Precise control of ABA signaling through post-translational protein modification

  • Jing Zhang
  • Muhammad Tariq Hafeez
  • Dongwei Di
  • Lei Wu
  • Li ZhangEmail author
Review paper


Abscisic acid (ABA) plays a key role in plant growth and development and during stress responses. Plants respond to ABA through recognition, signal transduction, and response cascades. The core ABA signaling pathway consists of ABA receptors (RCAR/PYL/PYRs), protein phosphatases (PP2Cs), kinases (SnRK2s), transcription factors and ion channel proteins. Protein phosphorylation plays a key role in this pathway. In the absence of ABA, PP2Cs inhibit SnRK2s activities by dephosphorylating SnRK2s. When ABA binds to RCAR/PYL/PYRs, the complex then binds to PP2Cs, resulting in inactivation of the PP2Cs and release of the SnRK2s, which then phosphorylate a series of substrates to activate ABA responses. Selective protein degradation by the ubiquitin–proteasome system also contributes to regulation of ABA homeostasis, transport, signaling, and desensitization. The small ubiquitin-like modifier (SUMO) enhances the stability of ABI5 but also inhibits its transcription. ABA-induced reactive nitrogen and oxygen species regulate multiple key components of the ABA signaling pathways through redox-induced modifications (REDOX), such as oxidation, nitration, and nitrosylation, forming a feedback regulation mechanism that precisely regulates ABA signaling. This review will detail the role of these post-translational modifications in the core ABA signaling pathway.


Abscisic acid Post-translational modification Phosphorylation Ubiquitination SUMOylation REDOX 



