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The MaASR gene as a crucial component in multiple drought stress response pathways in Arabidopsis

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Abstract

Abscisic acid (ABA)-, stress-, and ripening-induced (ASR) proteins are involved in abiotic stress responses. However, the exact molecular mechanism underlying their function remains unclear. In this study, we report that MaASR expression was induced by drought stress and MaASR overexpression in Arabidopsis strongly enhanced drought stress tolerance. Physiological analyses indicated that transgenic lines had higher plant survival rates, seed germination rates, and leaf proline content and lower water loss rates (WLR) and malondialdehyde (MDA) content. MaASR-overexpressing lines also showed smaller leaves and reduced sensitivity to ABA. Further, microarray and chromatin immunoprecipitation-based sequencing (ChIP-seq) analysis revealed that MaASR participates in regulating photosynthesis, respiration, carbohydrate and phytohormone metabolism, and signal transduction to confer plants with enhanced drought stress tolerance. Direct interactions of MaASR with promoters for the hexose transporter and Rho GTPase-activating protein (RhoGAP) genes were confirmed by electrophoresis mobility shift array (EMSA) analysis. Our results indicate that MaASR acts as a crucial regulator of photosynthesis, respiration, carbohydrate and phytohormone metabolism, and signal transduction to mediate drought stress tolerance.

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31071788), the earmarked fund for Modern Agro-industry Technology Research System (CARS-32), the Ministry of Science and Technology of the People’s Republic of China (2011AA10020605), and the Major Technology Project of Hainan (ZDZX2013023-1).

Authors’ contributions

ZQJ and BYX conceived the study. LLZ, YW, RJF, YDZ, JHL, CHJ, HXM, and JBZ performed the experiments and carried out the analysis. WH designed the experiments and wrote the manuscript. All authors read and approved the final manuscript.

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Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Resources of Tropical Crops, Ministry of Agriculture, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, Hainan, China

    Lili Zhang, Wei Hu, Yuan Wang, Renjun Feng, Yindong Zhang, Juhua Liu, Caihong Jia, Hongxia Miao, Jianbin Zhang, Biyu Xu & Zhiqiang Jin

  2. Hainan Key Laboratory of Banana Genetic Improvement, Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou, 570101, Hainan, China

    Zhiqiang Jin

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  1. Lili Zhang
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  2. Wei Hu
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  3. Yuan Wang
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Correspondence to Biyu Xu or Zhiqiang Jin.

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Lili Zhang and Wei Hu contributed equally to this work.

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Fig. S1

Alignment of MaASR sequence with homologues from other species: mASR1 (GU134740) from Musa acuminata subsp, mASR2 (GU134761) from Musa balbisiana, mASR4 (GU134735) from Musa banksii, TaASR1 (HQ287799) from Triticum aestivum, ZmASR2 (NP_001147703.1) from Zea mays, OsASR1 (AAX92999.1) from Oryza sativa. ABA/WDS motif was displayed in the box. Letters marked with double transverse lines showed a putative nuclear targeting signal. One His-rich region and two Ala-rich regions are underlined. Amino acid sequences alignment was performed by ClusterX 2.0. (GIF 79 kb)

High resolution Image (TIFF 855 kb)

Fig. S2

Phylogenetic analysis of MaASR with RcASR (XP_002524296.1) from Ricinus communis, VpASR (ABC86744.1) from Vitis pseudoreticulata, SlASR4 (AAY98026.1) from Solanum lycopersicum, ScASR4 (AAY98030.1) from Solanum corneliomuelleri, PpASR (BAA96451.1) from Pyrus pyrifolia, SpASR2 (ABY84856.1) from Solanum pimpinellifolium, SlASR2 (ABY84857.1) from Solanum lycopersicum, LpASR2 (ABS19518.1) from Lycopersicon peruvianum, NbASR (ACV52581.1) from Nicotiana benthamiana, mASR1 (GU134740) from Musa acuminata subsp. Burmannicoides, mASR2 (GU134761) from Musa balbisiana, mASR4 (GU134735) from Musa banksii, ZmASR2 (NP_001147703.1) from Zea mays, OsASR (AAX92999.1) from Oryza sativa, TaASR1 (HQ287799) from Triticum aestivum, LlASR (AAM51877.1) from Lilium longiflorum. Phylogenetic tree was constructed by using ClusterX 2.0 and Mega 4.0. (GIF 15 kb)

High resolution Image (TIFF 208 kb)

Fig. S3

Cluster data (A) and scatter plot (B) of differentially expressed genes identified by microarrays. (A) The red color represents upregulated genes with fold change ≥ 2, with screening criteria ratio ≥ 2; The green color represents downregulated genes with fold change ≥ 2 and screening criteria ratio ≤ 0.5. (B) X and Y axes represent the fluorescence signal intensity value of the WT and transgenic lines, respectively. Each point represents the hybridization signal of the gene in the expression profile microarray. The red color represents the genes with a screening criteria ratio ≥ 2, while the green color represents genes with a screening criteria ratio ≤ 0.5; The black color represents genes that have no significant changes with screening criteria of 0.5 < ratio < 2. (GIF 77 kb)

