Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

A meta-analysis of microarray data revealed hub genes and transcription factors involved in drought stress response in rice (Oryza sativa L.)

Sedigheh Soltanpour A , AliReza Tarinejad https://orcid.org/0000-0002-8418-7663 A * , Karim Hasanpur B and Mohammad Majidi B
+ Author Affiliations
- Author Affiliations

A Department of Agricultural Biotechnology, Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran.

B Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran.

* Correspondence to: tarinejad@yahoo.com

Handling Editor: Manuela Chaves

Functional Plant Biology 49(10) 898-916 https://doi.org/10.1071/FP22028
Submitted: 16 February 2022  Accepted: 21 June 2022   Published: 8 July 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Although there are various studies attempted to clarify the genetic mechanism of plant response to drought stress that reduces crop yield, a meta-analysis can integrate the results of them to provide a better picture of the issue. Therefore, in this study, several microarray datasets of rice were meta-analysed under drought stress and normal condition using the R packages. Accordingly, differentially expressed genes (meta-DEGs) were identified. The results showed 643 and 677 upregulated and downregulated genes, respectively. The significant common Gene Ontology (GO) terms between the up- and downregulated genes were responses to abiotic stimulus, water deprivation, oxygen-containing compound and abscisic acid. The transcription factors (TF) survey showed that bHLH under drought stress activates up genes 42% more than down genes while bzip Homeodomain activates down genes 54% more than up genes. The hub downregulated genes obtained from this study were mainly related to photosynthesis and the hub upregulated genes were mainly related to stress tolerance which include heat shock proteins (HSPs), late embryogenesis abundant (LEAs), calmodulin-like protein (CML), phosphatase 2C (PP2Cs) and IAA genes. Moreover, this meta-analysis data were compared with other experimental data and the results confirmed the up and down expression of them. Our findings can provide novel insights into the molecular mechanism of rice (Oryza sativa L.) response to drought stress.

Keywords: abiotic stress, CO2 fixation, functional genomic, gene discovery, gene ontology, Oryza sativa L., process, up-regulation.


References

Abdel-Ghany SE, Ullah F, Ben-Hur A, Reddy ASN (2020) Transcriptome analysis of drought-resistant and drought-sensitive sorghum (Sorghum bicolor) genotypes in response to PEG-induced drought stress. International Journal of Molecular Sciences 21, 772
Transcriptome analysis of drought-resistant and drought-sensitive sorghum (Sorghum bicolor) genotypes in response to PEG-induced drought stress.Crossref | GoogleScholarGoogle Scholar |

Ali F, Bano A, Fazal A (2017) Recent methods of drought stress tolerance in plants. Plant Growth Regulation 82, 363–375.
Recent methods of drought stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Bhargava A, Clabaugh I, To JP, et al. (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiology 162, 272–294.
Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23524861PubMed |

Bielsa B, Leida C, Rubio-Cabetas MJ (2016) Physiological characterization of drought stress response and expression of two transcription factors and two LEA genes in three Prunus genotypes. Scientia Horticulturae 213, 260–269.
Physiological characterization of drought stress response and expression of two transcription factors and two LEA genes in three Prunus genotypes.Crossref | GoogleScholarGoogle Scholar |

Cai B, Li Q, Xu Y, Yang L, Bi H, Ai X (2016) Genome-wide analysis of the fructose 1,6-bisphosphate aldolase (FBA) gene family and functional characterization of FBA7 in tomato. Plant Physiology and Biochemistry 108, 251–265.
Genome-wide analysis of the fructose 1,6-bisphosphate aldolase (FBA) gene family and functional characterization of FBA7 in tomato.Crossref | GoogleScholarGoogle Scholar | 27474933PubMed |

Chaudhary R, Baranwal VK, Kumar R, Sircar D, Chauhan H (2019) Genome-wide identification and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development. Functional & Integrative Genomics 19, 1007–1022.
Genome-wide identification and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development.Crossref | GoogleScholarGoogle Scholar |

Chen X, Wang Y, Lv B, et al. (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant and Cell Physiology 55, 604–619.
The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway.Crossref | GoogleScholarGoogle Scholar | 24399239PubMed |

