OsIPK1 frameshift mutations disturb phosphorus homeostasis and impair starch synthesis during grain filling in rice.


Journal

Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343

Informations de publication

Date de publication:
22 Aug 2024
Historique:
received: 07 04 2024
accepted: 10 07 2024
medline: 22 8 2024
pubmed: 22 8 2024
entrez: 22 8 2024
Statut: epublish

Résumé

Inositol 1,3,4,5,6-pentakisphosphate 2-kinase (IPK1) catalyzes the final step in phytic acid (InsP

Identifiants

pubmed: 39172289
doi: 10.1007/s11103-024-01488-z
pii: 10.1007/s11103-024-01488-z
doi:

Substances chimiques

Starch 9005-25-8
Phosphorus 27YLU75U4W
Plant Proteins 0
Phosphotransferases (Alcohol Group Acceptor) EC 2.7.1.-
Phytic Acid 7IGF0S7R8I

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

91

Subventions

Organisme : Natural Science Foundation of Tianjin
ID : 21JCYBJC00010
Organisme : Fundamental Research Funds for the Central Universities, Nankai University
ID : 60
Organisme : National Natural Science Foundation of China
ID : 32070349
Organisme : Rice Industry Technological System of Tianjin
ID : ITTRRS20211000-02

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Aggarwal S, Kumar A, Bhati KK, Kaur G, Shukla V, Tiwari S, Pandey AK (2018) RNAi-mediated downregulation of inositol pentakisphosphate kinase (IPK1) in wheat grains decreases phytic acid levels and increases Fe and Zn accumulation. Front Plant Sci 9:259. https://doi.org/10.3389/fpls.2018.00259
doi: 10.3389/fpls.2018.00259 pubmed: 29559984 pmcid: 5845732
Al Hasan SM, Hassan M, Saha S, Islam M, Billah M, Islam S (2016) Dietary phytate intake inhibits the bioavailability of iron and calcium in the diets of pregnant women in rural Bangladesh: a cross-sectional study. BMC Nutrit 2:24. https://doi.org/10.1186/S40795-016-0064-8
doi: 10.1186/S40795-016-0064-8
Ali N, Paul S, Gayen D, Sarkar SN, Datta K, Datta SK (2013) Development of low phytate rice by RNAi mediated seed-specific silencing of inositol 1,3,4,5,6-pentakisphosphate 2-kinase gene (IPK1). PLoS ONE 8:e68161. https://doi.org/10.1371/journal.pone.0068161
doi: 10.1371/journal.pone.0068161 pubmed: 23844166 pmcid: 3699528
Bhati KK, Aggarwal S, Sharma S, Mantri S, Singh SP, Bhalla S, Kaur J, Tiwari S, Roy JK, Tuli R, Pandey AK (2014) Differential expression of structural genes for the late phase of phytic acid biosynthesis in developing seeds of wheat (Triticum aestivum L.). Plant Sci 224:74–85. https://doi.org/10.1016/j.plantsci.2014.04.009
doi: 10.1016/j.plantsci.2014.04.009 pubmed: 24908508
Bohn L, Meyer AS, Rasmussen SK (2008) Phytate: impact on environment and human nutrition. A challenge for molecular breeding. J Zhejiang Univ-SC B 9:165–191. https://doi.org/10.1631/jzus.B0710640
doi: 10.1631/jzus.B0710640
Cominelli E, Pilu R, Sparvoli F (2020) Phytic acid and transporters: what can we learn from low phytic acid mutants? Plants 9:69. https://doi.org/10.3390/plants9010069
doi: 10.3390/plants9010069 pubmed: 31948109 pmcid: 7020491
Cridland C, Gillaspy G (2020) Inositol pyrophosphate pathways and mechanisms: what can we learn from plants? Molecules 25:2789. https://doi.org/10.3390/molecules25122789
doi: 10.3390/molecules25122789 pubmed: 32560343 pmcid: 7356102
Doyle J (1991) DNA protocols for plants. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular techniques in taxonomy. Springer, Berlin, pp 283–293
