Phytophthora Studies on Citrus Rootstocks J. O.Whiteside Introduction The common and widespread

-15-
PhytophthoraStudieson Citrus Rootstocks
J. O.Whiteside
Introduction
The commonand widespreadoccurrenceof phytophthora fungi that arepathogenk:to citrus continuesto havea great
influenceon the world rootstock situation. While much can be doneto preventseriousinfection by adoptingsafercultural
practicesand by usingsuitablepreventativemeasures,
the only certain solution to a severephytophthora diseaseproblem is to
usemore resistantrootstocks. Unfortunately, few citrus speciesor relativesarehighly resistantto phytophthora, and much of
this materialis unsatisfactoryfrom other standpoints. Thus, in practice,manysu8:eptiblerootstocksstill haveto be planted
becauseof their superiority in other more essentialrespects.
The severityof phytophthoraattack variesaccordingto local climatic and edaphicconditions. In citrus producingareasof
the world that havewell-drainedandwell-aeratedsoils,and whererainfall is not too frequent, it may still be reasonablysafeto
useas rootstocksany but the very highly susceptiblevarieties. Whereconditions are morefavorablefor diseasedevelopment,as
on soilsthat remainwet for long periodsfollowing rain or irrigation, it may be unwiseto useeventhose rootstocksthat are only
moderatelysusceptibleto phytophthora. Suchconsiderationsaffect the latitude tha1can be permitted in different citrus producingareaswith respectto the screeningout of phytophthorasusceptiblematerialin rootstock improvementprograms.
In Florida, serious lossesgenerallyoccur only wherehighly susceptiblevarietieshavebeenused8Srootstocks. Havingmade
this statement,I must hastento add that much of the more seriousdamagecausedby phytophthora in local nurseriesand grovesinvolvesprimarily the scionportion of the trunk and not the rootstock. This is not alwaysfully appreciatedand in many
casesthe rootstock variety is wrongly blamedfor the attack. The questionasto how much importanceshould be attachedin
Florida to the sel~tion of rootstocksthat are highly resistantto phytophthora will be consideredlater in this talk; becauseit
will be possibleto ex~minethis subiectobjectivelyonly after consideringin somedetai what is known about the host-parasite
relationshipand the possibleeffectsof phytophthora on tree performance.
Parts of tree affected by phytophthora
Certainpartsof citrustreesare more susceptibleto phytephthora attack than others,and the namesgivento the different
expressionsof the diseasesyndromevary accordingly. Particularlyproneto attack on suchhighly susceptiblespeciesas&Weet
orangeare the feederroots andthe bark of the crown roots and lower part of the trunk. Olderparts of the root systembetween
the fibrous roots and the regionwherethe rootsstart to form the crown portion of the trunk areaffectedlessfrequently. If
theseolder roots do becomeinfected,the lesionstend to be smallandself-limiting, givingriseto a symptom that hasbeendescribed asfrog-eye(7). Bark on the lf1Nerpart of the trunk is potentially more susceptibleto infection than bark below ground(9).
This is one of the reasonswhy treesshould be planted no deeperthan they stood in the nursery,the aim beingto reduceasmuch
aspossiblethe amount of highly susceptiblestembark in contactwith the soil.
In somevery wet areasof the world, infection of bari<can occur quite high on the trunk and evenon the limbs. Under Florida
conditions,hcmever,the bark of eventhe highly susceptiblescionvarietiesseldombecomesinfected,providedthat it is separated
from the soil by at least3 inchesof resistantrootstock bark.
On the moreresistantrootstock varieties,rotting of the bark on the crown roots and the trunk is uncommon. Someinfection
may, however,still occur on the feederroots of suchvarieties,thereby permitting the fungusto build up and threatenthe bark
of a susceptiblescionvariety if it is closeenoughto the ground. Thus,evenon so-calledresistantrootstocks,it is very important
to bud treesashigh aspractical.
