Color figures from:

Phytophthora: A Global Perspective

Edited by Kurt Lamour

March 2013 / Hardback / 256 Pages / 9781780640938

Book is available from CABI at the following address:

http://bookshop.cabi.org/?page=2633&pid=2611&site=191

Chapter 4. Characterizing populations. Kurt Lamour

Fig. 4.1. Association of Loss of Heterozyosity (LOH) with loss of pathogenicity in P. capsici. In 2005 and 2011, P. capsici isolates were inoculated onto wounded (site distal to stem) or un-wounded (site proximal to stem) sites on healthy jalapeno fruits. TN1 and TN2 are field isolates and TN31, TN37 and TN47 are sexual progeny produced in 2004. In 2011, the genomes for TN37 and TN47 had approximately 10% of the heterozygous nucleotide sites switched to homozygosity.

Chapter 5. Phytophthora Species Hybrids: A Novel Threat to Crops and Natural Ecosystems, Tibor Érsek and Willem A. Man in‘t Veld

A B

C D

Mdh‐1

Mdh‐2

Fig. 5.1. Scanning electron micrographs of P. alni gametangia showing A, the ornamented oogonial surface of P. alni subsp. alni and B, the smooth oogonial surface of P. alni subsp. uniformis. The two‐celled antheridia is visible for both subspecies. Bars: 20 µm. C, Dimeric malate dehydrogenase (Mdh) enzyme patterns at the Mdh‐1 and Mdh‐2 loci for subspecies of Phytophthora alni. Lane numbers are on top and relative band mobility is on the right. The banding patterns for subsp. multiformis (Mdh‐ 191/100 and Mdh‐294/94, Lane 1) and subsp. uniformis (Mdh‐183/83 and Mdh‐2100/100, Lane 2) are combined in subsp. alni isolates (Mdh‐183/91/100 and Mdh‐294/100, Lanes 3–5) including two atypical isolates in Lanes 4 and 5 with a Pau mitotype. Mdh‐1 band were visualized by prolonged electrophoresis to let Mdh‐2 bands run off the gel according to the manufacturer’s instructions (Helena Laboratories) (Reproduced by permission of Akadémiai Kiadó, Budapest, ). D, Electropherogram of part of the ITS of P. hedraiandra × P. cactorum hybrid strains showing double bases at three positions (see arrows) where the sequences of the parents differ (Reproduced by permission of Springer).

A B A B

C

Fig. 5.2. A, Loquat tree (Eriobotrya japonica) in Coayllo, Peru, with basal stemrot, caused by P. nicotianae × P. cactorum hybrids, showing dieback in the canopy. B, Death of a loquat tree in Peru caused by P. nicotianae × P. cactorum (Courtesy Liliana M. Aragon‐Caballero, Peru). C, Symptoms caused by a P. hedraiandra × P. cactorum hybrid on Penstemon sp. (Courtesy Monika Heupel, ).

Chapter 6. Phytophthora infestans and P. andina on solanaceous hosts in South America. Gregory A. Forbes, Juan G. Morales, Silvia Restrepo, Willmer Pérez, Soledad Gamboa, Romina Ruiz, Luis Cedeño, Gustavo Fermin, Adriana Andreu, Ivette Acuña and Ricardo Oliva. A B

C

Fig. 6.1. A and B, Typical fruit and leaf symptoms of blight on hosts in the Anarrhichomenum group and C, on the stem of Solanum betaceum in South America.

A B

C

Fig. 6.2. Typical symptoms of blight on Physalis peruviana, a species in the Anarrhichomenum group, in South America. A and B, leaf blight and C, fruit blight.

Chapter 7. Phytophthora infestans and Potato Late Blight in . David E.L. Cooke and Björn Andersson.

Chapter 8. Phytophthora infestans in the United States. Dennis Halterman and Amanda J. Gevens.

