Advertisement

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
  • 65 Downloads

Abstract

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.

Keywords

Soybean SUMOylation Phytophthora sojae Heat shock 

Abbreviations

SUMO

Small ubiquitin-like modifier

SAE SUMO

Activating enzyme

SCE SUMO

Conjugating enzyme

qRT-PCR

Quantitative real time PCR

RWC

Relative water content

SOD

Superoxide dismutase

POD

Peroxidase

CHL

Chlorophyll content

SP

Soluble protein

Notes

Acknowledgements

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 (http://www.liwenbianji.cn/ac), 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.
10725_2018_452_MOESM2_ESM.tif (179 mb)
Supplementary material 2 (TIF 183285 KB)
10725_2018_452_MOESM3_ESM.tif (102.5 mb)
Supplementary material 3 (TIF 104927 KB)
10725_2018_452_MOESM4_ESM.tif (234.1 mb)
Supplementary material 4 (TIF 239721 KB)
10725_2018_452_MOESM5_ESM.tif (100.7 mb)
Supplementary material 5 (TIF 103082 KB)
10725_2018_452_MOESM6_ESM.tif (6.4 mb)
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.
10725_2018_452_MOESM7_ESM.docx (17 kb)
Supplementary material 7 (DOCX 20 KB)
10725_2018_452_MOESM8_ESM.docx (22 kb)
Supplementary material 8 (DOCX 22 KB)
10725_2018_452_MOESM9_ESM.docx (17 kb)
Supplementary material 9 (DOCX 17 KB)

