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Edizioni ETS Pisa, 2012
S1.5
PSEUDOMONAS SYRINGAE pv. ACTINIDIAE
IN NEW ZEALAND
J.M. Young
49 Allendale Rd., Auckland 1025, New Zealand
SUMMARY
There are several populations of Pseudomonas syringae pv. actinidiae (Psa) that differ in virulence, in genetic characteristics, and in phenotypic characters. Primary concern is with highly virulent strains, here called
Psa –V. They cause most damage in gold fruit cultivars
of Actinidia chinensis. So far, attempts to manage the
disease by pruning, by sprays and by other measures
have been unsuccessful.
INTRODUCTION
Much information has been gathered concerning
bacterial epidemiology in the last 50 years, particularly
of the pathovars of P. syringae. Much of this literature
has been forgotten and does not inform the present
problem. The virulent strains of P.s. actinidae (Psa-V)
have been studied for 3-4 years in Italy (Ferrante and
Scortichini, 2010) and for two seasons in NZ.
Although this is a small research and observational
base, there is enough information in the literature, from
past general experience, and in local observations, to
draw preliminary conclusions. At present, virulent
strains of P.s. actinidiae (Psa-V) are found in New
Zealand in the Bay of Plenty, the main growing region,
and cannot be eradicated from the country. All outbreaks are identified in ‘priority zones’ by MAF Biosecurity as part of an effort to contain the pathogen.
P.s. actinidiae strains. At least three populations of
P.s. actinidiae have been reported. The first was recorded
in Japan (Takikawa et al., 1989), South Korea (Koh et al.,
1996, 2003, 2010) and in Italy in 1992 (Scortichini, 1994)
about 20 years ago. This pathogen formed the basis of
the pathovar name and first epidemiological observations. Subsequently, a second population that causes a
more serious form of the disease has been recorded in
gold kiwifruit (H16A) in Italy since 2008 and in New
Corresponding author: J.M. Young
Fax: +64.9. 849.4738
E-mail: [email protected]
Zealand in November 2010. These two populations appear to be genetically very similar and are considered to
be members of the same haplotype (Fig. 1). The virulent
and weakly virulent populations are now referred to as
Psa-V and Psa-LV, respectively. The third population has
been identified only in New Zealand so far (Chapman et
al., 2011). It is a distinct genetic haplotype of the
pathogen that, as inferred from its widespread distribution, has been present in New Zealand for many years
without being noticed. It appears to be weakly virulent.
Actinidia appears to be a diverse Chinese genus. It seems
probable that Psa is also diverse and that the three identified haplotypes only reflect a small proportion of the diversity of the pathovar as a whole. Differentiating these
populations by name is cumbersome, but the most accurate terminology, until further studies clarify matters, is to
recognise the pathovar, P. syringae pv. actinidiae haplotype 1, which includes Psa – V and Psa-LV. Haplotype 2
is here designated Psa-LV (NZ) (Fig. 1).
Distribution of Psa. Psa has now been recorded in all
countries where Actinidia chinensis and A. deliciosa
have been distributed; in Japan, Korea, Italy, France,
Portugal, Brazil, Chile, China and New Zealand
(Everett et al., 2011, Scortichini et al., 2011).
Since it was first observed in New Zealand in November, 2010, Psa-V is now (December 2011) widely distributed in the Bay of Plenty, the main growing region (Table
1). Its very rapid spread in the 2010-11 season suggests
that the pathogen was introduced very few seasons ago.
In March, 2011, Psa-V was identified on orchards comprising fewer than 500 ha. Since then the affected area
has risen exponentially to (November 2011) almost 5000
ha. Until recently, all outbreaks were to be found in the
Bay of Plenty. A single outbreak in the Manukau area has
occurred that seems to have no obvious connection with
previous records.
Kiwifruit cultivars. Favoured cultivars of gold kiwifruit (Actinidia chinensis) are Hort16A, Jin Tao and
Soreli. Other cultivars are now under investigation for
fruit quality and tolerance to Psa. Psa-V is more virulent
in these gold kiwifruit cultivars (A. chinensis) than in
green kiwifruit cv. Hayward (A. deliciosa). Nevertheless,
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Ps. syringae pv. actinidiae in New Zealand
Journal of Plant Pathology (2012), 94 (1, Supplement), S1.5-S1.10
the pathogen moves progressively in ‘Hayward’ and its
impact on this cultivar has not yet been adequately determined.
mation). Primers for Real-time PCR detection/identification have been developed that differentiate the pathogenic populations and are now being tested.