doi: 10.1007/978-3-642-83962-7_18
Fitzgerald MA, McCouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trends Plant Sci 14:133–139. https://doi.org/10.1016/j.tplants.2008.12.004
doi: 10.1016/j.tplants.2008.12.004 pubmed: 19230745
Freed C, Adepoju O, Gillaspy G (2020) Can inositol pyrophosphates inform strategies for developing low phytate crops? Plants 9:115. https://doi.org/10.3390/plants9010115
doi: 10.3390/plants9010115 pubmed: 31963418 pmcid: 7020182
Gulabani H, Goswami K, Walia Y, Roy A, Noor JJ, Ingole KD, Kasera M, Laha D, Giehl RFH, Schaaf G, Bhattacharjee S (2022) Arabidopsis inositol polyphosphate kinases IPK1 and ITPK1 modulate crosstalk between SA-dependent immunity and phosphate-starvation responses. Plant Cell Rep 41:347–363. https://doi.org/10.1007/s00299-021-02812-3
doi: 10.1007/s00299-021-02812-3 pubmed: 34797387
Huang B, Hennen-Bierwagen TA, Myers AM (2014) Functions of multiple genes encoding ADP-glucose pyrophosphorylase subunits in maize endosperm, embryo, and leaf. Plant Physiol 164:596–611. https://doi.org/10.1104/pp.113.231605
doi: 10.1104/pp.113.231605 pubmed: 24381067
Ibrahim S, Saleem B, Rehman N, Zafar SA, Naeem MK, Khan MR (2022) CRISPR/Cas9 mediated disruption of Inositol Pentakisphosphate 2-Kinase 1 (TaIPK1) reduces phytic acid and improves iron and zinc accumulation in wheat grains. J Adv Res 37:33–41. https://doi.org/10.1016/j.jare.2021.07.006
doi: 10.1016/j.jare.2021.07.006 pubmed: 35499048
Jeon JS, Ryoo N, Hahn TR, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiol Bioch 48:383–392. https://doi.org/10.1016/j.plaphy.2010.03.006
doi: 10.1016/j.plaphy.2010.03.006
Jiang M, Liu Y, Li R, Li S, Tan Y, Huang J, Shu Q (2021) An inositol 1,3,4,5,6-pentakisphosphate 2-kinase 1 mutant with a 33-nt deletion showed enhanced tolerance to salt and drought stress in rice. Plants 10:23. https://doi.org/10.3390/plants10010023
doi: 10.3390/plants10010023
Kim SI, Tai TH (2011) Identification of genes necessary for wild-type levels of seed phytic acid in Arabidopsis thaliana using a reverse genetics approach. Mol Genet Genomics 286:119–133. https://doi.org/10.1007/s00438-011-0631-2
doi: 10.1007/s00438-011-0631-2 pubmed: 21698461
Kuo HF, Chang TY, Chiang SF, Wang WD, Yy C, Chiou TJ (2014) Arabidopsis inositol pentakisphosphate 2-kinase, AtIPK1, is required for growth and modulates phosphate homeostasis at the transcriptional level. Plant J 80:503–515. https://doi.org/10.1111/tpj.12650
doi: 10.1111/tpj.12650 pubmed: 25155524
Kuo HF, Hsu YY, Lin WC, Chen KY, Munnik T, Brearley CA, Chiou TJ (2018) Arabidopsis inositol phosphate kinases IPK1 and ITPK1 constitute a metabolic pathway in maintaining phosphate homeostasis. Plant J 95:613–630. https://doi.org/10.1111/tpj.13974
doi: 10.1111/tpj.13974
Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546. https://doi.org/10.1007/s11103-007-9153-z
doi: 10.1007/s11103-007-9153-z pubmed: 17406793
Li WX, Zhao HJ, Pang WQ, Cui HR, Poirier Y, Shu QY (2014) Seed-specific silencing of OsMRP5 reduces seed phytic acid and weight in rice. Transgenic Res 23:585–599. https://doi.org/10.1007/s11248-014-9792-1
doi: 10.1007/s11248-014-9792-1 pubmed: 24648215
Li Q, Wang L, Zheng Y, Sun Y, Chen X, Chen D (2019) Editing rice phytate synthetase IPK1 gene using CRISPR/Cas9 technology. Acta Sci Nat Univ Nankaiensis 52:52–59