A B

C D

Fig. 8.1. Representative slides created in 1943 by Russ Larson, a University of Wisconsin plant pathologist, to illustrate blight to a broad audience. A, illustrates the historical importance of blight in the Midwest, B, C, the importance of the aerial phase of sporangia dispersal and D, the movement of inoculum to tubers.

A B

C D

Fig. 8.4. Typical late blight symptoms on potato tubers (A, B) and fruit (C) and foliage (D).

Chapter 9. Phytophthora sojae on Soybean. Anne E. Dorrance.

A

B

C Fig. 9.1. Morphological features of P. sojae and symptoms from early season disease. A, A single releasing zoospores, note the extended length of the pedicel. B, Oospore formed inside of tissue. C, Infection on cotyledon and hypocotyl of a seedling.

A

B

C

Fig. 9.2. Symptoms of Phytophthora stem rot. A, Stand reduction due to Phytophthora stem rot on a with no Rps genes and low levels of partial resistance. B, Close up of the distinctive brown lesion on the stem. C, Symptoms of flooding injury, not caused by P. sojae.

Chapter 10. Biology and Management of Phytophthora capsici in the southwestern United States. Soum Sanogo and Paul W. Bosland.

A B

C

Figure 10.1. Phytophthora blight of pepper. A, Lesion on pepper stem caused by Phytophthora capsici. B, Lesion on pepper fruit with conspicuous mycelium and sporangia production on lesion surface revealed as a whitish mat. C, Early phase of plant infection in a pepper field infested with Phytophthora capsici; note the row pattern of affected plants.

Chapter 11. Phytophthora capsici in the eastern United States. Leah Granke, Lina Quesada-Ocampo and Mary Hausbeck A B

C

Fig. 11.1. Phytophthora capsici causes economic losses of A, squash B, pepper, and C, snap bean in the eastern United States. Symptoms of disease include fruit rot, root and crown rot, or foliar blighting.

A

B C

Fig. 11.2. A, The use of a tolerant cultivar (right side of bed) can assist in managing crown rot of pepper and other diseases caused by P. capsici. Yellow squash plants with B, no fungicide applications, or C, fungicide applied as a drench.

Chapter 12. Taro Leaf Blight caused by Phytophthora colocasiae. Susan C. Miyasaka, Kurt Lamour, Mike Shintaku, Sandesh Shrestha and Janice Uchida

Fig. 12.1. Impact of TLB on taro production. A, Wetland taro field in Waipio Valley, Hawai’i in which plants exhibit symptoms of TLB. B, heavily infected taro leaf. C, Decreased corm yields of taro on a per hectare basis on the island of Kaua’i (data from Hawai’i Agricultural Statistics Service, 1974 – 2008).

Fig. 12.2. A, infected corm collected on Oahu, Hawai’i. B, TLB lesion with very heavy sporangia production collected at the Kaua’i Agricultural Research Center, Kapaa, Hawai’i. C, Photomicrograph of a sporangium of P. colocasiae releasing swimming zoospores.

Chapter 13. Phytophthora nicotianae. Victoria A. Ludowici, Weiwei Zhang, Leila M. Blackman and Adrienne R. Hardham

Fig. 13.1. Phytophthora nicotianae infection of leaves and . A, Lesions on leaves following inoculation with P. nicotianae zoospores. B, Necrotic lesion on lupin roots 3 days after a 10‐minute immersion in a suspension containing 500 P. nicotianae zoospores per ml.

