manage invasive pathogens. However, the
Australian Government environmental department (Department of Environment and Energy) has
international and statutory responsibilities relevant to invasive species (28), including the post-
border control of non-native species under the Environment Protection and Biodiversity Conservation
Act 1999 (EPBC Act) and international obligations for controlling or eradicating alien species
under the Convention on Biological Diversity.
One of the major avenues for environmental agencies to direct activities toward invasive species
is to identify an invasive species as a key threatening process, with a threatening process being
defined as a process that threatens or may threaten the survival, abundance, or evolutionary de-
velopment of a native species or ecological community [EPBC Act, s. 183 and s. 188]. Once a
threatening process is listed under the EPBC Act, a threat abatement plan can be put in place if
it is shown to be “a feasible, effective and efficient way” to abate the threatening process. Threat
abatement plans provide for research, management, and other actions to reduce the impacts of a
listed key threatening process on native species and ecological communities (EPBC Act, Part 13,
Division 5, Subdivision A, ss 267–284). However, there has been criticism of threat abatement
plans (25), which are documents that are not necessarily followed up by funding for on-the-ground
action. Furthermore, a substantial amount of time may elapse between the determination of a key
threatening process and development of a further strategy. For example, myrtle rust was deter-
mined to be a key threatening process in 2011 (83), and although a strategy has recently been
developed (86), no projects have been resourced as yet.
In plant industries, resources are often expended soon after a suspected significant invasive
species establishes, as there is a perceived cost:benefit for such expenditure (14). In the case of
myrtle rust, several plant industries conducted early research to determine whether this pathogen
would be a threat, including screening eucalypt germplasm (19, 62, 87) and lemon myrtle
plantations (35). There has been a paucity of research funds to investigate environmental impacts,
and until recently what there was came from the Plant Biosecurity Cooperative Research Centre
(http://www.pbcrc.com.au/news/2016/pbcrc/myrtle-rust-threat-australian-landscape-and-
plant-industries) and was conducted by researchers in primary industry institutes. Although a
Saving our Species Strategy has now been developed (86), earlier investment in research into the
environmental impacts of myrtle rust may have provided a more immediate understanding of its
potential broader impacts and allowed for a timelier response. Such a trickle of funding meant
that the true impact of myrtle rust took a long time to be made clear, delaying the message and
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awareness by senior environmental managers. More than seven years after myrtle rust established
and five years after we started to see a significant impact on native species, we only now have a
Saving our Species Strategy developed in NSW, one of the affected states (86). An adequately
funded program to investigate the potential impact of myrtle rust on the native environment
would have confirmed it to be a significant threat to many species and plant communities and
enabled earlier action to save such communities. As it is, some of these species are no longer
flowering due to myrtle rust, and there are no avenues for seed capture and storage. It is highly
likely that native species will become extinct due to this delay.
CONCLUSIONS
There is conclusive evidence that the initial decision to halt the myrtle rust emergency response
was made too hastily and lacked comprehensive consideration of all the relevant information. The
initial diagnosis of the rust as U. rangelii and coining of the name myrtle rust caused confusion
and resulted in the importance of the incursion being downplayed. Key industry (forestry) and
environmental stakeholders were not represented or fully considered, nor were they able to apply
pressure to continue the response; the lack of involvement by environmental agencies has since
proved to be a serious oversight. Although eradication may never have proved successful, the myrtle
rust experience has graphically demonstrated (a) the need for full participation in biosecurity by
environmental agencies, (b) that managing pests and pathogens once they have established in native
ecosystems is extremely challenging, and (c) that preventing establishment through pre-border,
border, and post-border biosecurity strategies needs to be a priority.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
The authors would like to thank Phil Cannon, Kathy Gott, Bob Makinson, Tim Low and
Andrew Cox for comments on an earlier draft of this manuscript, and acknowledge the support of
the Australian Government’s Cooperative Research Centres Program and the Plant Biosecurity
Cooperative Research Centre.