The variousnamesgivento the different types of damagecausedby phytophthora areasfollows: W11en
infection is confined
to the feederroots, the resultinginjury is called"feeder or fibrous root rot", If the damageto the root systemis more extensive
andyet doesnot extend upwardsto the crown roots, it is describedas"phytophthora root rot", Damageto the bark of crown
-16-
rootsand/or baseof the trunk is called"phytophthora gummosis,collar rot or foot rot" and it is the last mentionedname
that is generallyusedin Florida.
The term "foot rot" originatedin Florida in the last century and wasintendedto describea bark rotted condition on the
trunk baseor crown roots. Unfortunately,this term hasat times beenusedinterchangeablywith root rot. Suchbroad use
of the term foot rot tendsto obscurethe real natureof the phytophthora problemasit facesus in Florida. Hereafterin this
talk, "foot rot" will be usedto describea diseasedbark condition on the crown roots or lower part of the trunk, asdistinct
from feederr!)ot rot. It will alsobe usedto describethe situationwherethe diseaseactually startedon, or remainedconfined
to, the scionportion of the trunk.
Life cycle of phytophthora and mode of infection
Two speciesof phytophthora pathogenic to citrus have been recorded in Florida; they are Phytoph thora parasitica and P.
CI"trophthora. The latter is rarely encountered in this State (12), but is a serious problem in certain other citrus producing
areasof the worl d. In Florida, P. parasitica has been detected in th e soil of almost every grove and nursery tested. It has not,
however, been detected in soil samples collected from any sites where citrus has never been planted, suggestingpossibly that
this fungus can only survive and multiply in the presenceof a citrus substrate. Growth in the soil itself is very restricted, but
the fungus can survive for limited periods in the soil May from the host substrate in the form of drought-resisting resting
spores (11). Very little inoculum arises from the diseasedbark and direct spread of infection from the bark of diseasedtrees
to that of healthy trees is probably unlikely.
Invasion of host tissueis by motile, free-9Nimmingsporesknown aszoospores.Theseare producedin fruiting bodiescalled
sporangia that grow out in profusion from the surface of infected feeder roots and from germinating resting spores. Water, and
not just high humidity, is the key factor in almost all stagesof the I ife cycle. Water is required for sporangial formation,dispersal of zoospores as well as for spore germination.
Zoospores ~im through the soil water and, if they get closeenoughto young roots, they becomeattracted by a chemotactic
responseto the regionof cell elongationimmediatelybehindthe root tip (14). On older roots and stems,penetrationapparently occursonly wherethere is a breakin the bark (1,13). Oirect penetrationof stemsis, however,possibleon young shootsbe.
fore a protectivebarrier of corky tissuestartsto form in the outer layer of the stemcortex (13). A strong attraction of zoospores
to freshly madebreaksin the bark of older roots (1) and stemshasbeenobserved(13).
11haslong beenrecognizedthat foot rot often commencesat locationswherethe bark hasbeendamagedas,for example,
during cultivation or after removingunwantedshoot growth. But suchopeningsin the bark are not the only onesthat allow
fungal entl'Y. Penetrationcan alsooccur through growth cracks(13). Suchnaturally formed crackshavebeendetectedby using
the triphenyl tetrazoliumchloride (TTC) technique(13). This colorle~ chemicalturns redwhen it comesinto contact with liv.
ing cells. Because
aqueoussolutionsare unableto penetrateintact bark, the appearance
of a red stain in the underlyingliving
cellsafter applyingTTC to the surface of the trunk providesevidencefor the existenceof somekind of breakin the outer corky
layer of the bark.
In inoculation testswith zoosporesuspensions
carriedout at the lake Alfred Researchand EducationCenter(AREC), relatiwly
few uninjuredsweetorangetreesdevelopedfoot rot, whereasthe diseaseincidenceincreasedto almost 10(rl/oon trunks that had
beenintentionally injured before inoculation (13). Theseresultshaveservedto strengthenthe contention tf1atavoidanceof mechanicalinjury cal} greatly reducethe incidenceof foot rot.
