Enhancing the nutritional profile of rice by targeting starch branching enzymes using CRISPR/Cas9

Authors

DOI:

https://doi.org/10.14719/pst.5910

Keywords:

amylose, genome editing, resistant starch, rice, starch branching enzymes

Abstract

Rice is a fundamental staple in many Asian countries; however, excessive consumption can lead to significant health concerns, including diabetes. One effective strategy to mitigate these concerns is to increase the amylose content in rice, which enhances its resistant starch (RS) levels. Higher RS not only improves the nutritional profile of rice but also positively impacts its cooking qualities, offering various health benefits. Recent research highlights the role of dietary fibers like RS in modulating gut microbiota composition, presenting a promising approach for addressing non-communicable diseases. RS enhances the fermentation activity of gut microbiota, leading to production of beneficial metabolites that support gut barrier function, exhibit anti-inflammatory properties and influence metabolic pathways related to obesity and diabetes. This multifaceted impact on chronic disease outcomes emphasizes the need for rice varieties with increased amylose and consequently higher RS levels, to meet consumer nutritional demands. CRISPR/Cas9, a powerful genome editing tool, allows precise modifications of the targeted genes. This technology can effectively edit starch synthesis-related genes in rice to enhance starch content. This review focuses on the application of CRISPR/Cas9 in increasing RS content in rice and the potential health benefits it could provide to populations that rely on rice as a dietary staple. By integrating genetic innovation with nutritional science, healthier rice varieties can be developed, that align with the dietary needs of consumers.

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References

Mohidem NA, Hashim N, Shamsudin R, Che Man H. Rice for food security: Revisiting its production, diversity, rice milling process and nutrient content. Agriculture. 2022;12(6):741. https://doi.org/10.3390/agriculture12060741

Ball S, Guan H-P, James M, Myers A, Keeling P, Mouille G, et al. From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell. 1996;86(3):349–52. https://doi.org/10.1016/S0092-8674(00)80109-8

Englyst HN, Kingman S, Cummings J. Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition. 1992;46:S33–50. https://doi.org/10.1038/ejcn.1992.178

Raigond P, Dutt S, Singh B. Resistant Starch in Food. In: Mérillon JM, Ramawat KG, editors. Bioactive Molecules in Food. Reference Series in Phytochemistry. Springer, Cham; 2019. https://doi.org/10.1007/978-3-319-78030-6_30

Den Besten G, Van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research. 2013;54(9):2325–40. https://doi.org/10.1194/jlr.R036012

Silva YP, Bernardi A, Frozza RL. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Frontiers in Endocrinology. 2020;11:25. https://doi.org/10.3389/fendo.2020.00025

Rachmat R, Thahir R, Gummert M. The empirical relationship between price and quality of rice at market level in West Java. Indonesian Journal of Agricultural Science. 2006;7(1):27–33. https://doi.org/10.21082/ijas.v7n1.2006.p27-33

Chen L, Magliano DJ, Zimmet PZ. The worldwide epidemiology of type 2 diabetes mellitus—present and future perspectives. Nature Reviews Endocrinology. 2012;8(4):228–36. https://doi.org/10.1038/nrendo.2011.183

Biswas S, Ibarra O, Shaphek M, Molina-Risco M, Faion-Molina M, Bellinatti-Della Gracia M, et al. Increasing the level of resistant starch in ‘Presidio’ rice through multiplex CRISPR–Cas9 gene editing of starch branching enzyme genes. The Plant Genome. 2023;16(2):e20225. https://doi.org/10.1002/tpg2.20225

Feng F, Li Y, Qin X, Liao Y, Siddique KH. Changes in rice grain quality of indica and japonica type varieties released in China from 2000 to 2014. Frontiers in Plant Science. 2017;8:1863. https://doi.org/10.3389/fpls.2017.01863

Sestili F, Botticella E, Proietti G, Janni M, D’Ovidio R, Lafiandra D. Amylose content is not affected by overexpression of the Wx-B1 gene in durum wheat. Plant Breeding. 2012;131(6):700–6. https://doi.org/10.1111/j.1439-0523.2012.02009.x

