Plant Growth Regulation

, Volume 87, Issue 1, pp 69–82 | Cite as

Regulation of soybean SUMOylation system in response to Phytophthora sojae infection and heat shock

  • Shuping Li
  • Mengmeng Lin
  • Jinhui Wang
  • Liwei Zhang
  • Meijing Lin
  • Zhenbang Hu
  • Zhaoming Qi
  • Hongwei Jiang
  • Yongfu Fu
  • Dawei XinEmail author
  • Chunyan LiuEmail author
  • Qingshan ChenEmail author
Original paper


Modification of protein substrates by small ubiquitin-related modifier (SUMO) plays a vital role in plants under biotic and abiotic stresses. However, its role in the stress responses of soybean (Glycine max (L.) Merrill) is poorly understood. In this study, we explored SUMOylation in soybean in response to Phytophthora sojae race 1 infection and heat shock. We selected two soybean cultivars for these analyses; one resistant to P. sojae race 1 (SN10), and one susceptible (HF25). The transcription and expression levels of SUMOylation-related genes were detected in SN10 and HF25 after inoculation with P. sojae race 1 and after exposure to heat shock (42 °C). After inoculation with P. sojae race 1, GmSUMO2/3 and GmSAE1b accumulated in the roots. After the heat shock treatment, GmSCEd and GmE3f accumulated in the leaves. The transcript levels of GmESD4d increased in response to both P. sojae infection and heat shock. We monitored SUMOylation in the root, stem, and leaves after the stress treatments. We detected SUMO conjugates in the unifoliolate leaf, trifoliolate leaf, root, and stem after the heat shock treatment. SUMO conjugates accumulated mainly in the root and stem in response to heat shock, but mainly in the root in response to P. sojae race 1 infection. The accumulation of SUMO conjugates in response to stress indicated that SUMOylation enhanced the resistance of soybean to P. sojae and heat shock. These results provide a foundation for further research on the role of SUMOylation in resistance to P. sojae and heat shock.


Soybean SUMOylation Phytophthora sojae Heat shock 



Small ubiquitin-like modifier


Activating enzyme


Conjugating enzyme


Quantitative real time PCR


Relative water content


Superoxide dismutase




Chlorophyll content


Soluble protein



This study was financially supported by the National Natural Science Foundation of China (Grant No. 31501332), and the National Key Research & Development Program of China (Grant No. 2016YFD0100500, 2016YFD0100300 and 2016YFD0100201-21). We thank Jennifer Smith, PhD, from Liwen Bianji, Edanz Group China (, for editing the English text of a draft of this manuscript.

Author contributions

QC, CL, and DX designed the study. SL analyzed the data and wrote the paper. ML, JW, LZ, ML, ZH, ZQ, HJ, and YF participated in correcting the manuscript. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10725_2018_452_MOESM1_ESM.tif (238.8 mb)
Supplementary material 1 (TIF 244566 KB). Fig. S1 Structures of soybean and Arabidopsis SUMO families. (A) Domain structures of SUMO families in soybean (GmSUMO-1, -2, -3, -4, -5, -6) and Arabidopsis (AtSUMO-1, -2, -3, -4, -5, -6). (B) Domain structures of soybean and Arabidopsis SUMO E1 family (GmSAE-1a, -1b, GmSAE-2a, -2b, AtSAE-1a, -1b, and AtSAE2). (C) Domain structures of soybean and Arabidopsis SUMO E2 family (GmSCE-a, -b, -c, -d, and AtSCE1). (D) Domain structures of soybean and Arabidopsis SUMO E3 family (GmE3-a, -b, -c, -d, -e, -f, and AtSIZ1, AtMMS21, and PIAS-like). (E) Domain structures of soybean and Arabidopsis SUMO protease family (GmESD4-a, -b, -c, -d, and AtESD4). Blue rectangles represent exons; blue straight lines represent upstream or downstream; black straight lines represent introns.
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Supplementary material 2 (TIF 183285 KB)
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Supplementary material 3 (TIF 104927 KB)
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Supplementary material 4 (TIF 239721 KB)
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Supplementary material 5 (TIF 103082 KB)
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Supplementary material 6 (TIF 6534 KB). Fig. S2 Soybean seedlings treated with P. sojae race 1 and heat stress (42°C). GmPR1, GmPR5, and GmHSF12 were used as stress-positive controls.
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Supplementary material 7 (DOCX 20 KB)
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Supplementary material 8 (DOCX 22 KB)
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Supplementary material 9 (DOCX 17 KB)


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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Key Laboratory of Soybean Biology of Chinese Ministry of Education, Key Laboratory of Soybean Biology and Breeding/Genetics of Chinese Agriculture Ministry, College of ScienceNortheast Agricultural UniversityHarbinPeople’s Republic of China
  2. 2.MOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop SciencesChinese Academy of Agricultural SciencesBeijingPeople’s Republic of China

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