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Volume 49 Issue 5
May  2022
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Article Contents

OsbZIP60-mediated unfolded protein response regulates grain chalkiness in rice

doi: 10.1016/j.jgg.2022.02.002
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This study is supported by grants from the National Key Research and Development Program of China (2021YFF1000202), the National Natural Science Foundation of China (31771368, 31821005, 31701397), Ten-thousand Talents Programs of China, Fundamental Research Funds for the Central Universities (2662020SKPY006), Wuhan Applied Foundational Frontier Project (2020020601012257) and Hubei Hongshan Laboratory (2021hszd005), China.

  • Received Date: 2021-10-30
  • Accepted Date: 2022-02-07
  • Rev Recd Date: 2022-02-01
  • Publish Date: 2022-02-19
  • Grain chalkiness, an undesirable trait caused by complex factors, has great negative impacts on the quality and economic value of rice. However, little is known about the regulatory mechanism of grain chalkiness, particularly the effect of endoplasmic reticulum (ER) stress. Here, a genome-wide association study (GWAS) reveals that the transcription factor OsbZIP60 is a vital regulator of rice grain chalkiness. Genetic analysis demonstrates that knockout of OsbZIP60 results in extremely high grain chalkiness and aberrant structure of storage substances. Notably, the expression of unfolded protein response (UPR) genes, such as OsbZIP50, OsBiP1, OsBiP2 and OsBiP3, is up-regulated in the endosperm cells of osbzip60, and overexpression of all these UPR genes causes various degrees of chalkiness. Furthermore, OsbZIP60 is found to activate the expression of key genes related to grain chalkiness, such as GPA3, FSE1, FLO7, Chalk5, OsNF-YB1, and OsPK2, whose expression is significantly suppressed in osbzip60 and overexpression lines of OsbZIP50, OsBiP1, OsBiP2, and OsBiP3. Our study provides novel insights into the function of OsbZIP60 and the role of the UPR pathway in the formation of grain chalkiness in rice.
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  • Bart, R., Chern, M., Park, C.J., Bartley, L., Ronald, P.C., 2006. A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2, 13
    Boston, R.S., Fontes, E.B., Shank, B.B.,Wrobel, R.L., 1991. Increased expression of the maize immunoglobulin binding protein homolog b-70 in three zein regulatory mutants. Plant Cell 3, 497-505
    Cai, Y., Li, S., Jiao, G., Sheng, Z., Wu, Y., Shao, G., Xie, L., Peng, C., Xu, J., Tang, S., Wei, X., Hu, P., 2018a. OsPK2 encodes a plastidic pyruvate kinase involved in rice endosperm starch synthesis, compound granule formation and grain filling. Plant Biotechnol. J. 16, 1878-1891
    Cai, Y., Zhang, W., Jin, J., Yang, X., You, X., Yan, H., Wang, L., Chen, J., Xu, J., Chen, W., et al., 2018b. OsPKpa1 encodes a plastidic pyruvate kinase that affects starch biosynthesis in the rice endosperm. J. Integr. Plant Biol. 60, 1097-1118
    Che, P., Bussell, J.D., Zhou, W., Estavillo, G.M., Pogson, B.J., Smith, S.M., 2010. Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci. Signal. 3, ra69
    Chen, P., Shen, Z., Ming, L., Li, Y., Dan, W., Lou, G., Peng, B., Wu, B., Li, Y., Zhao, D., et al., 2018. Genetic basis of variation in rice seed storage protein (albumin, globulin, prolamin, and glutelin) content revealed by genome-wide association analysis. Front Plant Sci. 9, 612
    Chen, H., Zhao, Z., Jiang, L., Wan, X., Liu, L., Wu, X., Wan, J., 2011. Molecular genetic analysis on percentage of grains with chalkiness in rice (Oryza sativa L.). Afr. J. Biotechnol. 10, 6891-6903
