Phytophthora palmivora

Overview

Phytophthora palmivora (E. J. Butler) E. J. Butler (1919) is a cosmopolitan pathogen with a wide host range, including some very important economic crops such as cacao, papaya, black pepper, rubber, coconut, and citrus. The center of origin is believed to be southeastern Asia (McHaw and Coffey, 1994). In 1907, Butler originally described a new species, Pythium palmivorum, from palms and coconut. In 1918 it was reclassified as Phytophthora palmivora (R einking, 1923). P. palmivora was placed in morphological group II by Stamps et al. (1990) and in clade 4 (Balci et al., 2008; Cooke et al., 2000) on the basis of ITS sequences of genomic rDNA. 

Etymology: From Palmyra palm (Borassus flabellifer), one of the tree species from which the pathogen was originally isolated.

Morphology

P. palmivora is heterothallic with amphigynous antheridia and spherical oogonia. The caducous sporangia are papillate, varying in shape from ovoid-ellipsoid (Erwin and Ribeiro, 1996) to obpyriform (Q-Bank). Chlamydospores are terminal and intercalary averaging 33 µm in diameter.

Genetics

P. palmivora is placed in the phylogenetic clade 4 together with P. megakarya and P. quercetorum. Sequencing data (Cooke et al., 2000; Kron et al., 2004) confirm the proposition of Oudemans and Coffey (1991), McHau and Coffey (1994), and Martin and Tooley (2003) that P. palmivora and P. arecae are conspecific.

Growth

Colony morphology on V8 is a stellate pattern with aerial mycelium; hyphae are coralloid. Growth on CMA is sparse with no aerial mycelium. Growth occurs over the temperature range of 11° to 35° C; optimal temperature for growth is 27.5° to 30° C.

Distinguishing characteristics for identification

P. palmivora differs from P. megakarya morphologically in that it has narrow, medium length sporangial pedicels and spherical, narrow-stalk oogonia compared to the broad, short, and occluded sporangial pedicels and the pyriform, downward tapering oogonia of P. megakarya (Erwin and Ribeiro, 1996). P. quercetorum, also in clade 4, is homothallic in culture (Balci et al., 2008) while P. palmivora is heterothallic.

The searchable web-based database Phytophthora-ID is useful for rapid identification of Phytophthora species based on sequencing of the ITS or Cox spacer regions, followed by BLAST searching the database. Phytophthora-ID maintains a database of sequences that is selective for sequence accessions that come from trusted sources including published, peer-reviewed studies whenever possible.

Disease history

The primary forest disease caused by P. palmivora is black pod disease of cacao. The first published reports on cacao were in 1909 by Von Faber and by Maublanc, who described the causal pathogen as a new species, Phytophthora faberi (Ashby, 1929). In 1924, Butler reported that P. faberi and P. palmivora were the same species, so the earlier name, P. palmivora, took precedence. The primary impact of this disease is on the cacao pods (fruits), eventually infecting the beans within the pods rendering them of no commercial value. The disease is known throughout the world wherever cacao is grown. In Central and West Africa, P. palmivora is known to exist in the same areas with P. megakarya, and both species can cause black pod disease. P. palmivora is also known to have serious effects on other hosts such as citrus (canker, fruit rot, and root rot), coconut (bud rot and fruit rot), papaya (stem rot and root rot), black pepper (root rot and collar rot), and durian (canker, root rot, leaf blight, and fruit rot). Inoculum is spread through rain splash, wind, insects, and human activity.

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Impacts in the forest

Although P. palmivora has a wide host range of over a thousand plant species, including ornamental plants as well as horticultural and agricultural crops, the only major concern in a forest setting appears to be on cacao. P. palmivora is believed to be responsible for annual losses of 20-30% of the world's cacao crop (Erwin and Ribeiro, 1996). The isolation of P. palmivora from noncultivated forest soil in Ghana indicates that this species is indigenous to forest soils (Kakwa, 1974). Most other economically important hosts such as citrus, coconut, papaya, black pepper, and rubber are in closely managed agricultural settings, sometimes in close proximity to natural forests. In 1993, Bernard and Mitchell reported P. palmivora on red maple (Acer rubrum) for the first time in the U.S. However, no reports on the actual impact of this species on hardwood trees have been found to date.