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Annual Review of
Phytopathology
Volume 56, 2018
Contents
Organic Amendments, Beneficial Microbes, and Soil Microbiota:
Toward a Unified Framework for Disease Suppression
Giuliano Bonanomi, Matteo Lorito, Francesco Vinale, and Sheridan L. Woo pppppppppppppp1
The Genome Biology of Effector Gene Evolution in Filamentous
Plant Pathogens
Andrea S´anchez-Vallet, Simone Fouch´e, Isabelle Fudal, Fanny E. Hartmann,
Jessica L. Soyer, Aur´elien Tellier, and Daniel Croll pppppppppppppppppppppppppppppppppppppp21
Seeing the Light: The Roles of Red- and Blue-Light Sensing
in Plant Microbes
Gwyn A. Beattie, Bridget M. Hatfield, Haili Dong, and Regina S. McGrane pppppppppppp41
Advances in Wheat and Pathogen Genomics: Implications
for Disease Control
Beat Keller, Thomas Wicker, and Simon G. Krattinger pppppppppppppppppppppppppppppppppppp67
Joining the Crowd: Integrating Plant Virus Proteins into the Larger
World of Pathogen Effectors
Scott M. Leisner and James E. Schoelz ppppppppppppppppppppppppppppppppppppppppppppppppppppppp89
The Future of Nanotechnology in Plant Pathology
Wade Elmer and Jason C. White pppppppppppppppppppppppppppppppppppppppppppppppppppppppppp111
Mechanisms Underlying Establishment of Arbuscular
Mycorrhizal Symbioses
Jeongmin Choi, William Summers, and Uta Paszkowski pppppppppppppppppppppppppppppppp135
Antibiotic Resistance in Plant-Pathogenic Bacteria
George W. Sundin and Nian Wang ppppppppppppppppppppppppppppppppppppppppppppppppppppppp161
Xylella fastidiosa: Insights into an Emerging Plant Pathogen
Anne Sicard, Adam R. Zeilinger, Mathieu Vanhove, Tyler E. Schartel,
Dylan J. Beal, Matthew P. Daugherty, and Rodrigo P.P. Almeida ppppppppppppppppppp181
The Barberry Eradication Program in Minnesota for Stem Rust
Control: A Case Study
Paul D. Peterson ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp203
v
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Endosymbionts of Plant-Parasitic Nematodes
Amanda M.V. Brown ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp225
Structural, Functional, and Genomic Diversity of Plant NLR Proteins:
An Evolved Resource for Rational Engineering of Plant Immunity
Freddy Monteiro and Marc T. Nishimura ppppppppppppppppppppppppppppppppppppppppppppppppp243
The Changing Face of Bacterial Soft-Rot Diseases
Amy O. Charkowski ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp269
Biology of Fungi and Their Bacterial Endosymbionts
Teresa E. Pawlowska, Maria L. Gaspar, Olga A. Lastovetsky,
Stephen J. Mondo, Imperio Real-Ramirez, Evaniya Shakya,
and Paola Bonfante ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp289
Sclerotinia sclerotiorum: An Evaluation of Virulence Theories
Liangsheng Xu, Guoqing Li, Daohong Jiang, and Weidong Chen ppppppppppppppppppppppp311
Fitness Penalties in the Evolution of Fungicide Resistance
N.J. Hawkins and B.A. Fraaije pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp339
Multifaceted Impacts of Bacteriophages in the Plant Microbiome
Britt Koskella and Tiffany B. Taylor ppppppppppppppppppppppppppppppppppppppppppppppppppppppp361
Plant-Parasitic Nematodes and Food Security in Sub-Saharan Africa
Danny L. Coyne, Laura Cortada, Johnathan J. Dalzell,
Abiodun O. Claudius-Cole, Solveig Haukeland, Nessie Luambano,
and Herbert Talwana pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp381
The Rise and Rise of Nicotiana benthamiana: A Plant for All Reasons
Julia Bally, Hyungtaek Jung, Cara Mortimer, Fatima Naim,
Joshua G. Philips, Roger Hellens, Aureliano Bombarely, Michael M. Goodin,
and Peter M. Waterhouse pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp405
Wheat Blast: Past, Present, and Future
Paulo Cezar Ceresini, Vanina Lili´an Castroagud´ın, Fabr´ıcio ´
Avila Rodrigues,
Jonas Alberto Rios, Carlos Eduardo Aucique-P´erez, Silvino Intra Moreira,
Eduardo Alves, Daniel Croll, and Jo˜ao Leodato Nunes Maciel pppppppppppppppppppppppp427
Lessons from the Incursion of Myrtle Rust in Australia
Angus J. Carnegie and Geoff S. Pegg pppppppppppppppppppppppppppppppppppppppppppppppppppppp457
CRISPR Crops: Plant Genome Editing Toward Disease Resistance
Thorsten Langner, Sophien Kamoun, and Khaoula Belhaj pppppppppppppppppppppppppppppppp479
Understanding Cytoskeletal Dynamics During the Plant
Immune Response
Jiejie Li and Christopher J. Staiger pppppppppppppppppppppppppppppppppppppppppppppppppppppppp513
vi Contents
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PY56_FrontMatter ARI 3 August 2018 10:38
Hyperspectral Sensors and Imaging Technologies in Phytopathology:
State of the Art
A.-K. Mahlein, M.T. Kuska, J. Behmann, G. Polder, and A. Walter ppppppppppppppppppp535
Network Analysis: A Systems Framework to Address Grand
Challenges in Plant Pathology
K.A. Garrett, R.I. Alcal´a-Brise ˜no, K.F. Andersen, C.E. Buddenhagen,
R.A. Choudhury, J.C. Fulton, J.F. Hernandez Nopsa, R. Poudel,
and Y. Xing ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp559
RNA Interference Mechanisms and Applications in Plant Pathology
Cristina Rosa, Yen-Wen Kuo, Hada Wuriyanghan, and Bryce W. Falk pppppppppppppppp581
Multiple-Disease System in Coffee: From Crop Loss Assessment to
Sustainable Management
Jacques Avelino, Cl´ementine Allinne, Rolando Cerda, Laetitia Willocquet,
and Serge Savary ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp611
World Management of Geminiviruses
Maria R. Rojas, Monica A. Macedo, Minor R. Maliano, Maria Soto-Aguilar,
Juliana O. Souza, Rob W. Briddon, Lawrence Kenyon,
Rafael F. Rivera Bustamante, F. Murilo Zerbini, Scott Adkins, James P. Legg,
Anders Kvarnheden, William M. Wintermantel, Mysore R. Sudarshana,
Michel Peterschmitt, Moshe Lapidot, Darren P. Martin, Enrique Moriones,
Alice K. Inoue-Nagata, and Robert L. Gilbertson pppppppppppppppppppppppppppppppppppppp637
Errata
An online log of corrections to Annual Review of Phytopathology articles may be found at
http://www.annualreviews.org/errata/phyto
Contents vii
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