Itoh K, Ozaki H, Okada K, Hori H, Takeda Y, Mitsui T. Introduction of Wx transgene into rice wx mutants leads to both high-and low-amylose rice. Plant and Cell Physiology. 2003;44(5):473–80. https://doi.org/10.1093/pcp/pcg067

Carciofi M, Blennow A, Jensen SL, Shaik SS, Henriksen A, Buléon A, et al. Concerted suppression of all starch branching enzyme genes in barley produces amylose-only starch granules. BMC Plant Biology. 2012;12(1):1–16. https://doi.org/10.1186/1471-2229-12-223

Zhong Y, Liu L, Qu J, Li S, Blennow A, Seytahmetovna SA, et al. The relationship between the expression pattern of starch biosynthesis enzymes and molecular structure of high amylose maize starch. Carbohydrate Polymers. 2020;247:116681. https://doi.org/10.1016/j.carbpol.2020.116681

Hogg A, Gause K, Hofer P, Martin J, Graybosch RA, Hansen L, et al. Creation of a high-amylose durum wheat through mutagenesis of starch synthase II (SSIIa). Journal of Cereal Science. 2013;57(3):377–83. https://doi.org/10.1016/j.jcs.2013.01.009

Blennow A, Skryhan K, Tanackovic V, Krunic SL, Shaik SS, Andersen MS, et al. Non-GMO potato lines, synthesizing increased amylose and resistant starch, are mainly deficient in isoamylase debranching enzyme. Plant Biotechnology Journal. 2020;18(10):2096–108. https://doi.org/10.1111/pbi.13367

Kozlov SS, Blennow A, Krivandin AV, Yuryev VP. Structural and thermodynamic properties of starches extracted from GBSS and GWD suppressed potato lines. International Journal of Biological Macromolecules. 2007;40(5):449–60. https://doi.org/10.1016/j.ijbiomac.2006.11.004

Zhou H, Wang L, Liu G, Meng X, Jing Y, Shu X, et al. Critical roles of soluble starch synthase SSIIIa and granule-bound starch synthase Waxy in synthesizing resistant starch in rice. Proceedings of the National Academy of Sciences. 2016;113(45):12844–49. https://doi.org/10.1073/pnas.1615103113

Li L, Jiang H, Campbell M, Blanco M, Jane J-l. Characterization of maize amylose-extender (ae) mutant starches. Part I: Relationship between resistant starch contents and molecular structures. Carbohydrate Polymers. 2008;74(3):396–404. https://doi.org/10.1016/j.carbpol.2008.03.003

Regina A, Berbezy P, Kosar-Hashemi B, Li S, Cmiel M, Larroque O, et al. A genetic strategy generating wheat with very high amylose content. Plant Biotechnology Journal. 2015;13(9):1276–86. https://doi.org/10.1111/pbi.12339

Butardo VM, Fitzgerald MA, Bird AR, Gidley MJ, Flanagan BM, Larroque O, et al. Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA-and hairpin RNA-mediated RNA silencing. Journal of Experimental Botany. 2011;62(14):4927–41. https://doi.org/10.1093/jxb/err193

Regina A, Bird A, Topping D, Bowden S, Freeman J, Barsby T, et al. High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proceedings of the National Academy of Sciences. 2006;103(10):3546–51. https://doi.org/10.1073/pnas.0510737103

Warthmann N, Chen H, Ossowski S, Weigel D, Hervé P. Highly specific gene silencing by artificial miRNAs in rice. PLoS One. 2008;3(3):e1829. https://doi.org/10.1371/journal.pone.0001829

Ossowski S, Schwab R, Weigel D. Gene silencing in plants using artificial microRNAs and other small RNAs. The Plant Journal. 2008;53(4):674–90. https://doi.org/10.1111/j.1365-313X.2007.03362.x

Yano M, Okuno K, Kawakami J, Satoh H, Omura T. High amylose mutants of rice, Oryza sativa L. Theoretical and Applied Genetics. 1985;69:253–7. https://doi.org/10.1007/BF00272879

Loureiro A, da Silva GJ. CRISPR-Cas: Converting a bacterial defence mechanism into a state-of-the-art genetic manipulation tool. Antibiotics. 2019;8(1):18. https://doi.org/10.3390/antibiotics8010018

