Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Maize STARCH SYNTHESIS REGULATING PROTEIN1 positively regulates starch biosynthesis in rice endosperm

Long Chen A # , Ming Du A B # , Long Wang A # , Wei Yu A , Yirong Chen A , Beijiu Cheng A and Jiandong Wu https://orcid.org/0000-0002-0739-2479 A *
+ Author Affiliations
- Author Affiliations

A National Engineering Laboratory of Crop Stress Resistance, College of Life Science, Anhui Agricultural University, Hefei 230036, Anhui, China.

B Shanghai Zhongke Quanyin Molecular Breeding Technology, Shanghai 200030, China.

* Correspondence to: wujiandong@ahau.edu.cn
# These authors contributed equally to this paper

Handling Editor: Thomas Roberts

Functional Plant Biology 49(9) 773-783 https://doi.org/10.1071/FP21338
Submitted: 7 April 2021  Accepted: 9 April 2022   Published: 2 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Starch is a major component of the endosperm, directly determining grain yield and quality. Although the key enzymes of starch synthesis have been identified and characterised, the regulatory mechanisms remain unclear. In this study, we identified the novel maize STARCH SYNTHESIS REGULATING PROTEIN1 (ZmSSRP1), which encodes a typical carbohydrate-binding module 48 (CBM48) protein. Expression analysis revealed that ZmSSRP1 was highly expressed in the maize endosperm, while transient expression in maize leaf protoplasts showed localisation in the plastids, dependent on the N-terminal transit peptide. In addition, overexpression of ZmSSRP1 in rice resulted in a decrease in grain thickness and the 1000-grain weight, as well as affecting the starch content and structure of the rice endosperm. The physicochemical properties of starch in the rice endosperm were also altered compared with the wild-type seeds. Real-time quantitative reverse transcription polymerase chain reaction (qRT-PCR) was subsequently performed to determine the expression of starch synthesis-related genes, revealing upregulation of mRNA expression of most genes in the transgenic compared with wild-type lines. Collectively, these findings suggest that ZmSSRP1 acts as a potential regulator of starch synthesis, providing new insight for molecular breeding of high-yielding high-quality maize.

Keywords: CBM48, endosperm, maize, plastids, rice, seeds size, starch, ZmSSRP1.


References

Ballicora MA, Iglesias AA, Preiss J (2004) ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynthesis Research 79, 1–24.
ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis.Crossref | GoogleScholarGoogle Scholar | 16228397PubMed |

Boraston AB, Ficko-Blean E, Healey M (2007) Carbohydrate recognition by a large sialidase toxin from Clostridium perfringens. Biochemistry 46, 11352–11360.
Carbohydrate recognition by a large sialidase toxin from Clostridium perfringens.Crossref | GoogleScholarGoogle Scholar | 17850114PubMed |

Cano A, Jiménez A, Cháfer M, Gónzalez C, Chiralt A (2014) Effect of amylose:amylopectin ratio and rice bran addition on starch films properties. Carbohydrate Polymers 111, 543–555.
Effect of amylose:amylopectin ratio and rice bran addition on starch films properties.Crossref | GoogleScholarGoogle Scholar | 25037386PubMed |

Chen J, Yi Q, Cao Y, Wei B, Zheng L, Xiao Q, Xie Y, Gu Y, Li Y, Huang H, Wang Y, Hou X, Long T, Zhang J, Liu Han Liu Y, Yu G, Huang Y (2016) ZmbZIP91 regulates expression of starch synthesis-related genes by binding to ACTCAT elements in their promoters. Journal of Experimental Botany 67, 1327–1338.
ZmbZIP91 regulates expression of starch synthesis-related genes by binding to ACTCAT elements in their promoters.Crossref | GoogleScholarGoogle Scholar | 26689855PubMed |

Christiansen C, Hachem MA, Glaring MA, Viksø-Nielsen A, Sigurskjold BW, Svensson B, Blennow A (2009) A CBM20 low-affinity starch-binding domain from glucan, water dikinase. FEBS Letters 583, 1159–1163.
A CBM20 low-affinity starch-binding domain from glucan, water dikinase.Crossref | GoogleScholarGoogle Scholar | 19275898PubMed |

Denyer K, Johnson P, Zeeman S, Smith AM (2001) The control of amylose synthesis. Journal of Plant Physiology 158, 479–487.
The control of amylose synthesis.Crossref | GoogleScholarGoogle Scholar |

Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux J-L, Buleon A, Haebel S, Ritte G, Steup M, Falcon LI, Moreira D, Löffelhardt W, Raj JN, Plancke C, d’Hulst C, Dauvillée D, Ball S (2008) Metabolic symbiosis and the birth of the plant kingdom. Molecular Biology and Evolution 25, 536–548.
Metabolic symbiosis and the birth of the plant kingdom.Crossref | GoogleScholarGoogle Scholar | 18093994PubMed |

