An Introduction To The Genus Phytophthora

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An introduction to the genusPhytophthoraMatteo Garbelotto, U.C. BerkeleyRick Bostock, U.C. DavisDavid Rizzo, U.C. Davis&The Internet

What are Phytophthoras? Fungi ? Fungus-like organisms? Water molds ?

Oomycota Belong to a kingdom that includes kelp anddiatomes Kingdom used to be called Chromista(brown algae), it is now the Straminopila

Oomycota It includes many important plant pathogens:– Peronospora: mostly aerial– Pythium: mostly soilborne organisms– Phytophthora: mixed biology

agellatezoosporecoenocytic 2n mycelia

Oomycetes are not fungi Cellulose in cell wall Ploidy is 2n Result of sexual activity isoospore (2n) Meiosis, somatogamy,caryogamy all occur at thesame time Water adapted biology,flagellate phase No septa, holocoenocytichyphae Chitin in cell wall Ploidy is n, or n n Result of sexual activity isa spore n Meiosis,somatogamy,caryogamyare usually interupted byvegetative (somatic phase) Better adapted for aerialtransmission Septate hyphae

Blue mold of tobacco caused byPeronospora tabacina Ability to travel aerially for hundreds ofkilometers from Caribbean to Southern US Ability to predict arrival of inoculum basedon weather pattern Some species capable of over-wintering inbuds

Phythium Mostly soilborne pathogens of plants, but atleast one (P. insidiosum) causes a severe skindisease in mammals They are usually generalists, meaning they canaffect a broad range of hosts Together with Phytophthora, Rhizoctonia andFusarium responsible for a serious agriculturalproblem called damping off Some species are mycoparasites and have beenused as biocontrol agents

Life cycleDifferent thanPhytophthora

Important structures Sporangia: size, shape, L:B, papillate or not,deciduous or not Stalks: length Zoospores. Encysted zoospores Chlamydospores: how are they carried (lateral vs.terminal), size, color, ornamentation Oospores Hyphae: swellings present or absent, linear ortormented Colony morphology: appressed vs aerial, fastgrowing vs. slow-growing

Damping off: because of generalist nature and ofability to overwinter, this is a serious issue incommercial facilities and in reforestation projects Pre-emergencePre-emergence damping offin soybean Post emergencePost emergence damping offof yellow pine

Life history of damping off

Key genus for the understandingof ecological role of soilbornemicrobes Negative feedback processes: progressiveincrease in reduction of % success ofregeneration Optimal allocation of resources by cullingseedlings that are less fit early on in therevegetation process thus bringing populationsto viable density without wasting resources Major drivers of biodiversity: Janzen-Connellhypothesis

Janzen-Connell hypothesis“Adults, by harboring host-specific pathogens andherbivores, will locally reduce the recruitment success ofcon-specific juveniles”AAbundance of seedlingsB

Proportion of diseased seedlingsLower mortalityaway fromparent tree

Phytophthora Some important plant pathogens, with verywell known history– Phytophthora infestans and the Irish potatofamine– Phytopthora cinnamomi and the Jarrah diebackin Australia. Chestnut decline and littleleafdisease of pines in Southeastern USA

The Irish Potato Famine From 1845 to 1850 Phytophthorainfestans Resulted in the deathof 750,000 Emigration of over 2million, mainly to theUnited States.

Phytophthora: “plantdestructor” Best known pathogen whose long-distancetransport linked to agriculture.– Infected root-stocks– Infested soil– Infected plants

100 species of Phytophthora 60 until a few years ago, research accelerated,especially by molecular analyses Differentiated on basis of:––––––Type of sexual intercourseType of sexual activityNumber of hostsIdeal temperatureType of biology (soilborne, splash, airborne)Evolutionary history (Waterhouse-Cooke)

Type of sexual strategyHomothallic species, will produce bothoogonia and antheridia and mate bythemselves (hermaphrodite), low geneticvariability. Strong inbreeding.Heterothallic species need two individualswith different MATING TYPES. Normallydefined as A1 and A2. Out-crossing species.