Chin C-H, Chen S-H, Wu H-H, Ho C-W, Ko M-T, Lin C-Y (2014) cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Systems Biology 8, S11
cytoHubba: identifying hub objects and sub-networks from complex interactome.Crossref | GoogleScholarGoogle Scholar | 25521941PubMed |

da Maia LC, Cadore PRB, Benitez LC, Danielowski R, Braga EJB, Fagundes PRR, Magalhães AM, Costa de Oliveira A (2017) Transcriptome profiling of rice seedlings under cold stress. Functional Plant Biology 44, 419–429.
Transcriptome profiling of rice seedlings under cold stress.Crossref | GoogleScholarGoogle Scholar | 32480575PubMed |

de Abreu Neto JB, Frei M (2016) Microarray meta-analysis focused on the response of genes involved in redox homeostasis to diverse abiotic stresses in rice. Frontiers in Plant Science 6, 1260
Microarray meta-analysis focused on the response of genes involved in redox homeostasis to diverse abiotic stresses in rice.Crossref | GoogleScholarGoogle Scholar | 26793229PubMed |

Ding X, Li X, Xiong L (2013) Insight into differential responses of upland and paddy rice to drought stress by comparative expression profiling analysis. International Journal of Molecular Sciences 14, 5214–5238.
Insight into differential responses of upland and paddy rice to drought stress by comparative expression profiling analysis.Crossref | GoogleScholarGoogle Scholar | 23459234PubMed |

González-Gordo S, Bautista R, Claros MG, Cañas A, Palma JM, Corpas FJ (2019) Nitric oxide-dependent regulation of sweet pepper fruit ripening. Journal of Experimental Botany 70, 4557–4570.
Nitric oxide-dependent regulation of sweet pepper fruit ripening.Crossref | GoogleScholarGoogle Scholar | 31046097PubMed |

Grennan AK (2006) Abiotic stress in rice. An “Omic” approach. Plant Physiology 140, 1139–1141.
Abiotic stress in rice. An “Omic” approach.Crossref | GoogleScholarGoogle Scholar | 16607027PubMed |

Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao S-J (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants 9, 491
Transcription factors in plant stress responses: challenges and potential for sugarcane improvement.Crossref | GoogleScholarGoogle Scholar |

Khazaei Z, Esmaielpour B, Estaji A (2020) Ameliorative effects of ascorbic acid on tolerance to drought stress on pepper (Capsicum annuum L) plants. Physiology and Molecular Biology of Plants 26, 1649–1662.
Ameliorative effects of ascorbic acid on tolerance to drought stress on pepper (Capsicum annuum L) plants.Crossref | GoogleScholarGoogle Scholar | 32801493PubMed |

Lee HY, Jang G, Um T, Kim J-K, Lee JS, Do Choi Y (2015) The soluble ABA receptor PYL8 regulates drought resistance by controlling ABA signaling in Arabidopsis. Plant Biotechnology Reports 9, 319–330.
The soluble ABA receptor PYL8 regulates drought resistance by controlling ABA signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Li N, Zhang S, Liang Y, et al. (2018) Label-free quantitative proteomic analysis of drought stress-responsive late embryogenesis abundant proteins in the seedling leaves of two wheat (Triticum aestivum L.) genotypes. Journal of Proteomics 172, 122–142.
Label-free quantitative proteomic analysis of drought stress-responsive late embryogenesis abundant proteins in the seedling leaves of two wheat (Triticum aestivum L.) genotypes.Crossref | GoogleScholarGoogle Scholar | 28982538PubMed |

Li Y, Liu Pp, Ni X (2019a) Molecular evolution and functional analysis of rubredoxin-like proteins in plants. BioMed Research International 2019, 1–14.
Molecular evolution and functional analysis of rubredoxin-like proteins in plants.Crossref | GoogleScholarGoogle Scholar |

Li Z, Liu C, Zhang Y, Wang B, Ran Q, Zhang J (2019b) The bHLH family member ZmPTF1 regulates drought tolerance in maize by promoting root development and abscisic acid synthesis. Journal of Experimental Botany 70, 5471–5486.
The bHLH family member ZmPTF1 regulates drought tolerance in maize by promoting root development and abscisic acid synthesis.Crossref | GoogleScholarGoogle Scholar | 31267122PubMed |

Li H, Yuan H, Liu F, et al. (2020) BpTCP7 gene from Betula platyphylla regulates tolerance to salt and drought stress through multiple hormone pathways. Plant Cell, Tissue and Organ Culture (PCTOC) 141, 17–30.
BpTCP7 gene from Betula platyphylla regulates tolerance to salt and drought stress through multiple hormone pathways.Crossref | GoogleScholarGoogle Scholar |

