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Numerous Clones Resistant to Phytophthora Palmivora in the ‘‘Guiana’’ Genetic Group of Theobroma Cacao L

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Numerous Clones Resistant to Phytophthora Palmivora in the ‘‘Guiana’’ Genetic Group of Theobroma Cacao L Numerous Clones Resistant to Phytophthora palmivora in the ‘‘Guiana’’ Genetic Group of Theobroma cacao L Jean-Marc Thevenin1*, Vivien Rossi2, Michel Ducamp3, Fabien Doare1, Virgile Condina1, Philippe Lachenaud1 1 CIRAD, UPR Bioagresseurs : Analyse et Maıˆtrise du Risque, Kourou, Guyane, France, 2 CIRAD, UMR Ecofog, Kourou, Guyane, France, 3 CIRAD, UMR BGPI, Montpellier, France Abstract Cocoa black pod rot, a disease caused by Stramenopiles of the genus Phytophthora, and particularly by the pan-tropical species P. palmivora, causes serious production losses worldwide. In order to reduce the impact of these pests and diseases, preference is given to genetic control using resistant varieties and, to that end, breeders seek sources of resistance in wild cocoa trees. For instance, surveys of spontaneous cocoa trees in French Guiana between 1985 and 1995 led to the collection of abundant plant material forming a particular genetic group (the ‘‘Guiana’’ group). Following numerous one-off studies demonstrating the merits of this group as a source of resistance to Phytophthora, this article presents the results of a comprehensive study assessing the resistance of 186 ‘‘Guiana’’ clones in relation to the Guianan strain (GY 27) of P. palmivora. This study, undertaken in French Guiana, using an efficient methodology (ten series of tests and a statistical test adapted to the ordinal nature of the data) confirmed that the ‘‘Guiana’’ genetic group does indeed constitute an important source of resistance to P. palmivora, though with some variations depending on the demes of origin. Numerous clones (59) proved to be as resistant as the SCAVINA 6 resistance control, whilst nine were statistically more resistant. The ‘‘Resistant’’ and ‘‘Moderately Resistant’’ Guianan clones totalled 108 (58% of the total tested). Some of the clones more resistant than SCAVINA 6 could be incorporated into numerous cocoa breeding programmes, particularly those that also display other notable qualities. The same applies for numerous other clones equivalent to SCAVINA 6, especially the ‘‘elite’’’ clones GU 134-B, GU 139-A and GU 285-A. Citation: Thevenin J-M, Rossi V, Ducamp M, Doare F, Condina V, et al. (2012) Numerous Clones Resistant to Phytophthora palmivora in the ‘‘Guiana’’ Genetic Group of Theobroma cacao L. PLoS ONE 7(7): e40915. doi:10.1371/journal.pone.0040915 Editor: Randall P. Niedz, United States Department of Agriculture, United States of America Received January 16, 2012; Accepted June 14, 2012; Published July 26, 2012 Copyright: ß 2012 Thevenin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was part of the FEDER Convergence project (European Regional Development Fund) 2009–2012, the ‘‘Dicacao’’ project (Diversity of wild cocoa trees in French Guiana, ans associated endophytes. Merits and use in disease control). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction [2,3], which make up the particular ‘‘Guiana’’ genetic group [4], have been subjected to early tests of resistance to P. palmivora in the Cocoa black pod rot, a disease caused by Stramenopiles of the laboratory [5]. genus Phytophthora, and particularly the pan-tropical species The potential merits for genetic control of P. palmivora of palmivora, causes serious production losses in all cocoa growing some clones in the ‘‘Guiana’’ group, i.e. those originating from zones, varying from 30 to 90% depending on conditions [1]. the Camopi and Tanpok river basins and named ‘‘GU’’ clones Indeed, major losses result from infection of pods. Zoospores (‘‘GU’’ stands for ‘‘GUyane’’) [2], have already been revealed released in free water are spread to the pod. A brown lesion by early tests on leaf discs in the laboratory, in Ivory Coast, appears 2–3 days after penetration of the germ tube in the Ghana and France, but on limited samples [5–9]. In addition, mesocarp and develops quickly into a large brown lesion. Beans tests carried out by CIRAD in Montpellier (France) with P. can be more or less affected depending on the age of the pod when megakarya, a species existing only in Africa and currently in an the attack occurs. Losses can also be indirect as Phytophthora can invasive phase and tending to take over from P. palmivora on attack young leaves, flowers and roots, but also trunk and branches cocoa trees, involving 59 genotypes from 13 populations causing cankers. (originating from the basins of five rivers), revealed the Using varieties that are resistant to this scourge is an essential exceptional merits of these cocoa trees, with 61% of the clones ecological and economic solution for integrated and