References

  1. André DDAN, José TP, Joaquim EF (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94CrossRefGoogle Scholar
  2. Augustine RC, York SL, Rytz TC, Vierstra RD (2016) Defining the SUMO system in maize: SUMOylation is up-regulated during endosperm development and rapidly induced by stress. Plant Physiol 171:2191CrossRefGoogle Scholar
  3. Bohren KM, Nadkarni V, Song JH et al (2004) A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 279:27233–27238CrossRefGoogle Scholar
  4. Cai B, Kong X, Zhong C, Sun S, Zhou XF, Jin YH, Wang Y, Li X, Zhu Z, Jin JB (2017) SUMO E3 Ligases GmSIZ1a and GmSIZ1b regulate vegetative growth in soybean. J Integr Plant Biol 59:2–14CrossRefGoogle Scholar
  5. Campanaro A, Battaglia R, Galbiati M, Sadanandom A, Tonelli C, Conti L (2016) SUMO proteases OTS1 and 2 control filament elongation through a DELLA-dependent mechanism. Plant Reprod 29:1–4CrossRefGoogle Scholar
  6. Carranco R, Prietodapena P, Almoguera C et al (2017) SUMO-dependent synergism involving heat shock transcription factors with functions linked to seed longevity and desiccation tolerance. Front Plant Sci 8:974CrossRefGoogle Scholar
  7. Castaño-Miquel L, Mas A, Teixeira I, Seguí J, Perearnau A et al (2017) SUMOylation inhibition mediated by disruption of SUMO E1-E2 interactions confers plant susceptibility to necrotrophic fungal pathogens. Mol Plant 10:709–720CrossRefGoogle Scholar
  8. Castro PH, Tavares RM, Bejarano ER, Azevedo H (2012) SUMO, a heavyweight player in plant abiotic stress responses. Cell Mol Life Scie 69:3269–3283CrossRefGoogle Scholar
  9. Castro PH, Couto D, Freitas S et al (2016) SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana. Plant Mol Biol 92:143–159CrossRefGoogle Scholar
  10. Castro PH, Verde N, Tavares RM, Bejarano ER, Azevedo H (2018a) Sugar signaling regulation by arabidopsis SIZ1-driven sumoylation is independent of salicylic acid. Plant Signal Behav 13:e1179417CrossRefGoogle Scholar
  11. Castro PH, Santos M, Freitas S et al (2018b) Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development. J Exp Bot 69:4633–4649CrossRefGoogle Scholar
  12. Catala R, Ouyang J, Abreu IA, Hu Y, Seo H, Zhang X, Chua NH (2007) The Arabidopsis E3 SUMO Ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19:2952CrossRefGoogle Scholar
  13. Chaikam V, Karlson DT (2010) Response and transcriptional regulation of rice SUMOylation system during development and stress conditions. BMB Rep 43:103CrossRefGoogle Scholar
  14. Chen CC, Chen YY, Tang IC, Liang HM, Lai CC, Chiou JM, Yeh KC (2011) Arabidopsis SUMO E3 Ligase SIZ1 is involved in excess copper tolerance. Plant Physiol 156:2225–2234CrossRefGoogle Scholar
  15. Cheng X, Xiong R, Li Y, Li F, Zhou X, Wang A (2017) SUMOylation of Turnip mosaic virus RNA polymerase promotes viral infection by counteracting the host NPR1-mediated immune response. Plant Cell 29:508–525CrossRefGoogle Scholar
  16. Chung E, Kim KM, Lee JH (2013) Genome-wide analysis and molecular characterization of heat shock transcription factor family in Glycine max. J Genet Genomics 40:127–135CrossRefGoogle Scholar
  17. Colby T, Matthäi A, Boeckelmann A, Stuible HP (2006) SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol 142:318–332CrossRefGoogle Scholar
  18. Conti L, Price G, O’Donnell E et al (2009) Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and—2 regulate salt stress responses in Arabidopsis. Plant Cell 20:2894–2908CrossRefGoogle Scholar
  19. Cubeñaspotts C, Matunis MJ (2013) SUMO: a multifaceted modifier of chromatin structure and function. Dev Cell 24:1–12CrossRefGoogle Scholar
  20. Datta M, Kaushik S, Jyoti A et al (2017) SIZ1-mediated SUMOylation during phosphate homeostasis in plants: looking beyond the tip of the iceberg. Semin Cell Dev Biol 74:123–132CrossRefGoogle Scholar
  21. Deans CA, Sword GA, Lenhart PA (2018) Quantifying plant soluble protein and digestible carbohydrate content, using corn (Zea mays) as an exemplar. J Vis Exp Jove 6:138Google Scholar
  22. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine Max (L.) Merrill. Crop Sci 11:929–931CrossRefGoogle Scholar
  23. Golebiowski F, Matic I, Tatham MH et al (2009) System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2:ra24CrossRefGoogle Scholar
  24. Guerra D, Crosatti C, Khoshro HH et al (2015) Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms. Front Plant Sci 6:57CrossRefGoogle Scholar
  25. Hammoudi V, Fokkens L, Beerens B et al (2018) The Arabidopsis SUMO E3 ligase SIZ1 mediates the temperature dependent trade-off between plant immunity and growth. PLoS Genet 14:e1007157CrossRefGoogle Scholar