7ne association befi.\.eenfoot rot and low budding
The bark of most commercial-scion varieties is highly susceptible to Phytophthora infection. Thus, even if trees are gr(Ming
on resistant rootstocks, there is still a chance that foot rot can occur if the tree has been budded too low and/or planted too deeply. One of thq problems we have experienced in Florida in carrying out meaningful surveys to determine the involvement of the
rootstock in foot rot outbreaks, is that becauseof low budding it is frequently impossible to determine whether the infection
started above or below the bud union. The true situation can be further obscured by the fact that, by the time the diseasebecomes
evident, the roots may have already died from starvation due to the lack of food translocation from the tree canopy into the roots.
.17-
Young treescan succumbto stemgirdling in a matter of only a few months,and after the root systemhasdied, it is virtually
impo~ible to be certain of the causeof death. Neverttleless
there is a commontendencyto blamesuch "root rot" on phytophthora invasionof the rootstock.
Another factor that may influencethe true phytophthorapicture in Floridaisthat somerootstocks,
because
of certain
practicalproblemsin the nursery,tend to be buddedlower than others. Generally,roughlemon seedlingsare buddedlower
than sour orange,and this may account,at I~st partly, for the observationthat treeson roughlemon developfoot rot more
frequently than treeson sour orange. But other explanationsfor the reputedlyhigh susceptibiity of rough lemon to foot rot
arealsolikely, aswill be discussed
later.
TM relati~ importance of foot rot and feeder root injury in Florida citriculture
The economiceffects of foot rot in citriculture aremuch moreapparentthan thosedueto partial destructionor temporary
lossof feederroots following phytophthora attack. Evenafter allowingfor the fact that a greatdealof foot rot could beavoided by usingsafercultural practices.we know that it is still unwiseto plant treeson highly susceptiblestocks. High1ysusceptible
varieties.
therefore.needto beexcludedfromanyrootstockimprovement
program.
In contrast to foot rot, the economicsignificanceof feederroot infection in Florida is uncertain. Feederroot infection is,
of course,important from the standpointthat it buildsup inoculumto infect the trunk of the tree. Considerabledoubt remains,
however,asto whether the temporarylossof feederroots that can occur duringspellsof wet weatherreally hasany long-term
effect on tree growth. It could beconjecturedthat a partial lossof root absorbingsurfaceat timeswhen the soil is excessively
wet would be much lessseriousthan sucha loss(ascould becausedby other agents)when so~moisturelevelsare low. The ultimate effect on tree performancewould probably dependon the ability of a rootstock to producenew roots rapidly asthe so~
driesout andthe conditions becomelessfavorablefor the phytophthora pathogen.
Reliable and meaningful data on the importanceof feeder root rot wouklbe very difficult to obtain. Growth comparisons
between potted trees growing in phytophthora-infested and noninfested soil would hardly be trandatable to field or even nursery conditions. Nor would the results of soil fumigation tests necessarily provide the required information becausesuch treat.
mentscan affect tree performancethroulll their other effects on the soil microbiology.
Foot rot is often observedon treesthat had beengrowingexceptionallyvigorouslyup to the time that extensivetrunk girdling causedthe treesto go into a decline. Apparentty,the destructionof feederroots that must havebeenoccurringin such
groves for some time prior to the foot rot attack had little, if any, effect on tree growth. Perhapsthe situation could be different
on sites with high water tables, but here the urgency would be for better land drainage rather than to try and solve the problem
only by using stocks that are highly resistant to phytophthora. In the long term, feeder root infection in itself may not significantty affect tree performance, except in excessively wet groves and in nurseries that are irrigated too frequently.
