-
Fungal Diseases of Citrus Fruit and Foliage
Megan DewdneyPMA 5205
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Foliar Fungal Diseases to be CoveredoAlternaria Brown Spot (and
leaf spot of rough lemon)oGreasy spotoMelanoseoScab DiseasesoBlack
SpotoPostbloom Fruit DropoPseudocercospera Fruit and Leaf Spot
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What Is a Fungus?oEukaryotic microorganisms and members of
Kingdom FungioAbsorb dissolved molecules as food sourcesGenerally
secrete enzymes into environmentDo not photosynthesize
oMost fungi grow as tubular, elongated cellsTypified by
filamentous growthIndividual filamentous threads are called hyphaeA
group of hyphae is the mycelium
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Oomycetes and Fungi are Not Closely Related
Stramenopila/Oomycota
(“Oomycetes”)
Fungi
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Differences Between Oomycota & EumycotaFeature Oomycete True
Fungi
Neighboring taxonomic groups Diatoms and golden brown algae
Animals
Hyphal architecture Aseptate tubular hyphae Either single cell
or septated hyphaeOne or more nuclei per compartment
Vegetative hyphae ploidy Diploid except in cells leading to
gametes (haploid)
Typically haploid or dikaryotic; often with stable or
semi-stable diploid stage post-mating
Typical genome size (Mb) 50-250 10-40
Major components of cell walls Cellulose and glucose polymers
Chitin and/or chitosan and glucans
Asexual spore types Undesiccated, unicellular sporangia
(multinucleated cells)
Desiccated single or multicellular conidia (one
nucleous/cell)
Motile asexual spores Nearly universal biflagellated Rare, only
chytrids, and monoflagellated
Sexual spores Oospores on the end of specialized hyphae with one
zygotic nucleous
Varied types, often occur in large numbers within complex
structures
Modified from Howard S. Judelson & Flavio A. BlancoNature
Reviews Microbiology 3:47-58
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Note on TerminologyoMany Ascomycete fungi have historically had
what is know as an
anamorph and teleomorphAnamorph: asexual or imperfect
stageTeleomorph: sexual or perfect stageHave separate names but now
names are being consolidated (synonyms)
o Fungi where no sexual stage has been identified are grouped
into the ‘Fungi Imperfecti’ Synonym: DeuteromycteSome
Basidiomycetes have also lost sexual stage Ex. Rhizoctonia spp.
o Glossary of plant pathology terms: o
www.apsnet.org/edcenter/resources/illglossary/Pages/default.aspx
PresenterPresentation NotesSpeculation that the fungi imperfecti
have lost the need and/or ability to form sexual sporesOccasionally
the teleomorph and anamorph are matched and the anamorph is
reclassified as an ascomycete – Can be confusing!An organism should
be formally referred to by teleomorph stage in the literature Why
is this important?Diseases where no sexual stage knownDiseases
where only sexual stage is importantDiseases where the asexual
stage is most importantDiseases where both stages are important but
play separate roles
https://www.apsnet.org/edcenter/resources/illglossary/Pages/default.aspx
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Alternaria Brown Spot
oCausal agent: Alternaria alternataSynonyms: Alternaria citri
and A. alternata pv. citriNo known sexual stage
oImportant disease on tangerines and tangeloso1903 First
described in Australia on Emperor mandarin
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Alternaria Brown Spot cont.
o1974 First identified in FloridaoAlso found in South Africa,
Turkey, Israel, Spain, Colombia
and other countriesoHost specific toxinIsolates from tangerines
and tangelos do not infect rough lemon
except in rare circumstancesDisease on rough lemon same organism
with different toxinConsidered separate pathotypes of A.
alternata
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PresenterPresentation NotesLow molecular weight molecules
secondary metabolitesProduced during germination of the spores –
responsible for chlorotic halo around the lesionACR – unknown
target but speculated to be plasma membraneACT - mitochondria
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Alternaria alternataoNo sexual stage knownoNecrotrophicoConidia
are small, thick walled, pigmented and multicellularoThe
conidiophores are determinate and pigmentedoConidia are borne in
chains oHyphae penetrate host tissue directly; No appressorium
*appressorium = specialized structure at the end of a hyphae
thatanchors to the plant and forms further structures to infect the
plant
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Tissue Susceptibility
oHighly susceptible cultivars Dancy, Minneola, Orlando,
Sunburst, Murcott, Nova, and Lee
oLeaves susceptible from formation to when fully expanded and
hardened
oFruit are susceptible from petal fall to 5 cm (2 inch) in
diameter
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Symptoms
PresenterPresentation NotesIncubation period is 24-36 hours;
easily visible symptoms 2-3 days post infectionFirst symptoms are
necrotic flecks
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Alternaria Brown Spot Disease Cycle Caused by Alternaria
alternata
PresenterPresentation NotesConidia produced on lesions from
wilted twigs, mature leaves or leaf litter approximately 10 days
after infectionVery few conidia produced on fruitSurvival when no
susceptible tissue available on mature leaves and twigsFew periods
of the year when no spores are being produced
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When are the Conidia Released?oConidia released by rain
events
or sudden changes in relative humidity
oIn field trapping, number of conidia in the air related to leaf
wetness duration
oNumber of airborne conidia not related to infection severity
Timmer et al., 1988
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Infection Conditions
oOptimum temperatures 23-27°CCan get infection between
17-32°C
oInfection can occur with as little as 4-6 hours of leaf wetness
but disease severity increases with leaf wetnessWhat factor allows
for the 4 hour
infection period?Canihos et al., 1999
PresenterPresentation Notes73.4-80.6 °F63.6-89.6 °F
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Alternaria Brown Spot Disease Cycle Caused by Alternaria
alternata
PresenterPresentation NotesConidia produced on lesions from
wilted twigs, mature leaves or leaf litter long after
infectionMinimal conidia produced on fruitSurvival when no
susceptible tissue available is on mature leaves and twigsFew
periods of the year when no spores are being produced
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Cultural Controls
oDisease-free nursery treesoCareful choice of planting siteAir
drainage importantWider spacing
oNo vigorous rootstocksoNo over-fertilization or
over-wateringoHedge in late MarchoNo overhead irrigation
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FungicidesoCopper – Works well for fruit but not leavesoFerbam –
Only moderately effectiveoStrobilurins – Most effective but
specific MOAAzoxystrobinTrifloxystrobinPyraclostrobin
oFirst spray when spring flush ¼-1/2 full expansion; high
inoculum another before full expansion or at petal fall
oRest of the year maintain protective coating
PresenterPresentation NotesNo more than 4 sprays of any
combination of Strobilurins in the year
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ALTER-RATER: A Forecasting System
oWeather-based point system to better time fungicide
applications
oPoints assigned based on:Rainfall and leaf wetnessAverage daily
temperature
oThresholds vary by cultivar susceptibility
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The ALTER-RATERSuggested Threshold Scores
Score Situation
50Heavily infested Minneola, Dancy, Orlando, Sunburst; Many
flatwoodgroves, East coast, and SW Florida.