  26. Jin BJ, Jin YL, Lee J et al (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J Cell Mol Biol 53:530–540CrossRefGoogle Scholar
  27. Karan R, Subudhi PK (2012) A stress inducible SUMO conjugating enzyme gene (SaSce9) from a grass halophyte Spartina alterniflora enhances salinity and drought stress tolerance in Arabidopsis. BMC Plant Biol 12:187CrossRefGoogle Scholar
  28. Kerscher ORF et al (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159CrossRefGoogle Scholar
  29. Kim SI, Park BS, Kim DY, Yeu SY, Song SI, Song JT, Seo HS (2015) E3 SUMO ligase AtSIZ1 positively regulates SLY1-mediated GA signaling and plant development. Biochem J 469:299CrossRefGoogle Scholar
  30. Kim JY, Jang IC, Seo HS (2016) COP1 controls abiotic stress responses by modulating AtSIZ1 function through its E3 ubiquitin ligase activity. Front Plant Sci 7:1182Google Scholar
  31. Kim JY, Song JT, Seo HS (2017) Post-translational modifications of Arabidopsis E3 SUMO ligase AtSIZ1 are controlled by environmental conditions. FEBS Open Bio 7:1622–1634CrossRefGoogle Scholar
  32. Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and—2 conjugates is increased by stress. J Biol Chem 278:6862–6872CrossRefGoogle Scholar
  33. Lagrimini LM (1991) Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577CrossRefGoogle Scholar
  34. Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161:405–413CrossRefGoogle Scholar
  35. Lee J, Nam J, Park HC et al (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79CrossRefGoogle Scholar
  36. Li Z, Hu Q, Zhou M, Vandenbrink J, Li D, Menchyk N, Reighard S, Norris A, Liu H, Sun D, Luo H (2013) Heterologous expression of OsSIZ1, a rice SUMO E3 ligase, enhances broad abiotic stress tolerance in transgenic creeping bentgrass. Plant Biotechnol J 11:432–445CrossRefGoogle Scholar
  37. Li Y, Wang G, Xu Z, Li J, Sun M, Guo J, Ji W (2017) Organization and regulation of soybean SUMOylation system under abiotic stress conditions. Front Plant Sci 8:1458CrossRefGoogle Scholar
  38. Lim YJ, Kim KT, Lee YH (2018) SUMOylation is required for fungal development and pathogenicity in the rice blast fungus Magnaporthe oryzae. Mol Plant Pathol 19:9CrossRefGoogle Scholar
  39. Lin XL, Niu D, Hu ZL et al (2016) An Arabidopsis SUMO E3 ligase, SIZ1, negatively regulates photomorphogenesis by promoting COP1 activity. PLoS Genet 12:e1006016CrossRefGoogle Scholar
  40. Liu L, Jiang Y, Zhang X, Wang X, Wang Y, Han Y, Coupland G, Jin JB, Searle I, Fu YF, Chen F (2017) Two SUMO proteases SUMO PROTEASE RELATED TO FERTILITY 1 and—2 are required for fertility. Plant Physiol 175:1703–1719CrossRefGoogle Scholar
  41. Matuszak-Slamani R, Bejger R, Cieśla J (2017) Influence of humic acid molecular fractions on growth and development of soybean seedlings under salt stress. Plant Growth Regul 83:465Google Scholar
  42. Mishra N, Sun L, Zhu XL et al (2017) Overexpression of the rice SUMO E3 ligase gene OsSIZ1 in cotton enhances drought and heat tolerance, and substantially improves fiber yields in the field under reduced irrigation and rainfed conditions. Plant Cell Physiol 58:735–746CrossRefGoogle Scholar
  43. Mishra N, Srivastava AP, Esmaeili N, Hu W, Shen G (2018) Overexpression of the rice gene OsSIZ1in Arabidopsis improves drought-, heat-, and salt-tolerance simultaneously. PLoS ONE 13:1122Google Scholar
  44. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated SUMOylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414CrossRefGoogle Scholar
  45. Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) SUMOylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. PNAS 106:5418–5423CrossRefGoogle Scholar
  46. Miura K, Sato A, Ohta M, Furukawa J (2011a) Increased tolerance to salt stress in the phosphate-accumulating Arabidopsis mutants siz. and pho2 Planta 234:1191–1199CrossRefGoogle Scholar
  47. Miura K, Lee J, Gong Q et al (2011b) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000CrossRefGoogle Scholar
  48. Morgan JA (1984) Interaction of water supply and N in wheat. Plant Physiol 76:112–117CrossRefGoogle Scholar
  49. Mukhopadhyay D, Dasso M (2007) Modification in reverse: the SUMO proteases. Trends Biochem Sci 32:286–295CrossRefGoogle Scholar
  50. Nigam N, Singh A, Sahi C, Chandramouli A, Grover A (2008) SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response. Mol Genet Genomics 279:371–383CrossRefGoogle Scholar
  51. Park HJ, Kim WY, Park HC et al (2011) SUMO and SUMOylation in plants. Mol Cells 32:305–316CrossRefGoogle Scholar
  52. Pei W, Jain A, Sun Y, Zhang Z, Ai H, Liu X, Wang H, Feng B, Sun R, Zhou H, Xu G, Sun S (2017) OsSIZ2 exerts regulatory influences on the developmental responses and phosphate homeostasis in rice. Sci Rep 7:12280CrossRefGoogle Scholar
