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Home , Botrytis cinerea, Downy mildew

Cluster Rots and Quality Linda F. Bisson Department of and Enology University of California, Davis, CA

Outline of Presentation

u Introduction to Types of Rot u Factors Impacting Rot Incidence u The Fungal Rot Agents u Impact of Rot on Wine Quality

Rot Mythology

Saccharomyces and other native must yeast flora increase in numbers in rot conditions therefore a little bit of rot gives you a boost in native flora Rot Mythology

Saccharomyces and other native must yeast flora increase in numbers in rot conditions therefore a little bit of rot gives you a boost in native flora TRUE, BUT: Spoilage organisms also increase and to much, much higher levels and make it difficult for the good natives to compete

Rot Mythology

The total number of microbes only increase 10 to 100 fold in damaged clusters

Rot Mythology

The total number of microbes only increase 10 to 100 fold in damaged clusters TRUE, BUT: The organisms present are completely different genera than the normal native berry flora – Basidiomycetes become ascomycetes – Bacilli become acetic acid bacteria Rot Mythology

Disease stress leads to production of desirable components because there are more phenolic compounds and more hydrolytic enzymes are present that release bound aroma compounds

Rot Mythology

Disease stress leads to production of desirable grape components because there are more phenolic compounds and more hydrolytic enzymes are present that release bound aroma compounds TRUE, BUT: Off-characters are also produced, mycotoxins may be formed, aroma of fruit is often suppressed by mold and bacterial metabolites

INTRODUCTION TO TYPES OF ROT Types of Cluster Rots u Fungal Invasive Diseases u Fungal (Summer) Sour Rots – “Aerobic” rot u “True” Sour Rots (yeast and bacteria) – “Anaerobic” rot

Types of Fungal Attack u Invasive versus opportunistic – Invasives penetrate berry – Opportunists require pre-existing damage u Pre- versus post- rot – Some molds only grow on fruit post-harvest – Some opportunists not found post-harvest »? inhibited by other microbes

Fungal Invasive Diseases

u Directly invasive of berry tissue – Produce penetrating structures – Produce degradative enzymes – Excrete substances impacting berry surface integrity u Invade plant elsewhere and use vascular system to access berry Impacts of Grape Fungi on Fruit Quality

u Enzymatic destruction of berry tissues u Impede ripening u Off-flavor production u Flavor masking u Production of mycotoxins u Stimulation of spoilage bacteria and yeast u Stimulation of phenolic/pathogen responses of plant

FACTORS IMPACTING ROT INCIDENCE

Factors Impacting Rot

Vineyard Environmental ROT Management Conditions

Varietal Factors Factors Impacting Rot

Vineyard Environmental ROT Management Conditions

• management •Humidity/rainfall •UV exposure •Latitude •Trellis system Varietal Factors •Insect pressure •Soil management •Fungal reservoirs •Insect management •Hail/physical damage •Cluster architecture •Berry/cluster temperatures •Physical/spray damage •Seepage from berry •Cluster drop practices •/animal damage •Varietal composition •Wind •Invasion resistance •Underlying pathology

Varietal Factors Impacting Incidence of Rot

u Cluster architecture: density and self- imposed damage u Leakiness of berry cells to surface u Skin thickness/ease of penetration u Antifungal response mechanisms u Underlying pathologies: waterberry, berry shrivel, raisining

Pre- Shrivel Damage

Tyree Vineyard, UCD “Yellow Berry”

Very likely a plastid mutation

Tyree Vineyard, UCD

Sap on Leaves and Stems

Tyree Vineyard, UCD

Disease Elsewhere on

Fungal attack of stems

Tyree Vineyard, UCD Environmental Factors Impacting Rot

u Rainfall and relative humidity u Sunlight exposure and berry temperatures u Disease pressure – For entire vine – Presence of reservoirs u Insect presence and damage u Animal presence and damage u Wind

Fungal Reservoirs Near Vineyard

Powdery mildew on leaves on adjacent foliage – Tyree Vineyard

Insect Pressure

u Insects that attack or feed on berries u Insects that attack other parts of the plant such as phloem feeders u Insects that are just passing through – Leave sugary secretions behind – Leave microbial hitch-hikers behind “Leaf Bump”