Forest and wildland hosts and symptoms

On cacao, P. palmivora primarily causes a pod rot (black pod) but is also known to cause stem cankers and seedling blight. Black pod can be caused by either P. palmivora or P. megakarya. In Asia, Central America, and South America, the disease is caused by P. palmivora. In Central and West Africa, both species occur and either may cause black pod. Symptoms caused by P. megakarya and P. palmivora can be distinguished in the field because P. megakarya produces lesions with irregular edges on the fruit whereas lesions caused by P. palmivora have regular borders and are generally smaller (Erwin and Ribeiro, 1996). Pods are susceptible at all stages of development and may be infected at any place on the surface. The first symptom is a brown to black spot on the pod, which spreads rapidly in all directions and eventually covers the whole pod. The beans become infected internally about 15 days after the initial infection and are soon of no commercial value. Several other forest species are known to become infected and to maintain the pathogen at low levels but the impact on black pod disease itself is not fully understood.

P. palmivora also causes bud rot and fruit rot of coconut in wildland and agricultural settings. On other hosts, P. palmivora causes a range of symptoms such as root rot, cankers, and leaf blight. Economically important agricultural crops include durian, citrus, rubber, mango, black pepper, and papaya.

Educational materials

• Phytophthora palmivora
• STCP: Farmer training guide on ICPM cocoa
• Organic cocoa production: a guide for farmer field schools in Sierra Leone
• African organic agriculture training manual 09-14
• Diversity and management of Phytophthora in Southeast Asia
• 2014 Florida citrus pest management guide: Brown rot of fruit

References

Alconero R, Albuquerque F, Almeyda N, Santiago AG. 1972. Phytophthora foot rot of black pepper in Brazil and Puerto Rico. Phytopathology 62:144-148. doi: 10.1094/Phyto-62-144

Ashby SF. 1929. Strains and taxonomy of Phytophthora palmivora Butler (P. Faberi Maubl.). Transactions of the British Mycological Society 14(1-2):18-38. doi: 10.1016/S0007-1536(29)80025-3

Balci Y, Balci S, Blair JE, Park S-Y, Kang S, Macdonald WL. 2008. Phytophthora quercetorum sp. nov., a novel species isolated from eastern and north-central USA oak forest soils. Mycological Research 112(8):906-916. doi: 10.1016/j.mycres.2008.02.008

Barber PA, Paap T, Burgess TI, Dunstan W, Hardy GESJ. 2013. A diverse range of Phytophthora species are associated with dying urban trees. Urban Forestry & Urban Greening 12(4):569-575. doi: 10.1016/j.ufug.2013.07.009

Barnard EL, Mitchell DJ. 1993. Phytophthora basal canker of red maple. Florida Department of Agriculture & Consumer Services. Division of Plant Industry, Gainseville, FL. http://www.freshfromflorida.com/content/download/11368/144504/pp361.pdf

Blaha G, Hall G, Warokka JS, Concibido E, Ortiz-Garcia C. 1994. Phytophthora isolates from coconut plantations in Indonesia and Ivory Coast: characterization and identification by morphology and isozyme analysis. Mycological Research 98:1379-1389. http://www.sciencedirect.com/science/article/pii/S0953756209810678

Bowers JH, Bailey BA, Hebbar PK, Sanogo S, Lumsden RD. 2001. The impact of plant diseases on world chocolate production. Plant Health Progress. doi: 10.1094/PHP-2001-0709-01-RV

Brasier CM, Griffin MJ. 1979. Taxonomy of Phytophthora palmivora on cocoa. Transactions of the British Mycological Society 72(1):111-143. doi: 10.1016/S0007-1536(79)80015-7

Brooks F. 2005. Phytophthora palmivora. Pests and Diseases of American Samoa No. 12. American Samoa Community College Community & Natural Resources Cooperative Research and Extension. 2 pp. http://www2.ctahr.hawaii.edu/adap/ASCC_LandGrant/Dr_Brooks/BrochureNo12.pdf

Butler EJ. 1924. Bud rot of coconut and other palms. Report of Imperial Botanical Conference pp. 145-147.

Butler EJ. 1918–1919. Report of the imperial mycologist, Science Report Institute Pusa. 82 pp.