Pribylová A, Fischer L. How to use CRISPR/Cas9 in plants—from target site selection to DNA repair. Journal of Experimental Botany. 2024;erae147. https://doi.org/10.1093/jxb/erae147

Martens BM, Gerrits WJ, Bruininx EM, Schols HA. Amylopectin structure and crystallinity explains variation in digestion kinetics of starches across botanic sources in an in vitro pig model. Journal of Animal Science and Biotechnology. 2018;9(1):1–13. https://doi.org/10.1186/s40104-018-0244-x

Tester RF, Karkalas J, Qi X. Starch—composition, fine structure and architecture. Journal of Cereal Science. 2004;39(2):151–65. https://doi.org/10.1016/j.jcs.2003.12.001

Dobranowski PA, Stintzi A. Resistant starch, microbiome, and precision modulation. Gut Microbes. 2021;13(1):1926842. https://doi.org/10.1080/19490976.2021.1926842

Li H-T, Zhang W, Zhu H, Chao C, Guo Q. Unlocking the potential of high-amylose starch for gut health: Not all function the same. Fermentation. 2023;9(2):134. https://doi.org/10.3390/fermentation9020134

Ye X, Zhang Y, Qiu C, Corke H, Sui Z. Extraction and characterization of starch granule-associated proteins from rice that affect in vitro starch digestibility. Food Chemistry. 2019;276:754–60. https://doi.org/10.1016/j.foodchem.2018.10.025

Frei M, Siddhuraju P, Becker K. Studies on the in vitro starch digestibility and the glycemic index of six different indigenous rice cultivars from the Philippines. Food Chemistry. 2003;83(3):395–402. https://doi.org/10.1016/S0308-8146(03)00101-8

Tetlow IJ, Emes MJ. Starch biosynthesis in the developing endosperms of grasses and cereals. Agronomy. 2017;7(4):81. https://doi.org/10.3390/agronomy7040081

Nakamura Y. Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant and Cell Physiology. 2002;43(7):718–25. https://doi.org/10.1093/pcp/pcf114

Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, Hwang S-K, et al. Mutation of the plastidial a-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. The Plant Cell. 2008;20(7):1833–49. https://doi.org/10.1105/tpc.108.060053

Møller MS, Svensson B. Structural biology of starch-degrading enzymes and their regulation. Current Opinion in Structural Biology. 2016;40:33–42. https://doi.org/10.1016/j.sbi.2016.06.010

Chen M-H, Huang L-F, Li H-m, Chen Y-R, Yu S-M. Signal peptide-dependent targeting of a rice a-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiology. 2004;135(3):1367–77. https://doi.org/10.1104/pp.103.033803

Pandey MK, Rani NS, Madhav MS, Sundaram R, Varaprasad G, Sivaranjani A, et al. Different isoforms of starch-synthesizing enzymes controlling amylose and amylopectin content in rice (Oryza sativa L.). Biotechnology Advances. 2012;30(6):1697–706. https://doi.org/10.1016/j.biotechadv.2012.08.009

Nakamura Y, Utsumi Y, Sawada T, Aihara S, Utsumi C, Yoshida M, et al. Characterization of the reactions of starch branching enzymes from rice endosperm. Plant and Cell Physiology. 2010;51(5):776–94. https://doi.org/10.1093/pcp/pcq045

Sawada T, Itoh M, Nakamura Y. Contributions of three starch branching enzyme isozymes to the fine structure of amylopectin in rice endosperm. Frontiers in Plant Science. 2018;9:1536. https://doi.org/10.3389/fpls.2018.01536

Li E, Wu AC, Li J, Liu Q, Gilbert RG. Improved understanding of rice amylose biosynthesis from advanced starch structural characterization. Rice. 2015;8:1–8. https://doi.org/10.1186/s12284-015-0041-2

Okpala NE, Aloryi KD, An T, He L, Tang X. The roles of starch branching enzymes and starch synthase in the biosynthesis of amylose in rice. Journal of Cereal Science. 2022;104:103393. https://doi.org/10.1016/j.jcs.2021.103393