Erinose mites (Bud Mites)

Tyree Vineyard, UCD

Spider Infestations

Will impact berry microflora

Tyree Vineyard, UCD

Secondary Damage to Clusters Caused by Insects

Larval feeding resulting in damage to clusters Insect Feeding on Fruit

Thrips oviposition punctures

Vineyard Practices u Cluster exposure: reduces humidity and “standing water” on berry surface – Leaf removal – Trellis system u Insect management u Soil treatments as many beneficials are soil microbes u Removal of infected plant materials u Control of neighboring reservoirs

Spray Damage, Tyree Vineyard, UCD Decayed Clusters Are Reservoirs

Mixed Pathologies

Possible mite damage, sunburn and/or spray damage and measles Tyree Vineyard, UCD

THE FUNGAL ROT AGENTS Pre-Harvest Invasive and Opportunistic Fungi Invasive Opportunistic u Erysiphe necator u Penicillium expansum u cinerea u Aspergillus spp. u Guignardia bidwellii u Coniella petrakii u Phaeoacremonium u Rhizopus stolonifer u Alternaria alternata u Trichothecium roseum u viticola

Post-Harvest Fungal Infections

u Cladosporium herbarum u Mucor spp. u Pre-harvest fungi – Rhizopus – Penicillium

Invasive Fungi Causing Rot

u Erysiphe necator () – Can split berry skins u : () – Produces antimicrobials – Associated with acetic acid bacteria (sour rot) – Produces laccase – Produces gluconic acid – Under dry conditions infection may be positive under wet conditions get decay of fruit Powdery Mildew Tyree Vineyard

Botrytis Rot

Photo: UC IPM on line http://www.ipm.ucdavis.edu/PMG/r 302100111.html

Invasive Fungi Causing Rot u Guignardia bidwellii: black rot – Brownish red lesions on berry that become black pustules – Leads to drying and mummification of fruit – High rainfall/water demands for growth – Overwinters in mummified clusters – Found in abandoned u Phaeoacremonium: black measles (esca) Guignarida rot

Vidal blanc

Esca (Phaeoacremonium) Black measles Tyree Vineyard, UCD

Invasive Fungi Causing Rot u Alternaria alternata (Alternaria rot) – Causes berries to leak – Forms a characteristic black smut – Confers a moldy taste to the wine – Requires rainfall late in season and high humidity u Plasmopara viticola () – Can be an agent of immature berry rot, older berries are more resistant Downy mildew

Downy mildew Ohio State University Grape downy mildew Midwest Grape Production Guide Plant Pathology, Cornell Bulletin 919-05 http://ohioline.osu.edu/b919/0010.html

Invasive Fungi Causing Rot

u Phomopsis viticola – Disease of grape vine – Can enter berries via pedicel – Can lead to sour rot

Opportunistic Fungi Causing Rot

u Require physical damage to fruit – Hail – Insect damage – Bird/animal damage u Require high humidity u Generally found in warmer regions Agents of Opportunistic Sour Rot

u Aspergillus spp. (black rot) u Penicillium spp. (green/white rot) u Rhizopus spp. (brown/black rot) u Coniella petrakii (white rot) u Trichothecium roseum (pink rot)

Penicillium Sour Rot

Penicillium bunch rot: white and green

IMPACT OF ROT ON WINE QUALITY Rot and Wine Quality

u 5-10%: noticeable reduction in quality u 20-40%: marked reduction in quality u >80%: commercially unaceptable

Loinger, C. et al 1977 Am. J. Enol. Vit. 28:196-199

Impact of Rot on Wine Quality

u Direct chemical and metabolic effects of mold growth u Effects on plant metabolism and berry composition: plant pathogen response u Encouragement of consortia of spoilage u Indirect effects on yeast fermentation performance

Direct Chemical and Metabolic Effects

u Moldy taints u Bitterness u Hydrolytic enzymes u Oxidases Effects on plant metabolism and berry composition

u Plant response to invasion – Pathogen resistance proteins: cause haze issues – Phenolic array of compounds altered – Peroxide generation systems of plant amplified u Loss of nutrients u Leakage of berry components u Shut-off of plant vascular system to fruit

