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COG2 negatively regulates chilling tolerance through cell wall components altered in rice

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Abstract

Key message

Chilling-tolerant QTL gene COG2 encoded an extensin and repressed chilling tolerance by affecting the compositions of cell wall.

Abstract

Rice as a major crop is susceptible to chilling stress. Chilling tolerance is a complex trait controlled by multiple quantitative trait loci (QTLs). Here, we identify a QTL gene, COG2, that negatively regulates cold tolerance at seedling stage in rice. COG2 overexpression transgenic plants are sensitive to cold, whereas knockout transgenic lines enhance chilling tolerance. Natural variation analysis shows that Hap1 is a specific haplotype in japonica/Geng rice and correlates with chilling tolerance. The SNP1 in COG2 promoter is a specific divergency and leads to the difference in the expression level of COG2 between japonica/Geng and indica/Xian cultivars. COG2 encodes a cell wall-localized extensin and affects the compositions of cell wall, including pectin and cellulose, to defense the chilling stress. The results extend the understanding of the adaptation to the environment and provide an editing target for molecular design breeding of cold tolerance in rice.

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All data generated or analyzed during this study are included in this published article [and its supplementary information files].

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References

  • Bethke G, Thao A, Xiong G, Li B, Soltis NE, Hatsugai N, Hillmer RA, Katagiri F, Kliebenstein DJ, Pauly M, Glazebrook J (2016) Pectin biosynthesis is critical for cell wall integrity and immunity in Arabidopsis thaliana. Plant Cell 28:537–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  Google Scholar 

  • Borassi C, Sede AR, Mecchia MA, Salgado Salter JD, Marzol E, Muschietti JP, Estevez JM (2016) An update on cell surface proteins containing extensin-motifs. J Exp Bot 67:477–487

    Article  CAS  PubMed  Google Scholar 

  • Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, Chen L, Lamport DT, Chen Y, Kieliszewski MJ (2008) Self-assembly of the plant cell wall requires an extensin scaffold. Proc Natl Acad Sci USA 105:2226–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castilleux R, Plancot B, Vicre M, Nguema-Ona E, Driouich A (2021) Extensin, an underestimated key component of cell wall defence? Ann Bot 127:709–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Zhao Y, Xu S, Zhang Z, Xu Y, Zhang J, Chong K (2018) OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice. New Phytol 218:219–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Jiang L, Zheng J, Chen F, Wang T, Wang M, Tao Y, Wang H, Hong Z, Huang Y, Huang R (2019) A missense mutation in Large Grain Size 1 increases grain size and enhances cold tolerance in rice. J Exp Bot 70:3851–3866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Daher FB, Braybrook SA (2015) How to let go: pectin and plant cell adhesion. Front Plant Sci 6:523–530

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan C, Li Y, Hu Z, Hu H, Wang G, Li A, Wang Y, Tu Y, Xia T, Peng L, Feng S (2018) Ectopic expression of a novel OsExtensin-like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice. Plant Biotechnol J 16:254–263

    Article  CAS  PubMed  Google Scholar 

  • Fang C, Li K, Wu Y, Wang D, Zhou J, Liu X, Li Y, Jin C, Liu X, Mur LAJ, Luo J (2019) OsTSD2-mediated cell wall modification affects ion homeostasis and salt tolerance. Plant Cell Environ 42:1503–1512

    Article  CAS  PubMed  Google Scholar 

  • Guo S, Xu Y, Liu H, Mao Z, Zhang C, Ma Y, Zhang Q, Meng Z, Chong K (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4:1566–1577

    Article  PubMed  Google Scholar 

  • Guo X, Liu D, Chong K (2018) Cold signaling in plants: insights into mechanisms and regulation. J Integr Plant Biol 60:745–756

