Abstract
Penja pepper (Piper nigrum) produced in Cameroon has long been recognized for its exceptional organoleptic quality. The pepper vine is grown using a support tree (Spondias mombin) in Cameroon. A root disease is associated with plant deaths in both plants. The disease symptoms are characterized by collar cracking and gummosis and the disease was tentatively identified as Armillaria root rot. In this work the extent of the problem was characterized by surveying 35 farms in Cameroon. Samples were taken from diseased support trees and pepper vines. Support trees exhibiting typical symptoms were found in approximately one third of the surveyed farms. In these farms, disease incidence and Pepper vine mortality ranged from 1.3 to 50% and 1.2 to 87.7%, respectively. Analysis of the ribosomal internal transcribed spacer region (ITS) locus suggested that the isolates collected from S. mombin and P. nigrum are most likely, which is a first for both hosts, represented by Armillaria camerunensis (Henn.) Volk & Burdsall, a fungus previously associated with declining cacao trees in Cameroon. Given the increasing demand for Penja pepper and the great damaging potential of this root rot, research on management strategies should be prioritized.
Similar content being viewed by others
References
Ahmad N, Fazal H, Abbasi H, Farooq S, Ali M, Ali Khan M (2012) Biological role of Piper nigrum L. (Black pepper): A review. Asian Pacific Journal of Tropical Biomedicine 2:S1945-S1953
Anandaraj M, Ramana KV, Sarma YR (1996) Sequential inoculation of Phytophthora capsici, Radopholus similis and Meloidogyne incognita in causing slow decline of black pepper. Indian Phytopathology 49:297–299
Cardoso DE, Albuquerque FC (1979) Podridão radicular e tombamento de plântulas de pimenta-do-reino em videira causada por Pythium splendens. Fitopatologia Brasileira 4:17–23
Coetzee MPA, Brenda D, Wingfield BP, Wingfield MJ (2005) Phylogenetic analyses of DNA sequences reveal species partitions amongst isolates of Armillaria from Africa. Mycological Research 109:1223–1234
Costa SS, Moreira GM, Pfenning LH (2017) Development of a PCR protocol for the identification and detection of Fusarium solani f. sp. piperis from soil and roots of black pepper (Piper nigrum). Tropical Plant Pathology 42:55–59
Dade HA (1927) ‘Collar crack of cacao’: Armillaria mellea (Vahl.) Fr. Bulletin of Department of Agriculture Gold Coast. No. 5. 22p
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772
Denman S, Coetzee MPA, Wingfield BD, Wingfield MJ, Crous PW (2000) Armillaria root rot. A new disease of cut- flower proteas in South Africa. Fynbos Research 33:1–6
Faostat (2017) http://www.fao.org/faostat/en/#data (last Accessed 5/11/2019)
Ford KL, Henricot B, Baumgartner K, Bailey AM, Foster GD (2017) A faster inoculation assay for Armillaria using herbaceous plants. The Journal of Horticultural Science and Biotechnology 92:39–47
Hennings P (1895) Fungi camerunenses I. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 22:72–111
IPC (2017) http://www.ipcnet.org/index_n.php (last Accessed 5/11/2019)
Keuh TK (1990) Major diseases of black pepper and their management. Planter, Kuala Lumpur 66:59–69
Koch RA, Wilson AW, Séné O, Henkel TW, Aime C (2017) Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster. BMC Evolutionary Biology 17:33
Mbodiam BR (2019) Investir au Cameroun : agriculture, l’avenir du poivre de Penja en peril à cause des bioagresseurs qui détruisent les plantations. Consulted on August 23, 2019 [on line] URL https:// www.investiraucameroun.com
Meghwal M, Goswami TK (2012) Chemical composition nutritional, medical and functional properties of black pepper: a review. 1:172. https://doi.org/10.4172/scientificreports.172
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees in Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp 1–8 https://dl.acm.org/citation.cfm?id=2016785 (last Accessed 13/11/2019)
Möller EM, Bahnweg G, Sandermann H, Geiger HH (1992) A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Research 20:6115–6116
Otieno W, Jeger M, Termorshuizen A (2003) Effect of infesting soil with Trichoderma harzianum and amendment with coffee pulp on survival of Armillaria. Biological Control 26:293–301
Petchayo TS, Mfegue VC, Nguefack J, Tchotet TJM, Begoude BAD, Ducamp M, Djeugap JF, Ten Hoopen GM (2015) Penja pepper under threat in Cameroon! Poster Presented at the 6th Congress of European microbiologists (FEMS 2015) 7-11 June 2015 in Maastricht, the Netherlands
Ramana KV, Santhosh JE (2000) Nematode induced diseases of black pepper. In: Ravindran PN (ed) Black pepper, Piper nigrum. CRC Press, Amsterdam, pp 269–288
Ramana KV, Mohandas C, Balakrishnan R (1987) Role of plant parasitic nematodes in the slow wilt disease complex of black pepper (Piper nigrum L.) in Kerala. Indian Journl of Nematology 17:225–230
Ravindran PN (2000) Black pepper, Piper nigrum L. CRC Press, Amsterdam, p 526
Rishbeth J (1980) Armillaria on cacao in Sao Tome. Tropical Agriculture 57:155–165
Roux J, Coetzee MPA (2016) Armillaria root rot of Theobroma cacao. In: Bailey BA, Meinhardt LW (eds) Cacao diseases: a history of old enemies and new encounters. Springer International Publishing, Switzerland, pp 429–447.
