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Transcriptome profiling of cashew apples (Anacardium occidentale) genotypes reveals specific genes linked to firmness and color during pseudofruit development

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We found 34 and 71 key genes potentially involved in flavonoid biosynthesis and cell wall disassembly, respectively, which could be associated with specific peel coloration and softening of each genotype.

Abstract

Cashew apple (Anacardium occidentale) has a great economic importance worldwide due to its high nutritional value, peculiar flavor and aroma. During ripening, the peduncle develops different peel color and becomes quickly fragile due to its oversoftening, impacting its consumers’ acceptance. In view of this, the understanding about its transcriptional dynamics throughout ripening is imperative. In this study, we performed a transcriptome sequencing of two cashew apple genotypes (CCP 76 and BRS 265), presenting different firmness and color peel, in the immature and ripe stages. Comparative transcriptome analysis between immature and ripe cashew apple revealed 4374 and 3266 differentially expressed genes (DEGs) to CCP 76 and BRS 265 genotypes, respectively. These genes included 71 and 34 GDEs involved in the cell wall disassembly and flavonoid biosynthesis, respectively, which could be associated with firmness loss and anthocyanin accumulation during cashew apple development. Then, softer peduncle of CCP 76 could be justified by down-regulated EXP and up-regulation of genes involved in pectin degradation (PG, PL and PAE) and in cell wall biosynthesis. Moreover, genes related to flavonoid biosynthesis (PAL, C4H and CHS) could be associated with early high accumulation of anthocyanin in red-peel peduncle of BRS 265. Finally, expression patterns of the selected genes were tested by real-time quantitative PCR (qRT-PCR), and the qRT-PCR results were consistent with transcriptome data. The information generated in this work will provide insights into transcriptome responses to cashew apple ripening and hence, it will be helpful for cashew breeding programs aimed at developing genotypes with improved quality traits.

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Data availability

The sequencing project has been deposited at the SRA database under the accession number PRJNA657300.

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Acknowledgements

TGA and SA are grateful to CAPES for the Doctoral fellowship. AERO is grateful to FAPESP for the Postdoctoral fellowship (Grant Numbers 2019/22579-7 and 2013/08216-2). JHC is thankful to CNPq for the Researcher fellowship (Grant Number 309795/2017-6). The authors are grateful to Embrapa Agroindústria Tropical for providing the cashew apples. Genome sequence data of cashew trees used in this article was produced by the US Department of Energy Joint Genome Institute http://www.jgi.doe.gov/ in collaboration with the user community.

Funding

This research was supported by INCT, CNPq, FAPESP and CAPES.

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Authors and Affiliations

  1. Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Campus do Pici, Fortaleza, CE, CEP 60440-554, Brazil

    Thais Andrade Germano, Matheus Finger Ramos de Oliveira, Shahid Aziz & José Hélio Costa

  2. Departamento de Análises Clínicas e Toxicológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, SP, CEP 05508-900, Brazil

    Antonio Edson Rocha Oliveira

  3. Ciência e Tecnologia da Paraíba, Instituto Federal de Educação, Campus Princesa Isabel, Princesa Isabel, PB, CEP 58755-000, Brazil

    Kátia Daniella da Cruz Saraiva

  4. Departamento de Química, Universidade Estadual de Ponta Grossa, Campus Uvaranas, Ponta Grossa, PR, CEP 84030-900, Brazil

    Clesivan Pereira dos Santos

  5. Embrapa Agroindústria Tropical, Rua Dra. Sara Mesquita, Fortaleza, CE, CEP 60511-110, Brazil

    Carlos Farley Herbster Moura

Authors
  1. Thais Andrade Germano
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  2. Matheus Finger Ramos de Oliveira
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  3. Shahid Aziz
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  4. Antonio Edson Rocha Oliveira
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  5. Kátia Daniella da Cruz Saraiva
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  6. Clesivan Pereira dos Santos
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  7. Carlos Farley Herbster Moura
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  8. José Hélio Costa
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Contributions

The manuscript is a part of PhD study of TAG, she conceptualized, designed the study, and finalized the manuscript. MFRO and AERO helped in bioinformatics analysis. KDCS helped in qRT-PCR analysis and visualization of the obtained results. CPS contributed to the interpretation of results and reviewed the manuscript. CFHM was involved in management and orientation of cashew apple harvest. SA contributed to the development of scientific writing, final organization and reviewed the manuscript. JHC, supervised all stages of this work and submitted the manuscript.