  53. Reed JM, Dervinis C, Morse AM, Davis JM (2010) The SUMO conjugation pathway in Populus: genomic analysis, tissue-specific and inducible SUMOylation and in vitro de-SUMOylation. Planta 232:51–59CrossRefGoogle Scholar
  54. Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol Plant Microbe Interact 17:633–643CrossRefGoogle Scholar
  55. Rytz TC, Miller MJ, Mcloughlin F et al (2018) SUMOylome profiling reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress. Plant Cell 30:1077–1099CrossRefGoogle Scholar
  56. Saleh A, Withers J, Mohan R, Marqués J, Gu Y, Yan S, Zavaliev R, Nomoto M, Tada Y, Dong X (2015) Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe 18:169–182CrossRefGoogle Scholar
  57. Sandhu D, Tasma IM, Frasch R, Bhattacharyya MK (2009) Systemic acquired resistance in soybean is regulated by two proteins, orthologous to Arabidopsis NPR1. BMC Plant Biol 9:105CrossRefGoogle Scholar
  58. Saracco SA, Miller MJ, Kurepa J, Vierstra RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145:119–134CrossRefGoogle Scholar
  59. Shameer S, Prasad TNVKV (2018) Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul 84:1–13CrossRefGoogle Scholar
  60. Srivastava AK, Zhang C, Yates G, Bailey M, Brown A, Sadanandom A (2016) SUMO is a critical regulator of salt stress responses in rice. Plant Physiol 170:2378–2391CrossRefGoogle Scholar
  61. Srivastava AK, Zhang C, Caine RS, Gray J, Sadanandom A (2017) Rice SUMO protease overly tolerant to Salt 1 targets the transcription factor, OsbZIP23 to promote drought tolerance in rice. Plant J 92:1031–1043CrossRefGoogle Scholar
  62. Srivastava AK, Orosa B, Singh P, Cummins I, Walsh C, Zhang C, Grant M, Roberts MR, Anand GS, Fitches E (2018) SUMO suppresses the activity of the jasmonic acid receptor coronatine insensitive 1. Plant Cell 30:2099–2115CrossRefGoogle Scholar
  63. van den Burg HA, Kini RK, Schuurink RC, Takken FL (2010) Arabidopsis small ubiquitin-like modifier paralogs have distinct functions in development and defense. Plant Cell 22:1998–2016CrossRefGoogle Scholar
  64. Wang X, Du G, Wang X et al (2010) The function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana. Plant Cell Physiol 51:380–394CrossRefGoogle Scholar
  65. Wang HD, Sun R, Cao Y, Pei WX, Sun YF, Zhou HM, Wu XN, Zhang F, Luo L, Shen Q, Xu G, Sun SB (2015) OsSIZ1, a SUMO E3 ligase gene, is involved in the regulation of the responses to phosphate and nitrogen in rice. Plant Cell Physiol 56:2381–2395CrossRefGoogle Scholar
  66. Xin DW, Liao S, Xie ZP, Hann DR, Steinle L, Boller T, Staehelin C (2012) Functional analysis of NopM, a novel E3 ubiquitin ligase (NEL) domain effector of Rhizobium sp. strain NGR234. PLoS Pathogens 8:e1002707CrossRefGoogle Scholar
  67. Yan Q, Cui X, Su L, Xu N, Guo N, Xing H, Dou DL (2014) GmSGT1 is differently required for soybean Rps genes-mediated and basal resistance to Phytophthora sojae. Plant Cell Rep 33:1275–1288CrossRefGoogle Scholar
  68. Yoo CY, Miura K, Jin JB et al (2006) SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in arabidopsis independent of salicylic acid. Plant Physiol 142:1548–1558CrossRefGoogle Scholar
  69. Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A (2017) Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in citrus. Front Plant Sci 8:953CrossRefGoogle Scholar
  70. Zhang SZ, Xu PF, Wu JJ, Xue AG, Zhang JX, Li WB, Chen C, Chen WY, Lv HY (2010) Races of Phytophthora sojae and their virulences on soybean cultivars in Heilongjiang, China. Plant Dis 94:87–91CrossRefGoogle Scholar
  71. Zhang S, Qi Y, Liu M et al (2013a) SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana(F). J Integr Plant Biol 55:83–95CrossRefGoogle Scholar
  72. Zhang S, Qi Y, Liu M, Yang C (2013b) SUMO E3 Ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana. J Integr Plant Biol 55:83–95CrossRefGoogle Scholar
  73. Zhang RF, Guo Y, Li YY, Zhou LJ, Hao YJ, You CX (2016) Functional identification of MdSIZ1 as a SUMO E3 ligase in apple. J Plant Physiol 198:69–80CrossRefGoogle Scholar
  74. Zhang S, Wang S, Lv J, Liu Z, Wang Y, Ma N, Meng Q (2017a) SUMO E3 ligase SlSIZ1 facilitates heat tolerance in tomato. Plant Cell Physiol 59:58–71CrossRefGoogle Scholar
  75. Zhang S, Zhuang K, Wang S, Lv J, Ma N, Meng Q (2017b) A novel tomato SUMO E3 ligase, SISIZ1, confers drought tolerance in transgenic tobacco. J Integr Plant Biol 2:102–117CrossRefGoogle Scholar
  76. Zheng Y, Schumaker KS, Guo Y (2012) SUMOylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. PNAS 109:12822CrossRefGoogle Scholar

Copyright information

© 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

Personalised recommendations