How do Phytopthoras “score” . There has to be recognition of other sex, thenforeplay, then sex Two mating types (A1 and A2) code for differentlipids. Lipids are used to identify other sex Males and females thencommunicate throughpheromones Antheridiol (Raper 1939) is produced by the femaleand stimulates in the male: a)- the production of themale organ antheridium; b)- the production ofoogoniol that will then stimulate the female toproduce the oogonia

Nature of sexual contactOogonium (female sexual structure),trichogyne (receptive hyphae)Antheridium (male sexual structure)Amphiginous, Paragynous, Perigynous (basedon how the two mate)

Sexual Reproductionantheridiumoogoniumoospore

Two styles of attachment of antheridia and oogoniaantheridiumantheridiumamphigynousparagynous

oosporeoospore germinating toproduce sporangia

Type of sexual strategyIn area of origin expectations are:-Both mating types if heterothallic-Sexual activity and large number of differentgenotypes-If species is homothallic expectation is thatpopulations in isolated areas should be differentgenetically because of lack of gene flow andgenetic drift (basic Darwinian concept)

Type of sexual strategyIf species is exotic, expectations are:-Often one mating type only, or mating typesintroduced at different times.-Low genotypic diversity, prevalence of clonallineages-If species is homothallic expectation is that allindividuals will be similar, because there has beenno time for genetic differentiation

Type of sexual strategyWhy should we care about sex ?-Ability to recombine alleles, better potential ofadaptation to new conditions-Ability to exchange genes with other individuals,if gene pool is large, it can be a great adaptiveadvantage-For instance: ability to overcome the fungicidemetalaxyl happened when A1 and A2 of P.infestans got together and reproduced.

More reasons to care about sex Oospores that are the end result ofsuccessful mating are extremely hardy,thick walled spores that act like survivalstructures capable of enduring extremelyadverse conditions. Makes sanitationincredibly arduous Homothallic species tend to have a broaderecological range because they easilyproduce oospores

and even more reasons to careabout sex There may be different adaptive alleles linkedto the two different mating types genes. Thesealleles may not be recombined but presence ofboth A1 and A2 means that populations cancount on a broader array of genes P. cinnamomi: in general only A2 is foundwhere pathogen is exotic. However A1 appearsto be more aggressive on Camellias

However in the absence of sex Genetically isolated populations undergo anindependent evolution and adaptationresulting in so called lineages withdramatically different phenotypes Multiple introductions from differentlineages can have dramatic impacts, yetvery rarely are these lineages regulatedindependently

Number of hosts Single hosts, specialized: P. sojae, P. lateralis Multiple hosts, generalists: P. cinnamomi(3000 hosts!), P. ramorum ( 100). Theevolution of extreme polyphagy is a stunningtrait, really unique to this genus amongpathogenic microbes. It implies the ability toovercome host-specific defenses that arewildly different

Single vs. multiple hosts Single-host species can spread moreefficiently, depending on abundance anddistribution of host Multi-host species may spread more slowlybecause not all hosts sporulate or because ofdifferent susceptibility among hosts(dilution effect) In the case of generalists it is important tounderstand susceptibility and infectiousnessof each host

Generalist Phytophthoras Represent a challenge for modern society.How do you regulate 3000 host species? P.ramorum first generalist to be regulated, butcurrent regulations probably are notsustainable in the long time Need to understand different role played bydifferent hosts, and prioritize

Confirmed Susceptible SpeciesAndrew's clintonia bead lilyArdisiaBearberryBigleaf mapleBlueblossomCalifornia bay laurelCalifornia black oakCalifornia buckeyeCalifornia coffeeberryCalifornia hazelnutCalifornia honeysuckleCalifornia maidenhair fernCalifornia nutmegCalifornia wood fernCamellia speciesCamphor treeCanyon live oakCascaraChinese witchhazelChinese guger treeCoast live oakCoast redwoodDogwood speciesDouglas firEastern Joy Lotus TreeEuropean ashEuropean turkey oakEuropean yewEvergreen huckleberryEvergreen mapleFalse Solomon’s sealFormosa firethornFetterbushGoat willowGrand firGriseliniaHollyHolly oliveHolm oakHorse chestnutHybrid witchhazelJapanese evergreen oakLaurustinusLeucothoe speciesLilacLoropetalum speciesMadroneMagnolia varitiesManzanitaMicheliaMountain laurelMyrtle-leafed DistyliumNorthern red oakOleanderOregon ashOregon grapeOsmanthusPacific yewPersian ironwoodPieris varietiesPlanetree maplePoison oakPrunus speciesRed firRed lotus treeRed tip photiniaRedwood ivyRhododendron speciesRoble beechRosa species & hybridsRugosa roseSalalSalmonberryScotch heatherScribbly gumSessile oakSheep laurelShreve’s oakSouthern red oakSpicebushSpike witch hazelSpreading euonymusStar magnoliaStrawberry treeStriped bark mapleSweet bay laurelSweet chestnutSweet CicelySweet oliveTanoakToyonViburnum varietiesVictorian boxVine mapleWestern maidenhairfernWestern starflowerWhite firWinter's barkWitch hazelWood roseYew