Dong Q, Xu Q, Kong J, Peng X, Zhou W, Chen L, Wu J, Xiang Y, Jiang H, Cheng B (2019) Overexpression of ZmbZIP22 gene alters endosperm starch content and composition in maize and rice. Plant Science 283, 407–415.
Overexpression of ZmbZIP22 gene alters endosperm starch content and composition in maize and rice.Crossref | GoogleScholarGoogle Scholar | 31128711PubMed |

Figueroa CM, Lunn JE, Iglesias AA (2021) Nucleotide-sugar metabolism in plants: the legacy of Luis F. Leloir. Journal of Experimental Botany 72, 4053–4067.
Nucleotide-sugar metabolism in plants: the legacy of Luis F. Leloir.Crossref | GoogleScholarGoogle Scholar | 33948638PubMed |

Figueroa CM, Asencion Diez MD, Ballicora MA, Iglesias AA (2022) Structure, function, and evolution of plant ADP-glucose pyrophosphorylase. Plant Molecular Biology 108, 307–323.
Structure, function, and evolution of plant ADP-glucose pyrophosphorylase.Crossref | GoogleScholarGoogle Scholar | 35006475PubMed |

Fisher DK, Boyer CD, Hannah LC (1993) Starch branching enzyme II from maize endosperm. Plant Physiology 102, 1045–1046.
Starch branching enzyme II from maize endosperm.Crossref | GoogleScholarGoogle Scholar | 8278524PubMed |

Flint-Garcia SA, Bodnar AL, Scott MP (2009) Wide variability in kernel composition, seed characteristics, and zein profiles among diverse maize inbreds, landraces, and teosinte. Theoretical and Applied Genetics 119, 1129–1142.
Wide variability in kernel composition, seed characteristics, and zein profiles among diverse maize inbreds, landraces, and teosinte.Crossref | GoogleScholarGoogle Scholar | 19701625PubMed |

Fu F-F, Xue H-W (2010) Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiology 154, 927–938.
Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator.Crossref | GoogleScholarGoogle Scholar | 20713616PubMed |

Guillén D, Sánchez S, Rodríguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Applied Microbiology and Biotechnology 85, 1241–1249.
Carbohydrate-binding domains: multiplicity of biological roles.Crossref | GoogleScholarGoogle Scholar | 19908036PubMed |

Han X, Wang Y, Liu X, Jiang L, Ren Y, Liu F, Peng C, Li J, Jin X, Wu F, Wang J, Guo X, Zhang X, Cheng Z, Wan J (2012) The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. Journal of Experimental Botany 63, 121–130.
The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice.Crossref | GoogleScholarGoogle Scholar | 21984651PubMed |

Hedin N, Velazquez MB, Barchiesi J, Gomez-Casati DF, Busi MV (2022) CBM20CP, a novel functional protein of starch metabolism in green algae. Plant Molecular Biology 108, 363–378.
CBM20CP, a novel functional protein of starch metabolism in green algae.Crossref | GoogleScholarGoogle Scholar | 34546521PubMed |

Ito Y, Tomita T, Roy N, Nakano A, Sugawara-Tomita N, Watanabe S, Okai N, Abe N, Kamio Y (2003) Cloning, expression, and cell surface localization of Paenibacillus sp. strain W-61 xylanase 5, a multidomain xylanase. Applied and Environmental Microbiology 69, 6969–6978.
Cloning, expression, and cell surface localization of Paenibacillus sp. strain W-61 xylanase 5, a multidomain xylanase.Crossref | GoogleScholarGoogle Scholar | 14660338PubMed |

Janeček S, Svensson B, MacGregor EA (2011) Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzyme and Microbial Technology 49, 429–440.
Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals.Crossref | GoogleScholarGoogle Scholar | 22112614PubMed |

Jeon J-S, Ryoo N, Hahn T-R, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiology and Biochemistry 48, 383–392.
Starch biosynthesis in cereal endosperm.Crossref | GoogleScholarGoogle Scholar | 20400324PubMed |

Jiang Y, Zheng Q, Chen L, Liang Y, Wu J (2018) Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis. Acta Physiologiae Plantarum 40, 9
Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Kang H-G, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). The Plant Journal 42, 901–911.
White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB).Crossref | GoogleScholarGoogle Scholar | 15941402PubMed |

Kemp BE, Oakhill JS, Scott JW (2007) AMPK structure and regulation from three angles. Structure 15, 1161–1163.
AMPK structure and regulation from three angles.Crossref | GoogleScholarGoogle Scholar | 17937905PubMed |

Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M, Ritte G, Zeeman SC (2009) STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. The Plant Cell 21, 334–346.
STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 19141707PubMed |