Liu QL, Xu XH, Ren XL, Fu HW, Wu DX, Shu QY (2007) Generation and characterization of low phytic acid germplasm in rice (Oryza sativa L.). Theor Appl Genet 114:803–814. https://doi.org/10.1007/s00122-006-0478-9
doi: 10.1007/s00122-006-0478-9 pubmed: 17219209
Liu JX, Wu MW, Liu CM (2022) Cereal endosperms: development and storage product accumulations. Annu Rev Plant Biol 73:255–291. https://doi.org/10.1146/annurev-arplant-070221-024405
doi: 10.1146/annurev-arplant-070221-024405 pubmed: 35226815
Lloyd JP, Seddon AE, Moghe GD, Simenc MC, Shiua SH (2015) Characteristics of plant essential genes allow for within- and between-species prediction of lethal mutant phenotypes. Plant Cell 27:2133–2147. https://doi.org/10.1105/tpc.15.00051
doi: 10.1105/tpc.15.00051 pubmed: 26286535 pmcid: 4568498
Ma B, Zhang L, Gao Q, Wang J, Li X, Wang H, Liu Y, Lin H, Liu J, Wang X, Li Q, Deng Y, Tang W, Luan S, He Z (2021) A plasma membrane transporter coordinates phosphate reallocation and grain filling in cereals. Nat Genet 53:906–915. https://doi.org/10.1038/s41588-021-00855-6
doi: 10.1038/s41588-021-00855-6 pubmed: 33927398
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural water. Anal Chim Acta 27:31–36. https://doi.org/10.1016/s0003-2670(00)88444-5
doi: 10.1016/s0003-2670(00)88444-5
Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci 73:2781–2807. https://doi.org/10.1007/s00018-016-2250-x
doi: 10.1007/s00018-016-2250-x pubmed: 27166931 pmcid: 4919380
Poon JSY, Le Fevre RE, Carr JP, Hanke DE, Murphy AM (2020) Inositol hexakisphosphate biosynthesis underpins PAMP-triggered immunity to Pseudomonas syringae pv. tomato in Arabidopsis thaliana but is dispensable for establishment of systemic acquired resistance. Mol Plant Pathol 21:376–387. https://doi.org/10.1111/mpp.12902
doi: 10.1111/mpp.12902 pubmed: 31876373
Preiss J (1982) Regulation of the biosynthesis and degradation of starch. Annu Rev Plant Physiol 33:431–454. https://doi.org/10.1146/annurev.pp.33.060182.002243
doi: 10.1146/annurev.pp.33.060182.002243
Raboy V (1997a) Accumulation and storage of phosphate and minerals. In: Larkins BA, Vasil IK (eds) Cellular and molecular biology of plant seed development. Kluwer Academic Publishers, pp 441–477
doi: 10.1007/978-94-015-8909-3_12
Raboy V (2000) Low-phytic-acid grains. Food Nutrit Bull 21:423–427. https://doi.org/10.1177/156482650002100416
doi: 10.1177/156482650002100416
Raboy V (2001) Seeds for a better future: ‘low phytate’ grains help to overcome malnutrition and reduce pollution. Trends Plant Sci 6:458–462. https://doi.org/10.1016/s1360-1385(01)02104-5
doi: 10.1016/s1360-1385(01)02104-5 pubmed: 11590064
Raboy V (1997b) Low phytic acid mutants and selection thereof. United States Patent PAT:US6111168
Sahu A, Verma R, Gupta U, Kashyap S, Sanyal I (2024) An overview of targeted genome editing strategies for reducing the biosynthesis of phytic acid: an anti-nutrient in crop plants. Mol Biotechnol 66:11–25. https://doi.org/10.1007/s12033-023-00722-1
doi: 10.1007/s12033-023-00722-1 pubmed: 37061991
Saiardi A, Erdjument-Bromage H, Snowman AM, Tempst P, Snyder SH (1999) Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr Biol 9:1323–1326. https://doi.org/10.1016/s0960-9822(00)80055-x