Douglas-firBuckeyeredwoods

Bay/Oak associationBay YearlyCoast Live Oak (nosporulation)Canker margin in phloemWave yearsBleeding cankerSporangiaSoil

Number of Invasive Forest Pathogens

Type of IFPPathway ofintroductionOf IFP

Host species x pathogengenotype Diversity within a species of a pathogen anddifferent epidemiological role of differenthosts are key elements to be considered

Effect of variability withinpathogenTwo different lineages of Phytophthora ramorum cause a disease ofdifferent severity on the same host

Host x Lineage x Temperature!-Bays and Rhododendrons respond differently: baysremain very susceptible at low temperatures, not so forrhododendrons. This has implications for disease spread incolder climates- At intermediate temperatures, NA2 is more aggressive

Oak root canker(Phytophthora cinnamomi) Species originally from PNG/Borneo/Sumatra, a common agricultural pathogen Soilborne, waterborne common in the wild in other parts of the US If host not extremely susceptible, predisposing factors needed for mortality tooccur (e.g. oaks in Southern Europe)Dry spellMan-induced ecological alterationsP. cinnamomi causesLittleleaf disease of pineson former-agriculturalsoils with hardpan inthe Eastern US

Problem: Oak declineLocations:Del Dios Area (Lake Hodges)County ParksRural Areas

Oak Tree Survey at Del DiosResults:Of 474 Quercus agrifolia trees,27% had bleeding cankers on the trunk.Of 86 Quercus engelmannii trees,none showed bleeding.

Example of man-inducedenvironmental alterationPhytophthora cinnamomiIntroduced onCoast Live OakSan Diego Co.ReservoirOaks at mid-slope experiencefluctuations in the water table level: ifinfected by P. cinnamomi becomeextremely weak and attractive toinsects

Ione manzanita: endangered speciesIoneExtremely harsh ecosystems,serpentine soild (very acidic,rich in Fe ), miningoperations

Two major components ofplant cover are manzanitas:A. viscida (white manzanita)A. myrtifolia (ione manzanita)Ione manzanita is a rareendemic species of theIone area, one that haswell adapted to the localconditions, but it iscurrently in the list ofUS threatened species

Because of almost total susceptibility to soilborne P.cinnamomi

Genetic diversity of Pc in Ione isstaggering, it includes all of thediversity present in Californianatural ecosystems

How can we explain thisdiversity? At least four introductions of four distinctstrains Populations large enough that additionaldiversity generated locally (soilenvironment favorable to pathogen) One dominant strain is also present in CaChristmas tree farms also matching a strainfrom a severe outbreak of oak mortality inColima. This strain is novel

775998P3656 Papua New Guinea W [A1 7 II]P3662 Catstanopsis Papua New Guinea [A1 6 II]P2183 Soil Papua New GuineaP3659 Catstanopsis Papua New Guinea [A1 6 II]9a1 Manzanita CA W1005b1 Manzanita CA W2a1 Manzanita CA W26 25 Manzanita CA W24 1 Manzanita CA W1c0 Manzanita CA W19a5 Manzanita CA W13a2 Manzanita CA W12a2 Manzanita CA W11b2 Manzanita CA W10a2 Manzanita CA Wmc04 Oak Mexico Wmc15 Fir CA Cmc09 Manzanita CA Wmc14 Douglas Fir CA CP6493 Rhododendron China C [A1 8 III]P2136 Avocado CA C [A1 1 I]P6379 Ananas Taiwan C [A1 1 I]P2121 Avocado Madagascar C [A1 2 II]98P2160 Vitis South Africa CP2159 Vitis South Africa C [A1 3 II]P3664 Eucalyptus Australia W [A1 2 II]P2021 Camellia CA C [A1 1 I]P3233 Camellia China C [A1 1 I]P3237 Camellia China C [A1 1 I]P2170 Camellia CA CP2096 Camellia CA C [A1 1 I]P2100 Camellia CA CP3232 Rhododendron China C [A2 5 III]25 2 Manzanita CA WP2301 Rhododendron CA C [A2 5 III]7417a1 Manzanita CA Wmc12 Nordmann Fir CA C86mc03 Coast Live Oak CA Wmc07 Oak CA Wmc17 Soil CA593a2 Manzanita CA W20a1 Manzanita CA W15 0 Manzanita CA W7b1 Manzanita CA Wmc16 Fir CA C1b2 Manzanita CA W4b2 Manzanita CA W16 0 Manzanita CA Wmc06 Avocado CA CP6490 Avocado FL Cmc10 Coast Live Oak CA Wmc08 Coast Live Oak CA W29a2 Manzanita CA Wmc02 Coast Live Oak CA Wmc05 Blueberry FL Cmc11 White Fir CA CP2288 Pine CA C [A2 4 III]P2428 Avocado CA C [A2 4 III]P2444 Avocado CA C [A2 4 III]P544 CA WP543 CA WP542 CA WP541 CA W22a2 Manzanita CA Wmc01 CA W6b1 Manzanita CA WP547 CA WP545 CA WP546 CA WP549 Soil CAD2 2 CA WD8 3A CA WD9 4 CA WA4 CA WPC004 CA WABC1C2D1D2