Procedures for testing the relati~ susceptibility of rootstocks to phytophthora
Methodsusedto determinethe relativesusceptibility of rootstocksto phytophthora needto providethe folllMing information:
1) the relative rate of feederroot destructionunderconditionsfavorablefor phytophthoraattack; 2) the rateat which a root
systemis ableto regeneratenew roots following a reduction in diseasepressure;3) the susceptibilityof the crown roots and trunk
to the foot rot phaseof the diseasesyndromeand; 4) the ability of the rootstockto producecallustissuearound the diseasedbark,
therebypreventingextensivegirdling or renewedfoot rot activity at a later time.
Programs for testingthe relativesusceptibiity of rootstocksto phytophthora attack havebeenin operationin severalcitrusproducingareasof the world for manyyears(2,3,4,6,8,10). Two basicinoculation procedureshavebeenused;oneto test the
susceptibilityof the roots andthe other to test the susceptibilityof the stem bark to infection.
For testingthe relativesusceptibilityof the roots to phytophthora attack, young seedlingsor rooted cuttings are first grown
in a sterilemediumuntil a largenumberof healthy feederroots havebeenproduced. The plantsarelifted carefully to preserve
asmuch of the root systemaspossible,and the entire root systemis then placedin a tank containingaeratedwater, to which
zoospore-producing
inoculum is added. After leavingthe roots in the inoculation tank for a day or more,the plantsare planted
in pots in the greenhouseor in nurserybedsoutdoors. In order to encouragefurther infection and to provide optimum conditions
for diseasedevelopment,the plantsarewateredmore frequently than actually requiredfor growth. Undersuchheavydisease
.18.
pressure,young plantsof:high1ysusceptibleand evenmoderatelysusceptiblevarieuescan be rapidly killed. The resultsof
suchfeederroot inocula1iontestshavebeenmeasuredvariouslyin terms of plant survival,the.amountof root rot, or asa
reduction in root and shoot growth. A major weaknesswith this kind of test is that it.5 difficmt, or perhapsevenimpossible, to determinethe root regeneratingcapacityof the stock. The methodis thereforeusefulfor assessing
high revelsof
susceptibilityor resistance,but haslimited valuefor determiningthe likely field bel1aviorof thosemany rootstocksthat
fall in betweenthese2 extremes.
Teststo determinethe relativesusceptibilityof stembark to phytophthora havebeencarried out in the pastasfollows
(2,8,10): A smalldisk of bark extendingdown to the cambiumis removedfrom the trunk and a disk of agarculture of
phytophthorais insertedin its place. The areais then boundwith waterproof wrappingmaterial. After suitableperiods,
the wrappingis removedand the distancethat the rotted bark extendsawayfrom the point of inoculation is measured.
Usefulthough this steminoculationtechniquehasbeen,it certainly doesnot stimulatevery closelythe naturalinfection
process
in whichzoospores
arethe main,andperhaps
the onlykind of infectivepropagule.
Methods cuffently being in-.esti{F1tedat LAREC to determinethe relati-.esusceptibilityof rootstocksto foot rot
Since 1969,attemptshavebeenmadeat lake Alfred to devisea more naturalprocedurefor determiningthe susceptibility of the trunk bark to infection, usingzoosporesuspensions
asinoculum. The first requirementwasto developsome
systemwherebylargenumbersof zoosporescould be brought into contactwith stem bark without alsohavingto immerse
the root systemin the inoculum. This wasachievedon young potted plantsin the greenhouseby building a watertight
collar aroundthe stemwith segmentsof Tygon tubing. The resultingcollar,which restedon the soil surface,was sealedat
the baseby pouring in a melted 1:1 mixture of paraffin wax and vaseline.A measuredvolume of zoosporesuspensionof
standardizedconcentrationwasthen pouredinto eachcollar. The resultsof testsusingthis technique (13) showedthat
1) after the peridermhad formed, no infection could occur unlessa breakexistedin the outer bark; 2) relatively largenumbersof zoosporeswere requiredfor infection to occur at ~I; 3) an injury renderedthe stemsusceptibleto infection for up
to 2 weeksafter it had beenmadeand; 4) the chancesof infection were greaterwhen the injury extendedinto the cambium. It wasfound that only a minute cut in the barkwas requiredfor fun{PI1penetration. The procedureeventuallyadopted
for uniformly woundingthe stemsin variety susceptibilitytestsconsistedof making2 or 4 vertical cutswith the point of a
scalpelblade. Thesecuts extendedup the stemfor a distanceof 25 mm abovethe soil surface. Diseaseratingswere based
on the distancethat diseasedbark extendedlaterally from eachvertical cut.
