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Differences in specificity and compensatory functions among three major starch synthases determine the structure of amylopectin in rice endosperm

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Abstract

The lengths of amylopectin-branched chains are precise and influence the physicochemical properties of starch, which determine starch functionality. Three major isozymes of starch synthases (SSs), SSI, SSII(a), and SSIII(a), are primarily responsible for amylopectin chain elongation in the storage tissues of plants. To date, the majority of reported rice mutants were generated using japonica cultivars, which have almost inactive SSIIa. Although three SSs share some overlapping chain length preferences, whether they complement each other remains unknown due to the absence of suitable genetic combinations of materials. In this study, rice ss1/SS2a/SS3a and SS1/SS2a/ss3a were newly generated, and the chain length distribution patterns of all the possible combinations of presence and absence of SSI, SSIIa, and SSIIIa activities were compared. This study demonstrated that SSIIa can complement most SSI functions that use glucan chains with DP 6–7 to generate DP 8–12 chains but cannot fully compensate for the elongation of DP 16–19 chains. This suggests that SSIIa preferentially elongates outer but not inner chains of amylopectin. In addition, the results revealed that neither SSI nor SSIIIa compensate for SSIIa. Neither SSI nor SSIIa compensate for elongation of DP >30 by SSIIIa. SSIIa could not resolve the pleiotropic increase of SSI caused by the absence of SSIIIa; instead, SSIIa further elongated those branches elongated by SSI. These results revealed compensatory differences among three major SS isozymes responsible for lengths of amylopectin branches.

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Acknowledgements

The authors would like to thank Ms. Yuko Nakaizumi, Ms. Satoko Miura, and Ms. Misato Abe for taking care of the rice plants. The authors also would like to thank Enago for the English language review. This research project was partially supported by (1) The Science and Technology Research Promotion Program for Agriculture, Forestry and Fisheries and Food Industry (25033AB and 28029C; Naoko Fujita); (2) President’s Funds of Akita Prefectural University (Naoko Crofts and Dr. Naoko Fujita); (3) the Grant-in-Aid for JSPS fellows from Japan Society for the Promotion of Science (#15J40176; Naoko Crofts); and (4) The Japan Society for the Promotion of Science (#16K18571; Naoko Crofts).

Author contributions

NC designed, and both NC and KS performed the experiments. NFO provided technical assistance to KS. NC, YN and NF wrote the manuscript. The original research plan was conceived and supervised by NF.  

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Authors and Affiliations

  1. Department of Biological Production, Akita Prefectural University, 241-438 Shimoshinjo Nakano Kaidobata-Nishi, Akita City, Akita, 010-0195, Japan

    Naoko Crofts, Kyohei Sugimoto, Naoko F. Oitome, Yasunori Nakamura & Naoko Fujita

  2. Japan Society for the Promotion of Science (N.C.), Tokyo, Japan

    Naoko Crofts

  3. Akita Natural Science Laboratory, 25-44 Oiwake-Nishi, Tenno, Katagami City, Akita, 010-0101, Japan

    Yasunori Nakamura

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  1. Naoko Crofts
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  2. Kyohei Sugimoto
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Correspondence to Naoko Fujita.

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11103_2017_614_MOESM1_ESM.pdf

Supplemental Fig. 1 Replicative experiments for western blotting of the total and the starch granule-bound proteins demonstrating that the protein expression patterns agree with their genotypes (Fig. 3). (a) Western blotting of the total protein using the indicated antibodies. (b) Western blotting of the starch granule-bound proteins using the indicated antibodies, demonstrating that the active starch synthase (SS) IIa binds to the starch granules. Supplemental Fig. 2 Starch synthase (SS) activity staining without substrate adenosine diphosphate (ADP)-glucose. Gray arrowheads indicate outcomes of non-specific glucan hydrolysis activities. Supplemental Fig. 3 Chain length distribution analyses of ss1/SS2a/SS3a/Wx b-2 and average of segregates. (a) Chain length distribution patterns of starch synthases (SS)1/SS2a/SS3a (solid black), ss1/SS2a/SS3a-2 (green), SS1/ss2a/SS3a (pink), and ss1/ss2a/SS3a (dotted black) are compared to show the effect of with or without SSI and/or active SSIIa. (b) The differences in fine structure of amylopectin are shown as ΔMolar %. (ss1/SS2a/SS3a-1) – (SS1/SS2a/SS3a) is in green and (ss1/ss2a/SS3a) – (SS1/ss2a/SS3a) is dotted line. Statistical analyses were performed by averaging the values from four seeds of (data from individual ss1/SS2a/SS3a-1 seed) – (data from average of three SS1/SS2a/SS3a seeds). The bars represent standard error. (c) (ss1/SS2a/SS3a-2) – (SS1/SS2a/SS3a) is in light green. Statistical analyses were performed by averaging the values from four seeds of (data from individual ss1/SS2a/SS3a-2 seed) – (data from average of three SS1/SS2a/SS3a seeds). The bars represent standard error. (d) (SS1/SS2a/ss3a) – (SS1/SS2a/SS3a) is in blue and (SS1/ss2a/ss3a) – (SS1/ss2a/SS3a) is in gray. Statistical analyses were performed by averaging the values from four seeds of (data from individual SS1/SS2a/ss3a seed) – (data from average of three SS1/SS2a/SS3a seeds). The bars represent standard error. (PDF 428 KB)

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Crofts, N., Sugimoto, K., Oitome, N.F. et al. Differences in specificity and compensatory functions among three major starch synthases determine the structure of amylopectin in rice endosperm. Plant Mol Biol 94, 399–417 (2017). https://doi.org/10.1007/s11103-017-0614-8

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