    Article  PubMed  Google Scholar 

  • Gutaker RM, Groen SC, Bellis ES, Choi JY, Pires IS, Bocinsky RK, Slayton ER, Wilkins O, Castillo CC, Negrao S, Oliveira MM, Fuller DQ, Guedes JAD, Lasky JR, Purugganan MD (2020) Genomic history and ecology of the geographic spread of rice. Nat Plants 6:492–502

    Article  PubMed  Google Scholar 

  • Herger A, Dunser K, Kleine-Vehn J, Ringli C (2019) Leucine-rich repeat extensin proteins and their role in cell wall sensing. Curr Biol 29:R851–R858

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Sun S, Xu D, Lan H, Sun H, Wang Z, Bao Y, Wang J, Tang H, Zhang H (2012) A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (Oryza sativa L.). Plant Mol Biol 80:337–350

    Article  CAS  PubMed  Google Scholar 

  • Ke S, Luan X, Liang J, Hung YH, Hsieh TF, Zhang XQ (2019) Rice OsPEX1, an extensin-like protein, affects lignin biosynthesis and plant growth. Plant Mol Biol 100:151–161

    Article  CAS  PubMed  Google Scholar 

  • Kim SI, Andaya VC, Tai TH (2011) Cold sensitivity in rice (Oryza sativa L.) is strongly correlated with a naturally occurring I99V mutation in the multifunctional glutathione transferase isoenzyme GSTZ2. Biochem J 435:373–380

    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 

  • Lamport DT, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the extensin superfamily in primary cell wall architecture. Plant Physiol 156:11–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Ye K, Shi Y, Cheng J, Zhang X, Yang S (2017a) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10:545–559

    Article  CAS  PubMed  Google Scholar 

  • Li W, Zhu Z, Chern M, Yin J, Yang C, Ran L, Cheng M, He M, Wang K, Wang J, Zhou X, Zhu X, Chen Z, Wang J, Zhao W, Ma B, Qin P, Chen W, Wang Y, Liu J, Wang W, Wu X, Li P, Wang J, Zhu L, Li S, Chen X (2017b) A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170:114–126

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zeng Y, Pan Y, Zhou L, Zhang Z, 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 (2021a) 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 (2021b) Chilling tolerance in rice: past and present. J Plant Physiol 268:153576–153593

    Article  PubMed  Google Scholar 

  • Li Y, Liao S, Mei P, Pan Y, Zhang Y, Zheng X, Xie Y, Miao Y (2021c) OsWRKY93 dually functions between leaf senescence and in response to biotic stress in rice. Front Plant Sci 12:643011–643020

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Z, Wang B, Zhang Z, Luo W, Tang Y, Niu Y, Chong K, Xu Y (2021d) OsGRF6 interacts with SLR1 to regulate OsGA2ox1 expression for coordinating chilling tolerance and growth in rice. J Plant Physiol 260:153406–153414

    Article  CAS  PubMed  Google Scholar 

  • Lionetti V, Fabri E, De Caroli M, Hansen AR, Willats WG, Piro G, Bellincampi D (2017) Three pectin methylesterase inhibitors protect cell wall integrity for Arabidopsis immunity to botrytis. Plant Physiol 173:1844–1863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Ma Y, Chen N, Guo S, Liu H, Guo X, Chong K, Xu Y (2014) Overexpression of stress-inducible OsBURP16, the beta subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice. Plant Cell Environ 37:1144–1158

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Ou S, Mao B, Tang J, Wang W, Wang H, Cao S, Schlappi MR, Zhao B, Xiao G, Wang X, Chu C (2018a) Early selection of bZIP73 facilitated adaptation of japonica rice to cold climates. Nat Commun 9:3302–3313

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu CT, Wang W, Mao BG, Chu CC (2018b) Cold stress tolerance in rice: physiological changes, molecular mechanism, and future prospects. Yi Chuan 40:171–185