Identification. Psa is a member of LOPAT group I of
Pseudomonas syringae (Lelliott et al., 1966). With isolates
so identified, several DNA based methods have been reported to differentiate Psa from other pathovars (ReesGeorge et al., 2010). Mazzaglia et al. (2011) and Ferrante
and Scortichini (2010) report methods that differentiate
Psa-V and Psa-LV. Based on MLSA studies, Psa has been
allocated to a genomospecies that comprises two of those
created by Gardan et al. (1999), viz. 3 and 8 using
DNA:DNA hybridisation (Fig. 1). It can be allocated reliably to this genomospecies by any one of a number of
comparisons of housekeeping genes, such as acnB, dnaX,
cts, gapI, gltA, gyrB, pfk, pgi and rpoD (unpublished infor-
Aetiology. The three major environmental factors affecting primary infection are moisture, temperature and
light. When leaves transpire, the stomata are so numerous and open so widely that the lower leaf surface offers
practically no barrier to gas exchange or bacterial infection. Light is probably the most critical factor involved
in stomatal opening.
Quorum sensing (QS) is a well-established phenomenon in which bacteria are stimulated to specific metabolic action only when physically closely associated cells
act in concert. It has been shown that QS influences
many metabolic processes including several disease
steps in P. syringae (von Bodman et al., 2003; Quiñones
et al., 2005). The involvement of QS is being investigated as a possible means of inhibiting the main steps in infection. However, the available data indicate that the
multiplication of individual pathogenic cells begins
within a few hour of inoculation while the enlarged
populations capable of QS develop after one or more
This indicates that QS is not essential for multiplication.
Evolutionary considerations suggest that it would be fatal for a single-celled pathogen to require the multiple
invasions of infection sites for development.
Fig. 1. MLSA of Genomospecies 3 and 8 (Gardan et al., 1989)
based on partial sequences of pilD, pgi, dnaX and cts showing
that these represent a single genomospecies centred on P. avellanae that includes P.s. actinidiae (unpublished data).
Epidemiology. The occurrence and severity of epidemics is primarily determined by seasonal weather.
The micro-climate in orchards is critical in determining
the local severity and extent of disease. This means that,
while it may be possible to determine the extent to
which an area may be at risk, more detailed predictions
are impossible.
Weather conditions that favour bacterial infection
are usually sporadic, being confined to particular seasons and are associated with rainy, wet humid, conditions. Once infected, disease development is largely determined by temperature.
Practically all literature on Psa concerns the behaviour of Psa-LV in Japan and Psa-V in Italy. Detailed epidemiological studies have been made only in Japan (Serizawa and Ichikawa, 1993a, 1993b, 1993c; Serizawa et
al., 1989, 1994) Like P.s. syringae (Young, 1991), Psa
causes disease at relatively low temperatures, being
most active at ca.18°C and progressively reducing in
severity above 20°C and below 15°C. Cankers in trunks
and leaders, developing most rapidly in late winter and
spring, are the most serious symptom because they girdle whole limbs and kill entire vines. In Italy, infection
of vegetative and fruiting canes occurs in spring. Bacteria in cankers usually die out in spring-summer when
temperatures rise above 20°C (M. Scortichini, personal
communication). This is not the case in New Zealand,
where disease in canes continues through summer.
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Table 1. Distribution of Psa-V in New Zealand at 30 November 2011 (http://www.kvh.org.nz/statistics )
Number of infected orchards
Affected orchards (%)
Hectares of affected orchards
Infected hectares (%)
889
24
4356
32
79% of New Zealand’s kiwifruit hectares are now in a
Priority Zone.
35% of New Zealand’s kiwifruit hectares are in orchards
with a Psa – V positive result.
Symptoms. Symptoms in canes may primarily be the
result of leaf scar infections that occur in autumn. The
pathogen in leaf scars may rest during winter, becoming
active in spring, spreading in first and second year tissue. Infected canes lead to girdling and wilting of flowering shoots. In Italy, infection and disease ceases in
canes in summer, being carried over in infected leaves.
However, in New Zealand’s growing regions, which
have a mild maritime, practically frost-free, climate, disease in canes is practically unchecked, the disease
spreading in canes throughout the summer. It has yet to
be determined if cane cankers carry over to develop in
winter. Severe cankers appear in late winter and spring.
J.M. Young
S1.7
These produce gumming cankers from which the
pathogen can initially be isolated. Subsequently, cankers
are invaded by bactericidal plant phenolics, resulting in
red-brown gummosis from which the pathogen is increasingly difficult to isolate.
Leaf-spots in summer are usually trivial but they are
the likely source of next season’s inoculum; the
pathogen being carried over autumn in and on leaves to
leaf scars. Leaves remain infected into autumn. Infections of leaf scars appear to remain dormant until early
spring when the pathogen becomes active and infects
new season’s growth.
There is little evidence of significant movement of individual bacterial cells either in the parenchyma or vasculature. Cells multiply at lesion margins, pushing young
cells into the adjacent tissue, thus advancing the lesion.