sustainable proving ‘‘Resistant’’ or ‘‘Very Resistant’’ [10]. control. Resistance of cacao to Phytophthora is of horizontal type. Our aims were therefore (i) to carry out an exhaustive Only few resistant clones of various origins exist at the time being. laboratory test on the ‘‘Guiana’’ clones held in the Sinnamary Breeders are seeking sources of resistance in wild cocoa trees, in core collection (i.e. 186 clones) using a local strain of P. palmivora the species’ zones of origin (Amazonia and the Guianan Shield) in isolated in French Guiana (ii) to select resistant clones that could order to create, in their own producing countries, hybrids that will be used directly or as parents in breeding programmes. be locally tested. For instance, some wild cocoa trees in southeastern French Guiana, surveyed between 1985 and 1995 PLoS ONE | www.plosone.org 1 July 2012 | Volume 7 | Issue 7 | e40915 Resistance of Cacao ‘‘Guiana’’ to Phytophthora Materials and Methods megakarya [10], GU 138-A very susceptible to P. palmivora [9] and GF 24, classed susceptible to P. palmivora [8]. Plant Material Clones were randomised in a plot maintained under artificial The plant material studied consisted of 189 clones, comprising shade to homogenize the environmental conditions, particularly 186 clones of the ‘‘Guiana’’ genetic group and three representa- lighting [17]. It was a 0.135 ha budwood plot planted at Paracou- tives of other groups, used as controls. Combi in 2004–2005, with spacings of 2 m61.5 m, where the The ‘‘Guiana’’ clones came from wild mother-trees collected in trees were regularly pruned each year. Each clone was represented the basins of the Oyapok (called Kerindioutou in its upper by two neighbouring trees, except SCA 6 and ELP 40-B reaches), Camopi, Euleupousing, Yaloupi and Tanpok rivers, in represented each by two pairs of neighbouring trees. The French Guiana [2,3]. They were either cloned on site during the edapho-climatic conditions at the Paracou-Combi station were surveys or, mostly, selected and cloned in open-pollinated described in earlier work [18]. progenies after individual studies in the Sinnamary ex situ collection. The 186 clones represented 17 demes of natural Fungal Material populations, plus a subspontaneous clone (Table 1). These clones Strain GY 27 used for inoculation was isolated from an infected included 24 ortets,pre-selected after 10 years of observations at pod harvested from clone NA 32, in the Paracou-Combi Sinnamary for their high productivity and their excellent field collection. It was confirmed as belonging to the species P. palmivora performance against pod rot diseases (Table 2). All necessary permits to conduct the surveys in the primary by studying ITS sequences (using primers ITS 1 and ITS 4). This forest were obtained from the Representative of the French strain was of sexual compatibility type A2 like all the P. palmivora government, i.e. the Pre´fet de Guyane. No specific permit were strains isolated in this collection. It displayed the highest level of then required for observations as the material was planted in the aggressiveness of all the P. palmivora strains isolated in the Cirad research station in French Guiana. Theobroma cacao is not an Sinnamary plots. This primary evaluation was carried out on a endangered or protected species. range of clones displaying different levels of resistance to this The resistance control was the SCAVINA 6 clone ( = SCA 6), species (data not shown). the international reference used in tests involving P. palmivora [11– The strain was kept in a fungus culture collection by successive 15]. This control was duplicated in the tests (2 samples). In transfers every 6 to 8 weeks on diluted V8 medium (200 ml/L). In addition, two other clones were used as controls: the resistant order to maintain its pathogenicity, strain GY 27 was inoculated ‘‘Guiana’’ clone GU 255-V [8] and the moderately resistant approximately every three months on a mature green pod of clone Upper Amazon clone T60/887 [16]. NA 32 and left to incubate at 24uC and at 100% humidity for 4 to Four clones from French Guiana were used as ‘‘susceptibility 5 days. The strain was then isolated again under sterile conditions indicators’’, to check that the inoculation tests were working on water-agar medium (15 g of agar/L) in a Petri dish, then four properly: ELP 40-B and OYA 2-B, highly susceptible to P. days after on 1/5 V8 medium (40 ml/L). For inoculum preparation (sporocyst and zoospore formation), GY 27 was grown on V8 1/5+ Beta sitosterol medium for 3 days Table 1. Distribution by deme of the 186 ‘‘Guiana’’ clones in total darkness at 24uC, then for 7 days in indirect light at 24uC. studied. Zoospores were released after thermal shock (cold water +20 min at 4uC). The zoospore suspension was then calibrated at 300,000 zoospores/ml using a Malassez counting chamber.
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