High resolution Image (TIFF 910 kb)

Fig. S4

Expression of phytohormone-metabolic/-transduction-related genes determined by qRT-PCR analysis in WT and transgenic lines. Fourteen day old Arabidopsis seedlings of each sample were transferred to filter paper for 2 h or 6 h to induce dehydration. The fold difference in mRNA was relative to that of WT under normal conditions. Vertical bars indicate ± SE of three independent measurements. (GIF 95 kb)

High resolution Image (TIFF 1035 kb)

Fig. S5

Categorization of the differentially expressed genes identified from the Arabidopsis expression profile microarray (14 vs WT) according to position in the cellular component (A), molecular biological function (B) and biological processes (C). (GIF 82 kb)

High resolution Image (TIFF 920 kb)

Fig. S6

Categorization of the differentially expressed genes identified from the Arabidopsis expression profile microarray (Y vs W) according to position in the cellular component (A), molecular biological function (B) and biological processes (C). (GIF 90 kb)

High resolution Image (TIFF 951 kb)

Fig. S7

Analysis of the specificity of the MaASR monoclonal antibody used for chromatin immunoprecipitation (ChIP) assay. (A) SDS-PAGE analysis of expressed MaASR protein after Ni-agarose affinity chromatography. M: Protein Marker; 1: Purified protein of MaASR. (B) Western bolt analysis of the specificity of the MaASR monoclonal antibody. M: Protein marker; 1: Hybridization of MaASR monoclonal antibody with proteins expressed by vacant vector; 2: Hybridization of MaASR monoclonal antibody with purified MaASR protein. (GIF 22 kb)

High resolution Image (TIFF 341 kb)

Fig. S8

The expression of hexose transporter and RhoGAP genes determined by qRT-PCR analysis in WT and transgenic lines. Fourteen day old Arabidopsis seedlings of each sample were transferred to filter paper for 2 h or 6 h to induce dehydration. The fold difference in mRNA was relative to that of WT under normal conditions. Vertical bars indicate ± SE of three independent measurements. (GIF 25 kb)

High resolution Image (TIFF 262 kb)

Fig. S9

Network diagram (A) and connectivity (B) of differentially expressed genes in Y vs W. (A) Red represents upregulated genes and yellow represents downregulated genes. CX = mRNA co-expression between Arabidopsis genes; DC = Domain co-occurrence between Arabidopsis proteins; GN = Gene neighborhoods between Arabidopsis orthologs in bacterial genomes; LC = Literature-curated Arabidopsis protein interactions; PG = Phylogenetic profile similarity between Arabidopsis homologues. (B) The horizontal axis represents genes ID in the network diagram. The vertical axis represents gene connectivity in network diagram. (GIF 96 kb)

High resolution Image (TIFF 1163 kb)

Table S1

qRT-PCR primers used in this study. (XLS 26 kb)

Table S2

Upregulated genes in the expression profile microarray (14 vs WT). (XLS 114 kb)

Table S3

Downregulated genes in the expression profile microarray (14 vs WT). (XLS 54 kb)

Table S4

Upregulated genes in the expression profile microarray (Y vs W). (XLS 72 kb)

Table S5

Downregulated genes in the expression profile microarray (Y vs W). (XLS 89 kb)

Table S6

Differentially expressed genes related to water deprivation, photosynthesis, respiration, carbohydrate metabolism, amino acid metabolism and phytohormone metabolism and signal transduction in the expression profile microarray (14 vs WT). (XLS 70 kb)

Table S7

Differentially expressed genes related to water deprivation, photosynthesis, respiration, carbohydrate metabolism, amino acid metabolism and phytohormone metabolism and signal transduction in the expression profile microarray (Y vs W). (XLS 79 kb)

Table S8

Summary of genes and binding sites directly targeted by MaASR. (XLS 190 kb)

Table S9

Genes directly targeted by MaASR identified by comparing ChIP-seq and microarray (Y vs W) data. (XLS 24 kb)

Table S10

Statistics of sugar-responsive elements SURE1 (AATAGAAAA), sucrose box 3 (AAAATCA---TAA) and CE1 (CACCG) among genes directly targeted by MaASR. (XLS 28 kb)

Table S11

Corresponding genes according to GO enrichment analysis of MaASR directly regulated genes. (XLS 32 kb)

Table S12

(DOC 41 kb)

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Zhang, L., Hu, W., Wang, Y. et al. The MaASR gene as a crucial component in multiple drought stress response pathways in Arabidopsis . Funct Integr Genomics 15, 247–260 (2015). https://doi.org/10.1007/s10142-014-0415-y

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  • DOI: https://doi.org/10.1007/s10142-014-0415-y

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