    Chun, A., Song, J., Kim, K.J., Lee, H.J., 2010. Quality of head and chalky rice and deterioration of eating quality by chalky rice. J. Crop Sci. Biotechnol. 12, 239-244
    Deng, Y., Humbert, S., Liu, J.X., Srivastava, R., Rothstein, S.J., Howell, S.H., 2011. Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 108, 7247-7252
    Fontes, E.B., Shank, B.B., Wrobel, R.L., Moose, S.P., GR, O.B., Wurtzel, E.T.,Boston, R.S., 1991. Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant. Plant Cell 3, 483-496
    Gao, H., Brandizzi, F., Benning, C., Larkin, R.M., 2008. A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 105, 16398-16403
    Gao, Y., Zhao, Y., 2014. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol. 56:343-349
    Gong, J., Miao, J., Zhao, Y., Zhao, Q., Feng, Q., Zhan, Q., Cheng, B., Xia, J., Huang, X., Yang, S., et al., 2017. Dissecting the genetic basis of grain shape and chalkiness traits in hybrid rice using multiple collaborative populations. Mol. Plant 10, 1353-1356
    Han, X., Wang, Y., Liu, X., Jiang, L., Ren, Y., Liu, F., Peng, C., Li, J., Jin, X., Wu, F., et al., 2012. The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. J. Exp. Bot. 63, 121-130
    Hayashi, S., Takahashi, H., Wakasa, Y., Kawakatsu, T., Takaiwa, F., 2013a. Identification of a cis-element that mediates multiple pathways of the endoplasmic reticulum stress response in rice. Plant J. 74, 248-257
    Hayashi, S., Takaiwa, F., 2013. The plant-unique cis-element that mediates signaling from multiple endoplasmic reticulum stress sensors. Plant Signal. Behav. e24316
    Hayashi, S., Wakasa, Y., Takahashi, H., Kawakatsu, T., Takaiwa, F., 2012. Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice. Plant J. 69, 946-956
    Hayashi, S., Wakasa, Y., Takaiwa, F., 2013b. Recent advances in understanding the control of secretory proteins by the unfolded protein response in plants. Int. J. Mol. Sci. 14, 9396-9407
    Howell, S.H., 2013. Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 64, 477-499
    Howell, S.H., 2021. Evolution of the unfolded protein response in plants. Plant Cell Environ. 44, 2625-2635
    Huang, X., Han, B., 2014. Natural variations and genome-wide association studies in crop plants. Annu. Rev. Plant Biol. 65, 531-551
    Iwata, Y., Koizumi, N., 2005. An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc. Natl. Acad. Sci. USA 102, 5280-5285
    Iwata, Y., Koizumi, N., 2012. Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci. 17, 720-727
    Kim, C.S., Gibbon, B.C., Gillikin, J.W., Larkins, B.A., Boston, R.S., Jung, R., 2006. The maize mucronate mutation is a deletion in the 16-kDa gamma-zein gene that induces the unfolded protein response. Plant J. 48, 440-451
    Kim, J.S., Yamaguchi-Shinozaki, K., Shinozaki, K., 2018. ER-anchored transcription factors bZIP17 and bZIP28 regulate root elongation. Plant Physiol. 176, 2221-2230
    Kim, S.S., Lee, S.E., Kim, O.W., Kim, D. C., 2000. Physicochemical characteristics of chalky kernels and their effects on sensory quality of cooked rice. Cereal Chem. 77, 376-379
    Kleizen, B., Braakman, I., 2004. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16, 343-349
    Korte, A., Farlow, A., 2013. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9, 29
    Kudo, K., Ohta, M., Yang, L., Wakasa, Y., Takahashi, S., Takaiwa, F., 2013. ER stress response induced by the production of human IL-7 in rice endosperm cells. Plant Mol. Biol. 81, 461-475
    Li, Y., Fan, C., Xing, Y., Yun, P., Luo, L., Yan, B., Peng, B., Xie, W., Wang, G., Li, X., et al., 2014. Chalk5 encodes a vacuolar H+-translocating pyrophosphatase influencing grain chalkiness in rice. Nat. Genet. 46, 398-404