doi: 10.1016/s0960-9822(00)80055-x pubmed: 10574768
Saripalli G, Gupta PK (2015) AGPase: its role in crop productivity with emphasis on heat tolerance in cereals. Theor Appl Genet 128:1893–1916. https://doi.org/10.1007/s00122-015-2565-2
doi: 10.1007/s00122-015-2565-2 pubmed: 26152573
Sharpley AN, Chapra SC, Wedepohl R, Sims JT, Daniel TC, Reddy KR (1994) Managing agricultural phosphorus for protection of surface waters: issues and options. J Environ Qual 23:437–451. https://doi.org/10.2134/jeq1994.00472425002300030006x
doi: 10.2134/jeq1994.00472425002300030006x
Shi J, Wang H, Hazebroek J, Ertl DS, Harp T (2005) The maize low-phytic acid 3 encodes a myo-inositol kinase that plays a role in phytic acid biosynthesis in developing seeds. Plant J 42:708–719. https://doi.org/10.1111/j.1365-313X.2005.02412.x
doi: 10.1111/j.1365-313X.2005.02412.x pubmed: 15918884
Silva VM, Putti FF, White PJ, Reis ARd (2021) Phytic acid accumulation in plants: biosynthesis pathway regulation and role in human diet. Plant Physiol Biochem 164:132–146. https://doi.org/10.1016/j.plaphy.2021.04.035
doi: 10.1016/j.plaphy.2021.04.035 pubmed: 33991859
Song JH, Shin G, Kim HJ, Lee SB, Moon JY, Jeong JC, Choi H-K, Kim IA, Song HJ, Kim CY, Chung YS (2022) Mutation of GmIPK1 gene using CRISPR/Cas9 reduced phytic acid content in soybean seeds. Int J Mol Sci 23:10583. https://doi.org/10.3390/ijms231810583
doi: 10.3390/ijms231810583 pubmed: 36142495 pmcid: 9504718
Stevenson-Paulik J, Odom AR, York JD (2002) Molecular and biochemical characterization of two plant inositol polyphosphate 6-/3-/5-kinases. J Biol Chem 277:42711–42718. https://doi.org/10.1074/jbc.M209112200
doi: 10.1074/jbc.M209112200 pubmed: 12226109
Stevenson-Paulik J, Bastidas RJ, Chiou ST, Frye RA, York JD (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc Natl Acad Sci USA 102:12612–12617. https://doi.org/10.1073/pnas.0504172102
doi: 10.1073/pnas.0504172102 pubmed: 16107538 pmcid: 1194928
Sun YY, Xu WZ, Wu L, Wang RZ, He ZY, Ma M (2016) An Arabidopsis mutant of inositol pentakisphosphate 2-kinase AtIPK1 displays reduced arsenate tolerance. Plant Cell Environ 39:416–426. https://doi.org/10.1111/pce.12623
doi: 10.1111/pce.12623 pubmed: 26264234
Suzuki M, Tanaka K, Kuwano M, Yoshida KT (2007) Expression pattern of inositol phosphate-related enzymes in rice (Oryza sativa L.): implications for the phytic acid biosynthetic pathway. Gene 405:55–64. https://doi.org/10.1016/j.gene.2007.09.006
doi: 10.1016/j.gene.2007.09.006 pubmed: 17961936
Verbsky JW, Wilson MP, Kisseleva MV, Majerus PW, Wente SR (2002) The synthesis of inositol hexakisphosphate: characterization of human inositol 1,3,4,5,6-pentakisphosphate 2-kinase. J Biol Chem 277:31857–31862. https://doi.org/10.1074/jbc.M205682200
doi: 10.1074/jbc.M205682200 pubmed: 12084730
Wang X, Zhou W, Lu Z, Ouyang Y, Su OC, Yao J (2015) A lipid transfer protein, OsLTPL36, is essential for seed development and seed quality in rice. Plant Sci 239:200–208. https://doi.org/10.1016/j.plantsci.2015.07.016
doi: 10.1016/j.plantsci.2015.07.016 pubmed: 26398804
Wang W, Xie Y, Liu L, King GJ, White P, Ding G, Wang S, Cai H, Wang C, Xu F, Shi L (2022) Genetic control of seed phytate accumulation and the development of low-phytate crops: a review and perspective. J Agric Food Chem 70:3375–3390. https://doi.org/10.1021/acs.jafc.1c06831