Chen W, Djama ZR, Coffey MD, Martin FN, Bilodeau GJ, Radmer L, Denton G, Lévesque AC. 2013. Membrane-based oligonucleotide array developed from multiple markers for the detection of many Phytophthora species. Phytopathology 103(1):43-54. doi: 10.1094/PHYTO-04-12-0092-R

Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM. 2000. A molecular phylogeny of Phytophthora and related Oomycetes. Fungal Genetics and Biology 30:17-32. doi:10.1006/fgbi.2000.1202

Cooke DEL, Duncan JM. 1997. Phylogenetic analysis of Phytophthora species based on ITS1 and ITS2 sequences of the ribosomal RNA gene repeat. Mycological Research 101(6):667-677. doi: 10.1017/S0953756296003218

Dakwa JT. 1974. The occurrence of Phytophthora palmivora (Butl.) Butl. in soil in Ghana. Ghana Journal of Agriculture Science 7:37-41. http://gains.org.gh/articles/gjas_v7_1_p37_41.pdf

Despreaux D. 2004. Phytophthora diseases of Theobroma cacao. Pages 15–44 in: Cilas C, Despreaux D., eds. Improvement of cocoa tree resistance to Phytophthora diseases. CIRAD, Montpellier, France.

dos Santos ÃF, Luz EDMN, Finato PD, Tessmann DJ, Vida JB. 2004. First report of stem rot on peach palm caused by Phytophthora palmivora in the state of Paraná. Fitopatologia Brasileira 29(6):680-682. doi: 10.1590/S0100-41582004000600016

Erwin DC, Ribeiro OK. 1996. Phytophthora diseases worldwide. APS Press, St. Paul, MN. 562 pp.

Graham JH, Timmer LW, Dewdney MM. 2013. 2014 Florida Citrus Pest Management Guide: Brown Rot of Fruit. University of Florida IFAS Extension Publication PP-148. 2 pp. http://edis.ifas.ufl.edu/pdffiles/CG/CG02200.pdf

Hislop EC. 1963. Studies on the chemical control of Phytophthora palmivora (Butl.) Butl. on Theobroma cacao L. in Nigeria. Annals of Applied Biology 52(3):465-480. doi: 10.1111/j.1744-7348.1963.tb03770.x

Holderness M. 1990. Efficacy of neutralised phosphonic acid (phosphorous acid) against Phytophthora palmivora pod rot and canker of cocoa. Australasian Plant Pathology 19(4):130-131. doi: 10.1071/APP9900130

Jung T, Cooke DEL, Blaschke H, Duncan JM, Oßwald W. 1999. Phytophthora quercina sp. nov., causing root rot of European oaks. Mycological Research 103(7):785-98. doi: 10.1017/S0953756298007734

Kroon LPNM, Bakker FT, van den Bosch GBM, Bonants PJM, Flier WG. 2004. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 41(8):766-782. doi:10.1016/j.fgb.2004.03.007

Mchau GRA, Coffey MD. 1994. Isozyme diversity in Phytophthora palmivora: evidence for a southeast Asian centre of origin. Mycological Research 98(9):1035-1043. doi: 10.1016/S0953-7562(09)80430-9

Opoku IY, Akrofi AY, Appiah AA. 2007. Assessment of sanitation and fungicide application directed at cocoa tree trunks for the control of Phytophthora black pod infections in pods growing in the canopy. European Journal of Plant Pathology 117(2):167-175. doi: 10.1007/s10658-006-9082-8

Oudemans P, Coffey MD. 1991. A revised systematics of twelve papillate Phytophthora species based on isozyme analysis. Mycological Research 95(9):1025-1046. doi:10.1016/S0953-7562(09)80543-1

Reinking OA. 1923. Comparative study of Phytophthora faberi on coconut and cacao in the Philippine Islands. Journal of Agricultural Research 25:267-284. http://worldcocoafoundation.org/wp-content/files_mf/reinking1923.pdf

Ridge GA, Jeffers SN, Bridges WC, White SA. 2014. In situ production of zoospores by five species of Phytophthora in aqueous environments for use as inocula. Plant Disease 98(4):551-558. doi: 10.1094/PDIS-06-13-0591-RE

Rosenbaum J. 1917. Studies of the genus Phytophthora. Journal of Agricultural Research 8(7):233-276.

Seal JL. 1928. Coconut bud rot in Florida. University of Florida Agricultural Experiment Station Technical Bulletin 199. 87 pp. http://ufdc.ufl.edu/UF00027165/00001

Stamps DJ, Waterhouse GM, Newhook FJ, Hall GS. 1990. Revised tabular key to the species of Phytophthora. Mycological Papers 162:1-28.