100Moderately infested Minneola or Dancy, many Murcotts; Ridge
and north Florida groves.
150 Light infestations, any variety, mostly Ridge and north
Florida groves.
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ALTER- RATER Daily PointsRain > 0.1 inch LW > 10 hr Avg
daily Temp (°F) Assigned score
+ + 68-83 11+ + > 83 8+ + < 68 6+ _ 68-83 6+ _ > 83 4+
_ < 68 3_ + 68-83 6_ + > 83 6_ + < 68 4_ _ 68-83 3_ _ >
83 0_ _ < 68 0
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Greasy Spot
oCausal agent: Zasmidium citri-griseumSynonyms: Mycosphaerella
citriAnomorph only: Stenella citri-grisea; Cercospora
citri-grisea
oOther similar diseases described around world but caused by
other fungi in the Mycosphaerellaceae
oImportant disease on most types of citruso1915 First described
in Florida and Cuba
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Greasy Spot cont.
oAlso occurs in Texas, the Caribbean, Central and South America,
and parts of Asia
oPrimary effect is to cause defoliation which can lead to
decreases of yield and fruit sizeUp to 25% on sweet orange in
Florida Up to 45% on grapefruit
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Zasmidium citri-griseum
oLoculoascomycetePseudothecia up to 90 µmFound in leaf
litterAscospores fusiform and hyaline with one
septum (2-3 x 6-12 µm)
PresenterPresentation NotesPapillate ostiole – sticks up like a
nose
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Asexual form
oConidia are pale olive brown, cylindrical with indistinct
septae that can be in chains
oTwo types of conidiophoresMost common simple, smooth, dark and
erect Rare, in clusters (fasciculate) found in necrotic
areas on leaves
PresenterPresentation NotesThe more rare conidiophore is where
the original name of Cercospora grisea-citri came from as they were
the only fruiting bodies found associated with greasy spot
lesionsNecrotic spots are from freeze injury or fertilizer burn
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Mycelium
oEpiphytic hyphaeHighly branchedRough walls Olive brown color
when young but darken with age and the walls
become smoothoAppressoria formed in stomatal chambersoMycelia
within leaf grow intercellularly and are not very
branched
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Tissue Susceptibility
oHighly susceptible cultivarsGrapefruit, Pineapple, Hamlin, and
Tangelos
oLess susceptible cultivarsValencia, Temple, Murcott, and most
tangerines
oYoung and mature leaves susceptible to infectionoImmature fruit
susceptible
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Symptoms
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Greasy Spot Disease Cycle Caused by Zasmidium citri-griseum
PresenterPresentation NotesMajor inoculum is the
ascosporesDischarge with the rain or wetting from irrigationPeak
discharge from April and MayJune and July the leaves
decomposeConidia infections are very minor in the disease
cycleAscospores germinate to form the epiphytic phase which
penetrates through the stomatesMost of the infection is on mature
leaves and mainly occurs between June and September
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Pseudothecia MaturationMoisture
Mondal and Timmer, 2002
PresenterPresentation NotesMost growers irrigate 3X a week
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Pseudothecia MaturationTemperature
Mondal and Timmer, 2002
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Optimal Temperatures for Ascospore Productiono20 °C = 68.0 °Fo24
°C = 75.2 °Fo28 °C = 82.4 °Fo32 °C = 89.6 °F
Mondal and Timmer, 2002
PresenterPresentation NotesA little unusual that temperature is
so restrictive but the conditions are optimal many days in Florida
and the Caribbean.
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Peak Ascospore Ejection
o The peak ascospore ejection period has shifted to earlier in
seasonWhy?Is this beneficial?
0
5
10
15
20
25
30
35
A M J J A S O N D J F M
Months
Pe
rce
nt
of
tota
l as
cos
po
res
2000-012001-021969
PresenterPresentation NotesChange in irrigation technology from
overhead irrigation or no irrigation to microsprinklersMore
frequent wetting and drying of leaf litter which leads to more
rapid ascospore productionYes –conditions are not favorable for
ascospore germination
Chart3
A4.61773700310.6
Apr12.90519877681
M9.70642201832
May28.99082568813.4
J5.07645259947
June2.935779816517
J1.00917431196
July5.25993883795.2
A1.89602446483.8
August1.64525993881.3
S0.85626911310.9
Sept0.82568807341.5
O1.10091743121.3
Oct0.97859327220.4
N0.70336391440.6
Nov2.1406727829
D1.1559633028
Dec4.0305810398
J0.4892966361
Jan0.2140672783
F1.8042813456
Feb3.5779816514
M3.4250764526
Mar4.6422018349
2000-01
2001-02
1969
Months
Percent of total ascospores
4.2302016724
12.395474668
24.6679783571
20.2410231185
3.1480570585
4.8204623709
2.1888834235
4.9680275455
1.9675356616
1.6969995081
0.7624200689
0.4672897196
0.6148548942
1.436301033
1.2247909493
0.4918839154
1.7215937039
4.5253320216
0.5656665027
0.4426955239
0.0983767831
0.5656665027
1.598622725
5.1647811117
Chart1
M
May
J
June
J
July
A
August
S
Sept
O
Oct
N
Nov
D
Dec
J
Jan
F
Feb
M
Mar
Fig. Ascsopores traped at grapefruit groves using volometric
spore trap during 2000-2001.