Mizuno K, Kobayashi E, Tachibana M, Kawasaki T, Fujimura T, Funane K, et al. Characterization of an isoform of rice starch branching enzyme, RBE4, in developing seeds. Plant and Cell Physiology. 2001;42(4):349–57. https://doi.org/10.1093/pcp/pce034

Baysal C, He W, Drapal M, Villorbina G, Medina V, Capell T, et al. Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming. Proceedings of the National Academy of Sciences. 2020;117(42):26503–12. https://doi.org/10.1073/pnas.2012333117

Takeda Y, Guan H-P, Preiss J. Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydrate Research. 1993;240:253–63. https://doi.org/10.1016/0008-6215(93)80077-3

Tappiban P, Hu Y, Deng J, Zhao J, Ying Y, Zhang Z, et al. Relative importance of branching enzyme isoforms in determining starch fine structure and physicochemical properties of indica rice. Plant Molecular Biology. 2022:1–14. https://doi.org/10.1007/s11103-021-01252-y

Voytas DF, Gao C. Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biology. 2014;12(6):e1001877. https://doi.org/10.1371/journal.pbio.1001877

Haque E, Taniguchi H, Hassan MM, Bhowmik P, Karim MR, Smiech M, et al. Application of CRISPR/Cas9 genome editing technology for the improvement of crops cultivated in tropical climates: recent progress, prospects, and challenges. Frontiers in Plant Science. 2018;9:617. https://doi.org/10.3389/fpls.2018.00617

Pacesa M, Pelea O, Jinek M. Past, present, and future of CRISPR genome editing technologies. Cell. 2024;187(5):1076–100. https://doi.org/10.1016/j.cell.2024.03.012

Barrangou R, Marraffini LA. CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Molecular Cell. 2014;54(2):234–44. https://doi.org/10.1016/j.molcel.2014.03.011

Gostimskaya I. CRISPR–Cas9: A history of its discovery and ethical considerations of its use in genome editing. Biochemistry (Moscow). 2022;87(8):777–88. https://doi.org/10.1134/S0006297922080072

Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–23. https://doi.org/10.1126/science.1231143

Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816–21. https://doi.org/10.1126/science.1225829

Xu Y, Li Z. CRISPR-Cas systems: Overview, innovations and applications in human disease research and gene therapy. Computational and Structural Biotechnology Journal. 2020;18:2401–15. https://doi.org/10.1016/j.csbj.2020.08.023

Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E, et al. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science. 2014;343(6176):1247997. https://doi.org/10.1126/science.1247997

Westra ER, Dowling AJ, Broniewski JM, van Houte S. Evolution and ecology of CRISPR. Annual Review of Ecology, Evolution, and Systematics. 2016;47(1):307–31. https://doi.org/10.1146/annurev-ecolsys-121415-032247

Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S, Trevino AE, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154(6):1380–9. https://doi.org/10.1016/j.cell.2013.08.021

Hara S, Tamano M, Yamashita S, Kato T, Saito T, Sakuma T, et al. Generation of mutant mice via the CRISPR/Cas9 system using FokI-dCas9. Scientific Reports. 2015;5(1):11221. https://doi.org/10.1038/srep11221

Liu Q, Yang F, Zhang J, Liu H, Rahman S, Islam S, et al. Application of CRISPR/Cas9 in crop quality improvement. International Journal of Molecular Sciences. 2021;22(8):4206. https://doi.org/10.3390/ijms22084206

Xu R, Li H, Qin R, Wang L, Li L, Wei P, et al. Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice. 2014;7:1–4. https://doi.org/10.1186/s12284-014-0007-5

Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research. 2013;41(20):e188-e. https://doi.org/10.1093/nar/gkt780

Xie K, Yang Y. RNA-guided genome editing in plants using a CRISPR–Cas system. Molecular Plant. 2013;6(6):1975–83. https://doi.org/10.1093/mp/sst119

Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, et al. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Research. 2013;23(10):1233–6. https://doi.org/10.1038/cr.2013.123

Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnology Journal. 2014;12(6):797–807. https://doi.org/10.1111/pbi.12200

Zhou H, Liu B, Weeks DP, Spalding MH, Yang B. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Research. 2014;42(17):10903–14. https://doi.org/10.1093/nar/gku806

Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, et al. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Frontiers in Plant Science. 2016;7:377. https://doi.org/10.3389/fpls.2016.00377

Butt H, Jamil M, Wang JY, Al-Babili S, Mahfouz M. Engineering plant architecture via CRISPR/Cas9-mediated alteration of strigolactone biosynthesis. BMC Plant Biology. 2018;18:1–9. https://doi.org/10.1186/s12870-018-1485-8

Li S, Luo Y, Wei G, Zong W, Zeng W, Xiao D, et al. Improving yield-related traits by editing the promoter of the heading date gene Ehd1 in rice. Theoretical and Applied Genetics. 2023;136(12):239. https://doi.org/10.1007/s00122-023-04161-3

Li H, Zhang Y, Wu C, Bi J, Chen Y, Jiang C, et al. Fine-tuning OsCPK18/OsCPK4 activity via genome editing of phosphorylation motif improves rice yield and immunity. Plant Biotechnology Journal. 2022;20(12):2258–71. https://doi.org/10.1111/pbi.13883

Miao C, Xiao L, Hua K, Zou C, Zhao Y, Bressan RA, et al. Mutations in a subfamily of abscisic acid receptor genes promote rice growth and productivity. Proceedings of the National Academy of Sciences. 2018;115(23):6058–63. https://doi.org/10.1073/pnas.1804774115

Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, et al. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLOS One. 2016;11(4):e0154027. https://doi.org/10.1371/journal.pone.0154027

Xie W, Cao W, Lu S, Zhao J, Shi X, Yue X, et al. Knockout of transcription factor OsERF65 enhances ROS scavenging ability and confers resistance to rice sheath blight. Molecular Plant Pathology. 2023;24(12):1535–51. https://doi.org/10.1111/mpp.13351

Hu B, Zhou Y, Zhou Z, Sun B, Zhou F, Yin C, et al. Repressed OsMESL expression triggers reactive oxygen species-mediated broad-spectrum disease resistance in rice. Plant Biotechnology Journal. 2021;19(8):1511–22. https://doi.org/10.1111/pbi.13532

Macovei A, Sevilla NR, Cantos C, Jonson GB, Slamet-Loedin I, Cermák T, et al. Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant Biotechnology Journal. 2018;16(11):1918–27. https://doi.org/10.1111/pbi.12920

Lou D, Wang H, Liang G, Yu D. OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Frontiers in Plant Science. 2017;8:993. https://doi.org/10.3389/fpls.2017.00993

Park J-R, Kim E-G, Jang Y-H, Jan R, Farooq M, Asif S, et al. CRISPR/Cas9-mediated genome editing of OsCS511 enhances cold tolerance in Oryza sativa L. Environmental and Experimental Botany. 2024;226:105932. https://doi.org/10.1016/j.envexpbot.2023.105932

Huang X, Zeng X, Li J, Zhao D. Construction and analysis of tify1a and tify1b mutants in rice (Oryza sativa) based on CRISPR/Cas9 technology. Journal of Agricultural Biotechnology. 2017;25(6):1003–12. https://doi.org/10.3724/SP.J.1012.2017.00007

Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, et al. Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9. Nature Plants. 2016;2(10):1–6. https://doi.org/10.1038/nplants.2016.150

Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, et al. Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Molecular plant. 2016;9(4):628–31. https://doi.org/10.1016/j.molp.2016.01.001

Zhou H, He M, Li J, Chen L, Huang Z, Zheng S, et al. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Scientific reports. 2016;6(1):37395. https://doi.org/10.1038/srep37395

Li Q, Zhang D, Chen M, Liang W, Wei J, Qi Y, et al. Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. Journal of Genetics and Genomics. 2016;43(6):415–9. https://doi.org/10.1016/j.jgg.2016.05.003

Shao G, Xie L, Jiao G, Wei X, Sheng Z, Tang S, et al. CRISPR/Cas9-mediated editing of the fragrant gene Badh2 in rice. Chinese Journal of Rice Science. 2017;31(2):216. https://doi.org/10.1101/169013

