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Integrative omics approaches revealed a crosstalk among phytohormones during tuberous root development in cassava

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Integrative omics approaches revealed a crosstalk among phytohormones during tuberous root development in cassava.

Abstract

Tuberous root formation is a complex process consisting of phase changes as well as cell division and elongation for radial growth. We performed an integrated analysis to clarify the relationships among metabolites, phytohormones, and gene transcription during tuberous root formation in cassava (Manihot esculenta Crantz). We also confirmed the effects of the auxin (AUX), cytokinin (CK), abscisic acid (ABA), jasmonic acid (JA), gibberellin (GA), brassinosteroid (BR), salicylic acid, and indole-3-acetic acid conjugated with aspartic acid on tuberous root development. An integrated analysis of metabolites and gene expression indicated the expression levels of several genes encoding enzymes involved in starch biosynthesis and sucrose metabolism are up-regulated during tuberous root development, which is consistent with the accumulation of starch, sugar phosphates, and nucleotides. An integrated analysis of phytohormones and gene transcripts revealed a relationship among AUX signaling, CK signaling, and BR signaling, with AUX, CK, and BR inducing tuberous root development. In contrast, ABA and JA inhibited tuberous root development. These phenomena might represent the differences between stem tubers (e.g., potato) and root tubers (e.g., cassava). On the basis of these results, a phytohormonal regulatory model for tuberous root development was constructed. This model may be useful for future phytohormonal studies involving cassava.

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Acknowledgements

We thank Dr. Salome Prato (Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología, Madrid, Spain.) and Dr. Uwe Sonnewald (Biochemistry, Department of Biology, Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany) for their critical suggestions and discussion. This work was financially supported by the East Asia Science and Innovation Area Joint Research Program (to M.S.), the Strategic Funds for the Promotion of Science and Technology (to M.S.), and the EIG CONCERT-Japan (JPMJSC16C4) 4th Call under the Strategic International Research Cooperative Program (to M.S.) of the Japan Science and Technology Agency (JST) as well as the Science and Technology Research Partnership for Sustainable Development (to M.S.) of the JST/Japan International Cooperation Agency and the RIKEN Center for Sustainable Resource Science (to M.S.). We thank Edanz Group (https://en-author-services.edanzgroup.com/) for editing a draft of this manuscript.

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Authors and Affiliations

  1. RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan

    Yoshinori Utsumi, Maho Tanaka, Chikako Utsumi, Satoshi Takahashi, Akihiro Matsui, Atsushi Fukushima, Makoto Kobayashi, Ryosuke Sasaki, Akira Oikawa, Miyako Kusano, Kazuki Saito, Mikiko Kojima, Hitoshi Sakakibara & Motoaki Seki

  2. RIKEN Cluster for Pioneering Research, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

    Maho Tanaka, Satoshi Takahashi, Akihiro Matsui & Motoaki Seki

  3. Faculty of Agriculture, Yamagata University, Tsuruoka, Japan

    Akira Oikawa

  4. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Miyako Kusano

  5. Graduate School of Pharmaceutical Sciences, Chiba University, Chiba, Chiba, 260-8675, Japan

    Kazuki Saito

  6. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan

    Hitoshi Sakakibara

  7. Department of Biotechnology, Faculty of Science, Mahidol University, Bangkok, Thailand

    Punchapat Sojikul & Jarunya Narangajavana

  8. Kihara Institute for Biological Research, Yokohama City University, 641-12 Maioka-cho, Totsuka-ku, Yokohama, Kanagawa, 244-0813, Japan

    Motoaki Seki

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  1. Yoshinori Utsumi
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Contributions

YU and MS supervised the experiments and wrote the manuscript. YU analyzed the data. YU and MT completed the gene expression analysis. YU and CU were responsible for plant management. AM and ST assisted with the transcriptome analysis. AF, Makoto K, RS, Miyako K, AO, and KS completed the metabolome analysis. HS and MK completed the phytohormone analysis. PS and JN prepared the cassava samples.

Corresponding authors

Correspondence to Yoshinori Utsumi or Motoaki Seki.