Months
Ascospores
5015
4115
640
980
445
1010
400
345
155
95
125
292
249
100
350
920
115
90
20
115
325
1050
Chart2
M
May
J
June
J
July
A
August
S
Sept
O
Oct
N
Nov
D
Dec
J
Jan
F
Feb
M
Mar
2000-2001
Months
Ascospores
5015
4115
640
980
445
1010
400
345
155
95
125
292
249
100
350
920
115
90
20
115
325
1050
Sheet1
Ascospore in the air
2000-20012001-2002
A860755
Apr25202110
M50151587
May41154740
J640830
June980480
J445165
July1010860
A400310
August345269
S155140
Sept95135
O125180
Oct292160
N249115
Nov100350
D350189
Dec920659
J11580
Jan9035
F20295
Feb115585
M325560
Mar1050759
&RFigure 1 of Plant DiseaseMondal and Timmer
Sheet1
2000-2001
2001-2002
Ascospores
Sheet2
2000-20012000-012001-20022001-02
A8604.2302016724203307554.6177370031163500.6
Apr252012.395474668211012.90519877681
M501524.667978357115879.70642201832
May411520.2410231185474028.99082568813.4
J6403.14805705858305.07645259947
June9804.82046237094802.935779816517
J4452.18888342351651.00917431196
July10104.96802754558605.25993883795.2
A4001.96753566163101.89602446483.8
August3451.69699950812691.64525993881.3
S1550.76242006891400.85626911310.9
Sept950.46728971961350.82568807341.5
O1250.61485489421801.10091743121.3
Oct2921.4363010331600.97859327220.4
N2491.22479094931150.70336391440.6
Nov1000.49188391543502.1406727829
D3501.72159370391891.1559633028
Dec9204.52533202166594.0305810398
J1150.5656665027800.4892966361
Jan900.4426955239350.2140672783
F200.09837678312951.8042813456
Feb1150.56566650275853.5779816514
M3251.5986227255603.4250764526
Mar10505.16478111177594.6422018349
Total2033116348
A
C
Sheet3
Fig. 5.
Sheet3
A4.61773700310.6
Apr12.90519877681
M9.70642201832
May28.99082568813.4
J5.07645259947
June2.935779816517
J1.00917431196
July5.25993883795.2
A1.89602446483.8
August1.64525993881.3
S0.85626911310.9
Sept0.82568807341.5
O1.10091743121.3
Oct0.97859327220.4
N0.70336391440.6
Nov2.1406727829
D1.1559633028
Dec4.0305810398
J0.4892966361
Jan0.2140672783
F1.8042813456
Feb3.5779816514
M3.4250764526
Mar4.6422018349
2000-01
2001-02
1969
Months
Percent of total ascospores
4.2302016724
12.395474668
24.6679783571
20.2410231185
3.1480570585
4.8204623709
2.1888834235
4.9680275455
1.9675356616
1.6969995081
0.7624200689
0.4672897196
0.6148548942
1.436301033
1.2247909493
0.4918839154
1.7215937039
4.5253320216
0.5656665027
0.4426955239
0.0983767831
0.5656665027
1.598622725
5.1647811117
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Epiphytic Growth
oOccurs during the wet summer months
oAscospore dose does not determine level of epiphytic growth
oSimilar patterns on fruit and leaves
Mondal and Timmer, 2005
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Epiphytic Growth and Infection
oTissue penetrated only through stomata
oHigh density of penetration required for symptoms
oRequires high humidityoSymptoms caused by swelling
stimulated by hyphae
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Greasy Spot Disease Cycle Caused by Zasmidium citri-griseum
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Cultural Controls
oReduce leaf litter in winter and early springDiskingFrequent
irrigation to promote decompositionMulch leaf litterPut urea or
lime on the leaf litter
oProblem with this approachNot enough of the leaf litter is
decomposed
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FungicidesoPetroleum oil – gives adequate control on less
susceptible
cultivarsoCopper – more consistent control than oiloStrobilurins
– same concerns about
MOAAzoxystrobinTrifloxystrobinPyraclostrobin
oFenbuconazole – moderate risk for resistanceDMI fungicide or
sterol biosynthesis inhibitors
PresenterPresentation NotesOil can burn in temperatures above
94F
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Spray Timing
oLess susceptible cultivarsOne spray between May and June often
sufficient especially in
Northern production regionsoIn South Florida, more susceptible
cultivars and in groves
with severe defoliationTwo sprays; one mid-May – June, the
second once flush has
expandedA third and final spray may be needed for fresh
grapefruit in a
grove that was heavily infested the previous year
PresenterPresentation NotesWhy is the timing not as critical for
greasy spot?
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Spray Timing Effects
0
1
2
3
4
5
May Jun Jul Aug Sep Oct Nov Dec Jan
Epip
hytic
myc
elia
l gro
wth
Unsprayed controlMay sprayJuly sprayAugust sprayMay+June
spray
Chart4
MayMayMayMayMay
MayMayMayMayMay
JunJunJunJunJun
JunJunJunJunJun
JulJulJulJulJul
JulJulJulJulJul
AugAugAugAugAug
AugAugAugAugAug
SepSepSepSepSep
SepSepSepSepSep
OctOctOctOctOct
OctOctOctOctOct
NovNovNovNovNov
NovNovNovNovNov
DecDecDecDecDec
DecDecDecDecDec
JanJanJanJanJan
Unsprayed control
May spray
July spray
August spray
May+June spray
Epiphytic mycelial growth
0.38
0.46
0.67
0
0
0.62
0
0
0.6
0.23
0
1.45
0.19
0.68
0.1
2.35
0.33
0.73
1.3
0.37
2.35
0.6
0.73
1.15
0.2
2.38
0.66
0.63
1.02
0.2
2.13
0.63
0.61
0.96
0.16
2.35
0.86
0.8
1.18
0.23
2.55
0.73
0.6
1.31
0.21
2.5
0.61
0.6
1.36
0.28
2.51
0.75
1.23
1.85
0.38
2.88
0.85
0.76
2.11
0.26
2.63
0.95
0.76
1.96
0.2
2.88
0.85
0.83
2.1
0.2
Chart1
Sheet1!#REF!
Sheet1!#REF!
Sheet1!#REF!