    PubMed  Google Scholar 

  • Liu C, Schlappi MR, Mao B, Wang W, Wang A, Chu C (2019) The bZIP73 transcription factor controls rice cold tolerance at the reproductive stage. Plant Biotechnol J 17:1834–1849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Yang L, Xu S, Lyu M-J, Wang J, Wang H, Zheng H, Xin W, Liu J, Zou D (2022) OsWRKY115 on qCT7 links to cold tolerance in rice. Theor Appl Genet. https://doi.org/10.1007/s00122-022-04117-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo W, Huan Q, Xu Y, Qian W, Chong K, Zhang J (2021) Integrated global analysis reveals a vitamin E-vitamin K1 sub-network, downstream of COLD1, underlying rice chilling tolerance divergence. Cell Rep 36:109397–109414

    Article  CAS  PubMed  Google Scholar 

  • Ma Q, Dai X, Xu Y, Guo J, Liu Y, Chen N, Xiao J, Zhang D, Xu Z, Zhang X, Chong K (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150:244–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (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 ZY, Yu Y, Li L, Peng C, Fan T, Zhu Y, Guo YL, Wang S, Lu D, Xing Y, Yuan L, Chen C (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 

  • Marzol E, Borassi C, Bringas M, Sede A, Rodriguez Garcia DR, Capece L, Estevez JM (2018) Filling the gaps to solve the extensin puzzle. Mol Plant 11:645–658

    Article  CAS  PubMed  Google Scholar 

  • Mishler-Elmore JW, Zhou Y, Sukul A, Oblak M, Tan L, Faik A, Held MA (2021) Extensins: self-assembly, crosslinking, and the role of peroxidases. Front Plant Sci 12:664738–664750

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandit E, Tasleem S, Barik SR, Mohanty DP, Nayak DK, Mohanty SP, Das S, Pradhan SK (2017) Genome-wide association mapping reveals multiple QTLs governing tolerance response for seedling stage chilling stress in indica rice. Front Plant Sci 8:552–572

    Article  PubMed  PubMed Central  Google Scholar 

  • Saito K, Hayano-Saito Y, Kuroki M, Sato Y (2010) Map-based cloning of the rice cold tolerance gene Ctb1. Plant Sci 179:97–102

    Article  CAS  Google Scholar 

  • Sang T, Ge S (2007) Genetics and phylogenetics of rice domestication. Curr Opin Genet Dev 17:533–538

    Article  CAS  PubMed  Google Scholar 

  • Su CF, Wang YC, Hsieh TH, Lu CA, Tseng TH, Yu SM (2010) A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol 153:145–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Y, Gao C-C, Gao Y, Yang Y, Shi B, Yu J-L, Lyu C, Sun B-F, Wang H-L, Xu Y, Yang Y-G, Chong K (2020) OsNSUN2-mediated 5-methylcytosine mRNA modification enhances rice adaptation to high temperature. Dev Cell 53:272–286

    Article  CAS  PubMed  Google Scholar 

  • Tolmie F, Poulet A, McKenna J, Sassmann S, Graumann K, Deeks M, Runions J (2017) The cell wall of Arabidopsis thaliana influences actin network dynamics. J Exp Bot 68:4517–4527

    Article  CAS  PubMed  Google Scholar 

  • Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Article  CAS  PubMed  Google Scholar 

  • Verma RK, Santosh Kumar VV, Yadav SK, Pushkar S, Rao MV, Chinnusamy V (2019) Overexpression of ABA receptor PYL10 gene confers drought and cold tolerance to indica rice. Front Plant Sci 10:1488–1503