Ashokkumar S, Jaganathan D, Ramanathan V, Rahman H, Palaniswamy R, Kambale R, et al. Creation of novel alleles of fragrance gene OsBADH2 in rice through CRISPR/Cas9 mediated gene editing. PloS one. 2020;15(8):e0237018. https://doi.org/10.1371/journal.pone.0237018

Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Scientific reports. 2017;7(1):14438. https://doi.org/10.1038/s41598-017-14787-5

Che J, Yamaji N, Ma JF. Role of a vacuolar iron transporter OsVIT2 in the distribution of iron to rice grains. New Phytologist. 2021;230(3):1049–62. https://doi.org/10.1111/nph.17203

Yang Y, Guo M, Sun S, Zou Y, Yin S, Liu Y, et al. Natural variation of OsGluA2 is involved in grain protein content regulation in rice. Nature communications. 2019;10(1):1949. https://doi.org/10.1038/s41467-019-09891-4

Wang S, Yang Y, Guo M, Zhong C, Yan C, Sun S. Targeted mutagenesis of amino acid transporter genes for rice quality improvement using the CRISPR/Cas9 system. The Crop Journal. 2020;8(3):457–64. https://doi.org/10.1016/j.cj.2020.02.006

Akama K, Akter N, Endo H, Kanesaki M, Endo M, Toki S. An in vivo targeted deletion of the calmodulin-binding domain from rice glutamate decarboxylase 3 (Os GAD3) increases ?-aminobutyric acid content in grains. Rice. 2020;13:1–12. https://doi.org/10.1186/s12284-020-00407-w

Sun S-K, Xu X, Tang Z, Tang Z, Huang X-Y, Wirtz M, et al. A molecular switch in sulfur metabolism to reduce arsenic and enrich selenium in rice grain. Nature Communications. 2021;12(1):1392. https://doi.org/10.1038/s41467-021-21606-4

Le VT, Kim M-S, Jung Y-J, Kang K-K, Cho Y-G. Research trends and challenges of using CRISPR/Cas9 for improving rice productivity. Agronomy. 2022;12(1):164. https://doi.org/10.3390/agronomy12010164

Xu J, Xing Y, Xu Y, Wan J. Breeding by design for future rice: Genes and genome technologies. Elsevier; 2021. p. 491–6. https://doi.org/10.1016/B978-0-12-822935-5.00028-2

Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Molecular plant. 2015;8(8):1274–84. https://doi.org/10.1016/j.molp.2015.05.002

Wang M, Lu Y, Botella JR, Mao Y, Hua K, Zhu J-K. Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Molecular plant. 2017;10(7):1007–10. https://doi.org/10.1016/j.molp.2017.04.003

Tetlow IJ, Morell MK, Emes MJ. Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of experimental botany. 2004;55(406):2131–45. https://doi.org/10.1093/jxb/erh246

Sun Y, Jiao G, Liu Z, Zhang X, Li J, Guo X, et al. Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Frontiers in plant science. 2017;8:298. https://doi.org/10.3389/fpls.2017.00298

Regina A, Kosar-Hashemi B, Ling S, Li Z, Rahman S, Morell M. Control of starch branching in barley defined through differential RNAi suppression of starch branching enzyme IIa and IIb. Journal of experimental botany. 2010;61(5):1469–82. https://doi.org/10.1093/jxb/erp420

Mizuno K, Kawasaki T, Shimada H, Satoh H, Kobayashi E, Okumura S, et al. Alteration of the structural properties of starch components by the lack of an isoform of starch branching enzyme in rice seeds. Journal of Biological Chemistry. 1993;268(25):19084–91. https://doi.org/10.1016/S0021-9258(18)48901-1

Nishi A, Nakamura Y, Tanaka N, Satoh H. Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant physiology. 2001;127(2):459–72. https://doi.org/10.1104/pp.127.2.459

Sun Y, Jiao G, Liu Z, Zhang X, Li J, Guo X, et al. Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Frontiers in Plant Science. 2017;8:298. https://doi.org/10.3389/fpls.2017.00298

Zhu L, Gu M, Meng X, Cheung SC, Yu H, Huang J, et al. High-amylose rice improves indices of animal health in normal and diabetic rats. Plant Biotechnology Journal. 2012;10(3):353–62. https://doi.org/10.1111/j.1467-7652.2012.00706.x