In trunks and leaders spread of the pathogen appears
to be through several tissue elements, including outer
parenchyma (Fig. 2C,D) and internal woody sclerenchyma (Fig. 2E). It has been suggested that infection is systemic, moving from leaf spots down into canes through
the vascular cortex. However, invasion of leaf veins from
leaf spots (Fig. 2B) appears to be rare. Shoots emerging
in late spring can be severely infected (Fig. 2A). As yet,
sites of infection, at the abaxial or adaxial ends of
cankers, have not been established. The role of systemic
Fig. 2. A. Infected emerging shoot (courtesy of R. Baker). B. Leaf lesions invariably delimited by veins: absence of systemic spread
(courtesy of J. P. Wilkie). C. Infection of outer parenchyma (courtesy of G.M. Balestra). D. Incipient girdling of trunk (courtesy of
M. Scortichini). E. Pseudomonas syringae pv. actinidiae oozing from woody sclerenchyma (courtesy of R. Baker).
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Journal of Plant Pathology (2012), 94 (1, Supplement), S1.5-S1.10
movement in vines is unclear (Y. Takikawa, personal
communication).
Dispersal. It has been known for decades that bacterial pathogens are dispersed for hundreds of metres,
perhaps kilometres in clouds of inoculum generated as
aerosols in wind-driven rain, which spread between
blocks and orchards. Where a localized infection site is
observed, then it follows that the pathogen is already
present in all surrounding vines and blocks. Spread between orchards on implements can occur, but it will be
secondary in importance to natural spread. Courtesy requires that orchardists observe sensible hygienic measures moving equipment between orchards.
Localized expression, sometimes only in one part of a
single vine, is due to the highly specific environmental
conditions required for disease development. Fundamental to an understanding of bacterial epidemiology is that
epidemics usually occur sporadically, sometimes after
years of bacterial association with the host at sub-clinical
levels (e.g., P. syringae pv. pisi). Given the virulence of
Psa-V, epidemics can be expected to be more regular
than those occurring in weaker pathogens, but absence of
symptoms of the pathogen is not evidence of its absence.
Containment. Only significant geographical breaks between infected and uninfected orchards will delay further
spread of the pathogen, with rigorous attention to preventing the movement of infected material between regions. The recent confirmations of a single isolated outbreak of Psa-V spread outside the initial infection zone is
most probably on inadequately disinfected vehicles or
equipment. For some vehicles, decontamination is practically impossible. Attempts at active containment in other
crops in the past have never been effective (the eradication of citrus canker in Florida in the 1930s using draconian measures being the exception). Recent attemps at
eradication of Citrus canker and Citrus huanglongbing
caused by Candidatus Liberibacter spp. (Gottwald, 2010)
were ineffective and this confirms that efforts to contain
bacterial pathogens, including Psa, by local eradication in
identified containment zones are unrealistic.
Climate. Epidemics occur under precisely prescribed
conditions, usually occurring regionally or sub-regionally. Southern growing regions are likely to be at greater
risk. Several important questions about the behaviour of
Psa could be framed in terms of NZ’s seasonal conditions compared with those in Italian regions. A study of
historical daily temperatures and rainfall may indicate to
what extent conditions mimic those of Italy and Japan
and hence likely regional severity. Only when the
pathogen is distributed more widely, in a wider climatic
range, will it be possible to establish possible areas for
future planting and those to avoid.
Management and Control. Any proposed control
protocol must be cost-effective; the return in crop yield
from the treatment must exceed labour and material
costs. It is only by crop surveys that the severity of a disease can be described accurately.
Pruning. Pruning was introduced to control fungal
diseases in the 19th century when it was realized that
spore production occurred mainly after plant tissue was
killed. Spore production and dispersal in this way was a
main source of further fungal infection. This practice
has been recommended for bacterial control since then:
(i) To remove prunings to reduce future infection in
subsequent years. Compared with inoculum still present
in living plants, infected prunings are only likely to be a
secondary source. Stringent removal of prunings is unlikely to lead to significant reduction in disease in the
long term. Numbers of pruning wounds is small compared with natural infection sites.
(ii) To prevent further spread of disease in a block,
orchard or region (‘aggressive containment’; the removal of all leaders, canes and leaves, shortening the
vine to trunk stumps). Aggressive pruning appears to
arise from a confusion between eradication and control.
Disease will certainly reappear with any new growth,
arising from the block itself or from adjacent orchards.
Recovery of vines that have been aggressively pruned
may be doubly difficult because the gross imbalance between roots and shoots means that sprouts and grafted
scions are the most susceptible of all young tissue and
now are confronted with a virulent pathogen.
