A Genome-Wide Expression Profile of Salt-Responsive Genes in the Apple Rootstock Malus zumi
Abstract
:1. Introduction
2. Results
2.1. Salt-Responsive Genes Identified by Microarray Experiment and Semi-Quantitative RT-PCR Validation
2.2. Promoter Analysis
2.3. Regulatory Network during Salt Stress
3. Discussion
3.1. Characteristics of Constructed cDNA Library
3.2. Regulatory Network during Salt Stress
3.3. Salt Stress Signaling
3.4. Analysis of cis-Elements
3.5. Cellular Response Strategies to Salt Stress in Malus zumi
3.6. Stable Photosynthesis Suggests a Novel Salt Tolerance Mechanism in Malus zumi
3.7. Epigenetic and Novel Regulation in Salt Stress Response
4. Experimental Section
4.1. Plant Materials
4.2. RNA Extraction and Construction of the Normalized Full-Length cDNA Library of Malus zumi
4.3. Preparation of Slides for cDNA Microarrays
4.4. Probe Labeling, Slide Hybridization and Scanning
4.5. Data Analysis of Microarray Results
4.6. RT-PCR Analysis
4.7. Promoter Analysis
4.8. Exploring the Interaction Network
5. Conclusions
Supplementary Information
ijms-14-21053-s001.pdfFunctional category | Percentage of unigenes (%) |
---|---|
Photosynthesis | 16 |
Transporter | 5 |
Metabolism | 17 |
Stress tolerance | 7 |
Signal transduction | 6 |
Protein related | 7 |
ROS elimination | 6 |
Osmoprotection | 5 |
Cell maintenance and development | 6 |
Others | 4 |
Unknown protein | 21 |
Cis-element | ABRE | ARE | TC-rich repeats | HSE | DRE | LTR | ERE | MBS | |
---|---|---|---|---|---|---|---|---|---|
Genes with the cis-element among the Regulatory genes | 9/14 | 13/14 | 10/14 | 9/14 | 0/14 | 8/14 | 7/14 | 10/14 | |
Genes with the cis-element among the functional genes | ROS elimination | 7/10 | 5/10 | 8/10 | 8/10 | 0/10 | 4/10 | 3/10 | 7/10 |
Osmoregulation | 7/9 | 7/9 | 7/9 | 2/9 | 1/9 | 1/9 | 2/9 | 7/9 | |
Stress tolerance | 9/14 | 10/14 | 10/14 | 6/14 | 2/14 | 2/14 | 2/14 | 12/14 | |
Photosynthesis | 21/26 | 20/26 | 17/26 | 13/26 | 1/26 | 12/26 | 7/26 | 18/26 | |
Transporter | 7/9 | 7/9 | 6/9 | 7/9 | 0/9 | 3/9 | 1/9 | 7/9 | |
Metabolism | 17/23 | 19/23 | 15/23 | 16/23 | 0/23 | 10/23 | 8/23 | 18/23 | |
Protein related | 4/11 | 10/11 | 8/11 | 6/11 | 0/11 | 10/11 | 8/11 | 18/11 | |
Cell maintenance and development | 2/9 | 7/9 | 4/9 | 7/9 | 0/9 | 3/9 | 1/9 | 2/9 | |
Average number of the cis-elements per gene | 2.43 | 2.24 | 1.75 | 2.04 | 1.00 | 1.45 | 1.19 | 2.10 |
Number | Expression a | Putative annotation | Genebank accession | Identities | p-value b |
---|---|---|---|---|---|
Kinase | |||||
1 | I | leucine-rich repeat transmembrane protein kinase | NP_199948 | 64% | 5.41 × 10−5 |
1 | S | leucine-rich repeat family protein kinase | NP_179336 | 42% | 1.02 × 10−4 |
1 | I | tousled-like serine/threonine kinase | NP_568405 | 82% | 3.20 × 10−5 |
1 | I | CIPK5 | NP_568241 | 79% | 7.74 × 10−5 |
1 | S | CIPK6 | NP_194825 | 80% | 1.98 × 10−7 |
1 | S | protein kinase family protein | NP_194952 | 50% | 2.25 × 10−5 |
Transcription factor | |||||
1 | I | IAA-LEUCINE RESISTANT3 | NP_200279 | 89% | 4.97 × 10−4 |
1 | I | IAA26 | NP_188271 | 80% | 3.58 × 10−6 |
1 | S | GT-like trihelix DNA-binding protein | NP_177814 | 37% | 3.04 × 10−6 |
1 | S | zinc finger (CCCH-type) family protein | NP_200670 | 59% | 8.13 × 10−5 |
1 | I | WRKY family transcription factor | NP_001078015 | 50% | 4.52 × 10−5 |
1 | S | GRAS family transcription factor | XP_002322514 | 52% | 3.58 × 10−4 |
2 | S | AP2 transcription factor | NP_173355 | 70% | 4.26 × 10−6 |
1 | I | SALT TOLERANCE homolog protein | NP_849598 | 68% | 5.37 × 10−7 |
1 | S | Auxin response factor | NP_182176 | 70% | 2.78 × 10−3 |
Number | Expression a | Putative annotation | Genebank accession | Identities | p-value b |
---|---|---|---|---|---|