Corresponding author

Correspondence to José Hélio Costa.

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Supplementary Information

Below is the link to the electronic supplementary material.

11103_2022_1257_MOESM1_ESM.docx

Supplementary file1 (DOCX 95 KB)—Supplementary. geNorm analyses. (A) Average expression stability values of candidate reference genes and (B) determination of the optimal number of candidate reference genes for normalization

Supplementary file2 (XLS 5556 KB)—Number of filters reads mapped to cashew tree genome

11103_2022_1257_MOESM3_ESM.docx

Supplementary file3 (DOCX 16 KB)—Primer sequence, optimal annealing temperature and amplicon size of each evaluated gene in this study

Supplementary file4 (XLS 6776 KB)—Normalized counts in Fragments Per Kilobase Million (FPKM)

11103_2022_1257_MOESM5_ESM.doc

Supplementary file5 (DOC 45 KB)—Summary of sequencing and data mapping. Total raw reads; total filter reads; Q30 percentage: proportion of nucleotides with quality value > 30; GC content percentage: GC content of total nucleotides; Mapped reads (%)

11103_2022_1257_MOESM6_ESM.xlsx

Supplementary file6 (XLSX 1275 KB)—Identified differentially expressed genes (DEGs) to each studied comparison in this study. The first column of table shows gene ID followed by its base mean, log2 fold change value, P-value, adjusted P-value and differential expression (up or downregulated). BI: BRS 265 immature; BR: BRS 265 ripe; CI: CCP 76 immature; CR: CCP 76 ripe

11103_2022_1257_MOESM7_ESM.xlsx

Supplementary file7 (XLSX 168 KB)—Common and exclusive differentially expressed genes (DEGs) during CCP 76 and BRS 265 cashew apple development. The table consists of gene ID and its identification in relation to Arabidopsis thaliana to each studied comparison. BI: BRS 265 immature; BR: BRS 265 ripe; CI: CCP 76 immature; CR: CCP 76 ripe

11103_2022_1257_MOESM8_ESM.xlsx

Supplementary file8 (XLSX 212 KB)—GO enrichment analysis during the cashew apple development. The table consists of name and ID of GO term, besides its gene ontology classes: biological process (BP), cellular component (CC) and molecular function (MF). Over and under represented P-value calculated to each GO term based on information present in fourth and fifth columns. Only those GO terms with over represented P-value < 0.05 are shown. The fourth column lists the number of up and downregulated genes to the studied comparisons assigned to each GO term. The fifth column lists the number of background genes mapped to each GO term. The last column shows the ID of DEGs enriched each GO term

11103_2022_1257_MOESM9_ESM.xlsx

Supplementary file9 (XLSX 95 KB)—Enriched metabolic pathways represented during the cashew apple development according to the Kyoto Encyclopedia of Genes and Genomes (KEGG). The first three columns show the name, database and ID of pathways. The fourth column lists the number of up or downregulated genes to the studied comparisons assigned to each pathway. The fifth column lists the number of background genes mapped to each pathway. The last columns list the P-value and corrected P-value of the statistical test, genes names and hyperlink to visualization of genes pathway in website. BI: BRS 265 immature; BR: BRS 265 ripe; CI: CCP 76 immature; CR: CCP 76 ripe

11103_2022_1257_MOESM10_ESM.xlsx

Supplementary file10 (XLSX 134 KB)—Gene ID, transcription factor family, best hit in Arabidopsis thaliana, e-value and description for the best hit in each studied comparison in this study

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Germano, T.A., de Oliveira, M.F.R., Aziz, S. et al. Transcriptome profiling of cashew apples (Anacardium occidentale) genotypes reveals specific genes linked to firmness and color during pseudofruit development. Plant Mol Biol 109, 83–100 (2022). https://doi.org/10.1007/s11103-022-01257-w

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