doi: 10.1021/acs.jafc.1c06831 pubmed: 35275483
Wilson MP, Majerus PW (1997) Characterization of a cDNA encoding Arabidopsis thaliana inositol 1,3,4-trisphosphate 5/6-kinase. Biochem Bioph Res Co 232:678–681. https://doi.org/10.1006/bbrc.1997.6355
doi: 10.1006/bbrc.1997.6355
Xu Y, Yang J, Wang YH, Wang JC, Wan JM (2017) OsCNGC13 promotes seed-setting rate by facilitating pollen tube growth in stylar tissues. PLoS Genet 1:e1006906. https://doi.org/10.1371/journal.pgen.1006906
doi: 10.1371/journal.pgen.1006906
Yang X, Shears SB (2000) Multitasking in signal transduction by a promiscuous human Ins(3,4,5,6)P
doi: 10.1042/BJ3510551 pubmed: 11042108 pmcid: 1221393
Yang SY, Lu WC, Ko SS, Sun CM, Hung JC, Chiou TJ (2020) Upstream open reading frame and phosphate-regulated expression of rice OsNLA1 controls phosphate transport and reproduction1. Plant Physiol 182:393–407. https://doi.org/10.1104/pp.19.01101
doi: 10.1104/pp.19.01101 pubmed: 31659125
Yuan FJ, Zhao HJ, Ren XL, Zhu SL, Fu XJ, Shu QY (2007) Generation and characterization of two novel low phytate mutations in soybean (Glycine max L. Merr.). Theor Appl Genet 115:945–957. https://doi.org/10.1007/s00122-007-0621-2
doi: 10.1007/s00122-007-0621-2 pubmed: 17701395
Yuan FJ, Zhu DH, Tan YY, Dong DK, Fu XJ, Zhu SL, Li BQ, Shu QY (2012) Identification and characterization of the soybean IPK1 ortholog of a low phytic acid mutant reveals an exon-excluding splice-site mutation. Theor Appl Genet 125:1413–1423. https://doi.org/10.1007/s00122-012-1922-7
doi: 10.1007/s00122-012-1922-7 pubmed: 22733447
Zhao NC, Zhang QF, Wu DX, Wei KS, Zhang XM, Cheng FM (2008) Characteristics of grain starch synthesis at filling stage and translocation of carbohydrates in leaves and sheaths for low phytic acid mutant rice. Acta Agron Sin 34:1977–1984. https://doi.org/10.1016/S1875-2780(09)60017-1
doi: 10.1016/S1875-2780(09)60017-1
Zhou Y (2015) Screening of rice genes with highly endosperm-specificexpression pattern and preliminary analysis of the promoter of Latex-1 gene [Master, Fujian Agricultural and Forest University] (in Chinese with English abstract)

Auteurs

Lina Wang (L)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.

Jing Cui (J)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.

Ning Zhang (N)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.

Xueqin Wang (X)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.

Jingping Su (J)

Tianjin Key Laboratory of Crop Genetics and Breeding, Crop Research Institute, Tianjin Academy of Agricultural Sciences, Tianjin, 300384, China.

María Pilar Vallés (MP)

Department of Genetics and Plant Breeding, Aula Dei Experimental Station, Spanish National Research Council (EEAD-CSIC), Zaragoza, 50059, Spain.

Shian Wu (S)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.

Wei Yao (W)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.

Xiwen Chen (X)

Department of Biochemistry and Molecular Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China. xiwenchen@nankai.edu.cn.

Defu Chen (D)

Department of Genetics and Cell Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China. chendefu@nankai.edu.cn.
Southwest United Graduate School, Kunming, 650092, China. chendefu@nankai.edu.cn.

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