    Lin, Y.J., Zhang, Q., 2005. Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep. 23, 540-547
    Lippert, C., Listgarten, J., Liu, Y., Kadie, C., Davidson, R., Heckerman, D., 2011. FaST linear mixed models for genome-wide association studies. Nat. Methods 8, 833-835
    Liu, F., Ren, Y., Wang, Y., Peng, C., Zhou, K., Lv, J., Guo, X., Zhang, X., Zhong, M., Zhao, S., et al., 2013. OsVPS9A functions cooperatively with OsRab5A to regulate post-Golgi dense vesicle-mediated storage protein trafficking to the protein storage vacuole in rice endosperm cells. Mol. Plant 6, 1918-1932
    Liu, J., Howell, S., 2016. Managing the protein folding demands in the endoplasmic reticulum of plants. New Phytol. 211, 418-428
    Liu, J., Srivastava, R., Che, P., Howell, S., 2007. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19, 4111-4119
    Liu, X.H., Lyu, Y.S., Yang, W., Yang, Z.T., Lu, S.J., Liu, J.X., 2020. A membrane-associated NAC transcription factor OsNTL3 is involved in thermotolerance in rice. Plant Biotechnol. J. 18, 1317-1329
    Livak, K., Schmittgen, T., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CT method. Methods 25, 402-408
    Long, W., Wang, Y., Zhu, S., Jing, W., Wang, Y., Ren, Y., Tian, Y., Liu, S., Liu, X., Chen, L., et al., 2018. Floury shrunken endosperm 1 connects phospholipid metabolism and amyloplast development in rice. Plant Physiol. 177, 698-712
    Lou, G., Chen, P., Zhou, H., Li, P., Xiong, J., Wan, S., Zheng, Y., Alam, M., Liu, R., Zhou, Y., et al., 2021. Floury endosperm 19 encoding a class I glutamine amidotransferase affects grain quality in rice. Mol. Breeding 41, 36
    Lu, S., Yang, Z., Sun, L., Sun, L., Song, Z., Liu, J., 2012. Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol. Plant 5, 504-514
    Misra, G., Anacleto, R., Badoni, S., Butardo, V., Molina, L., Graner, A., Demont, M., Morell, M.K., Sreenivasulu, N., 2019. Dissecting the genome-wide genetic variants of milling and appearance quality traits in rice. J. Exp. Bot. 70, 5115-5130
    Misra, G., Badoni, S., Parween, S., Singh, R., Leung, H., Ladejobi, O., Mott, R., Sreenivasulu, N., 2021. Genome-wide association coupled gene to gene interaction studies unveil novel epistatic targets among major effect loci impacting rice grain chalkiness. Plant Biotechnol. J. 19, 910-925
    Moreno, A., Mukhtar, M., Blanco, F., Boatwright, J., Moreno, I., Jordan, M., Chen, Y., Brandizzi, F., Dong, X., Orellana, A., et al., 2012. IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS One 7, e31944
    Nagashima, Y., Mishiba, K., Suzuki, E., Shimada, Y., Iwata, Y., Koizumi, N., 2011. Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep. 1, 29
    Oono, Y., Wakasa, Y., Hirose, S., Yang, L., Sakuta, C., Takaiwa, F., 2010. Analysis of ER stress in developing rice endosperm accumulating β-amyloid peptide. Plant Biotechnol. J. 8, 691-718
    Pang, J., Zhou, J., Yang, D., 2020. Knock-in at GluA1 locus improves recombinant human serum albumin expression in rice grain. J. Biotechnol. 321, 87-95
    Pastor-Cantizano, N., Ko, D., Angelos, E., Pu, Y., Brandizzi, F., 2020. Functional diversification of ER stress responses in Arabidopsis. Trends Biochem. Sci. 45, 123-136
    Peng, C., Wang, Y., Liu, F., Ren, Y., Zhou, K., Lv, J., Zheng, M., Zhao, S., Zhang, L., Wang, C., et al., 2014. Floury endosperm 6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J. 77, 917-930
    Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M., Bender, D., Maller, J., Sklar, P., de Bakker, P., Daly, M.J., et al., 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575
