Skip to main content
Log in

Identification of hub genes that variate the qCSS12-mediated cold tolerance between indica and japonica rice using WGCNA

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Cold-tolerant QTL qCSS12-regulated 14 hub genes are involved in the chloroplastic biological processes and in the protein synthesis and degradation processes in japonica rice.

Abstract

Low temperature is a main constraint factor for rice growth and production. To better understand the regulatory mechanisms underlying the cold tolerance phenotype in rice, here, we selected a cold-sensitive nearly isogenic line (NIL) NIL(qcss12) as materials to identify hub genes that are mediated by the cold-tolerant locus qCSS12 through weighted gene co-expression network analysis (WGCNA). Fourteen cold-responsive genes were identified, of which, 6 are involved in regulating biological processes in chloroplasts, including the reported EF-Tu, Prk, and ChlD, and 8 are involved in the protein synthesis and degradation processes. Differential expression of these genes between NIL(qcss12) and its controls under cold stress may be responsible for qCSS12-mediated cold tolerance in japonica rice. Moreover, natural variations in 12 of these hub genes are highly correlated with the cold tolerance divergence in two rice subspecies. The results provide deep insights into a better understanding of the molecular basis of cold adaptation in rice and provide a theoretical basis for molecular breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The raw sequence data reported in this paper have been deposited in the Genome Sequence Archive (Genomics, Proteomics & Bioinformatics 2021) in National Genomics Data Center (Nucleic Acids Res 2022), and China National Center for Bioinformation/Beijing Institute of Genomics, Chinese Academy of Sciences (GSA: CRA011931) that are publicly accessible at https://ngdc.cncb.ac.cn/gsa. The other datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Boisnard A, Albar L, Thiéméle D, Rondeau M, Ghesquière A (2007) Evaluation of genes from eIF4E and eIF4G multigenic families as potential candidates for partial resistance QTLs to Rice yellow mottle virus in rice. Theor Appl Genet 116:53–62

    Article  CAS  PubMed  Google Scholar 

  • Bu D, Luo H, Huo P, Wang Z, Zhang S, He Z, Wu Y, Zhao L, Liu J, Guo J (2021) KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res 49:W317–W325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai L, Liu Z, Cai L, Yan X, Hu Y, Hao B, Xu Z, Tian Y, Liu X, Liu L, Jiang L, Zhou S, Wan J (2022) Nuclear encoded elongation factor EF-Tu is required for chloroplast development in rice grown under low-temperature conditions. J Genet Genom 49:502–505

    Article  CAS  Google Scholar 

  • Cen W, Liu J, Lu S, Jia P, Yu K, Han Y, Li R, Luo J (2018) Comparative proteomic analysis of QTL CTS-12 derived from wild rice (Oryza rufipogon Griff.), in the regulation of cold acclimation and de-acclimation of rice (Oryza sativa L.) in response to severe chilling stress. BMC Plant Biol 18:1–17

    Article  Google Scholar 

  • Chaston JJ, Smits C, Aragão D, Wong AS, Ahsan B, Sandin S, Molugu SK, Molugu SK, Bernal RA, Stock D (2016) Structural and functional insights into the evolution and stress adaptation of type II chaperonins. Structure 24:364–374

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Yu T, Xiong J, Zhang Y, Hua Y, Li Y, Zhu Y (2005) Molecular cloning and expression analysis of rice phosphoribulokinase gene that is regulated by environmental stresses. Mol Biol Rep 31:249–255

    Article  Google Scholar 

  • Chen X, Lin S, Liu Q, Huang J, Zhang W, Lin J, Wang Y, Ke Y, He H (2014) Expression and interaction of small heat shock proteins (sHsps) in rice in response to heat stress. Biochim Biophys Acta 1844:818–828

    Article  CAS  PubMed  Google Scholar 

  • Childs KL, Davidson RM, Buell CR (2011) Gene coexpression network analysis as a source of functional annotation for rice genes. PLoS ONE 6:e22196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Zhu J, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du H, Guo Z, Xiong L (2018) Determination of relative rice leaf water content. Bio 101:e1010157

    Google Scholar 

  • Gan P, Liu F, Li R, Wang S, Luo J (2019) Chloroplasts—beyond energy capture and carbon fixation: tuning of photosynthesis in response to chilling stress. Int J Mol Sci 20:5046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ju F, Sun L, Xiong C, Wang Z, Yu H, Pang J, Bai H, Zhao W, Zhou Z, Chen B (2023) Weighted gene co-expression network analysis revealed the key pathways and hub genes of potassium regulating cotton root adaptation to salt stress. Front Plant Sci 14:1132877

    Article  PubMed  PubMed Central  Google Scholar 

  • Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from Japonica rice. Science 301:376–379

    Article  PubMed  Google Scholar 

  • Kim JH, Lim SD, Jang CS (2020) Oryza sativa drought-, heat-, and salt-induced RING finger protein 1 (OsDHSRP1) negatively regulates abiotic stress-responsive gene expression. Plant Mol Biol 103:235–252