Lai J, Dey N, Kim C-S, Bharti AK, Rudd S, Mayer KFX, Larkins BA, Becraft P, Messing J (2004) Characterization of the maize endosperm transcriptome and its comparison to the rice genome. Genome Research 14, 1932–1937.
Characterization of the maize endosperm transcriptome and its comparison to the rice genome.Crossref | GoogleScholarGoogle Scholar | 15466291PubMed |

Leloir LF, Rongine De Fekete MA, Cardini CE (1961) Starch and oligosaccharide synthesis from uridine diphosphate glucose. The Journal of Biological Chemistry 236, 636–641.
Starch and oligosaccharide synthesis from uridine diphosphate glucose.Crossref | GoogleScholarGoogle Scholar | 13760681PubMed |

Lin Q, Huang B, Zhang M, Zhang X, Rivenbark J, Lappe RL, James MG, Myers AM, Hennen-Bierwagen TA (2012) Functional interactions between starch synthase III and isoamylase-type starch-debranching enzyme in maize endosperm. Plant Physiology 158, 679–692.
Functional interactions between starch synthase III and isoamylase-type starch-debranching enzyme in maize endosperm.Crossref | GoogleScholarGoogle Scholar | 22193705PubMed |

McBride A, Ghilagaber S, Nikolaev A, Hardie DG (2009) The glycogen-binding domain on the AMPK β subunit allows the kinase to act as a glycogen sensor. Cell Metabolism 9, 23–34.
The glycogen-binding domain on the AMPK β subunit allows the kinase to act as a glycogen sensor.Crossref | GoogleScholarGoogle Scholar | 19117544PubMed |

Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T (1995) Production of waxy (amylose-free) wheats. Molecular and General Genetics MGG 248, 253–259.
Production of waxy (amylose-free) wheats.Crossref | GoogleScholarGoogle Scholar | 7565586PubMed |

Nelson O, Pan D (1995) Starch synthesis in maize endosperms. Annual Review of Plant Physiology and Molecular Biology 46, 475–496.
Starch synthesis in maize endosperms.Crossref | GoogleScholarGoogle Scholar |

Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochemical and Biophysical Research Communications 9, 297–300.
The enzymatic deficiency in the waxy mutant of maize.Crossref | GoogleScholarGoogle Scholar | 13938053PubMed |

Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiology 127, 459–472.
Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm.Crossref | GoogleScholarGoogle Scholar | 11598221PubMed |

Peng C, Wang Y, Liu F, Ren Y, Zhou K, Lv J, Zheng M, Zhao S, Zhang L, Wang C, Jiang L, Zhang X, Guo X, Bao Y, Wan J (2014) FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. The Plant Journal 77, 917–930.
FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm.Crossref | GoogleScholarGoogle Scholar | 24456533PubMed |

Peymanpour G, Marcone M, Ragaee S, Tetlow I, Lane CC, Seetharaman K, Bertoft E (2016) On the molecular structure of the amylopectin fraction isolated from “high-amylose” ae maize starches. International Journal of Biological Macromolecules 91, 768–777.
On the molecular structure of the amylopectin fraction isolated from “high-amylose” ae maize starches.Crossref | GoogleScholarGoogle Scholar | 27296443PubMed |

Qu J, Xu S, Zhang Z, Chen G, Zhong Y, Liu L, Zhang R, Xue J, Guo D (2018) Evolutionary, structural and expression analysis of core genes involved in starch synthesis. Scientific Reports 8, 12736
Evolutionary, structural and expression analysis of core genes involved in starch synthesis.Crossref | GoogleScholarGoogle Scholar | 30143668PubMed |

Recondo E, Leloir LF (1961) Adenosine diphosphate glucose and starch synthesis. Biochemical and Biophysical Research Communications 6, 85–88.
Adenosine diphosphate glucose and starch synthesis.Crossref | GoogleScholarGoogle Scholar | 14490887PubMed |

Seung D, Soyk S, Coiro M, Maier BA, Eicke S, Zeeman SC (2015) PROTEIN TARGETING TO STARCH is required for localising GRANULE-BOUND STARCH SYNTHASE to starch granules and for normal amylose synthesis in Arabidopsis. PLoS Biology 13, e1002080
PROTEIN TARGETING TO STARCH is required for localising GRANULE-BOUND STARCH SYNTHASE to starch granules and for normal amylose synthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25710501PubMed |

Seung D, Boudet J, Monroe J, Schreier TB, David LC, Abt M, Lu K-J, Zanella M, Zeeman SC (2017) Homologs of PROTEIN TARGETING TO STARCH control starch granule initiation in Arabidopsis leaves. The Plant Cell 29, 1657–1677.
Homologs of PROTEIN TARGETING TO STARCH control starch granule initiation in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 28684429PubMed |