Chart2
Chart3
MayMayMayMay
MayMayMayMay
JunJunJunJun
JunJunJunJun
JulJulJulJul
JulJulJulJul
AugAugAugAug
AugAugAugAug
SepSepSepSep
SepSepSepSep
OctOctOctOct
OctOctOctOct
NovNovNovNov
NovNovNovNov
DecDecDecDec
DecDecDecDec
JanJanJanJan
Unsprayed control
May spray
August spray
May+June spray
Months
Epiphytic mycelial growth (0-5 scale)
0.38
0.46
0.67
0
0
0.62
0
0
0.6
0.23
0
1.45
0.19
0.1
2.35
0.33
1.3
0.37
2.35
0.6
1.15
0.2
2.38
0.66
1.02
0.2
2.13
0.63
0.96
0.16
2.35
0.86
1.18
0.23
2.55
0.73
1.31
0.21
2.5
0.61
1.36
0.28
2.51
0.75
1.85
0.38
2.88
0.85
2.11
0.26
2.63
0.95
1.96
0.2
2.88
0.85
2.1
0.2
Sheet1
2000-2001
Unsprayed controlMay sprayJuly sprayAugust sprayMay+June
spray
May0.38
May0.46
Jun0.6700
Jun0.6200
Jul0.60.230
Jul1.450.190.680.1
Aug2.350.330.731.30.37
Aug2.350.60.731.150.2
Sep2.380.660.631.020.2
Sep2.130.630.610.960.16
Oct2.350.860.81.180.23
Oct2.550.730.61.310.21
Nov2.50.610.61.360.28
Nov2.510.751.231.850.38
Dec2.880.850.762.110.26
Dec2.630.950.761.960.2
Jan2.880.850.832.10.2
2001-2002
Unsprayed controlJune sprayJuly sprayAugust sprayJune+July
spray
May0.36
May0.6
Jun0.650.060
Jun0.90.30
Jul1.110.2310.13
Jul2.450.180.680.2
Aug2.430.230.860.16
Aug2.40.230.751.230.21
Sep2.810.510.511.260.23
Sep3.150.431.12.160.2
Oct2.980.50.82.130.26
Oct3.210.611.132.730.28
Nov2.810.330.882.060.15
Nov3.110.410.952.40.28
Dec3.050.630.952.080.35
2001-02
Summer2001-02
Unsrayed controlJuly spray
JulyUnsprayed controlJuly spraySE (UNS)SE Fung
July0.860July0.500.080
Aug1.550Aug1.5600.050
Aug10.15Aug1.700.10
Sept1.150.33Sep1.500.10
Sept0.930.08Sep1.760.20.150
Oct10.26Oct1.960.260.050.05
Oct1.460.16Oct1.860.30.150.1
Nov1.680.15Nov1.70.260.20.11
Nov1.310.3Nov1.830.460.110.11
Dec1.280.3Dec1.70.360.10.05
Dec1.80.560.20.05
Jan1.90.560.2080.05
&RFigure 2 of Plant DiseaseMondal and Timmer
Sheet1
Unsprayed control
May spray
July spray
August spray
May+June spray
Epiphytic mycelial growth
Sheet2
&RFigure 2 of Plant DiseaseMondal and Timmer
Unsprayed control
June spray
July spray
August spray
June+July spray
Epiphytic mycelial growth
Sheet3
JulyJuly
JulyJuly
AugAug
AugAug
SepSep
OctOct
OctOct
NovNov
NovNov
DecDec
A
B
Unsprayed control
July spray
Epiphytic mycelial growth
July
July
Aug
Aug
Aug
Aug
Sep
Sep
Sep
Sep
Oct
Oct
Oct
Oct
Nov
Nov
Nov
Nov
Dec
Dec
Dec
Dec
Jan
Jan
0.5
0
1.56
0
1.7
0
1.5
0
1.76
0.2
1.96
0.26
1.86
0.3
1.7
0.26
1.83
0.46
1.7
0.36
1.8
0.56
1.9
0.56
Unsprayed control
July spray
Months
Epiphytic mycelial growth
0
0.86
0
1.55
0.15
1
0.33
0.93
0.1
1
0.26
1.46
0.16
1.68
0.15
1.31
0.3
1.28
0.3
Figure 3 - Spray timing on spring flush
C
D
MayMayMayMayMay
MayMayMayMayMay
JunJunJunJunJun
JunJunJunJunJun
JulJulJulJulJul
JulJulJulJulJul
AugAugAugAugAug
AugAugAugAugAug
SepSepSepSepSep
SepSepSepSepSep
OctOctOctOctOct
OctOctOctOctOct
NovNovNovNovNov
NovNovNovNovNov
DecDecDecDecDec
DecDecDecDecDec
JanJanJanJanJan
Unsprayed control
May spray
July spray
August spray
May+June spray
Epiphytic mycelial growth
0.38
0.46
0.67
0
0
0.62
0
0
0.6
0.23
0
1.45
0.19
0.68
0.1
2.35
0.33
0.73
1.3
0.37
2.35
0.6
0.73
1.15
0.2
2.38
0.66
0.63
1.02
0.2
2.13
0.63
0.61
0.96
0.16
2.35
0.86
0.8
1.18
0.23
2.55
0.73
0.6
1.31
0.21
2.5
0.61
0.6
1.36
0.28
2.51
0.75
1.23
1.85
0.38
2.88
0.85
0.76
2.11
0.26
2.63
0.95
0.76
1.96
0.2
2.88
0.85
0.83
2.1
0.2
MayMayMayMayMay
MayMayMayMayMay
JunJunJunJunJun
JunJunJunJunJun
JulJulJulJulJul
JulJulJulJulJul
AugAugAugAugAug
AugAugAugAugAug
SepSepSepSepSep
SepSepSepSepSep
OctOctOctOctOct
OctOctOctOctOct
NovNovNovNovNov
NovNovNovNovNov
DecDecDecDecDec
Unsprayed control
June spray
July spray
August spray
June+July spray
Epiphytic mycelial growth
0.36
0.6
0.65
0.06
0
0.9
0.3
0
1.11
0.23
1
0.13
2.45
0.18
0.68
0.2
2.43
0.23
0.86
0.16
2.4
0.23
0.75
1.23
0.21
2.81
0.51
0.51
1.26
0.23
3.15
0.43
1.1
2.16
0.2
2.98
0.5
0.8
2.13
0.26
3.21
0.61
1.13
2.73
0.28
2.81
0.33
0.88
2.06
0.15
3.11
0.41
0.95
2.4
0.28
3.05
0.63
0.95
2.08
0.35
A
B
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Melanose
oCausal agent: Diaporthe citriSynonym: Phomopsis citri
(Anomorphic stage)
oDisease is present in most citrus producing countriesoImportant
only where fresh fruit is produced in humid areasoCauses lesions on
fruit and leavesoAll citrus susceptible but grapefruit and lemons
are the most
susceptible
-
Diaporthe citri
oAscospores formed in perithecia Spherical with flattened base
(125-160 µm) Long tapered beaks (200-800 µm)
oAscospores are hyaline 2 cells each with 2 oil droplets
(guttulae) 3.2-4.5 x 11.5-14.2 µm
-
Asexual Stage
oPycnidia are dark, ovoid and erumpent with thick walls Found
scattered on dead twigs 200-450 µm Spores are extruded in a tendril
(cirrhus)
-
Asexual Stage cont.