    Article  CAS  PubMed  Google Scholar 

  • Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578–587

    Article  CAS  PubMed  Google Scholar 

  • Krab IM, Parmeggiani A (2002) Mechanisms of EF-Tu, a pioneer GTPase. Prog Nucleic Acid Res Mol Biol 71:513–551

    Article  CAS  PubMed  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  CAS  PubMed  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:1–13

    Article  Google Scholar 

  • Li X, Chao D, Wu Y, Huang X, Chen K, Cui L, Su L, Ye W, Chen H, Chen H (2015) Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat Genet 47:827–833

    Article  CAS  PubMed  Google Scholar 

  • Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S (2017) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43:630–642

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zeng PY, Zhou ZZ, Guo H, Lou Q, Shui G, Huang H, Tian H, Guo Y, Yuan P, Yang H, Pan G, Wang R, Zhang H, Yang S, Guo Y, Ge S, Li J, Li Z (2021) Stepwise selection of natural variations at CTB2 and CTB4a improves cold adaptation during domestication of japonica rice. New Phytol 231:1056–1072

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhang Z, Chong K, Xu Y (2022) Chilling tolerance in rice: past and present. J Plant Physiol 268:153576

    Article  CAS  PubMed  Google Scholar 

  • Lin J, Yu M, Xu X, Wang Y, Zhu Y (2020) Identification of biomarkers related to CD8+ T cell infiltration with gene co-expression network in clear cell renal cell carcinoma. Aging 12:3694–3712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Deng H (2009) Development of genetic and QTLs analysis for cold tolerance in rice. Chin Agric Sci Bull 25:45–50

    Google Scholar 

  • Liu X, Lan J, Huang Y, Cao P, Zhou C, Ren Y, He N, Liu S, Tian Y, Nguyen T (2018) WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress. J Exp Bot 69:3949–3961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Zhou Y, Fan F, Peng J, Zhang J (2020) Coordination of light, circadian clock with temperature: the potential mechanisms regulating chilling tolerance in rice. J Integr Plant Biol 62:737–760

    Article  PubMed  Google Scholar 

  • Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D (2015) COLD1 confers chilling tolerance in rice. Cell 160:1209–1221

    Article  CAS  PubMed  Google Scholar 

  • Mao D, Xin Y, Tan Y, Hu X, Bai J, Liu Z, Yu Y, Li L, Peng C, Fan T (2019) Natural variation in the HAN1 gene confers chilling tolerance in rice and allowed adaptation to a temperate climate. Proc Natl Acad Sci USA 116:3494–3501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, Matsukura S, Takasaki H, Sakurai T, Yamamoto YY, Yoshiwara K (2012) Identification of cis-acting promoter elements in cold-and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19:37–49

    Article  CAS  PubMed  Google Scholar 

  • Masuda T, Fujita Y (2008) Regulation and evolution of chlorophyll metabolism. Photochem Photobiol Sci 7:1131–1149

    Article  CAS  PubMed  Google Scholar 

  • Park YC, Lim SD, Moon JC, Jang CS (2019) A rice really interesting new gene H2-type E3 ligase, OsSIRH2-14, enhances salinity tolerance via ubiquitin/26S proteasome-mediated degradation of salt-related proteins. Plant, Cell Environ 42:3061–3076

    Article  CAS  PubMed  Google Scholar 

  • Pradhan SK, Pandit E, Nayak DK, Behera L, Mohapatra T (2019) Genes, pathways and transcription factors involved in seedling stage chilling stress tolerance in indica rice through RNA-Seq analysis. BMC Plant Biol 19:1–17

    Article  CAS  Google Scholar 

  • Ruan B, Gao Z, Zhao J, Zhang B, Zhang A, Hong K, Yang S, Jiang H, Liu C, Chen G (2017) The rice YGL gene encoding an Mg 2+-chelatase ChlD subunit is affected by temperature for chlorophyll biosynthesis. J Plant Biol 60:314–321

    Article  CAS  Google Scholar 

  • Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang C, Iwamoto M, Abe T (2013) Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibahara T, Kawasaki H, Hirano H (2002) Identification of the 19S regulatory particle subunits from the rice 26S proteasome. Eur J Biochem 269:1474–1483

    Article  CAS  PubMed  Google Scholar 

  • Song J, Wei X, Shao G, Sheng Z, Chen D, Liu C, Jiao G, Xie L, Tang S, Hu P (2014) The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions. Plant Mol Biol 84:301–314

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47:D607–D613

    Article  CAS  PubMed  Google Scholar 

  • Tan J, Tan Z, Wu F, Sheng P, Heng Y, Wang X, Ren Y, Wang J, Guo X, Zhang X (2014) A novel chloroplast-localized pentatricopeptide repeat protein involved in splicing affects chloroplast development and abiotic stress response in rice. Mol Plant 7:1329–1349