Manzanita775998P3656 Papua New Guinea W [A1 7 II]P3662 Catstanopsis Papua New Guinea [A1 6 II]P2183 Soil Papua New GuineaP3659 Catstanopsis Papua New Guinea [A1 6 II]9a1 Manzanita CA W1005b1 Manzanita CA W2a1 Manzanita CA W26 25 Manzanita CA W24 1 Manzanita CA W1c0 Manzanita CA W19a5 Manzanita CA W13a2 Manzanita CA W12a2 Manzanita CA W11b2 Manzanita CA W10a2 Manzanita CA Wmc04 Oak Mexico Wmc15 Fir CA Cmc09 Manzanita CA Wmc14 Douglas Fir CA CP6493 Rhododendron China C [A1 8 III]P2136 Avocado CA C [A1 1 I]P6379 Ananas Taiwan C [A1 1 I]P2121 Avocado Madagascar C [A1 2 II]98P2160 Vitis South Africa CP2159 Vitis South Africa C [A1 3 II]P3664 Eucalyptus Australia W [A1 2 II]P2021 Camellia CA C [A1 1 I]P3233 Camellia China C [A1 1 I]P3237 Camellia China C [A1 1 I]P2170 Camellia CA CP2096 Camellia CA C [A1 1 I]P2100 Camellia CA CP3232 Rhododendron China C [A2 5 III]25 2 Manzanita CA WP2301 Rhododendron CA C [A2 5 III]7417a1 Manzanita CA Wmc12 Nordmann Fir CA C86mc03 Coast Live Oak CA Wmc07 Oak CA Wmc17 Soil CA593a2 Manzanita CA W20a1 Manzanita CA W15 0 Manzanita CA W7b1 Manzanita CA Wmc16 Fir CA C1b2 Manzanita CA W4b2 Manzanita CA W16 0 Manzanita CA Wmc06 Avocado CA CP6490 Avocado FL Cmc10 Coast Live Oak CA Wmc08 Coast Live Oak CA W29a2 Manzanita CA Wmc02 Coast Live Oak CA Wmc05 Blueberry FL Cmc11 White Fir CA CP2288 Pine CA C [A2 4 III]P2428 Avocado CA C [A2 4 III]P2444 Avocado CA C [A2 4 III]P544 CA WP543 CA WP542 CA WP541 CA W22a2 Manzanita CA Wmc01 CA W6b1 Manzanita CA WP547 CA WP545 CA WP546 CA WP549 Soil CAD2 2 CA WD8 3A CA WD9 4 CA WA4 CA WPC004 CA WABC1C2D1D2

How can we explain such asevere effect on manzanita spp.? Host is very susceptible Multiple lineages of the pathogen wereintroduced. Because lineages are differentthere is synergism resulting in higher infectionlevels One lineage is novel and it has been reportedin a serious outbreak in Colima, Mexico, innew outbreaks in Christmas tree farms inCalifornia and in Ione

Andrew's clintonia bead lily Ardisia Bearberry Bigleaf maple Blueblossom California bay laurel California black oak California buckeye California coffeeberry California hazelnut California honeysuckle California maidenhair fern California nutmeg California wood fern Camellia species Ca

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