Fig. 13.2. Stages in the asexual life cycle of P. nicotianae. A–D, differential interference contrast light micrographs of vegetative hyphae (A), sporulating hyphae (B), zoospores (C) and germinated cysts (D). In B, a sporangium (Sp) and a (Ch) are present. In C, the two flagella (arrowheads) emerge from the centre of the ventral groove (vg). E–G, cryoscanning electron micrographs of P. nicotianae cysts on the surface of tobacco roots. In E, have encysted in an aggregate on the root surface. In F, mucilage‐like material (arrows) has been secreted by the encysting zoospores. One cyst has germinated and developed an appressorium‐like swelling (ap) where the germ tube penetrates the plant epidermis. In G, germinated cysts penetrate the tobacco root epidermis. H–K, immunofluorescence micrographs of P. nicotianae zoospores and cysts labelled with antibodies against adhesive proteins. In H, small vesicles on the ventral surface of the zoospores are labelled by an antibody directed against the Vsv protein. In I, material secreted onto the ventral surface of young cysts is labelled by the Vsv antibody. In J, small vesicles occurring predominantly on the zoospore dorsal surface are labelled by an antibody directed against PnCcp. In K, cysts have been labelled with the antibody against PnCcp. Scale bars in A–B = 20 µm; in C–K = 10 µm.

Chapter 14. Phytophthora cinnamomi in Australia. Wei Y. Hee , Pernelyn S. Torreña, Leila M. Blackman and Adrienne R. Hardham

Fig. 14.1. P. cinnamomi occurrence, detection and control in the Brisbane Ranges National Park, Victoria. A, Healthy eucalypt forest with an understorey of grass trees, Xanthorrhoea australis. B, Area of forest infected by P. cinnamomi. Grass trees are especially susceptible. C, Dipstick array for use in a 96‐well enzyme‐linked immunosorbent assay format. D, Dipstick membrane with numerous adherent P. cinnamomi cysts stained blue in a specific immunoreaction. E, Cleaning and disinfecting footwear to remove all adhering soil or plant debris before moving between infected and non‐infected areas within the Brisbane Range National Park.

Fig. 14.2. P. cinnamomi zoospores, cysts and germinated cysts. A, Elongation zone of an root surrounded by encysted spores. B, Hyphae and uncleaved sporangium. C, Sporangium that has cleaved and is in the process of releasing zoospores. D, Zoospores (z) and cysts (c). Two flagella (arrowheads) emerge from a groove (g) along the zoospore ventral surface. The ventral surface remains flat for 1–2 minutes after encystment (arrows). E, Cryoscanning electron micrograph of germinated cysts on the surface of an alfalfa root. An appressorium‐like swelling (ap) has formed where the germ tube has penetrated along the anticlinal wall between two epidermal cells. Bar in A = 200 µm; bars in B–E = 10 µm.

Chapter 15. Phytophthora in US Forests Yilmaz Balci and John C. Bienapfl

A

B C

Figure 15.1 Impact of Phytophthora ramorum on woodlands in California. A, B, Aerial and close-up view of extensive tanoak mortality in Sonoma County, California. C, Bleeding canker on tanoak in Mendocino County, California.

A B

C

Figure 15.2 Symptoms of Phytophthora ramorum on conifer and broadleaf hosts. A, Dieback on the leader shoot of Douglas fir (Pseudotsuga menziesii), B, Foliar necrosis on coast redwood (Sequoia sempervirens) and C, Leaf lesions on maidenhair fern.

Chapter 16. The impact of invasive Phytophthora species on European forests, Thomas Jung, Anna Maria Vettraino, Thomas Cech and Andrea Vannini

Fig. 16.1. Ink disease of chestnut and decline. A, Flame-shaped inner bark lesion caused by Phytophthora cambivora at the collar of a mature in . B, Crown of a mature declining in Germany with thinning and dieback due to root and collar rot caused by Phytophthora plurivora. C, Series of aerial bleeding bark cankers caused by Phytophthora plurivora on stem of a mature Fagus sylvatica in a mountain forest in Germany.

Fig. 16.2: decline and root and collar rot of . A, Small woody roots (diameter 2–5 mm) of a declining mature in Germany with severe losses of lateral roots and fine roots and open lesions caused by Phytophthora quercina. B, Crown dieback of riparian trees in Germany due to root and collar rot caused by Phytophthora alni ssp. alni. C, Severe collar rot with tarry spots at the outer bark and tongue‐shaped orange‐brown necrosis of the inner bark caused by Phytophthora alni ssp. alni on a young planted Alnus glutinosa in Germany.

