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Expression of a novel PSK-encoding gene from soybean improves seed growth and yield in transgenic plants

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Abstract

Main conclusion

Expression of GmPSKγ1 , a novel PSK-encoding gene from soybean, increases seed size and yield in transgenic plants by promoting cell expansion.

Phytosulfokine-α (PSK-α), a sulfated pentapeptide hormone with the sequence YIYTQ, plays important roles in many aspects of plant growth and development. In this study, we identified a pair of putative precursor genes in soybean, GmPSKγ1 and -2, encoding a PSK-like peptide: PSK-γ. Similar to PSK-α in amino acid composition, the sequence of PSK-γ is YVYTQ, and the tyrosines undergo sulfonylation. Treatment of Arabidopsis seedlings with synthetic sulfated PSK-γ significantly enhanced root elongation, indicating that PSK-γ might be a functional analog of PSK-α. Expression pattern analysis revealed that the two GmPSKγ genes, especially GmPSKγ1, are primarily expressed in developing soybean seeds. Heterologous expression of GmPSKγ1 under the control of a seed-specific promoter markedly increased seed size and weight in Arabidopsis, and this promoting effect of PSK-γ on seed growth was further confirmed in transgenic tobacco constitutively expressing GmPSKγ1. Cytological analysis of transgenic Arabidopsis seeds revealed that PSK-γ promotes seed growth by inducing embryo cell expansion. In addition, expression analysis of downstream candidate genes suggested that PSK-γ signaling might regulate cell wall loosening to promote cell expansion in Arabidopsis seeds. Overall, our results shed light on the mechanism by which PSK-γ promotes seed growth, paving the way for the use of this new peptide for biotechnological improvement of crop seed/grain size and yield.

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Abbreviations

DAP:

Days after pollination

PSK:

Phytosulfokine

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31500197 and 31570241), the 973 National Key Basic Research Program in China (2015CB158300), and the Shanghai Key Program of Supporting Program (15230500100).

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Author notes

  1. Liangliang Yu and Yumin Liu contributed equally to this work.

Authors and Affiliations

  1. Shanghai Key Lab of Bio-energy Crops, Plant Science Center, School of Life Sciences, Shanghai University, Shanghai, 200444, China

    Liangliang Yu, Yumin Liu, Shuang Zeng, Junhui Yan & Li Luo

  2. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, 200032, China

    Ertao Wang

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  1. Liangliang Yu
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425_2019_3101_MOESM1_ESM.jpg

Fig. S1 Expression patterns of GmPSKα genes. Quantitative RT-PCR analyses of the expression patterns of GmPSKα genes in various soybean tissues. Values are the mean ± SD of three independent biological replicates normalized against the reference gene GmEF1β

425_2019_3101_MOESM2_ESM.jpg

Fig. S2 AtOLEO4 is specifically expressed in Arabidopsis seeds. a Quantitative RT-PCR analysis of the AtOLEO4 expression profile. AtOLEO4 is specifically and highly expressed in developing seeds. Values are the mean ± SD of three independent biological replicates normalized against the reference gene AtActin2. b Microarray data from PlaNet (http://aranet.mpimp-golm.mpg.de/, probeset ID: 258240_at) show that AtOLEO4 is primarily expressed in seed embryos at various stages, including triangle, heart, torpedo, and mature stages

425_2019_3101_MOESM3_ESM.jpg

Fig. S3 Seed-specific expression of GmPSKγ1 does not influence Arabidopsis vegetative growth. a Four-week-old wild-type and OLEOp:GmPSKγ1 transgenic Arabidopsis plants. Bar = 2 cm. b, c Measurement of the leaf length (the 7th and 8th leaves, b) and fresh weight (c) of the 4-week-old Arabidopsis plants shown in a. n =34–44. d Ten-day-old seedlings of the indicated genotypes grown on vertical MS-agar plates. Bars = 2 cm. e Primary root length of the Arabidopsis seedlings shown in d. n =26–34

425_2019_3101_MOESM4_ESM.jpg

Fig. S4 Quantitative RT-PCR analysis of GmPSKγ1 transcript levels in leaves of 35S:GmPSKγ1 transgenic tobacco lines. Values are the mean ± SD of three independent biological replicates normalized against the reference gene NtUBC2

Table S1 List of primers used in this study. Restriction sites in the primers for cloning are underlined

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Yu, L., Liu, Y., Zeng, S. et al. Expression of a novel PSK-encoding gene from soybean improves seed growth and yield in transgenic plants. Planta 249, 1239–1250 (2019). https://doi.org/10.1007/s00425-019-03101-w

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