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes RR, Zhang F, Mansueto L, Copetti D, Sanciangco M, Palis KC, Xu J, Sun C, Fu B, Zhang H, Gao Y, Zhao X, Shen F, Cui X, Yu H, Li Z, Chen M, Detras J, Zhou Y, Zhang X, Zhao Y, Kudrna D, Wang C, Li R, Jia B, Lu J, He X, Dong Z, Xu J, Li Y, Wang M, Shi J, Li J, Zhang D, Lee S, Hu W, Poliakov A, Dubchak I, Ulat VJ, Borja FN, Mendoza JR, Ali J, Li J, Gao Q, Niu Y, Yue Z, Naredo MEB, Talag J, Wang X, Li J, Fang X, Yin Y, Glaszmann JC, Zhang J, Li J, Hamilton RS, Wing RA, Ruan J, Zhang G, Wei C, Alexandrov N, McNally KL, Li Z, Leung H (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557:43–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Z, Zhang M, Wang L, Tu Y, Zhang J, Xie G, Zou W, Li F, Guo K, Li Q, Gao C, Peng L (2013) Biomass digestibility is predominantly affected by three factors of wall polymer features distinctive in wheat accessions and rice mutants. Biotechnol Biofuels 6:183–196

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia C, Gong Y, Chong K, Xu Y (2021) Phosphatase OsPP2C27 directly dephosphorylates OsMAPK3 and OsbHLH002 to negatively regulate cold tolerance in rice. Plant Cell Environ 44:491–505

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Zhao Q, Du P, Xu C, Wang B, Feng Q, Liu Q, Tang S, Gu M, Han B, Liang G (2010) Developing high throughput genotyped chromosome segment substitution lines based on population whole-genome re-sequencing in rice (Oryza sativa L.). BMC Genomics 11:656–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Hu D, Hou X, Shen J, Liu J, Cen X, Fu J, Li X, Hu H, Xiong L (2020) OsTMF attenuates cold tolerance by affecting cell wall properties in rice. New Phytol 227:498–512

    Article  CAS  PubMed  Google Scholar 

  • Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H, Kaku H, Minami E, Nishizawa Y (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64:5085–5097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Xu Y, Guo S, Zhu J, Huan Q, Liu H, Wang L, Luo G, Wang X, Chong K (2012) Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet 8:e1002686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Chen Q, Wang S, Hong Y, Wang Z (2014) Rice and cold stress: methods for its evaluation and summary of cold tolerance-related quantitative trait loci. Rice 7:24–35

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Luo W, Zhao Y, Xu Y, Song S, Chong K (2016) Comparative metabolomic analysis reveals a reactive oxygen species-dominated dynamic model underlying chilling environment adaptation and tolerance in rice. New Phytol 211:1295–1310

    Article  CAS  PubMed  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 8:14788–14800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Guo X, Xu Y, Li H, Ma L, Yao X, Weng Y, Guo Y, Liu CM, Chong K (2019) OsCIPK7 point-mutation leads to conformation and kinase-activity change for sensing cold response. J Integr Plant Biol 61:1194–1200

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Gao Y, Zhang L, Zhou Y (2021) The plant cell wall: biosynthesis, construction, and functions. J Integr Plant Biol 63:251–272

    Article  PubMed  Google Scholar 

  • Zhao J, Zhang S, Dong J, Yang T, Mao X, Liu Q, Wang X, Liu B (2017) A novel functional gene associated with cold tolerance at the seedling stage in rice. Plant Biotechnol J 15:1141–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Zayed O, Yu Z, Jiang W, Zhu P, Hsu CC, Zhang L, Tao WA, Lozano-Duran R, Zhu JK (2018) Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci USA 115:13123–13128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to Dr. Jingquan Li (Institute of Botany, Chinese Academy of Sciences) for her excellent technical assistance with confocal microscopy.

Funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Science (Grant No. XDA24010301) and the Basic Science Center Project of National Natural Science Foundation of China (Grant No. 31788103).

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JLF designed the research, performed the experiments, and wrote the manuscript. ZTL and WL performed the experiments and data analysis. GHL, YYX and KC designed the research and wrote the manuscript.

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Correspondence to Kang Chong.

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Communicated by Takuji Sasaki.

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Feng, J., Li, Z., Luo, W. et al. COG2 negatively regulates chilling tolerance through cell wall components altered in rice. Theor Appl Genet 136, 19 (2023). https://doi.org/10.1007/s00122-023-04261-w

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