Guo L, Li J, Gui Y, Zhu Y, Cui B. Improving waxy rice starch functionality through branching enzyme and glucoamylase: Role of amylose as a viable substrate. Carbohydrate polymers. 2020;230:115712. https://doi.org/10.1016/j.carbpol.2019.115712

Asai H, Abe N, Matsushima R, Crofts N, Oitome NF, Nakamura Y, et al. Deficiencies in both starch synthase IIIa and branching enzyme IIb lead to a significant increase in amylose in SSIIa-inactive japonica rice seeds. Journal of Experimental Botany. 2014;65(18):5497–507. https://doi.org/10.1093/jxb/eru297

Kaur B, Ranawana V, Henry J. The glycemic index of rice and rice products: A review, and table of GI values. Critical reviews in food science and nutrition. 2016;56(2):215–36. https://doi.org/10.1080/10408398.2013.830724

Kang M-S, Jang K-A, Kim H-R, Song S. Association of dietary resistant starch intake with obesity and metabolic syndrome in Korean adults. Nutrients. 2024;16(1):158. https://doi.org/10.3390/nu16010158

Lin C-H, Chang D-M, Wu D-J, Peng H-Y, Chuang L-M. Assessment of blood glucose regulation and safety of resistant starch formula-based diet in healthy normal and subjects with type 2 diabetes. Medicine. 2015;94(33):e1417. https://doi.org/10.1097/MD.0000000000001417

Liang D, Zhang L, Chen H, Zhang H, Hu H, Dai X. Potato resistant starch inhibits diet-induced obesity by modifying the composition of intestinal microbiota and their metabolites in obese mice. International Journal of Biological Macromolecules. 2021;180:458–69. https://doi.org/10.1016/j.ijbiomac.2021.03.055

Blaak E, Canfora E, Theis S, Frost G, Groen A, Mithieux G, et al. Short chain fatty acids in human gut and metabolic health. Beneficial microbes. 2020;11(5):411–55. https://doi.org/10.3920/BM2020.0035

Wang W, Chen L, Zhou R, Wang X, Song L, Huang S, et al. Increased proportions of Bifidobacterium and the Lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. Journal of Clinical Microbiology. 2014;52(2):398–406. https://doi.org/10.1128/JCM.03111-13

Den Besten G, Bleeker A, Gerding A, van Eunen K, Havinga R, van Dijk TH, et al. Short-chain fatty acids protect against high-fat diet–induced obesity via a PPAR?-dependent switch from lipogenesis to fat oxidation. Diabetes. 2015;64(7):2398–408. https://doi.org/10.2337/db14-1519

Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SE, et al. Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut. 2015;64(11):1744–54. https://doi.org/10.1136/gutjnl-2014-307312

De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell. 2014;156(1):84–96. https://doi.org/10.1016/j.cell.2013.12.016

Eghbalsaied S, Lawler C, Petersen B, Hajiyev RA, Bischoff SR, Frankenberg S. CRISPR/Cas9-mediated base editors and their prospects for mitochondrial genome engineering. Gene Therapy. 2024;31(5):209–23. https://doi.org/10.1038/s41434-024-00206-9

Liao H, Wu J, VanDusen NJ, Li Y, Zheng Y. CRISPR-Cas9-mediated homology-directed repair for precise gene editing. Molecular Therapy Nucleic Acids. 2024;35(4):550–61. https://doi.org/10.1016/j.omtn.2024.01.007

Kim M, Hwang Y, Lim S, Jang H-K, Kim H-O. Advances in nanoparticles as non-viral vectors for efficient delivery of CRISPR/Cas9. Pharmaceutics. 2024;16(9):1197. https://doi.org/10.3390/pharmaceutics16091197

Asmamaw Mengstie M, Teshome Azezew M, Asmamaw Dejenie T, Teshome AA, Tadele Admasu F, Behaile Teklemariam A, et al. Recent Advancements in Reducing the Off-Target Effect of CRISPR-Cas9 Genome Editing. Biologics: Targets and Therapy. 2024:21–8. https://doi.org/10.2147/BTT.S379542