Encouragement of Consortia of Spoilage

u Bacteria are responsible for the “sour” in sour rot (acetic acid bacteria bloom, not so much lactics) u Fermentative yeasts bloom (acid tolerant ones, not necessarily the ones you want)

Rot Impact on Bacterial Species

u – See an increase in Lactobacilli such as Lb. kunkeei and Lb. Lindneri – See slight increases in all lactics that are probably not significant with respect to wine quality u Bacilli and Pseudomonads – See a decrease in the aerobic bacteria that normally colonize plant surfaces Rot Impact on Bacterial Species

u Acetic Acid Bacteria – Dramatic increase in numbers »Acetobacter aceti »Acetobacter pasteurianus »Gluconobacter oxydans – Dominate flora of rot u Filamentous Bacteria – Some studies report increases in Streptomyces with rot

Rot Impact on Yeast Species u Aerobic (oxidative) basidiomycetes decrease in number u Fermentative ascomycetes bloom – to 106 - 107 cfu/ml – Hanseiaspora uvarum Ethyl acetate producers – Candida krusei – Issatchenkia orientalis – Candida vanderwaltii – Zygoascus hellenicus – Zygosaccharomyces bailii and Z. bisporus

Rot Impact on Yeast Species

u Select for acid tolerant species u Direct competition with Saccharomyces for nutrients u Saccharomyces has limited acid tolerance Indirect Effects on Yeast Fermentation Performance u Stress imposed by high acid levels u Stress from antimicrobial fungal metabolites: mycotoxins u Stress from high bioloads of microbes u Loss of needed nutrients (macro and micro – consumed by fungi) u Higher alcohol yields as have less growth/ cell mass

Minimizing Rot Impact on Quality u In Vineyard: – Drop infected clusters/plant components – Open canopies and expose clusters to air drafts – Minimize spray and other damage – Control insect populations – Judicious use of antifungal agents – Monitor adjacent fungal reservoirs – Eliminate vineyard overwintering fungal reservoirs – Manage for late rainfall

Minimizing Rot Impact on Quality u In Winery: – Cluster sort – Limit opportunities for post-harvest rot – Limit oxygen exposure – Consider HTST treatments (high temperature short time) – Use robust inocula – Avoid feeding spoilage populations – Inhibit growth of spoilage organisms »Sulfite »pH adjustment Resources on Grape Diseases

u UC IPM http://www.ipm.ucdavis.edu/PMG/selectnewpest.grape s.html u Database of IPM Resources http://ipmnet.org/cicp/fruit/grape.html u Michigan State University http://www.canr.msu.edu/vanburen/grapeweb.htm u Ohio State University http://newfarm.osu.edu/crops/grapes.html u Virginia Tech http://www.virginiafruit.ento.vt.edu/grape- fruit-ipm.html

Pest Management Guides and Manuals

u WSU Grape Pest Management Guide: http://cru.cahe.wsu.edu/CEPublications/eb0762/e b0762.pdf u Oregon State University Pest Management Guide http://extension.oregonstate.edu/catalog/pdf/em/e m8898.pdf u Cornell University http://www.nysipm.cornell.edu/publications/grape man/

The Rot Tasting

Zinfandel Sour Rot – “100%” sour rot (mix of true and fungal sour rots) – “No-rot” control – Native “no-rot” control Detection of Rot Characters – Commercial Control – Spiked with varying percentages of rot Acknowledgements

u Autumn Martinelli and John Ellenberg for taking the vineyard photos u Nick Bokulich for making the , conducting the analyses and writing the report u Kay Bogart for assisting in making the wines u Chik Brenneman for letting me ruin his Zinfandel and giving the mealybugs, mites and ants free reign in the vineyard

Cluster Rot Tasting

u Glass 1: Control Zinfandel u Glass 2: Native Fermentation Zinfandel u Glass 3: Zinfandel Cluster Rot u Glass 4: Commercial Zinfandel u Glass 5: Commercial Zinfandel: 1% Rot u Glass 6: Commercial Zinfandel: 10% Rot