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11103_2020_1033_MOESM1_ESM.tif

Supplementary Figure 1. Data obtained from metabolome, simultaneous analysis of phytohormones, and transcriptome analyses. We collected 59,135 data points from our transcriptome analysis, 1,125 data points from our metabolome analysis (221 data points by GC-MS and 904 data points by CE-MS), 25 data points from our phytohormone analysis and data regarding the starch content after the filtering process. Integrated data are presented in this report. Supplementary file1 (TIF 742 kb)

11103_2020_1033_MOESM2_ESM.tif

Supplementary Figure 2. Identification of differentially accumulated metabolites from the metabolome data of the pre-tuberous root, parenchyma, and cortex samples. Supplementary file2 (TIF 2610 kb)

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Supplementary Figure 3. Heat map analysis of 135 metabolites in all samples. Red and blue represent increasing and decreasing metabolite contents, respectively, relative to the levels in F4 root or L4 leaf samples. Supplementary file3 (TIF 2671 kb)

11103_2020_1033_MOESM4_ESM.tif

Supplementary Figure 4. Heat map of Pearson’s correlation coefficients for the characteristic metabolites. The correlation coefficients represent the relationships between the metabolites at each stage. Correlation coefficients are presented with a continuous color gradient, where significant positive and negative correlations are marked in red and blue, respectively. Yellow indicates no significant correlation. Color bars represent the significance of the correlation coefficients. Supplementary file4 (TIF 5799 kb)

11103_2020_1033_MOESM5_ESM.tif

Supplementary Figure 5. Selection of differentially expressed genes (DEGs) predominantly induced in parenchyma and cortex (bark) at 8 weeks and 12 weeks after cutting. a Venn diagrams presenting the co-occurrence of DEGs (BH FDR < 0.05, fold change ≥ 2.0 or ≤ 2.0) in the parenchyma at 8 and 12 weeks. DEGs were compared to the gene expression of each gene in F4 and that of each parenchyma sample (I8_Pa, S8_Pa, I12_Pa and S12_Pa). The upregulated and downregulated genes compared with the gene expression of F4 was represented as UP and DOWN, respectively. b Venn diagrams presenting the co-occurrence of DEGs (BH FDR < 0.05, fold change ≥ 2.0 or ≤ 2.0) in the cortex at 8 and 12 weeks. DEGs were compared to the gene expression of each gene in F4 and that of each cortex (bark) sample (I8_Co, S8_Co, I12_Co and S12_Co). The upregulated and downregulated genes compared with the gene expression of F4 was represented as UP and DOWN, respectively. Supplementary file5 (TIF 1834 kb)

11103_2020_1033_MOESM6_ESM.tif

Supplementary Figure 6. GO functional categories of up-regulated DEGs in the parenchyma (Figure 6b). GO biological process functional categories for 2,848 genes were identified with the Singular Enrichment Analysis (SEA) of agriGO. The first pair of numerals represents the number of genes in the input list associated with the GO term and the number of genes in the input list. The second pair of numerals represents the number of genes associated with the GO term in the Arabidopsis database, the total number of Arabidopsis genes with GO annotations, and the p-value in parentheses. The color of the arrows indicates the relationship among the GO terms. Black stands for ‘is a’, which means that the whole of genes in upper GO term is included in the lower GO term on hierarchical tree. Orange stands for ‘part of’, which means that the part of genes in upper GO term is included in lower GO term on hierarchical tree. Red stands for ‘positive regulate’. Purple stands for ‘regulate’. Green indicates ‘negative regulate’. Long dashed lines indicate ‘two significant nodes’, and short dashed lines stands for ‘one significant node’. Long dashed, short dashed, and solid lines represent two-, one- and zero- enriched terms between connected boxes, respectively. Box colors indicate the levels of statistical significance: yellow < 0.01; orange < 0.001. White boxes indicate non-significant terms. Supplementary file6 (TIF 2063 kb)

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Supplementary Figure 7. GO functional categories of up-regulated DEGs in the cortex (Figure 6b). GO biological process functional categories for 548 genes were identified with the Singular Enrichment Analysis (SEA) of agriGO. The first pair of numerals represents the number of genes in the input list associated with the GO term and the number of genes in the input list. The second pair of numerals represents the number of genes associated with the GO term in the Arabidopsis database, the total number of Arabidopsis genes with GO annotations, and the p-value in parentheses. The color of the arrows indicates the relationship among the GO terms. Black stands for ‘is a’, which means that the whole of genes in upper GO term is included in the lower GO term on hierarchical tree. Orange stands for ‘part of’, which means that the part of genes in upper GO term is included in lower GO term on hierarchical tree. Red stands for ‘positive regulate’. Purple stands for ‘regulate’. Green indicates ‘negative regulate’. Long dashed lines indicate ‘two significant nodes’, and short dashed lines stands for ‘one significant node’. Long dashed, short dashed, and solid lines represent two-, one- and zero- enriched terms between connected boxes, respectively. Box colors indicate levels of statistical significance: yellow < 0.01; orange < 0.001. White boxes indicate non-significant terms. Supplementary file7 (TIF 1471 kb)

