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Structural and Functional Genomics of the Resistance of Cacao to Phytophthora palmivora.

ABSTRACT: Black pod disease, caused by Phytophthora spp., is one of the main diseases that attack cocoa plantations. This study validated, by association mapping, 29 SSR molecular markers flanking to QTL (Quantitative Trait Loci) associated with Phytophthora palmivora Butler (Butler) (PP) resistance, in three local ancient varieties of the Bahia (Comum, Pará, and Maranhão), varieties that have a high potential in the production of gourmet chocolate. Four SSR loci associated with resistance to PP were detected, two on chromosome 8, explaining 7.43% and 3.72% of the Phenotypic Variation (%PV), one on chromosome 2 explaining 2.71%PV and one on chromosome 3 explaining 1.93%PV. A functional domains-based annotation was carried out, in two Theobroma cacao (CRIOLLO and MATINA) reference genomes, of 20 QTL regions associated with cocoa resistance to the pathogen. It was identified 164 (genome CRIOLLO) and 160 (genome MATINA) candidate genes, hypothetically involved in the recognition and activation of responses in the interaction with the pathogen. Genomic regions rich in genes with Coiled-coils (CC), nucleotide binding sites (NBS) and Leucine-rich repeat (LRR) domains were identified on chromosomes 1, 3, 6, 8, and 10, likewise, regions rich in Receptor-like Kinase domain (RLK) and Ginkbilobin2 (GNK2) domains were identified in chromosomes 4 and 6.

SUBMITTER: Mucherino Munoz JJ

PROVIDER: S-EPMC8398157 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The oomycete pathogen Phytophthora palmivora, which causes black pod rot (BPR) on cacao (Theobroma cacao L.), is responsible for devastating yield losses worldwide. Genetic variation in resistance to Phytophthora spp. is well documented among cacao cultivars, but variation has also been observed in the incidence of BPR even among trees of the same cultivar. In light of evidence that the naturally occurring phyllosphere microbiome can influence foliar disease resistance in other host-pathogen systems, it was hypothesized that differences in the phyllosphere microbiome between two field accessions of the cultivar Gainesville II 164 could be responsible for their contrasting resistance to P. palmivora. Bacterial alpha diversity was higher but fungal alpha diversity was lower in the more resistant accession MITC-331, and the accessions harbored phyllosphere microbiomes with distinct community compositions. Six bacterial and 82 fungal amplicon sequence variants (ASVs) differed in relative abundance between MITC-333 and MITC-331, including bacterial putative biocontrol agents and a high proportion of fungal pathogens, and nine fungal ASVs were correlated with increased lesion development. The roles of contrasting light availability and host mineral nutrition, particularly potassium, are also discussed. Results of this preliminary study can be used to guide research into microbiome-informed integrated pest management strategies effective against Phytophthora spp. in cacao. IMPORTANCE Up to 40% of the world's cacao is lost each year to diseases, the most devastating of which is black pod rot, caused by Phytophthora palmivora. Though disease resistance is often attributed to cacao genotypes (i.e., disease-resistant rootstocks), this study highlights the role of the microbiome in contributing to differences in resistance even among accessions of the same cacao cultivar. Future studies of plant-pathogen interactions may need to account for variation in the host microbiome, and optimizing the cacao phyllosphere microbiome could be a promising new direction for P. palmivora resistance research.