    Qiao, Y., Lee, S., Piao, R., Jiang, W., Ham, T., Chin, J., Piao, Z., Han, L., Kang, S., Koh, H., 2010. Fine mapping and candidate gene analysis of the floury endosperm gene, flo(a), in rice. Mol. Cells 29, 167-174
    Quero, G., Gutierrez, L., Monteverde, E., Blanco, P., Perez de Vida, F., Rosas, J., Fernandez, S., Garaycochea, S., McCouch, S., Berberian, N., et al., 2018. Genome-wide association study using historical breeding populations discovers genomic regions involved in high-quality rice. Plant Genome 11
    Ren, Y., Wang, Y., Liu, F., Zhou, K., Ding, Y., Zhou, F., Wang, Y., Liu, K., Gan, L., Ma, W., et al., 2014. Glutelin precursor accumulation 3 encodes a regulator of post-Golgi vesicular traffic essential for vacuolar protein sorting in rice endosperm. Plant Cell 26, 410-425
    Ren, Y., Wang, Y., Pan, T., Wang, Y., Wang, Y., Gan, L., Wei, Z., Wang, F., Wu, M., Jing, R., et al., 2020. GPA5 encodes a Rab5a effector required for post-Golgi trafficking of rice storage proteins. Plant Cell 32, 758-777
    Sandhu, J., Irvin, L., Liu, K., Staswick, P., Zhang, C., Walia, H., 2021. Endoplasmic reticulum stress pathway mediates the early heat stress response of developing rice seeds. Plant Cell Environ. 44, 2604-2624
    She, K.C., Kusano, H., Koizumi, K., Yamakawa, H., Hakata, M., Imamura, T., Fukuda, M., Naito, N., Tsurumaki, Y., Yaeshima, M., et al., 2010. A novel factor floury endosperm 2 is involved in regulation of rice grain size and starch quality. Plant Cell 22, 3280-3294
    Shin, J.-H., Blay, S., Graham, J., McNeney, B., 2006. LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J. Stat. Softw. 16 (c03)
    So, J., 2018. Roles of endoplasmic reticulum stress in immune responses. Mol. Cells 41, 705-716
    Sun, J., Li, J., Wang, M., Song, Z.,Liu, J., 2021. Protein quality control in plant organelles: Current progress and future perspectives. Mol. Plant 14, 95-114
    Sun, L., Zhang, S., Lu, S., Liu, J., 2015. Site-1 protease cleavage site is important for the ER stress-induced activation of membrane-associated transcription factor bZIP28 in Arabidopsis. Sci. China Life Sci. 58, 270-275
    Tabassum, R., Dosaka, T., Ichida, H., Morita, R., Ding, Y., Abe, T., Katsube-Tanaka, T., 2020. Floury endosperm 11-2 encodes plastid HSP70-2 involved with the temperature-dependent chalkiness of rice (Oryza sativa L.) grains. Plant J. 103, 604-616
    Takahashi, H., Kawakatsu, T., Wakasa, Y., Hayashi, S., Takaiwa, F., 2012. A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol. 53, 144-153
    Tan, Y.F., Li, J.X., Yu, S.B., Xing, Y.Z., Xu, C.G., Zhang, Q., 1999. The three important traits for cooking and eating quality of rice grains are controlled by a single locus in an elite rice hybrid, Shanyou 63. Theor. Appl. Genet. 99, 642-648
    Teng, X., Zhong, M., Zhu, X., Wang, C., Ren, Y., Wang, Y., Zhang, H., Jiang, L., Wang, D., Hao, Y., et al., 2019. Floury endosperm 16 encoding a NAD-dependent cytosolic malate dehydrogenase plays an important role in starch synthesis and seed development in rice. Plant Biotechnol. J. 17, 1914-1927
    Vitale, A., Boston, R.S., 2008. Endoplasmic reticulum quality control and the unfolded protein response: Insights from plants. Traffic 9, 1581-1588
    Wakasa, Y., Yasuda, H., Oono, Y., Kawakatsu, T., Hirose, S., Takahashi, H., Hayashi, S., Yang, L., Takaiwa, F., 2011. Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. Plant J. 65, 675-689
    Wakasa, Y., Hayashi, S., Takaiwa, F., 2012. Expression of OsBiP4 and OsBiP5 is highly correlated with the endoplasmic reticulum stress response in rice. Planta 236, 1519-1527
    Wang, Q., Tang, J., Han, B., Huang, X., 2020. Advances in genome-wide association studies of complex traits in rice. Theor. Appl. Genet. 133, 1415-1425
