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Deep RNAseq indicates protective mechanisms of cold-tolerant indica rice plants during early vegetative stage

Plant Cell Reports volume 37, pages 347–375 (2018)Cite this article

Abstract

Key message

Cold-tolerance in rice may be related to increased cellulose deposition in the cell wall, membrane fatty acids unsaturation and differential expression of several newly identified genes.

Abstract

Low temperature exposure during early vegetative stages limits rice plant’s growth and development. Most genes previously related to cold tolerance in rice are from the japonica subspecies. To help clarify the mechanisms that regulate cold tolerance in young indica rice plants, comparative transcriptome analysis of 6 h cold-treated (10 °C) leaves from two genotypes, cold-tolerant (CT) and cold-sensitive (CS), was performed. Differentially expressed genes were identified: 831 and 357 sequences more expressed in the tolerant and in the sensitive genotype, respectively. The genes with higher expression in the CT genotype were used in systems biology analyses to identify protein–protein interaction (PPI) networks and nodes (proteins) that are hubs and bottlenecks in the PPI. From the genes more expressed in the tolerant plants, 60% were reported as affected by cold in previous transcriptome experiments and 27% are located within QTLs related to cold tolerance during the vegetative stage. Novel cold-responsive genes were identified. Quantitative RT-PCR confirmed the high-quality of RNAseq libraries. Several genes related to cell wall assembly or reinforcement are cold-induced or constitutively highly expressed in the tolerant genotype. Cold-tolerant plants have increased cellulose deposition under cold. Genes related to lipid metabolism are more expressed in the tolerant genotype, which has higher membrane fatty acids unsaturation, with increasing levels of linoleic acid under cold. The CT genotype seems to have higher photosynthetic efficiency and antioxidant capacity, as well as more effective ethylene, Ca2+ and hormone signaling than the CS. These genes could be useful in future biotechnological approaches aiming to increase cold tolerance in rice.

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Acknowledgements

This work was supported by Universidade do Vale do Taquari - UNIVATES and the Brazilian funding agencies FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). The authors thank IRGA (Instituto Rio-Grandense do Arroz) for providing the rice seeds, for access to its facilities and for technical support.

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    1. Centro de Ciências Biológicas e da Saúde (CCBS), Programa de Pós-Graduação em Biotecnologia (PPGBiotec), Universidade do Vale do Taquari-UNIVATES, Lajeado, RS, Brazil

      Raul Antonio Sperotto

    2. Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

      Artur Teixeira de Araújo Junior, Ben-Hur Neves de Oliveira & Janette Palma Fett

    3. Departamento de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

      Janete Mariza Adamski, Rinaldo Pires dos Santos & Janette Palma Fett

    4. Departamento de Agronomia, Universidade Federal da Fronteira Sul (UFFS), Erechim, RS, Brazil

      Denise Cargnelutti

    5. Departamento de Biologia, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil

      Felipe Klein Ricachenevsky

    6. Departamento de Plantas de Lavoura, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

      Renata Pereira da Cruz

    7. Departamento de Zootecnia, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil

      Leila Picolli da Silva

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    1. Raul Antonio Sperotto
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    Raul Antonio Sperotto, Artur Teixeira de Araújo Junior and Janete Mariza Adamski contributed equally to this work.

    Communicated by Marcelo Menossi.

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    299_2017_2234_MOESM1_ESM.jpg

    Fig. 1. Visual symptoms of rice plants from the cold-tolerant (CT) and cold-sensitive (CS) genotypes after 10 days under control (28 °C) or cold (10 °C) treatment, followed by 7 days of recovery at 28 °C. Bar in figure (A) indicates 7 cm. The experiment was performed twice with similar results (JPG 2062 KB)

    299_2017_2234_MOESM2_ESM.jpg

    Fig. 2. Analysis of genes expressed in leaves from two indica rice genotypes (cold-tolerant (CT) and cold-sensitive (CS)). (A) Scatter plot comparing the gene expression levels between the CT and the CS genotypes. (B) Genes identified by red dots have adjusted p-value lower than 0.000001 (calculated using EdgeR). FC: fold change; CPM: counts per million (JPG 2368 KB)

    Table 1. Gene-specific PCR primers used for RT-qPCR (DOC 42 KB)

    299_2017_2234_MOESM4_ESM.xlsx

    Table 2. Differentially expressed genes revealed by RNAseq in leaves of rice plants exposed to cold treatment (10 °C) for 6 h. First panel: genes with higher expression in the cold-tolerant genotype (IRGA 959-1-2-2F-4-1-4-A). Second panel: genes with higher expression in the cold-sensitive genotype (IRGA 959-1-2-2F-4-1-4-D-1-CA-1) (XLSX 296 KB)

    299_2017_2234_MOESM5_ESM.xlsx

    Table 3. Meta-analysis of cold-responsive genes. All genes considered differentially expressed in this work (with higher expression in the cold-tolerant or in the cold-sensitive genotypes after plant exposure to 10 °C for 6 h) were used in searches for matching genes in tables of differentially expressed genes (in rice plants under cold treatment) reported in previous large-scale research papers. Details from each experiment are provided in the third spreadsheet. In the first two spreadsheets, genes that were reported as cold-responsive in at least one of the previous works are shown in red letters. Results obtained with rice genotypes considered cold-tolerant are shaded in blue, while results from cold-sensitive genotypes are shaded in yellow. Results obtained with rice Nipponbare are not shaded, because there is controversy about its sensitivity to cold. In the fourth spreadsheet, gene locations were compared with locations of QTLs previously identified as related to cold tolerance in rice plants during the vegetative stage. Genes with corresponding locations (“hits”) are marked with X in the corresponding columns and are shown in blue letters (XLSX 376 KB)

    299_2017_2234_MOESM6_ESM.xlsx

    Table 4. Descriptions of genes/proteins present in the response interactome of the cold-tolerant indica rice plants. Nodes with differentially expressed genes (higher expression in the cold-tolerant than in the sensitive plants) revealed by RNAseq in leaves of rice plants exposed to cold treatment (10 °C) for 6 h have fold change (FC Tolerant/Sensitive) shown in column D. The description (Hit) and gene ontology of each node was obtained from the Rice Genome Annotation Project (RGAP) database. The data of node degree and betweeneess centrality were obtained with a plugin network analyzer in the Cytoscape software. The metabolism categories were determined using the KEGG database (XLSX 70 KB)

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    Sperotto, R.A., de Araújo Junior, A.T., Adamski, J.M. et al. Deep RNAseq indicates protective mechanisms of cold-tolerant indica rice plants during early vegetative stage. Plant Cell Rep 37, 347–375 (2018). https://doi.org/10.1007/s00299-017-2234-9

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    Keywords

    • Cellulose
    • Cold tolerance
    • Cell wall
    • Transcriptome
    • Fatty acid
    • Indica rice