oTwo forms of hyaline conidiao α-conidia are unicellular 2 oil
droplets (biguttulate)2.5-4 x 5-9 µm
o β-conidia Filiform and hookedDon’t germinate and are
predominant form in older pycnidiaLikely a spermatial spore for
mating0.7-1.5 x 20-30 µm
-
Tissue Susceptibility
oSpring flush usually not severely infectedoOn summer flush,
infection can lead to defoliation especially
after diebackoLeaves become resistant once fully expandedoFruit
resistant 12 weeks after petal fall and when infection
occurs later during the 12 weeks, lesions are smallerGrapefruit
are susceptible until 7-10 cm in diameter
PresenterPresentation NotesEast coast can have problems with
spring flush with early rains
-
Symptoms
-
Melanose Disease Cycle Caused by Diaporthe citri
PresenterPresentation NotesMain spore form is the alpha conidia
which is splash dispersed onto susceptible tissueSpores are not
produced on fruit or leaves so the disease is essentially
monocyclicAscospores are airborne (forcibly ejected?) and can serve
as propagules over long distancesPerithecia produced on older,
larger dead limbsMain reproductive cycle is from twig to twig
-
Pycnidia Production
Mondal et al., 2004
-
Pycnidia Production
oWetting period, twig diameter, temperature and disease severity
on the twig all had significant effects on pycnidia formation
oFormation takes between 3-5 months in field and can occur on
dead twigs
Mondal et al., 2004
-
Conidia Production
oMost of the inoculum is produced on twigs that die between
January and April
oConidia produced at low %RH are viable for several weeks to
months
Mondal et al., 2007
-
Infection
oConidia germinate6 hrs at 16°C4 hrs 20 to 28°C
oLiterature has varying times and temperatures needed for
infection
oOptimum temp determined to be 24-28°C
Agostini et al., 2003
-
Melanose Disease Cycle Caused by Diaporthe citri
-
Cultural Controls
oSelect younger groves for fresh fruitLess dead wood for
inoculum production
oRemove dead wood from canopy
oClear out brush piles
-
Fungicides
oCopper –Most economical but can cause blemishes in hot dry
weather
oStrobilurins – Low residual activity compared to copper but
useful in hot weatherAzoxystrobinTrifloxystrobinPyraclostrobin
PresenterPresentation NotesBlemishes are spotting as well as the
darkening of existing blemishes
Strobilurins shouldn’t be used or more than twice a year
-
Spray Timing
oOranges and TangerinesFirst spray mid to late AprilOne to two
applications sufficient
oGrapefruit (fresh market)First application when fruit ¼ to ½
inchCopper to be applied every 3 weeks until fruit resistant in
late June
to early JulyThere is a model to determine whether copper
residues are
sufficient to control disease based on weathering of copper and
the growth rate of fruit
PresenterPresentation NotesUnless orange trees have large
quantities of dead wood
-
Citrus Scab
oCausal agent: Elsinoë fawcettiiSynonym: Sphaceloma
fawcettii
oFound in most humid citrus production regionsoImportant for
fresh fruit productionoSweet orange scab: E. australis (syn. S.
australis)Found in southern South America and South KoreaNewly
discovered in Texas and Louisiana
-
Elsinoë fawcettii and E. australis
oOnly been found in BraziloDistinguished by ascospore sizeE.
