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Pho1 cooperates with DPE1 to control short maltooligosaccharide mobilization during starch synthesis initiation in rice endosperm

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Abstract

Key message

Plastidial α-glucan phosphorylase is a key factor that cooperates with plastidial disproportionating enzyme to control short maltooligosaccharide mobilization during the initiation process of starch molecule synthesis in developing rice endosperm.

Abstract

Storage starch synthesis is essential for grain filling. However, little is known about how cereal endosperm controls starch synthesis initiation. One of core events for starch synthesis initiation is short maltooligosaccharide (MOS) mobilization consisting of long MOS primer production and excess MOS breakdown. By mutant analyses and biochemical investigations, we present here functional identifications of plastidial α-glucan phosphorylase (Pho1) and disproportionating enzyme (DPE1) during starch synthesis initiation in rice (Oryza sativa) endosperm. Pho1 deficiency impaired MOS mobilization, triggering short MOS accumulation and starch synthesis reduction during early seed development. The mutant seeds differed significantly in MOS level and starch content at 15 days after flowering and exhibited diverse endosperm phenotypes during mid-late seed development: ranging from pseudonormal to shrunken (Shr), severely or excessively Shr. The level of DPE1 was almost normal in the PN seeds but significantly reduced in the Shr seeds. Overexpression of DPE1 in pho1 resulted in plump seeds only. DPE1 deficiency had no obvious effects on MOS mobilization. Knockout of DPE1 in pho1 completely blocked MOS mobilization, resulting in severely and excessively Shr seeds only. These findings show that Pho1 cooperates with DPE1 to control short MOS mobilization during starch synthesis initiation in rice endosperm.

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Data availability

All data supporting the findings of this study are available within the paper and within its supplementary materials published online.

Abbreviations

DAF:

Days after flowering

DP:

Degree of polymerization

MOS:

Maltooligosaccharide

PN:

Pseudonormal

Shr:

Shrunken

WC:

White-core

WT:

Wild type

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Acknowledgements

We thank Mr. Tong Sun (Institute of Microbiology, Chinese Academy of Sciences) for his excellent technical assistance on HPAEC-PAD. We thank Ms. Li Wang and Ms. Jindan Zhang (Institute of Botany, Chinese Academy of Sciences) for  their help with protein purification and starch fine structure.

Funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDA24010401) to L.Q.Q., the Natural Science Foundation of China (No. 31771697, 31070226) to X.B.D., and National Program of Transgenic Variety Development of China (2016ZX08001-006) to L.Q.Q.

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Authors and Affiliations

  1. Key Laboratory of Plant Molecular Physiology, Institute of Botany, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing, 100093, China

    Xiangbai Dong, Liangke Chen, Huifang Yang, Lihong Tian, Fengqin Dong, Yaru Chai & Le Qing Qu

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Liangke Chen, Huifang Yang, Yaru Chai & Le Qing Qu

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  1. Xiangbai Dong
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Contributions

X.D. and L.Q.Q. designed the research and wrote the article. X.D. performed most of the experiments. L.C. performed some experiments. X.D. analyzed the data. H.Y., L.T., F.D. and Y.C. provided technical assistance to X.D. All authors reviewed the results and approved to submit the manuscript to your journal.

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Correspondence to Le Qing Qu.

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Communicated by Ian D. Godwin.

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Dong, X., Chen, L., Yang, H. et al. Pho1 cooperates with DPE1 to control short maltooligosaccharide mobilization during starch synthesis initiation in rice endosperm. Theor Appl Genet 136, 47 (2023). https://doi.org/10.1007/s00122-023-04250-z

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