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Resistant and susceptible cacao genotypes exhibit defense gene polymorphism and unique early responses to Phytophthora megakarya inoculation

  • Désiré N. Pokou
  • Andrew S. Fister
  • Noah Winters
  • Mathias Tahi
  • Coulibaly Klotioloma
  • Aswathy Sebastian
  • James H. Marden
  • Siela N. Maximova
  • Mark J. GuiltinanEmail author
Article

Abstract

Key message

Key genes potentially involved in cacao disease resistance were identified by transcriptomic analysis of important cacao cultivars. Defense gene polymorphisms were identified which could contribute to pathogen recognition capacity.

Abstract

Cacao suffers significant annual losses to the water mold Phytophthora spp. (Oomycetes). In West Africa, P. megakarya poses a major threat to farmer livelihood and the stability of cocoa production. As part of a long-term goal to define key disease resistance genes in cacao, here we use a transcriptomic analysis of the disease-resistant cacao clone SCA6 and the susceptible clone NA32 to characterize basal differences in gene expression, early responses to infection, and polymorphisms in defense genes. Gene expression measurements by RNA-seq along a time course revealed the strongest transcriptomic response 24 h after inoculation in the resistant genotype. We observed strong regulation of several pathogenesis-related genes, pattern recognition receptors, and resistance genes, which could be critical for the ability of SCA6 to combat infection. These classes of genes also showed differences in basal expression between the two genotypes prior to infection, suggesting that prophylactic expression of defense-associated genes could contribute to SCA6’s broad-spectrum disease resistance. Finally, we analyzed polymorphism in a set of defense-associated receptors, identifying coding variants between SCA6 and NA32 which could contribute to unique capacities for pathogen recognition. This work is an important step toward characterizing genetic differences underlying a successful defense response in cacao.

Keywords

Theobroma cacao Phytophthora megakarya Defense response Transcriptome 

Notes

Acknowledgements

Thank you to Dr. Craig Praul at the Penn State Genomics Core facility for providing library preparation and transcriptome sequencing services. Thank you to Dr. Istvan Albert at the Penn State Bioinformatics Support Center for advice regarding processing of RNA-seq data. Thank you to Lena Sheaffer for assistance with project management. Thank you to Affian Kacou and Amah Yao for arranging the experiment in shade net house. We thank Irie Boua, Herve Kouakou, Lassana Bakayoko, and Koffi Cyrille at CNRA for their support in maintaining plant and inoculating plant material.

Author contributions

DNP designed the experiments, oversaw generation of plant material, inoculated and collected leaf samples, extracted RNA, and drafted the manuscript. ASF inoculated and collected samples, performed statistical analyses of RNA-seq data, and wrote and edited the manuscript. NW analyzed polymorphism in the cacao genotypes, identified candidate defense-associated receptor genes, and wrote and edited the manuscript. MT propagated the grafted plants from stock trees in the germplasm collection. KC prepared pathogen inoculum and zoospore suspension for inoculation. AS performed bioinformatic analysis of RNA-seq data and calculated differential gene expression. JHM contributed to data analyses and edited the manuscript. SNM and MJG contributed to experimental design, oversaw experimental progress, and contributed to manuscript writing and editing.

Funding

This work was supported by the Fulbright International exchange Program Number G-1-0005, a Grant from the USDA Foreign Agriculture Service, The Pennsylvania State University College of Agricultural Sciences, the Huck Institutes of the Life Sciences, the Penn State Endowed Program in Molecular Biology of Cacao, NSF Plant Genome Research Award 1546863 and by the USDA National Institute of Food and Agriculture, Federal Appropriations under Project PEN04569 and Accession Number 1003147.

Supplementary material

11103_2019_832_MOESM1_ESM.pdf (57 kb)
Supplemental Figure S1. Shade net house layout. Pink and blue stripes represent rows of SCA6 and NA32 plants. Black borders around striped areas represent border plants (either genotype) which were excluded from sampling. 1 m wide walking paths between blocks are indicated. (PDF 57 KB)
11103_2019_832_MOESM2_ESM.pdf (16 kb)
Supplemental Figure S2. Heatmap of transcriptome correlations. Analysis is based on mean expression value calculated from biological replicates. S/N indicates genotype; 0,6,24,72 indicates time point; C/P indicates control or pathogen treatment. (PDF 16 KB)
11103_2019_832_MOESM3_ESM.pdf (47 kb)
Supplemental Figure S3. Heatmap of transcriptome correlations. S/N indicates genotype; 0,6,24,72 indicates time point; C/P indicates control or pathogen treatment. Final number (1-5) indicates biological replicate. (PDF 46 KB)
11103_2019_832_MOESM4_ESM.pdf (99 kb)
Supplemental Figure S4. Scatterplots showing correlations between expression levels of A) defense associated receptors and B) PR genes between NA32 and SCA6 samples collected at time zero. Measurements are the average log10 transformed DESeq2 normalized counts calculated from eight replicates at time zero. (PDF 98 KB)
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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Désiré N. Pokou
    • 1
  • Andrew S. Fister
    • 2
  • Noah Winters
    • 3
    • 4
  • Mathias Tahi
    • 1
  • Coulibaly Klotioloma
    • 1
  • Aswathy Sebastian
    • 4
    • 5
  • James H. Marden
    • 4
    • 6
  • Siela N. Maximova
    • 2
    • 4
  • Mark J. Guiltinan
    • 2
    • 4
    Email author
  1. 1.Centre National de Recherche Agronomique, Laboratoire Central de BiotechnologieAbidjan 01Côte d’Ivoire
  2. 2.Department of Plant Sciences, Life Sciences BuildingPennsylvania State UniversityUniversity ParkUSA
  3. 3.Intercollege Graduate Degree Program in EcologyPennsylvania State UniversityUniversity ParkUSA
  4. 4.The Huck Institutes of the Life SciencesThe Pennsylvania State UniversityUniversity ParkUSA
  5. 5.Department of Biochemistry and Molecular BiologyPennsylvania State UniversityUniversity ParkUSA
  6. 6.Department of BiologyPennsylvania State UniversityUniversity ParkUSA

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