fawcettii 5-6 x 10-12 µmE. australis 12-20 x 15-30 µm
oFunction in the disease cycle is unknown but clearly not
essential
-
Asexual Stage
oConidia are hyaline, single celled and
ellipticalIndistinguishable between speciesCan reproduce by
budding
oAlso fusiform conidia (E. fawcettii)PigmentedGerminate to form
hyaline conidia
oConidia borne in acervuli
-
Host Range and Tissue Susceptibility
oYoung leaves and fruit are susceptibleLeaves immune to
infection in a few days Fruit remain susceptible up to two
months
oSummer flush can be especially badly affected
oThe host range of E. fawcettii is complicated oMatter of
considerable ongoing phylogenic research
PresenterPresentation NotesLeaves half expandedNot practical to
treat summer flush with fungicide but contributes greatly to over
wintering inoculum
-
Host RangeDisease Pathogen Pathotype Hosts
Citrus scab Elsinoëfawcettii
FBHR Lemon, grapefruit, Temples, sour orange, sweet orange,
Satsuma, many tangerines
FNHR Lemon, grapefruit, Satsuma
Tyron’s Lemon, CleopatraLemon LemonSRCG Satsuma, Rough
lemon,
Clementine, grapefruitSweet orange scab E. australis Sweet
orange Sweet oranges, tangerines
Natsudaidai Natsudaidai
FBHR – FL broad host range; FNHR – FL narrow host range; SRCG –
satsuma, rough lemon, clementine, grapefruit
PresenterPresentation NotesThis is being reoganized based on new
phylogenetic research
-
Symptoms
-
Citrus Scab/Sweet Orange Scab Disease Cycles Caused by Elsinoë
fawcetti and E.australis
F
PresenterPresentation NotesSpindle-shaped conidia rare and are
mainly involved in airborne transportThey are formed on the lesion
following periods of dewNo infection on leaves by E. australis. No
one knows how E. australis overwintersHyaline conidia are fragile
and die quickly when exposed to dry conditions or direct
sunlightThe fungus survives without susceptible tissue in pustules
on leaves, fruit and stemsAscospores appear not to play a role in
the life cycle
-
InfectionoContradictory information in the
literature about leaf wetness and temperature
oOptimal temperature range 23.5 to 27 °C
oOptimal leaf wetnessBetween 12 and 24 hrs
Agostini et al., 2003
PresenterPresentation NotesSour orange greatest amount of fungal
growth at 21CBest sporulation between 21 and 27CNo infection above
23C Fawcett
Rough lemon 24-28C with min wetting period of 2.5-3 hours; max
lesions at 7 hours - WhitesideIs there a cultivar difference? Don’t
know
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Conidia Production
oConidia can be produced in 1-2 hours with sufficient
wetness
oOptimum temperature 24-28°CoSpores are splash dispersedoThe
greater the number of spores, the greater the number of
lesionsoTend to see more disease with low lying areas where
there
more dew and longer dew periods
-
Citrus Scab/Sweet Orange Scab Disease Cycles Caused by Elsinoë
fawcetti and E.australis
F
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Cultural Controls
oDisease-free nursery treesStart clean and problems are
unlikely
oHedge and top badly-affected plantingsDoes not move far even
within trees
oNo vigorous rootstocksoNo overhead irrigation
-
Fungicides
oCopperoFerbamoStrobulurins – Most effective but specific
MOAAzoxystrobinTrifloxystrobinPyraclostrobin
oFenbuconazole
PresenterPresentation NotesNo more than 4 sprays of any
combination of Strobilurin in the year
-
Spray Timing
oSprays are mainly for groves with a recent history of
ScaboFirst spray – spring flush 2-3 inches can be omitted if
severity was light
oPetal falloThree week after petal fall
PresenterPresentation NotesLast spray can also control
melanoseDon’t used two strobilurins in a row
-
Black Spot
oCausal agent: Phyllosticta citricarpa Synonyms: Guignardia
citricarpa; Phoma citricarpa
oHosts : Citrus species and hybrids oSweet oranges, mandarins
and tangerines, lemons,
grapefruito‘Tahiti’ lime - non-symptomatic infection
-
Black Spot cont.oRind spots cause the most economic damage
Internal quality unaffected
oReduces fruit value for the fresh market
oRestricts export of fresh fruitsMostly to European countries
and formerly the U.S
oCauses premature fruit drop reducing yieldParticularly with
late harvest cultivars
-
World Distribution as of 2019oOccurs mostly in summer rainfall
areas or areas with prolonged dew
or fog in warm weather
https://gd.eppo.int/
-
oFive Counties with DiseaseCollierHendryPolkLeeCharlotte
oNewest finds in Lee and Charlotte
Current Quarantine Areas
-
Phyllosticta citricarpa (sexual stage)
oNever found in fruit – in leaf litteroForm aggregated ascomata
- peritheciod
pseudothecium100-175 µm diameter
oAscopores are aseptate, hyaline, multiguttulate and
cylindricalwith swollen middles4.5-6.5 x 12.5-16 µm
Tran et al., 2017
-
Asexual Stage
oForms pycnidiaDark brown or blackForm on fruit, leaves, twigs
and fruit pedicles115-190 µm
oConidia are obovate, hyaline, aseptate, and multiguttalate5.5-7
x 8-10.5 µm
oSpermatia are dumbbell shaped5 -8 x 0.5-1
Glienke et al. 2011
Baayen et al. 2002
-
Tissue Susceptibility
oHosts include Citrus species and hybrids oSymptomatic hosts:
Sweet oranges, mandarins and
tangerines, lemons, grapefruitoNon-symptomatic host: ‘Tahiti’
limeProduces ascospores from leaves
oFruit are susceptible for 5-6 months post-petal fallLeaf
susceptibility period still uncertain
-
Symptoms
PresenterPresentation NotesHard spot, false melanose, early
virulent spot, late false melanoseLeaf and stem symptoms quite rare
– occur mainly on lemons
-
Black Spot Disease Cycle Caused by Phyllosticta citricarpa
-
Inoculum Basics
oMajor source of inoculum: decomposing infected leaves on
orchard floor (ascospores)
oAdditional source of inoculum: lesions on infected fruits,
leaves and branches (conidia)
oMeans of spread: Wind (ascospores); Water splash (ascospores
and conidia)
-
Infection Conditions
oOptimal conditions for infection: Temp 21 – 32 °CWetting period
24 - 48h
oSymptom expression: 1 – 12 monthsVery long latent period
oSurvival of the fungus: leaves, twigs, fruits, peduncles, and
leaf litter
-
What is Needed for AscosporesoRequirement for two opposite
mating types to be present to
get ascosporesoOnly one mating type found in FloridaMAT1-2
Wang et al. 2016
-
The Lonely PeninsulaoWanted to know the proportion of mating
types in Florida
compared to Queensland, AuState, Country Location
Total number
Number of isolates
Alpha HMG Hetero-karyon
Florida, US
Collier 50 0 50 0Hendry 62 0 62 0Polk 1 0 1 0Total 113 0 113
0
Queens-land Australia
Beerwah 2 0 2 0Emerald 1 1 0 0Gayndah 4 1 3 0Mundubbera 16 8 5
3Tiaro 3 2 1 0Total 26 12 11 3
Wang et al. 2016
-
Still Only One Mating Type
oGlobal population study found 2 mating types in all locations
except Florida
oGreatest genetic diversity from Australia and ChinaoSouth
Africa and Brazil had low genetic diversityLikely founder
effect
oFlorida population was clonal even with expanded marker set
oCarstens et al. 2017
-
Role of P. citricarpa Spermatia
oSpermatia are commonly found in culture and leaf litter
samplesRole in life cycle hypothesized to be male gametes
oFirst ascospores produced in cultureDemonstrated meiosis via
multilocus genotyping of ascosporesNeeded direct contact of
isolates carrying opposite idomorphs or
spermatia suspensionoTran et al. 2017
-
Black Spot Disease Cycle Caused by Phyllosticta citricarpa
-
Cultural Controls
oIncrease air flow in trees to reduce leaf wetness where
possible
oAvoid cultivars with significant off-season bloomOlder fruit
can supply inoculum to infect new fruit
oReduce leaf litter to reduce inoculumoMinimize trash when
picking to avoid inadvertent
movement of the fungus from one location to anotheroClean
equipment between groves with disinfestantsQuaternary ammonium
(2000 ppm) or bleach (200 ppm)
-
FungicidesoCopper - all formulations; use maximum label
rateoStrobilurinsazoxystrobinpyraclostrobintrifloxystrobin
ofenbuconazoleoPremixed Fungicidespyraclostrobin and
boscalidazoxystrobin and difenoconazole
-
Black Spot Application Timing
Late Spring (April/May)
Copper
Continue applications at 1 month intervals
o Fruit is susceptible for 5-6 months post-petal fallCopper
and/or strobilurins
CopperCopper and/or strobilurins
Copper
Use strobilurins when concerned about copper phytotoxicity
-
Postbloom Fruit Drop
oCausal agent: Colletotrichum acutatumSynonym: Glomerella
acutataFormerly thought to be Colletotrichum
gloeosporioidesApproximately 5% of blossoms can be infected by C.