1 | S | 1-deoxy-D-xylulose-5-phosphate synthase | NP_193291. | 41% | 5.20 × 10−4 |
1 | I | lil3 protein | NP_199522 | 51% | 2.56 × 10−7 |
2 | I | photosystem II subunit R | NP_178025 | 75% | 3.43 × 10−6 |
1 | I | CHLOROPHYLL A/B BINDING PROTEIN 1 | NP_174286 | 67% | 4.38 × 10−3 |
2 | I | PSAF (photosystem I subunit F) | NP_174418 | 72% | 3.75 × 10−5 |
1 | I | photosystem II CP43 chlorophyll apoprotein | YP_002149729 | 90% | 6.54 × 10−8 |
1 | I | photosystem I subunit D-2 | NP_171812 | 72% | 8.79 × 10−4 |
1 | I | Thylakoid membrane phosphoprotein of 14 kda | NP_566086 | 64% | 9.54 × 10−7 |
1 | I | Photosystem I light harvesting complex gene 3 | NP_176347 | 81% | 5.37 × 10−6 |
1 | I | cytochrome b6 | NP_051088 | 98% | 5.86 × 10−7 |
1 | I | ATP synthase gamma chain | NP_567265 | 77% | 7.35 × 10−4 |
1 | I | NADH dehydrogenase subunit 7 | NP_051115 | 87% | 2.36 × 10−7 |
2 | I | photosystem II 44 kDa protein | NP_051055 | 97% | 5.38 × 10−5 |
5 | I | light-harvesting complex I protein Lhca3 | XP_002321218 | 81% | 6.67 × 10−6 |
1 | I | Oxygen-evolving enhancer protein | NP_201458 | 83% | 4.31 × 10−3 |
1 | I | PSBP-1 (PHOTOSYSTEM II SUBUNIT P-1) | NP_172153 | 64% | 3.34 × 10−4 |
1 | I | FERREDOXIN-NADP(+)-OXIDOREDUCTASE 1 | NP_201420 | 76% | 4.53 × 10−5 |
1 | I | plastid-lipid-associated protein | NP_192311 | 44% | 5.61 × 10−4 |
65 | I | ribulose-1,5-bisphosphate carboxylase | CAA79857 | 91% | 5.64 × 10−6 |
1 | I | photosystem I P700 chlorophyll a apoprotein A2 | NP_051058 | 98% | 6.35 × 10−3 |
7 | I | light-harvesting complex II protein Lhcb2 | XP_002321186 | 92% | 6.89 × 10−7 |
1 | I | light-harvesting complex I protein Lhca4 | XP_002330127 | 75% | 8.32 × 10−6 |
1 | I | light-harvesting complex I protein Lhca2 | XP_002299309 | 94% | 3.57 × 10−4 |
1 | I | PHOTOSYSTEM II SUBUNIT O-2 | NP_190651 | 75% | 4.25 × 10−5 |
1 | S | PsbP domain-containing protein | NP_565131 | 65% | 6.31 × 10−7 |
5 | I | light-harvesting complex II protein Lhcb1 | XP_002316737 | 95% | 2.58 × 10−2 |
6 | I | light-harvesting complex II protein Lhcb6 | XP_002303160 | 82% | 5.34 × 10−5 |
1 | I | light-harvesting complex II protein Lhcb5 | XP_002329192 | 81% | 6.41 × 10−7 |
2 | I | photosystem II 22 kDa protein | NP_001150026 | 91% | 3.59 × 10−3 |
2 | I | protochlorophyllide reductase | NP_200230 | 65% | 5.34 × 10−7 |
1 | I | Clp protease proteolytic subunit 6 | NP_563893 | 45% | 4.37 × 10−5 |
2 | I | magnesium chelatase H subunit | ACO57443 | 100% | 1.82 × 10−8 |
1 | I | Photosystem I P700 chlorophyll A apoprotein | NP_001044491 | 60% | 2.59 × 10−4 |
1 | I | carbonic anhydrase | NP_186799 | 61% | 1.56 × 10−4 |
1 | I | starch synthase | NP_174566 | 36% | 8.24 × 10−5 |
1 | I | glucose-1-phosphate adenylyltransferase | NP_197423 | 81% | 2.34 × 10−7 |
1 | I | ribulose-phosphate 3-epimerase, RPE | NP_200949. | 83% | 5.20 × 10−4 |
Acknowledgments
Conflicts of Interest
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Li, Q.; Liu, J.; Tan, D.; Allan, A.C.; Jiang, Y.; Xu, X.; Han, Z.; Kong, J. A Genome-Wide Expression Profile of Salt-Responsive Genes in the Apple Rootstock Malus zumi. Int. J. Mol. Sci. 2013, 14, 21053-21070. https://doi.org/10.3390/ijms141021053
Li Q, Liu J, Tan D, Allan AC, Jiang Y, Xu X, Han Z, Kong J. A Genome-Wide Expression Profile of Salt-Responsive Genes in the Apple Rootstock Malus zumi. International Journal of Molecular Sciences. 2013; 14(10):21053-21070. https://doi.org/10.3390/ijms141021053
Chicago/Turabian StyleLi, Qingtian, Jia Liu, Dunxian Tan, Andrew C. Allan, Yuzhuang Jiang, Xuefeng Xu, Zhenhai Han, and Jin Kong. 2013. "A Genome-Wide Expression Profile of Salt-Responsive Genes in the Apple Rootstock Malus zumi" International Journal of Molecular Sciences 14, no. 10: 21053-21070. https://doi.org/10.3390/ijms141021053