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Suppression of ROS generation mediated by higher InsP3 level is critical for the delay of seed germination in lpa rice

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Abstract

The breeding of low phytic acid (lpa) crop is considered as an effective strategy to improve crop nutrition, but these crops have an inferior performance in seed germination. In this paper, two rice genotypes, cv. 9311 and its lpa mutant (9311-lpa), were used to clarify the relationship of InsP3 and ROS concentration in sprouting seeds with the occurrence of retarded seed germination for lpa crop. Results showed that the inferior performance of seed germination for 9311-lpa was mostly characterized by the delay of seed germination progression, with insignificant difference in seed germination rate between the two genotypes after a longer imbibition duration. The retarded seed germination of 9311-lpa was closely associated with the genotypic difference in InsP3 and ROS concentrations in germinating seeds, with the considerably higher InsP3 level and lower ROS concentration for 9311-lpa relative to the wild type. Under an appropriate range of concentration, exogenous H2O2 treatment promoted seed germination, while the activator of InsP3 (m-3M3FBS) had an inhibitory effect on seed germination. The delay of seed germination occurred mainly as the results of the higher InsP3 level and the lower ROS concentration in the germinating seeds of 9311-lpa. Furthermore, the germinating seeds of 9311-lpa had relatively lower activities of ROS scavenging enzymes (SOD, CAT, POD, and APX) and ROS generating enzyme (NOX) than those of the wild type. m-3M3FBS significantly suppressed NOX activity and NOX transcripts in sprouting seeds, which then resulted in the lowered ROS generation in sprouting seeds and the decreased seed germination rate. Thus, the retarded seed germination of 9311-lpa, with lower ROS level in germinating seeds, was mostly caused by the weaker ability of ROS generation in the presence of higher InsP3 level, rather than the effective detoxification of ROS burst during seed germination.

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Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

DAB:

3,3-diaminobenzidine

DPI:

Diphenyliodonium

EMS:

Ethylmethylsulfonate

H2O2 :

Hydrogen peroxide

InsP3 :

Inositol-1,4,5-trisphosphate

lpa :

Low phytic acid mutant

m-3M3FBS:

2,4,6-trimethyl-N-[3-(trifluoromethyl)phenyl]benzenesulfonamide

MDA:

Malondialdehyde

NBT:

Nitrobluetetrazolium

NOX:

Nicotinamide adenine dinucleotide phosphate oxidase

O2 ·− :

Superoxide radical

OsNOX :

NOX gene

PA:

Phytic acid

Pi:

Inorganic phosphorus

PLC:

Phospholipid-specific phospholipase C

POD:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

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Acknowledgements

The authors are indebted to National Natural Science Foundation of China (Nos. 31571602 and 31771688) and National Key Research and Development Plan of China (No. 2016YFD0300502) for its financial support to this research project.

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Authors and Affiliations

  1. Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

    Lujian Zhou, Yu Ye, Qian Zhao, Xiaoxia Du, Shamsu Ado Zakari, Da Su, Gang Pan & Fangmin Cheng

  2. Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing, China

    Qian Zhao & Fangmin Cheng

Authors
  1. Lujian Zhou
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  2. Yu Ye
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  3. Qian Zhao
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  4. Xiaoxia Du
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  5. Shamsu Ado Zakari
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  6. Da Su
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  7. Gang Pan
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  8. Fangmin Cheng
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Contributions

FC and LZ designed the research; LZ, YY, and QZ performed research; and LZ, XD, SZ, DS and GP analyzed data, LZ and FC wrote the paper. All authors read and approved the manuscript.

Corresponding author

Correspondence to Fangmin Cheng.

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The authors declare that they have no conflict of interest.

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Zhou, L., Ye, Y., Zhao, Q. et al. Suppression of ROS generation mediated by higher InsP3 level is critical for the delay of seed germination in lpa rice. Plant Growth Regul 85, 411–424 (2018). https://doi.org/10.1007/s10725-018-0402-8

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  • DOI: https://doi.org/10.1007/s10725-018-0402-8

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