Sheen J (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiology 127, 1466–1475.
Signal transduction in maize and Arabidopsis mesophyll protoplasts.Crossref | GoogleScholarGoogle Scholar | 11743090PubMed |

Smith AM, Zeeman SC (2020) Starch: a flexible, adaptable carbon store coupled to plant growth. Annual Review of Plant Biology 71, 217–245.
Starch: a flexible, adaptable carbon store coupled to plant growth.Crossref | GoogleScholarGoogle Scholar | 32075407PubMed |

Syahariza ZA, Sar S, Hasjim J, Tizzotti MJ, Gilbert RG (2013) The importance of amylose and amylopectin fine structures for starch digestibility in cooked rice grains. Food Chemistry 136, 742–749.
The importance of amylose and amylopectin fine structures for starch digestibility in cooked rice grains.Crossref | GoogleScholarGoogle Scholar | 23122122PubMed |

Takeda Y, Hizukuri S, Juliano BO (1986) Purification and structure of amylose from rice starch. Carbohydrate Research 148, 299–308.
Purification and structure of amylose from rice starch.Crossref | GoogleScholarGoogle Scholar |

Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiology 128, 1212–1222.
The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase.Crossref | GoogleScholarGoogle Scholar | 11950970PubMed |

Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, Esposito S, Kosar-Hashemi B, Morell MK, Emes MJ (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein–protein interactions. The Plant Cell 16, 694–708.
Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein–protein interactions.Crossref | GoogleScholarGoogle Scholar | 14973170PubMed |

Tetlow IJ, Beisel KG, Cameron S, Makhmoudova A, Liu F, Bresolin NS, Wait R, Morell MK, Emes MJ (2008) Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiology 146, 1878–1891.
Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes.Crossref | GoogleScholarGoogle Scholar | 18263778PubMed |

Tian Z, Qian Q, Liu Q, Yan M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D, Wang Y, Yu J, Gu M, Li J (2009) Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proceedings of the National Academy of Sciences of the United States of America 106, 21760–21765.
Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities.Crossref | GoogleScholarGoogle Scholar | 20018713PubMed |

Wang J-C, Xu H, Zhu Y, Liu Q-Q, Cai X-L (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. Journal of Experimental Botany 64, 3453–3466.
OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm.Crossref | GoogleScholarGoogle Scholar | 23846875PubMed |

Wang X, Zhou W, Lu Z, Ouyang Y, O CS, Yao J (2015) A lipid transfer protein, OsLTPL36, is essential for seed development and seed quality in rice. Plant Science 239, 200–208.
A lipid transfer protein, OsLTPL36, is essential for seed development and seed quality in rice.Crossref | GoogleScholarGoogle Scholar | 26398804PubMed |

Wang W, Wei X, Jiao G, Chen W, Wu Y, Sheng Z, Hu S, Xie L, Wang J, Tang S, Hu P (2019) GBSS-BINDING PROTEIN, encoding a CBM48 domain-containing protein, affects rice quality and yield. Journal of Integrative Plant Biology 62, 948–966.
GBSS-BINDING PROTEIN, encoding a CBM48 domain-containing protein, affects rice quality and yield.Crossref | GoogleScholarGoogle Scholar | 31449354PubMed |

Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES (2002) Genetic diversity and selection in the maize starch pathway. Proceedings of the National Academy of Sciences of the United States of America 99, 12959–12962.
Genetic diversity and selection in the maize starch pathway.Crossref | GoogleScholarGoogle Scholar | 12244216PubMed |

Wu Y, Messing J (2014) Proteome balancing of the maize seed for higher nutritional value. Frontiers in Plant Science 5, 240
Proteome balancing of the maize seed for higher nutritional value.Crossref | GoogleScholarGoogle Scholar | 24910639PubMed |

Wu J, Chen L, Chen M, Zhou W, Dong Q, Jiang H, Cheng B (2019a) The DOF-domain transcription factor ZmDOF36 positively regulates starch synthesis in transgenic maize. Frontiers in Plant Science 10, 465
The DOF-domain transcription factor ZmDOF36 positively regulates starch synthesis in transgenic maize.Crossref | GoogleScholarGoogle Scholar | 31031791PubMed |

Wu J, Jiang Y, Liang Y, Chen L, Chen W, Cheng B (2019b) Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants. Plant Physiology and Biochemistry 137, 179–188.
Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 30798172PubMed |

Zhang L, Li N, Zhang J, Zhao L, Qiu J, Wei C (2022) The CBM48 domain-containing protein FLO6 regulates starch synthesis by interacting with SSIVb and GBSS in rice. Plant Molecular Biology 108, 343–361.
The CBM48 domain-containing protein FLO6 regulates starch synthesis by interacting with SSIVb and GBSS in rice.Crossref | GoogleScholarGoogle Scholar | 34387795PubMed |