Liang Y, Tabien RE, Tarpley L, Mohammed AR, Septiningsih EM (2021) Transcriptome profiling of two rice genotypes under mild field drought stress during grain-filling stage. AoB PLANTS 13, plab043
Transcriptome profiling of two rice genotypes under mild field drought stress during grain-filling stage.Crossref | GoogleScholarGoogle Scholar | 34354811PubMed |

Liu H, Gao Y, Wu M, et al. (2020a) TCP10, a TCP transcription factor in moso bamboo (Phyllostachys edulis), confers drought tolerance to transgenic plants. Environmental and Experimental Botany 172, 104002
TCP10, a TCP transcription factor in moso bamboo (Phyllostachys edulis), confers drought tolerance to transgenic plants.Crossref | GoogleScholarGoogle Scholar |

Liu H, Wang Z, Xu W, et al. (2020b) Bacillus pumilus LZP02 promotes rice root growth by improving carbohydrate metabolism and phenylpropanoid biosynthesis. Molecular Plant-Microbe Interactions 33, 1222–1231.
Bacillus pumilus LZP02 promotes rice root growth by improving carbohydrate metabolism and phenylpropanoid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 32597697PubMed |

Liu S, Zenda T, Dong A, Yang Y, Wang N, Duan H (2021) Global transcriptome and weighted gene co-expression network analyses of growth-stage-specific drought stress responses in maize. Frontiers in Genetics 12, 645443
Global transcriptome and weighted gene co-expression network analyses of growth-stage-specific drought stress responses in maize.Crossref | GoogleScholarGoogle Scholar | 33574835PubMed |

Magwanga RO, Lu P, Kirungu JN, et al. (2018) Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genetics 19, 6
Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton.Crossref | GoogleScholarGoogle Scholar | 29334890PubMed |

Park S-H, Chung PJ, Juntawong P, et al. (2012) Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice. Plant Physiology 159, 1111–1124.
Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice.Crossref | GoogleScholarGoogle Scholar | 22566494PubMed |

Rabbani MA, Maruyama K, Abe H, et al. (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiology 133, 1755–1767.
Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.Crossref | GoogleScholarGoogle Scholar | 14645724PubMed |

Ramazan S, Nazir I, Yousuf W, John R (2022) Environmental stress tolerance in maize (Zea mays): role of polyamine metabolism. Functional Plant Biology
Environmental stress tolerance in maize (Zea mays): role of polyamine metabolism.Crossref | GoogleScholarGoogle Scholar | 35300784PubMed |

Ransbotyn V, Yeger-Lotem E, Basha O, et al. (2015) A combination of gene expression ranking and co-expression network analysis increases discovery rate in large-scale mutant screens for novel Arabidopsis thaliana abiotic stress genes. Plant Biotechnology Journal 13, 501–513.
A combination of gene expression ranking and co-expression network analysis increases discovery rate in large-scale mutant screens for novel Arabidopsis thaliana abiotic stress genes.Crossref | GoogleScholarGoogle Scholar | 25370817PubMed |

Razi K, Muneer S (2021) Drought stress-induced physiological mechanisms, signaling pathways and molecular response of chloroplasts in common vegetable crops. Critical Reviews in Biotechnology 41, 669–691.
Drought stress-induced physiological mechanisms, signaling pathways and molecular response of chloroplasts in common vegetable crops.Crossref | GoogleScholarGoogle Scholar | 33525946PubMed |

Rest JS, Wilkins O, Yuan W, Purugganan MD, Gurevitch J (2016) Meta-analysis and meta-regression of transcriptomic responses to water stress in Arabidopsis. The Plant Journal 85, 548–560.
Meta-analysis and meta-regression of transcriptomic responses to water stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26756945PubMed |

Samarah NH, Mullen RE, Cianzio SR, Scott P (2006) Dehydrin-like proteins in soybean seeds in response to drought stress during seed filling. Crop Science 46, 2141–2150.
Dehydrin-like proteins in soybean seeds in response to drought stress during seed filling.Crossref | GoogleScholarGoogle Scholar |

Seong SY (2017) Overexpression of OsTZF8, a CCCH-Tandem Zinc finger, increases drought tolerance in rice. Master’s Thesis, Department of International Agricultural Technology, Graduate School of International Agricultural Technology, Seoul National University.