.
For inoculatinglargertreesoutdoorswith zoospores,a muchsimplertechniquehasbeensuccessfullyused(13). Four
vertical cutswerefirst madeat the baseof the trunk with a pointed pocket knife blade. A 6-inch high collar of absorbent
cotton waswrappedaroundthe baseof the trunk, which wasthen bankedwith soil to the top of the cotton collar. After
saturatingthe cotton with lakewater or rain water, a freshly preparedzoosporesuspension
waspouredaroundthe bark
in sucha mannerthat it would run down the stem overthe areascontainingthe vertical cuts.
Microscopicexaminationsrevealedthat only a short period of wetting was requiredfor infection (13). Zoosporessettled on the exposedinner bark tissuealmostimmediately. They germinatedin lessthan 30 min, and the germtubes mostly
penetratedthe living tissueadjacentto the cut in lessthan 60 min after inoculation. Sufficient fungal growthwithin the
bark to causefoot rot only occurred,however,if the bark waskept moist for a further period after fungalpenetration.
This wasachievedby pouringsmall amountsof water overthe cotton 2 or 3 times a day for the next 2 days. Thereafter,
the collarswere kept moist during dry weatherby applying overheadsprinkler irrigation asrequired. Treeswere inoculated
mostly in June.July. On susceptiblevarieties,foot rot developedvery rapidly and the trunk of 1.3 year old trees often le.
comecompletelygirdledin lessthan a month. lesion developmentstartedto slow down by October-November,
and callus
tissuebeganto developat the peripheryof the rotted area. The soil bankswerethen removedand the amount of trunk
girdling and callusformation was recorded.
The reactionof somecurrently usedand experimentalrootstocksto zoosporeinoculation hasnow beenstudied both in
the greenhouse
and in the field. Somevarietiesshowedthe samerelativeresponsein both environments.For example,
'Pineapple'orangeseedlingsalwaysshoweda highly susceptiblereactionboth when testedasyoung seedlingsin the green.
houseand asolder plantsin the field. At the other extreme,trifoliate orange,'Carrizo' and 'Troyer' citrangesconsistently
showeda highly resistantreaction. With someclones,however,particularlywithin the roughlemon group,different resc.
tions occurredbetweenthe greenhouseand outdoor tests. For example,certain rough lemontypes that hadappeared
moderatelysusceptiblein greenhouse
testsshoweda highly resistantreaction in the field tests (Whiteside,unpublished
.19-
data),suggestingthat the bark had becomemoreresi~tantwith age. The reversesituation hasalsooccurred. Onerough
lemon variantthat appearedto be only moderatetysusceptiblein the greenhouse
testsshoweda highly susceptiblereaction
in field tests. Suchdiscrepancies
havecastdoubtsfJnthe reliability of greenhouse
testson young plantsfor determiningthe
likely "field" reactionof rootstocksto phytophthora attactc.
Becauseof the current importanceof rough lemon in Floridacitriculture and the greatvariability that existsin this species
andthe contradictingreportsthat havebeenmadeconcerningits susceptibilityto foot rot, specialattention is beinggivenat
lake Alfred to the field testing of different roughlemoncultivarsfor susceptibilityto foot rot.