Kaupbayeva B, Tsoy A, Safarova Y, Nurmagambetova A, Murata H, Matyjaszewski K, et al. Unlocking Genome Editing: Advances and Obstacles in CRISPR/Cas Delivery Technologies. Journal of Functional Biomaterials. 2024;15(11):324. https://doi.org/10.3390/jfb15110324

Jobling SA, Schwall GP, Westcott RJ, Sidebottom CM, Debet M, Gidley MJ, et al. A minor form of starch branching enzyme in potato (Solanum tuberosum L.) tubers has a major effect on starch structure: cloning and characterisation of multiple forms of SBE A. The Plant Journal. 1999;18(2):163–71. https://doi.org/10.1046/j.1365-313x.1999.00457.x

Schwall GP, Safford R, Westcott RJ, Jeffcoat R, Tayal A, Shi Y-C, et al. Production of very-high-amylose potato starch by inhibition of SBE A and B. Nature biotechnology. 2000;18(5):551–4. https://doi.org/10.1038/74552

Wang L, Wang Y, Makhmoudova A, Nitschke F, Tetlow IJ, Emes MJ. CRISPR–Cas9-mediated editing of starch branching enzymes results in altered starch structure in Brassica napus. Plant Physiology. 2022;188(4):1866–86. https://doi.org/10.1093/plphys/kiac282

Rowe D, Garwood D. Effects of Four Maize Endosperm Mutants on Kernel Vigor 1. Crop Science. 1978;18(5):709–12. https://doi.org/10.2135/cropsci1978.0011183X001800050015x

Ma M, Sun S, Zhu J, Qi X, Li G, Hu J, et al. Engineering high amylose and resistant starch in maize by CRISPR/Cas9-mediated editing of starch branching enzymes. The Crop Journal. 2024;12(4):1252–8. https://doi.org/10.1016/j.cj.2024.04.005

Chen J, Wang S, Jiang S, Gan T, Luo X, Shi R, et al. Overexpression of Calcineurin B-like Interacting Protein Kinase 31 Promotes Lodging and Sheath Blight Resistance in Rice. Plants. 2024;13(10):1306. https://doi.org/10.3390/plants13101306

Zhou Y, Xu S, Jiang N, Zhao X, Bai Z, Liu J, et al. Engineering of rice varieties with enhanced resistances to both blast and bacterial blight diseases via CRISPR/Cas9. Plant biotechnology journal. 2022;20(5):876–85. https://doi.org/10.1111/pbi.13742

Dong OX, Yu S, Jain R, Zhang N, Duong PQ, Butler C, et al. Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nature communications. 2020;11(1):1178. https://doi.org/10.1038/s41467-020-14990-5

Pérez L, Soto E, Farré G, Juanos J, Villorbina G, Bassie L, et al. CRISPR/Cas9 mutations in the rice Waxy/GBSSI gene induce allele-specific and zygosity-dependent feedback effects on endosperm starch biosynthesis. Plant cell reports. 2019;38:417–33. https://doi.org/10.1007/s00299-019-02441-w

Zhang JinShan ZJ, Zhang Hui ZH, Botella J, Zhu JianKang ZJ. Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. Journal of Integrative Plant Biology. 2018;60(5):369. https://doi.org/10.1016/j.plantsci.2018.06.004

Yin X, Biswal AK, Dionora J, Perdigon KM, Balahadia CP, Mazumdar S, et al. CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant cell reports. 2017;36:745–57. https://doi.org/10.1007/s00299-017-2135-9

Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, et al. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. Journal of Genetics and Genomics. 2016;43(8):529–32. https://doi.org/10.1016/j.jgg.2016.08.003

Li X, Zhou W, Ren Y, Tian X, Lv T, Wang Z, et al. High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. Journal of genetics and genomics. 2017;44(3):175–8. https://doi.org/10.1016/j.jgg.2017.02.003

Published

22-12-2024

How to Cite

1.
Jayavigneshwari M, Kokiladevi E, Kumar K, Uma D, Manonmani S. Enhancing the nutritional profile of rice by targeting starch branching enzymes using CRISPR/Cas9. Plant Sci. Today [Internet]. 2024 Dec. 22 [cited 2025 Jan. 6];11(sp4). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/5910

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