Following the initial outbreak, a compensation
scheme was introduced that indemnified all growers
who agreed to the removal of blocks and orchards as
part of aggressive containment. This scheme was retracted when it was realized that it was ineffective.
Psa-V does infect through pruning cuts, but recent
trials in Italy have shown that the cuts are, for practical
purposes, impossible to sterilize, even in a rigorous trial
involving cauterizing wounds with a blow-lamp and
sealing them immediately after pruning (C. Kay, Zespri,
personal communication). Commercial pruning will not
be effective as a disease preventative.
Numerically, there are many more natural infection
sites than pruning wounds and, although the latter are
more susceptible, they make a lesser contribution to infection. There have been many attempts to control
pathogens by pruning. Only in conditions where the
pathogen induces relatively mild symptoms have there
been claims of success. Pruning is usually for general
hygiene, not for bacterial control.
Spray control. Attempts at bacterial control with inseason biocidal sprays have been made for more than a
century. Many compounds have been tested with little
or no success and have been abandoned. In testing the
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efficacy of sprays, the most common practice has been
to assay leaf spots and leaf damage. Past observations
suggest that this does not give a measure of crop yield.
Copper sprays are most commonly recommended
but it has been shown that many plants, including kiwifruit (unpublished information), suffer from severe
phytotoxicity. Once the pathogen has penetrated leaves,
whether or not symptoms are expressed, it is impossible
for control sprays, coppers or antibiotics, to affect them.
Sprays in spring therefore have no efficacy. However, in
desperation, kiwifruit growers continue to apply exotic
compounds including organic extracts (garlic extract,
citrus seed extract, propolis), hypochlorite, quaternary
ammonium compounds, terpenes, chitin-based products, and other unproved ‘snake-oils’.
A spray programme, proved to be effective in other
tree crops and pathogens, entails copper sprays applied
during leaf-fall to cover leaf scars as infection sites in
autumn (Young, 1982 and other references).
Streptomycin was applied to many crops but is now
banned in most jurisdictions. In trials in many crops in
the past, the antibiotic gave unreliable results. Serizawa
et al. (1989) report the reduction of Psa on kiwifruit
leaves using streptomycin in spring. Past studies of injection of streptomycin into kiwifruit trunks resulted in
the direct transmission of the antibiotic to the leaves
where it caused chlorosis with severe stunting of the leaf
margins (unpublished information).
The genes for streptomycin and copper resistance
have been reported in Psa (Marcelletti et al., 2011;
Nakajima et al., 2002) and in other pathogens. However, it is rare to find a report in which resistant strains are
proved to be the cause of epidemics (Young, 1977).
Biocontrol. There appears to be only one approach
to characterizing biocontrol agents. Saprobes are
screened in culture for antagonism to the target
pathogen. In glass-house trials, antagonistic strains are
briefly inhibitory if the antagonist is applied in numbers
at least an order of magnitude greater than the pathogen
and immediately prior to, or at the same time as inoculation of the pathogen. Such experiments seldom lead
to reports of successful field trials.
The reasons for failure of this approach are now wellunderstood. The characteristic of pathogens is to induce
leakage in the host cell wall, releasing the cellular contents as nutrients for their multiplication and secondarily for saprobes. Although pathogens grow more slowly
than saprobes in culture, the latter are dependent on the
prior activity of the pathogenic cells for growth in the
plant. Saprobes survive in or on leaves for some hours
or days. If the populations are examined over extended
periods, it will be found that the saprobes decline except under unusual circumstances, but the pathogen
multiplies exponentially after a resting phase of a few
hours. It follows that the saprobe can have little influ-
J.M. Young
S1.9
ence on the pathogenic population. Spore-forming bacteria as biocontrol agents are also inactive in their plant
association but they instantly form resting spores in adverse conditions, which is why high populations can be
recorded after copper sprays.
Bacteriophages were tested exhaustively in the 1970s
- 80s without success. The reason is probably that phage
particles are immobile and unable to reach bacterial
populations in plants.
Breeding for resistance. As noted, some cultivar selections of gold kiwifruit offer tolerance to Psa-V and
may serve as substitutes for the present favoured cultivars. The only long-term solution is to introduce resistance genes into existing cultivars that have favourable
marketing characteristics. Studies in China indicate that
there are several possible sources of resistance (Li et al.,
2004). The selection of crosses of resistant and commercially favourable cultivars will be slow and painstaking.
Epilogue. Canker of kiwifruit is so severe in Italy and
New Zealand that producing organizations are considering abandoning cv. Hort16A in these countries.
ACKNOWLEDGEMENTS
Thanks to J.D. Janse, K.R. Everett, M. Scortichini,
G.M. Balestra and Y. Takikawa for advice, and B.W.
Weir and D.-C. Park for producing the MLSA.
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