Chapter 17. Phytophthora pinifolia: the cause of Daño Foliar del Pino on Pinus radiata in Chile. Rodrigo Ahumada, Alessandro Rotella, Miguel Poisson, Álvaro Durán and Michael J. Wingfield

A

B

C Fig. 17.1. Symptoms of P. pinifolia on Pinus radiata. A, infected adult trees, B, defoliated trees, and C, aerial photo of infected trees with a southern exposure (white arrows) and adjacent healthy trees with a northern exposure (red arrows).

A

B C

Fig. 17.2. Phytophthora pinifolia on needles of P. radiata. A, infected needle with black bands (arrows), B, close-up of the resinous translucent band, and C, sporangia on the needle surface observed by fluorescent light microscopy.

Chapter 18. Phytophthora in woody ornamental nurseries. Ana Pérez-Sierra and Thomas Jung A

B C

Fig. 18.1. A, Leaf necrosis, wilting and dieback of Azalea sp. caused by P. plurivora. B, Wilting of Lavandula sp. caused by P. nicotianae. C, Chlorosis and wilting of Syringa vulgaris due to root rot caused by P. citrophthora.

A

B C

Fig. 18.2. A, Thuja occidentalis killed by root rot caused by P. cinnamomi. B, Gum exudation on stem lesion of ornamental Prunus sp. caused by P. nicotianae. C, Root rot of Agave sp. caused by P. cryptogea.

Chapter 19. Distribution and biology of Phytophthora tropicalis. Janice Uchida and Chris Y. Kadooka

A B C

Fig. 19.1. A, Close monoclasial sporangia formation typical for P. tropicalis. B, Severe vine and leaf blight of English Ivy caused by P. tropicalis. C, Epipremnum (Pothos) blights developing five days following inoculation with zoospores of P. tropicalis.

A

B C

Fig. 19.2. A, Diseased pothos in the landscape. B, Anthurium spadix infected with P. tropicalis. The spadix is composed of many flowers with the ovaries protruding and triangular tepals surround the ovary. C, Macadamia raceme blight caused by P. tropicalis.

Chapter 20. Phytophthora palmivora in Tropical Tree Crops. André Drenth and David Guest

A

B

C

Fig. 20.1. A, Splitting cocoa pods. B, Phytophthora pod rot of cocoa. C, Seedling blight in the nursery.

A

B

Fig. 20.2. A, Piles of empty pod cases become breeding sites for flying beetles and sources of inoculum and B, Stem canker, with the bark removed to show the underlying lesion.

Chapter 21. Phytophthora root rot of avocado. Randy C. Ploetz

Fig. 21.1. An avocado tree in Queensland, Australia severely affected by Phytophthora root rot (PRR). Note the sparsely foliated canopy, and wilted, small leaves, and in the upper portions of the canopy, the prevalence of tip‐burned leaves, another aboveground symptom of PRR.

Chapter 22. The occurrence and impact of Phytophthora on the African continent. Jan H. Nagel, Marieka Gryzenhout, Bernard Slippers, Michael J. Wingfield

Fig. 22.1. Plantation trees affected by Phytophthora diseases. A, Dead, defoliated Eucalyptus spp. caused by P. cinnamomi infection. Basal stem canker of Acacia mearnsii suffering from black butt disease with B, exposed stem lesion and C, bleeding stem cankers. (Photographs courtesy of Jolanda Roux)

Figure 22.2: Dieback of Leucodendron argenteum (Proteaceae) caused by P. cinnamomi. A, Cracking of the bark, covering affected areas of the tree stem and early signs of wilting visible from the leaves. B, A severely wilted tree (left) with grey discoloured leaves.