gloeosporiodies in
Brazil
oWidespread throughout humid subtropics and tropics of the
Americas
oProblematic in years with high rainfall around bloomoFirst
reported in Belize in 1979
PresenterPresentation NotesC. acutatum based on ITS sequence
(nuclear ribosomal internal transcribed spacer)However, only group
C isolates have been shown to produce the teleomorph - ie blueberry
and a few other isolates. The only report in nature is one
from Norway. The others are artificial crosses. Mondal
tried really hard with citrus isolates, but they won’t form it even
with blueberry isolates. Steve found some evidence of
hybridization with fern isolates in the paper we are finishing
up
-
Colletotrichum acutatumoConidia are fusiform rather than
roundPigmented to give spore mass a salmon
colorSlower growing than C. gloeosporioides
oBorne in an acervulus Few setae on host tissue or in
cultureoAppressoria are the survival structures
-
Host Range
oAffects most citrus cultivarsoMost severe on sweet oranges,
lemons, and limesoLess severe on grapefruit and tangerinesoIs a
limiting factor for citrus production in high rainfall
areas of Belize, Mexico, Costa Rica, and the Caribbean
islands
-
Susceptible TissueoOpen flowers are the most
susceptibleoUnopened or pin-head bloom much less severe
infectionoDoes not appear to affect the foliage except that around
the
calyxes which is distorted with large veinsoFruitlets abscise at
base of ovary to form persistent calyxes
or ‘buttons’ Pinhead Popcorn Open
-
Symptoms
-
Post Bloom Fruit Drop Disease Cycle Caused by Colletotrichum
acutatum
PresenterPresentation NotesConidia are from quiescent
appressorial infections in leaves.Appressoria are stimulated to
‘germinate’ by petal exudates, produce short hyphae and conidia
(not acervulus)Conidia cause primary infection on early
flowersAmplification of inoculum on successive waves of bloomSpread
by wind-blown rainPersistent calyces form
-
oFlowering solid lineOpen and nearly open flowers
up to 100oFlower disease incidence
dashed lineOn newly open flowers at time
of assessment
Timmer and Zitko, 1993
PresenterPresentation NotesSolid line = flowering; broken line =
% flowers affected; bars rain
-
Disease ProgressoInoculum levels most importantoRainfall and
leaf wetness are important oNeed infection of early bloom to get
inoculum build upAmplifies inoculum levels for subsequent waves of
bloom
oOptimum temperature for conidia germination is 23°C but over
50% of conidia can germinate between 10-30°C
-
Post Bloom Fruit Drop Disease Cycle Caused by Colletotrichum
acutatum
-
Cultural Controls
oNo overhead irrigationIf necessary only at nightGet an expected
wetness period overnight so not changing disease
outcome considerablyoIf there are trees in decline from other
diseases such as
tristeza, blight, or HLB that promote off season bloom, remove
them from your PFD prone block
-
FungicidesoFerbamoStrobulurins – Most effective but specific
MOAAzoxystrobinTrifloxystrobinPyraclostrobin
oPremixed fungicidesAzoxystrobin and
difenoconazolePyraclostrobin and boscalidPyraclostrobin and
fluxapyroxad
-
Application TimingoTiming specific to grove
situationoHighly weather dependentoDisease will not wait for
the
next time sprayer availableohttp://pfd.ifas. ufl.edu/
-
Needed Information
oShould be scouting bloom several times a week during
bloomIncluding off-season bloomBloom intensityBloom
stagePin-headPopcorn bloomOpen flowers
-
Needed Information cont.oDisease history for last 5
yearsPersistent calyxes Declining trees?Was there PFD on early
bloom?Is there PFD now and is it scattered?
oRainfall 5 previous daysIn millimeters; from inches multiply by
25.4Approximate leaf wetnessHow many separate rain events
oWhen was the last fungicide application?
-
New PFD Infection Forecasting Program
oHosted on Agroclimate.orgUnder tools/crop diseasesSimilar to
Strawberry
Advisory System (SAS)Each circle represents a
FAWN weather station
-
Criteria to select
oPalmdale station selectedMap zooms in automatically
oNeed to indicate bloom intensityWill I recoup costs if
application made?oFlowering stageoLast fungicide application
Sufficient bloom
None
Many open flowers, some pinhead or button bloom remaining
-
If there is an infection event
oConditions could allow for infection event
oStill need sufficient bloom
oFungicide applications minimum 7 days apart
oRecommendations change based on risk level
Link to current FPG
Fungicide recommendations
-
Disease simulation taboGraphical representation
of infection riskCan select time frame
oForecasted risk (from NOAA weather data) for three days from
actual dateHelp plan if infection will
be favored by weather in near term
-
Infection risk levelsoHigh risk (red area)Index above 0.51;
Spray as
soon as possibleoModerate risk (yellow area)Index between 0.21
-0.5;
Spray recommendedoLow risk (green area)Index between 0-0.2;
No
spray recommended
-
Daily summary of dataoGives leaf wetness,
temperature, PFD index and risk levelWeather variables
daily averagePFD index max.