A major problemin the growingof rough lemon asa tree outdoorsin Florida is the very stunted growth that is causedby
the almostconstantalternarialeaf spot attack. Because
th~ diseaseis very difficult to control by fungicidespraying,the ob.
vioussolution was to bud the greenhouse-grown
treeswith sweetorangebeforeplanting outdoors. This enabledthe inherently vigorousrough lemonstock to grow asfast as,and evenfasterthan, treeson other rootstock. It wasmainly becauseof
the specialproblemwith roughlemon that the decisionwasmadeto bud all rootstock varietieswith sweetomngebeforetes.
ting them for foot rot susceptibility. But anotheradvantagein makingthe testson buddedtreessoonbecameapparent. By
makinginoculationsacrossthe bud union, a further checkcould be obtainedasto whethera rootstock had failed to develop
foot rot becauseof inoculationfailure or becauseit wastruly geneticallyresistant. This inoculationtechnique ensuredthat
therewould be a doublechanceof foot rot developingon the stock;either by direct penetrationof the rootstock at the time
of inoculation,or by growth of the fungusacrossthe bud union from the highly susceptibleand almost invariablyinfected
Meet orangebark.
To date,perhaps the most surprisingresultthat hasbeenobtainedfrom thesefield inoculationsis the apparentlyhigh resistanceto foot rot of most (though not all) sourcesof rough lemon. This rootstock hasearneda ~putation for beingmoderatelyto highly susceptibleto foot rot in somecitrus growingareasof the world. This view is alsowidely held in Florida,
althoughthe experiencein manylocal grovesdoesnot really supportthis contention. Many caseshavebeenobservedlocally in which foot rot hasremainedconfined to the scion portion of the trunk on treesgrowingon rough lemonstock. Perhapsthe apparentcontradictionsin the behaviorof roughlemon stock are relatedto the greatgeneticvariability which
occurswithin this species.Differencesin the susceptibilityof feederroots to infection havepreviouslybeenreported (5).
In field testsat lake Alfred lar!p!differencesin the incidenceof foot rot havebeenobservedbetweenclonesof rough lemon
(Whiteside,unpublisheddata). In fact, someclonesappearedto be assusceptibleto foot rot assweetorange.The majority,
however,appearedto be moderatelyresistantto this disease.Therefore,at leastsomeof the locally severeoutb~aks of
foot rot that haveoccurredin Floridacould, in fact, havebeendueto tI1eunwitting useof highly susceptibleclonesof rough
lemon. Rootsproutpropagationshavebeenmadefrom severalgrovesin which foot rot hasoccurredon supposedlyrough
lemon stock. The relativesusceptibilityof tI1esecloneswill eventuallybe determinedin controlled field inoculation tests.
r,. citrus rootstock-phytophthorasituation in Florida in perspecti~
The only long-termpracticalmethodfor preventingfoot rot and phytophthoraroot rot is to usesufficiently resistant
rootstocksand to bud the treesat least3 inchesabovegroundlevel. In view of the Florida habit of buddingtreesvery low,
it is perhapssurprisingthat foot rot hasnot becomean evengreaterproblemin our citrus groves.Probablywhat prevents
this happeningis the sandynature of the soil andthe fact that the bark on the trunk seldomstayswet for long periodsafter
rain. In fact, infection usuallystartson those parts of the crown roots and trunk lying below groundlevel. If infection does
occur aboveground,this is usuallyassociatedwith the piling of plant residuesor soil againstthe trunk.