    Article  CAS  PubMed  Google Scholar 

  • The 3000 rice genomes project (2014) The 3000 rice genomes project. Gigascience 3:1–6

    Google Scholar 

  • The UniProt Consortium (2023) UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res 51:D523–D531

    Article  Google Scholar 

  • Tian J, Ma Y, Tian L, Huang C, Chen M, Wei A (2021) Comparative physiology and transcriptome response patterns in cold-tolerant and cold-sensitive varieties of Zanthoxylum bungeanum Maxim. Ind Crop Prod 167:113562

    Article  CAS  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  PubMed  Google Scholar 

  • Wang J, Qi M, Liu J, Zhang Y (2015) CARMO: a comprehensive annotation platform for functional exploration of rice multi-omics data. Plant J 83:359–374

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Ren Y, Zhou K, Liu L, Wang J, Xu Y, Zhang H, Zhang L, Feng Z, Wang L (2017) WHITE STRIPE LEAF4 encodes a novel P-type PPR protein required for chloroplast biogenesis during early leaf development. Front Plant Sci 8:1116

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, Yu H, Huang J, Wang W, Faruquee M, Zhang F, Zhao X, Fu B, Chen K, Zhang H (2019) Towards a deeper haplotype mining of complex traits in rice with RFGB v2. 0. Plant Biotechnol J 18:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Deng C, Ai P, Zhang Z (2021) ALM1, encoding a Fe-superoxide dismutase, is critical for rice chloroplast biogenesis and drought stress response. Crop J 9:1018–1029

    Article  Google Scholar 

  • Wu L, Wu J, Liu Y, Gong X, Xu J, Lin D, Dong Y (2016) The rice pentatricopeptide repeat gene TCD10 is needed for chloroplast development under cold stress. Rice 9:1–13

    Article  Google Scholar 

  • Xu D, Ni Y, Zhang X, Guo Y (2022) Multiomic analyses of two sorghum cultivars reveals the change of membrane lipids in their responses to water deficit. Plant Physiol Biochem 176:44–56

    Article  CAS  PubMed  Google Scholar 

  • You J, Fang Y, Xiong L (2018) Reactive oxygen detection. Bio 101:e1010170

    Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu J, Cheng Y, Feng K, Ruan M, Ye Q, Wang R, Li Z, Zhou G, Yao Z, Yang Y (2016) Genome-wide identification and expression profiling of tomato Hsp20 gene family in response to biotic and abiotic stresses. Front Plant Sci 7:1215

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu B, Liu J, Wu D, Liu Y, Cen W, Wang S, Li R, Luo J (2020) Weighted gene coexpression network analysis-based identification of key modules and hub genes associated with drought sensitivity in rice. BMC Plant Biol 20:478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng D, Tian Z, Rao Y, Dong G, Yang Y, Huang L, Leng Y, Xu J, Sun C, Zhang G (2017) Rational design of high-yield and superior-quality rice. Nat Plants 3:1–5

    Article  Google Scholar 

  • Zhang Z, Li J, Li F, Liu H, Yang W, Chong K, Xu Y (2017a) OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell 43:731–743

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Li J, Pan Y, Li J, Zhou L, Shi H, Zeng Y, Guo H, Yang S, Zheng W, Yu J, Sun X, Li G, Ding Y, Ma L, Shen S, Dai L, Zhang H, Yang S, Guo Y, Li Z (2017b) Natural variation in CTB4a enhances rice adaptation to cold habitats. Nat Commun 8:14788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Yao W, Ouyang Y, Yang W, Wang G, Lian X, Xing Y, Chen L, Xie W (2015) RiceVarMap: a comprehensive database of rice genomic variations. Nucleic Acids Res 43:D1018–D1022

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Hongxuan Lin (Institute of Plant physiology and Ecology, Shanghai, China) and Prof. Wensheng Wang (Chinese Academy of Agricultural Sciences, Beijing, China) for kindly providing the rice materials for this study.

Funding

This work was supported by the National Natural Science Foundation of China (CN) (31671646), the State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources (SKLCUSA-a08), the Talent, Science, and technology projects (Barenke-20220001), and the Natural Science Foundation of Guangxi Province (2018GXNSFDA138004).

Author information

Authors and Affiliations

Authors

Contributions

JL, PG, and RL conceived and designed the experiments. PG and HW performed all the lab experiments. PG, XL, and HW conducted the field trials and collected the samples for RNA-Seq. PG and YH performed WGCNA and data processing. PG drafted the manuscript. JL revised the manuscript. All the authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Jijing Luo.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Communicated by Haitao Shi.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gan, P., Luo, X., Wei, H. et al. Identification of hub genes that variate the qCSS12-mediated cold tolerance between indica and japonica rice using WGCNA. Plant Cell Rep 43, 24 (2024). https://doi.org/10.1007/s00299-023-03093-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00299-023-03093-8

Keywords

Navigation