daily value
-
Weather dataoCan look at the
weather data for every 15 min.Temperature, relative
humidity, rainfall, leaf wetness
oFind out when drying periods occurAfter 4 hours of
drying, PFD index resets to zero
-
Pseudocercospora Fruit and Leaf Spot
oPseudocercospora angolensisoSyn.: Phaeoramularia angolensisNo
know teleomorph
oSerious disease of fruit and foliage in much of Sub-Saharan
Africa except South Africa
oFirst described in Angola and Mozambique in 1952oQuarantine
disease
-
Host Range
oAll citrus speciesoMost susceptibleGrapefruit, oranges, pummelo
and mandarin
oLess susceptibleLemon
oLeast susceptibleLime
oYield losses between 50-100% not uncommon
-
Pseudocercospora angolensis
oForms dense tufts (synnemata) of light chestnut multi-septate
conidiophores
oEmerge from the stromata through stomata on lower leaf
surfaces
oConidia are single or catenulate (2-4)Hyaline, cylindrical and
slightly flexuousOne to six septate (mostly 3-4)3-7 x 240 µm
-
Pseudocercospora angolensis
-
Susceptible Tissue
oYoung leaves are highly susceptible to infection from lesions
older tissues
oYoung fruit up to golf ball size are highly susceptibleoNot
certain whether the fruit have a reduced susceptibility
or become immune
-
Symptoms
-
Disease Spread
oSo far restricted to humid tropics of Africa between 80-1500
m
oFavoured by prolonged wet weather followed by dry periods with
temps between 22-26°C
oLong distance spread by windborne conidiaInfected planting
material may also contribute to long distance
spreadoWithin orchard spread by splash dispersed conidia
-
Environmental Conditions
Pretorius, 2005
-
Controlso Inoculum control via collecting and destroying all
fallen fruit and
leaves in affected orchardsBurying or burning
o Plant windbreaks around the citrus orchards Wind is the
primary dispersal agent spores
oDiscouraging inter-planting in affected orchards with mature
producing treesPrevents creation of a microclimate of relatively
cool temperatures and high
RHPotential inoculum source for young trees
o Judicious pruning of shoots to allow light penetration into
aeration within the tree canopy shorten leaf wetness period, lower
RH and moderate temperatures
Seif and Hillocks, 1993
-
FungicidesoAlternate benylate and copper sprays every 2 weeks
from a
week following the onset of rainsoWhen fruit are golf ball sized
an addition 3 copper sprays
should be applied followed by another benylate
Seif and Hillocks, 1993 and 1997
Fungal Diseases of Citrus Fruit and FoliageFoliar Fungal
Diseases to be CoveredWhat Is a Fungus?Oomycetes and Fungi are Not
Closely RelatedDifferences Between Oomycota & EumycotaNote on
TerminologyAlternaria Brown SpotAlternaria Brown Spot cont.Slide
Number 9Alternaria alternataTissue SusceptibilitySymptomsAlternaria
Brown Spot Disease Cycle Caused by Alternaria alternataWhen are the
Conidia Released?Infection ConditionsAlternaria Brown Spot Disease
Cycle Caused by Alternaria alternataCultural
ControlsFungicidesALTER-RATER: A Forecasting SystemThe
ALTER-RATER�Suggested Threshold ScoresALTER- RATER Daily
PointsGreasy SpotGreasy Spot cont.Zasmidium citri-griseumAsexual
formMyceliumTissue SusceptibilitySymptomsGreasy Spot Disease Cycle
Caused by Zasmidium citri-griseumPseudothecia
Maturation�MoisturePseudothecia Maturation�TemperatureOptimal
Temperatures for Ascospore ProductionPeak Ascospore
EjectionEpiphytic GrowthEpiphytic Growth and InfectionGreasy Spot
Disease Cycle Caused by Zasmidium citri-griseumCultural
ControlsFungicidesSpray TimingSpray Timing EffectsMelanoseDiaporthe
citriAsexual StageAsexual Stage cont.Tissue
SusceptibilitySymptomsMelanose Disease Cycle Caused by Diaporthe
citriPycnidia ProductionPycnidia ProductionConidia
ProductionInfectionMelanose Disease Cycle Caused by Diaporthe
citriCultural ControlsFungicidesSpray TimingCitrus ScabElsinoë
fawcettii and E. australisAsexual StageHost Range and Tissue
SusceptibilityHost RangeSymptoms Citrus Scab/Sweet Orange Scab
Disease Cycles Caused by Elsinoë fawcetti and E.
australisInfectionConidia ProductionCitrus Scab/Sweet Orange Scab
Disease Cycles Caused by Elsinoë fawcetti and E. australisCultural
ControlsFungicidesSpray TimingBlack SpotBlack Spot cont.World
Distribution as of 2019Current Quarantine AreasPhyllosticta
citricarpa (sexual stage)Asexual StageTissue
SusceptibilitySymptomsBlack Spot Disease Cycle Caused by
Phyllosticta citricarpaInoculum BasicsInfection ConditionsWhat is
Needed for AscosporesThe Lonely PeninsulaStill Only One Mating
TypeRole of P. citricarpa SpermatiaBlack Spot Disease Cycle Caused
by Phyllosticta citricarpaCultural ControlsFungicidesBlack Spot
Application TimingPostbloom Fruit DropColletotrichum acutatumHost
RangeSusceptible TissueSymptomsPost Bloom Fruit Drop Disease Cycle
Caused by Colletotrichum acutatumSlide Number 94Disease
ProgressPost Bloom Fruit Drop Disease Cycle Caused by
Colletotrichum acutatumCultural ControlsFungicidesApplication
TimingNeeded InformationNeeded Information cont.New PFD Infection
Forecasting ProgramCriteria to selectIf there is an infection
eventDisease simulation tabInfection risk levelsDaily summary of
dataWeather dataPseudocercospora Fruit and Leaf SpotHost
RangePseudocercospora angolensisPseudocercospora
angolensisSusceptible TissueSymptomsDisease SpreadEnvironmental
ConditionsControlsFungicides