    Wang, X., Pang, Y., Wang, C., Chen, K., Zhu, Y., Shen, C., Ali, J., Xu, J., Li, Z., 2016a. New candidate genes affecting rice grain appearance and milling quality detected by genome-wide and gene-based association analyses. Front. Plant Sci. 7, 1998
    Wang, Y., Liu, F., Ren, Y., Wang, Y., Liu, X., Long, W., Wang, D., Zhu, J., Zhu, X., Jing, R., et al., 2016b. GOLGI TRANSPORT 1B regulates protein export from the endoplasmic reticulum in rice endosperm cells. Plant Cell 28, 2850-2865
    Wang, Y., Ren, Y., Liu, X., Jiang, L., Chen, L., Han, X., Jin, M., Liu, S., Liu, F., Lv, J., et al., 2010. OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. Plant J. 64, 812-824
    Wu, M., Ren, Y., Cai, M., Wang, Y., Zhu, S., Zhu, J., Hao, Y., Teng, X., Zhu, X., Jing, R., et al., 2019. Rice floury endosperm 10 encodes a pentatricopeptide repeat protein that is essential for the transsplicing of mitochondrial nad1 intron 1 and endosperm development. New Phytol. 223, 736-750
    Xi, M., Lin, Z., Zhang, X., Liu, Z., Li, G., Wang, Q., Wang, S., Ding, Y., 2014. Endosperm structure of white-belly and white-core rice grains shown by scanning electron microscopy. Plant Prod. Sci. 17, 285-290
    Xu, J., Zhang, X., Xue, H., 2016. Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. J. Exp. Bot. 67, 6399-6411
    Xue, M., Liu, L., Yu, Y., Zhu, J., Gao, H., Wang, Y., Wan, J., 2019. Lose-of-function of a rice nucleolus-localized pentatricopeptide repeat protein is responsible for the floury endosperm14 mutant phenotypes. Rice. 12, 100
    Yang, Z.T., Lu, S.J., Wang, M.J., Bi, D.L., Sun, L., Zhou, S.F., Song, Z.T., Liu, J.X., 2014a. A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis. Plant J. 79, 1033-1043
    Yang, Z.T., Wang, M.J., Sun, L., Lu, S.J., Bi, D.L., Sun, L., Song, Z.T., Zhang, S.S., Zhou, S.F.,Liu, J.X., 2014b. The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet. 10, e1004243
    Yasuda, H., Hirose, S., Kawakatsu, T., Wakasa, Y., Takaiwa, F., 2009. Overexpression of BiP has inhibitory effects on the accumulation of seed storage proteins in endosperm cells of rice. Plant Cell Physiol. 50, 1532-1543
    Zhang, Y., Su, J., Duan, S., Ao, Y., Dai, J., Liu, J., Wang, P., Li, Y., Liu, B., Feng, D., et al., 2011. A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7, 30
    Zhang, L., Jiang, D., Pang, J., Chen, R., Wang, X., Yang, D., 2013. The endoplasmic reticulum stress induced by highly expressed OsrAAT reduces seed size via pre-mature programmed cell death. Plant Mol. Biol. 83, 153-161
    Zhang, L., Ren, Y., Lu, B., Yang, C., Feng, Z., Liu, Z., Chen, J., Ma, W., Wang, Y., Yu, X., et al., 2016. Floury endosperm 7 encodes a regulator of starch synthesis and amyloplast development essential for peripheral endosperm development in rice. J. Exp. Bot. 67, 633-647
    Zhang, S.S., Yang, H., Ding, L., Song, Z.T., Ma, H., Chang, F., Liu, J.X., 2017. Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis. Plant Cell 29, 1007-1023
    Zhang, J., Zhang, D., Fan, Y., Li, C., Xu, P., Li, W., Sun, Q., Huang, X., Zhang, C., Wu, L., Yang, H., Wang, S., Su, X., Li, X., Song, Y., Wu, M., Lian, X., Li, Y., 2021. The identification of grain size genes by RapMap reveals directional selection during rice domestication. Nat. Commun. 12, 5673
    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, D1018-1022
    Zhu, J., Ren, Y., Wang, Y., Liu, F., Teng, X., Zhang, Y., Duan, E., Wu, M., Zhong, M., Hao, Y., et al., 2019. OsNHX5-mediated pH homeostasis is required for post-Golgi trafficking of seed storage proteins in rice endosperm cells. BMC Plant Biol. 19, 295
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