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Supplementary Figure 8. GO functional categories of up-regulated DEGs in both the cortex and parenchyma (Figure 6b). GO biological process functional categories for 1,250 genes were identified with the Singular Enrichment Analysis (SEA) of agriGO. The first pair of numerals represents the number of genes in the input list associated with the GO term and the number of genes in the input list. The second pair of numerals represents the number of genes associated with the GO term in the Arabidopsis database, the total number of Arabidopsis genes with GO annotations, and the p-value in parentheses. The color of the arrows indicates the relationship among the GO terms. Black stands for ‘is a’, which means that the whole of genes in upper GO term is included in the lower GO term on hierarchical tree. Orange stands for ‘part of’, which means that the part of genes in upper GO term is included in lower GO term on hierarchical tree. Red stands for ‘positive regulate’. Purple stands for ‘regulate’. Green indicates ‘negative regulate’. Long dashed lines indicate ‘two significant nodes’, and short dashed lines stands for ‘one significant node’. Long dashed, short dashed, and solid lines represent two-, one- and zero- enriched terms between connected boxes, respectively. Box colors indicate levels of statistical significance: yellow < 0.01; orange < 0.001. White boxes indicate non-significant terms. Supplementary file8 (TIF 2000 kb)

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Supplementary Figure 9. GO functional categories of down-regulated DEGs in both the cortex and parenchyma (Figure 6b). GO biological process functional categories for 1,235 genes were identified with the Singular Enrichment Analysis (SEA) of agriGO. The first pair of numerals represents the number of genes in the input list associated with the GO term and the number of genes in the input list. The second pair of numerals represents the number of genes associated with the GO term in the Arabidopsis database, the total number of Arabidopsis genes with GO annotations, and the p-value in parentheses. The color of the arrows indicates the relationship among the GO terms. Black stands for ‘is a’, which means that the whole of genes in upper GO term is included in the lower GO term on hierarchical tree. Orange stands for ‘part of’, which means that the part of genes in upper GO term is included in lower GO term on hierarchical tree. Red stands for ‘positive regulate’. Purple stands for ‘regulate’. Green indicates ‘negative regulate’. Long dashed lines indicate ‘two significant nodes’, and short dashed lines stands for ‘one significant node’. Long dashed, short dashed, and solid lines represent two-, one- and zero- enriched terms between connected boxes, respectively. Box colors indicate levels of statistical significance: yellow < 0.01; orange < 0.001. White boxes indicate non-significant terms. Supplementary file9 (TIF 1582 kb)

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Supplementary Figure 10. GO functional categories of down-regulated DEGs in the parenchyma (Figure 6b). GO biological process functional categories for 2,059 genes were identified with the Singular Enrichment Analysis (SEA) of agriGO. The first pair of numerals represents the number of genes in the input list associated with the GO term and the number of genes in the input list. The second pair of numerals represents the number of genes associated with the GO term in the Arabidopsis database, the total number of Arabidopsis genes with GO annotations, and the p-value in parentheses. The color of the arrows indicates the relationship among the GO terms. Black stands for ‘is a’, which means that the whole of genes in upper GO term is included in the lower GO term on hierarchical tree. Orange stands for ‘part of’, which means that the part of genes in upper GO term is included in lower GO term on hierarchical tree. Red stands for ‘positive regulate’. Purple stands for ‘regulate’. Green indicates ‘negative regulate’. Long dashed lines indicate ‘two significant nodes’, and short dashed lines stands for ‘one significant node’. Long dashed, short dashed, and solid lines represent two-, one- and zero- enriched terms between connected boxes, respectively. Box colors indicate levels of statistical significance: yellow < 0.01; orange < 0.001. White boxes indicate non-significant terms. Supplementary file10 (TIF 1293 kb)

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Supplementary Figure 11. Heat map presenting relative expression values (log2) of DEGs identified by one-way ANOVA with the BH method (FDR < 5e-10) from whole data sets. Red and blue represent high and low gene expression levels, respectively, relative to the levels in the F4 root or L4 leaf samples. Supplementary file11 (TIF 2306 kb)

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Supplementary Figure 12. Correlation between each BEL and ARF gene and the genes involved in phytohormone signaling. Positive and negative correlations are marked by red and blue lines, respectively. Supplementary file12 (TIF 6846 kb)

Supplementary file13 (XLSX 17860 kb)

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Utsumi, Y., Tanaka, M., Utsumi, C. et al. Integrative omics approaches revealed a crosstalk among phytohormones during tuberous root development in cassava. Plant Mol Biol 109, 249–269 (2022). https://doi.org/10.1007/s11103-020-01033-8

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