Roux J, Mbenoun M, Misse C, Coetzee MPA, Begoude DA, Wingfield MJ (2012) Molecular identification of Armillaria isolates associated with root-rot disease of cacao in Cameroon. 17th international Cocoa Research Congress (COPAL). 15-20 Oct. Yaoundé, Cameroon
Shahnazi S, Meon S, Vadamalai G, Ahmad K, Nejat N (2012) Morphological and molecular characterization of Fusarium spp. associated with yellowing disease of black pepper (Piper nigrum L.) in Malaysia. Journal of General Plant Pathology 78:160–169
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms, Diversity and Evolution 12:335–337
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
Tchotet Tchoumi JM, Coetzee MPA, Vivas M, Rajchenberg M, Roux J (2017) Wood-rotting basidiomycetes associated with declining native trees in timber-harvesting compartments of the garden route National Park of South Africa. Austral Ecology 42:947–963
Thomidis T, Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36:49–51
Truong NV, Burgess LW, Liew ECY (2008) Prevalence and aetiology of Phytophthora foot rot of black pepper in Vietnam. Australasian Plant Pathology 37:431
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
Worrall JJ (1991) Media for selective isolation of hymenomycetes. Mycologia 83:296–202
Worrall JJ (2004) Armillaria root disease. The Plant Health Instructor. American Phytopathological Society. https://doi.org/10.1094/PHI-I-2004-0706-01
Acknowledgements
The authors would like to thank the Penja Pepper Geographical Indication Group (IGPP) producers, in particular René Claude Metomo Elogo (President of Association) and Emmanuel Nzenowo (Executive Secretary) for allowing database and field access. We also thank Fokou Rodrigue, Diazem Clovis, Tocké, Ngonga Florian, and Njonkam Ferdinand, agricultural technicians who assisted in the surveys. Funding and resources were provided by CIRAD, IRAD, the University of Pretoria and through the “Debt reduction-development contract (C2D) France Cameroon” Poivre de Penja project. The authors were free to publish any or all results originating from their work.
Author information
Authors and Affiliations
Contributions
Conceptualization: Petchayo TS, M Ndoumbé Nkeng, GM ten Hoopen; Methodology: Petchayo TS, JM Tchotet Tchoumi, M Ndoumbé Nkeng, GM ten Hoopen; Investigation: Petchayo TS, JM Tchotet Tchoumi, M. Mbenoun, GM ten Hoopen; Formal analysis: Petchayo TS, JM Tchotet Tchoumi, J Roux, M Mbenoun, M Ndoumbé Nkeng, GM ten Hoopen; Resources: J Roux, GM ten Hoopen; Funding acquisition: CV Mfegue, GM ten Hoopen; Project administration: S Nyassé; Supervision: J Nguefack, BAD Begoude, GM ten Hoopen; Writing original draft: Petchayo TS, GM ten Hoopen; Manuscript revision: Petchayo TS, GM ten Hoopen, M Mbenoun, JM Tchotet Tchoumi, J Roux. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Petchayo Tigang, S., Tchotet Tchoumi, J.M., Roux, J. et al. Armillaria root rot threatens Cameroon’s Penja pepper (Piper nigrum L.). Trop. plant pathol. 45, 534–543 (2020). https://doi.org/10.1007/s40858-020-00361-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-020-00361-w