Shaik R, Ramakrishna W (2013) Genes and co-expression modules common to drought and bacterial stress responses in Arabidopsis and rice. PLoS ONE 8, e77261
Genes and co-expression modules common to drought and bacterial stress responses in Arabidopsis and rice.Crossref | GoogleScholarGoogle Scholar | 24130868PubMed |

Sharma R, Singh G, Bhattacharya S, Singh A (2018) Comparative transcriptome meta-analysis of Arabidopsis thaliana under drought and cold stress. PLoS ONE 13, e0203266
Comparative transcriptome meta-analysis of Arabidopsis thaliana under drought and cold stress.Crossref | GoogleScholarGoogle Scholar | 30192796PubMed |

Singh A, Jha SK, Bagri J, Pandey GK (2015) ABA inducible rice protein phosphatase 2C confers ABA insensitivity and abiotic stress tolerance in Arabidopsis. PLoS ONE 10, e0125168
ABA inducible rice protein phosphatase 2C confers ABA insensitivity and abiotic stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25886365PubMed |

Sirohi P, Yadav BS, Afzal S, Mani A, Singh NK (2020) Identification of drought stress-responsive genes in rice (Oryza sativa) by meta-analysis of microarray data. Journal of Genetics 99, 35
Identification of drought stress-responsive genes in rice (Oryza sativa) by meta-analysis of microarray data.Crossref | GoogleScholarGoogle Scholar | 32482924PubMed |

Sun X, Wang Y, Sui N (2018) Transcriptional regulation of bHLH during plant response to stress. Biochemical and Biophysical Research Communications 503, 397–401.
Transcriptional regulation of bHLH during plant response to stress.Crossref | GoogleScholarGoogle Scholar | 30057319PubMed |

Tang J, Bassham DC (2022) Autophagy during drought: function, regulation, and potential application. The Plant Journal 109, 390–401.
Autophagy during drought: function, regulation, and potential application.Crossref | GoogleScholarGoogle Scholar | 34469611PubMed |

Tseng GC, Ghosh D, Feingold E (2012) Comprehensive literature review and statistical considerations for microarray meta-analysis. Nucleic Acids Research 40, 3785–3799.
Comprehensive literature review and statistical considerations for microarray meta-analysis.Crossref | GoogleScholarGoogle Scholar | 22262733PubMed |

Wairich A, de Oliveira BHN, Wu L-B, et al. (2021) Chromosomal introgressions from Oryza meridionalis into domesticated rice Oryza sativa result in iron tolerance. Journal of Experimental Botany 72, 2242–2259.
Chromosomal introgressions from Oryza meridionalis into domesticated rice Oryza sativa result in iron tolerance.Crossref | GoogleScholarGoogle Scholar | 33035327PubMed |

Wang J, Leeflang M (2019) Recommended software/packages for meta-analysis of diagnostic accuracy. Journal of Laboratory and Precision Medicine 4, 22
Recommended software/packages for meta-analysis of diagnostic accuracy.Crossref | GoogleScholarGoogle Scholar |

Wang X-S, Zhu H-B, Jin G-L, Liu H-L, Wu W-R, Zhu J (2007) Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.). Plant Science 172, 414–420.
Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theoretical and Applied Genetics 115, 35–46.
Over-expression of a LEA gene in rice improves drought resistance under the field conditions.Crossref | GoogleScholarGoogle Scholar | 17426956PubMed |

Zang G, Zou H, Zhang Y, et al. (2016) The de-etiolated 1 homolog of Arabidopsis modulates the ABA signaling pathway and ABA biosynthesis in rice. Plant Physiology 171, 1259–1276.
The de-etiolated 1 homolog of Arabidopsis modulates the ABA signaling pathway and ABA biosynthesis in rice.Crossref | GoogleScholarGoogle Scholar | 27208292PubMed |

Zegzouti H, Jones B, Marty C, et al. (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding. Plant Molecular Biology 35, 847–854.
ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding.Crossref | GoogleScholarGoogle Scholar | 9426604PubMed |

Zeng H, Xu L, Singh A, Wang H, Du L, Poovaiah BW (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Frontiers in Plant Science 6, 600
Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 26322054PubMed |