In spiteof the sandyandwell-drainedpropertiesof the soil, experiencehasshownthat the incidenceof foot rot on highly
susceptiblecitrus speciesand varietiescan be very high. Thus, it is important to avoid usingsuchkinds of citrus as rootstocksif at all possible.The questionarises,however,asto how much resistanceor toleranceto phytophthora is really required under Florida conditions. Any speciesthat is ashighly susceptibleto foot rot assweetorange,grapefruit,andsmooth
lemon certainly needsto be avoided. But it is doubtful whether there is any justification for goingto the other extremeand
retainingaspossiblerootstock candidatesonly thosevarietiesthat are highly resistantto phytophthora. Certainlyin Florida
this doesnot seemto be necessary.For commercialplanting,rootstockshaveto meet many other requirements,including
resistanceto somediseases
that areevenmore devastatingthan phytophthora. Therefore,high resistanceto phytophthora
frequently becomesa secondaryconsiderationin the choiceof rootstock. However,it is important to know whether a candidaterootstock is highly susceptibleto foot rot under groveconditions. It is alsoimportant to know what capacityan
easily infectedvarietyhasfor sealing
off areasof diseased
barkby producingcallustissue.Reliableinformationon these
.20-
matterscan probably only be obtainedby testingthe susceptibilityof stem bark under field conditions,and after buddingthe
tree with a locally usedscionvariety. It is to be hopedthat the inoculationtechniquesnow beingtestedat lake Alfred might
proveusefulin theserespects.
.21-
Literature Cited
1. Broadbent,P. 1969. Observationson the modeof infection of Phytophthoracitrophthor8 in resistantand susceptible
citrus roots. Proc. First IntI. CitrusSymp. Univ. Calif., Riverside3: 1207-1210.
2. Broadbent, P., L. R. Fraser and V. WatelWorth. 1971. The reaction of seedlings of Citrus spp. and related genera to Phytophthora citrophthora. Proc. Linn. Soc. New. South Wales 96: 119.127.
3. Carpenter,
J. B.,andJ. R.Furr.1962. Evaluationof toleranceto root rot causedby Phytophthoraparasiticain seedlings
of citrus and relatedgenera.Phytopathology 52: 1211-1285.
4. Grimm, G. R. and D. J. Hutchison. 1973. A procedurefor evaluatingresistanceof citrus seedlingsto Phytophthoraparasilica. Plant Dis. Rep. 57: 669-672.
5. D. J. Hutchisonand G. R. Grimm. 1972. Variation in phytophthora resistanceof Florida rough lemon and sour orange
clones. Proc. Fla. State Hart. Soc. 85: 38-39.
6. Klotz, l. J., W. P. Bitters,T. A. DeWolfeand M. J. Garber. 1968. Somefactors in resistanceof citrus to Phytophthora
spp. Plant Ois. Rep. 52: 952-955.
7. Klotz, t. J. and T. A. DeWolfe. 1967. Testingsweetorangerootstocks. Calif. Citrograph 52: 387.388.
8. Klotz, l. J. and H. S. Fawcett. 1930. The relativeresistanceof varietiesand speciesof citrus toPythiacystis gummosis
and other bark disease.J. Agf. Res.41: 415425.
9. Klotz, L. J. and E. C. Calavan.1969. Gum diseases
of citrus in California. Calif. Agf. Exp. St8. Ext. Slrvice. CifC.396.
26 p.
10. Rossetti,Victoria. 1947. Estudossobrea "gumosede Phytophthora" d oscitrus. I. Suscetibilidadede diversesespecies
citricasa algumasespeciesde "Phytophthora." Arg./nst. BioI. 18: 97-124.
11. 15ao,P. H. 1969. Studieson the saprophyticbehaviorof Phytophthoraparasiticain soil. First IntI. Citrus Symp.Proc.
Univ. Calif., Riverside3: 1221-1230.
12. Whiteside,J. O. 1970. Factorscontributing to the {estrictedoccurrenceof citrus brown rot in Florida. Plant Oil. Rep.
54: 608-612.
13. Whiteside,J. O. 1971. Somefactors affectingthe occurrenceand developmentof foot rot on citrus trees. PhytopatholDgy
61: 1233.1238.
14. Zentmver.G. A. 1961. Chemotaxisof zoosporesfor root exudates.Science133: 1595-1596