Project description:Black pod rot, caused by Phytophthora palmivora, is a devastating disease of Theobroma cacao L. (cacao) leading to huge losses for farmers and limiting chocolate industry supplies. To understand resistance responses of cacao leaves to P. palmivora, Stage 2 leaves of genotypes Imperial College Selection 1 (ICS1), Colección Castro Naranjal 51 (CCN51), and Pound7 were inoculated with zoospores and monitored for symptoms up to 48 h. Pound7 consistently showed less necrosis than ICS1 and CCN51 48 h after inoculation. RNA-Seq was carried out on samples 24 h post inoculation. A total of 24,672 expressed cacao genes were identified, and 2,521 transcripts showed induction in at least one P. palmivora-treated genotype compared to controls. There were 115 genes induced in the P. palmivora-treated samples in all three genotypes. Many of the differentially expressed genes were components of KEGG pathways important in plant defense signal perception (the plant MAPK signaling pathway, plant hormone signal transduction, and plant pathogen interactions), and plant defense metabolite biosynthesis (phenylpropanoid biosynthesis, α-linolenic acid metabolism, ethylene biosynthesis, and terpenoid backbone biosynthesis). A search of putative cacao resistance genes within the cacao transcriptome identified 89 genes with prominent leucine-rich repeat (LRR) domains, 170 protein kinases encoding genes, 210 genes with prominent NB-ARC domains, 305 lectin-related genes, and 97 cysteine-rich RK genes. We further analyzed the cacao leaf transcriptome in detail focusing on gene families-encoding proteins important in signal transduction (MAP kinases and transcription factors) and direct plant defense (Germin-like, ubiquitin-associated, lectin-related, pathogenesis-related, glutathione-S-transferases, and proteases). There was a massive reprogramming of defense gene processes in susceptible cacao leaf tissue after infection, which was restricted in the resistant genotype Pound7. Most genes induced in Pound7 were induced in ICS1/CCN51. The level of induction was not always proportional to the infection level, raising the possibility that genes are responding to infection more strongly in Pound7. There were also defense-associated genes constitutively differentially expressed at higher levels in specific genotypes, possibly providing a prepositioned defense. Many of the defense genes occur in blocks where members are constitutively expressed at different levels, and some members are induced by Ppal infection. With further study, the identified candidate genes and gene blocks may be useful as markers for breeding disease-resistant cacao genotypes against P. palmivora.

Project description:Phytophthora megakarya (Pmeg) and Phytophthora palmivora (Ppal) cause black pod rot of Theobroma cacao L. (cacao). Of these two clade 4 species, Pmeg is more virulent and is displacing Ppal in many cacao production areas in Africa. Symptoms and species specific sporangia production were compared when the two species were co-inoculated onto pod pieces in staggered 24 h time intervals. Pmeg sporangia were predominantly recovered from pod pieces with unwounded surfaces even when inoculated 24 h after Ppal. On wounded surfaces, sporangia of Ppal were predominantly recovered if the two species were simultaneously applied or Ppal was applied first but not if Pmeg was applied first. Pmeg demonstrated an advantage over Ppal when infecting un-wounded surfaces while Ppal had the advantage when infecting wounded surfaces. RNA-Seq was carried out on RNA isolated from control and Pmeg and Ppal infected pod pieces 3 days post inoculation to assess their abilities to alter/suppress cacao defense. Expression of 4,482 and 5,264 cacao genes was altered after Pmeg and Ppal infection, respectively, with most genes responding to both species. Neural network self-organizing map analyses separated the cacao RNA-Seq gene expression profiles into 24 classes, 6 of which were largely induced in response to infection. Using KEGG analysis, subsets of genes composing interrelated pathways leading to phenylpropanoid biosynthesis, ethylene and jasmonic acid biosynthesis and action, plant defense signal transduction, and endocytosis showed induction in response to infection. A large subset of genes encoding putative Pr-proteins also showed differential expression in response to infection. A subset of 36 cacao genes was used to validate the RNA-Seq expression data and compare infection induced gene expression patterns in leaves and wounded and unwounded pod husks. Expression patterns between RNA-Seq and RT-qPCR were generally reproducible. The level and timing of altered gene expression was influenced by the tissues studied and by wounding. Although, in these susceptible interactions gene expression patterns were similar, some genes did show differential expression in a Phytophthora species dependent manner. The biggest difference was the more intense changes in expression in Ppal inoculated wounded pod pieces further demonstrating its rapid progression when penetrating through wounds.

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Structural and Functional Genomics of the Resistance of Cacao to Phytophthora palmivora.

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