This work was supported by grants from the Fundamental Research Funds for the Central Universities (Grant No. lzujbky-2018-kb05) and the National Natural Science Foundation of China-Youth Science Fund (Grant No. 31600218).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Albertos P, Romero-Puertas MC, Tatematsu K, Mateos I, Sanchez-Vicente I, Nambara E, Lorenzo O (2015) S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat Commun 6:8669CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amagai A, Honda Y, Ishikawa S, Hara Y, Kuwamura M, Shinozawa A, Sugiyama N, Ishihama Y, Takezawa D, Sakata Y, Shinozaki K, Umezawa T (2018) Phosphoproteomic profiling reveals ABA-responsive phosphosignaling pathways in Physcomitrella patens. Plant J 94(4):699–708CrossRefPubMedGoogle Scholar
  3. An JP, Yao JF, Xu RR, You CX, Wang XF, Hao YJ (2018) Apple bZIP transcription factor MdbZIP44 regulates abscisic acid-promoted anthocyanin accumulation. Plant Cell Environ 41(11):2678–2692CrossRefPubMedGoogle Scholar
  4. Antoni R, Gonzalez-Guzman M, Rodriguez L, Rodrigues A, Pizzio GA, Rodriguez PL (2012) Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiol 158(2):970–980CrossRefPubMedGoogle Scholar
  5. Augustine RC, Vierstra RD (2018) SUMOylation: re-wiring the plant nucleus during stress and development. Curr Opin Cell Biol 45(Pt A):143–154CrossRefGoogle Scholar
  6. Batistic O, Rehers M, Akerman A, Schlucking K, Steinhorst L, Yalovsky S, Kudla J (2012) S-acylation-dependent association of the calcium sensor CBL2 with the vacuolar membrane is essential for proper abscisic acid responses. Cell Res 22(7):1155–1168CrossRefPubMedPubMedCentralGoogle Scholar
  7. Begara-Morales JC, Chaki M, Valderrama R, Sanchez-Calvo B, Mata-Perez C, Padilla MN, Corpas FJ, Barroso JB (2018) Nitric oxide buffering and conditional nitric oxide release in stress response. J Exp Bot 69(14):3425–3438CrossRefPubMedGoogle Scholar
  8. Belda-Palazon B, Rodriguez L, Fernandez MA, Castillo MC, Anderson EM, Gao C, Gonzalez-Guzman M, Peirats-Llobet M, Zhao Q, De Winne N, Gevaert K, De Jaeger G, Jiang L, Leon J, Mullen RT, Rodriguez PL (2016) FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. Plant cell 28(9):2291–2311CrossRefPubMedPubMedCentralGoogle Scholar
  9. Belin C, de Franco PO, Bourbousse C, Chaignepain S, Schmitter JM, Vavasseur A, Giraudat J, Barbier-Brygoo H, Thomine S (2006) Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol 141(4):1316–1327CrossRefPubMedPubMedCentralGoogle Scholar
  10. Belkhadir Y, Jaillais Y (2015) The molecular circuitry of brassinosteroid signaling. New Phytol 206(2):522–540CrossRefPubMedGoogle Scholar
  11. Bhatnagar N, Min MK, Choi EH, Kim N, Moon SJ, Yoon I, Kwon T, Jung KH, Kim BG (2017) The protein phosphatase 2C clade A protein OsPP2C51 positively regulates seed germination by directly inactivating OsbZIP10. Plant Mol Biol 93(4–5):389–401CrossRefPubMedGoogle Scholar
  12. Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109(26):10593–10598CrossRefPubMedGoogle Scholar
  13. Brugiere N, Zhang W, Xu Q, Scolaro EJ, Lu C, Kahsay RY, Kise R, Trecker L, Williams RW, Hakimi S, Niu X, Lafitte R, Habben JE (2017) Overexpression of RING domain E3 ligase ZmXerico1 confers drought tolerance through regulation of ABA homeostasis. Plant Physiol 175(3):1350–1369CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bueso E, Rodriguez L, Lorenzo-Orts L, Gonzalez-Guzman M, Sayas E, Munoz-Bertomeu J, Ibanez C, Serrano R, Rodriguez PL (2014) The single-subunit RING-type E3 ubiquitin ligase RSL1 targets PYL4 and PYR1 ABA receptors in plasma membrane to modulate abscisic acid signaling. Plant J 80(6):1057–1071CrossRefPubMedGoogle Scholar
  15. Cai Z, Liu J, Wang H, Yang C, Chen Y, Li Y, Pan S, Dong R, Tang G, Barajas-Lopez Jde D, Fujii H, Wang X (2014) GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis. Proc Natl Acad Sci USA 111(26):9651–9656CrossRefPubMedGoogle Scholar
  16. 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(1):2–14CrossRefPubMedPubMedCentralGoogle Scholar
  17. Castillo MC, Lozano-Juste J, Gonzalez-Guzman M, Rodriguez L, Rodriguez PL, Leon J (2015) Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8(392):ra89CrossRefPubMedGoogle Scholar
  18. Castro PH, Tavares RM, Bejarano ER, Azevedo H (2012) SUMO, a heavyweight player in plant abiotic stress responses. Cell Mol Life Sci 69(19):3269–3283CrossRefPubMedGoogle Scholar
  19. Castro PH, Couto D, Freitas S, Verde N, Macho AP, Huguet S, Botella MA, Ruiz-Albert J, Tavares RM, Bejarano ER, Azevedo H (2016) SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana. Plant Mol Biol 92(1–2):143–159CrossRefPubMedGoogle Scholar
  20. 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(9):2952–2966CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chen L, Lee JH, Weber H, Tohge T, Witt S, Roje S, Fernie AR, Hellmann H (2013a) Arabidopsis BPM proteins function as substrate adaptors to a cullin3-based E3 ligase to affect fatty acid metabolism in plants. Plant cell 25(6):2253–2264CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chen YT, Liu H, Stone S, Callis J (2013b) ABA and the ubiquitin E3 ligase KEEP ON GOING affect proteolysis of the Arabidopsis thaliana transcription factors ABF1 and ABF3. Plant J 75(6):965–976CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chen HH, Qu L, Xu ZH, Zhu JK, Xue HW (2018) EL1-like casein kinases suppress ABA signaling and responses by phosphorylating and destabilizing the ABA receptors PYR/PYLs in Arabidopsis. Mol Plant 11(5):706–719CrossRefPubMedGoogle Scholar
  24. Cheng C, Wang Z, Ren Z, Zhi L, Yao B, Su C, Liu L, Li X (2017) SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet 13(8):e1006947CrossRefPubMedPubMedCentralGoogle Scholar
  25. Cohen P (2002) The origins of protein phosphorylation. Nat Cell Biol 4(5):E127–E130CrossRefPubMedGoogle Scholar
  26. Dai M, Xue Q, McCray T, Margavage K, Chen F, Lee JH, Nezames CD, Guo L, Terzaghi W, Wan J, Deng XW, Wang H (2013) The PP6 phosphatase regulates ABI5 phosphorylation and abscisic acid signaling in Arabidopsis. Plant cell 25(2):517–534CrossRefPubMedGoogle Scholar
  27. Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48CrossRefPubMedGoogle Scholar
  28. Feng CZ, Chen Y, Wang C, Kong YH, Wu WH, Chen YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80(4):654–668CrossRefPubMedGoogle Scholar
  29. Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106(20):8380–8385CrossRefPubMedGoogle Scholar
  31. Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant cell 19(2):485–494CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50(12):2123–2132CrossRefPubMedGoogle Scholar
  33. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124(4):509–525CrossRefPubMedGoogle Scholar
  34. Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147(1):15–27CrossRefPubMedGoogle Scholar
  35. Garcia ME, Lynch T, Peeters J, Snowden C, Finkelstein R (2008) A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Mol Biol 67(6):643–658CrossRefPubMedGoogle Scholar
  36. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106(50):21425–21430CrossRefPubMedGoogle Scholar
  37. Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KA, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107(17):8023–8028CrossRefPubMedGoogle Scholar
  38. Han SK, Sang Y, Rodrigues A, Biol F, Wu MF, Rodriguez PL, Wagner D (2012) The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24(12):4892–4906CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hauser F, Li Z, Waadt R, Schroeder JI (2017) SnapShot: abscisic acid signaling. Cell 171 (7):1708–1708 e1700Google Scholar
  40. Himmelbach A, Hoffmann T, Leube M, Hohener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21(12):3029–3038CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hou YJ, Zhu Y, Wang P, Zhao Y, Xie S, Batelli G, Wang B, Duan CG, Wang X, Xing L, Lei M, Yan J, Zhu X, Zhu JK (2016) Type one protein phosphatase 1 and its regulatory protein inhibitor 2 negatively regulate ABA signaling. PLoS Genet 12(3):e1005835CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hu Y, Yu D (2014) BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant cell 26(11):4394–4408CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hu R, Zhu Y, Shen G, Zhang H (2014) TAP46 plays a positive role in the ABSCISIC ACID INSENSITIVE5-regulated gene expression in Arabidopsis. Plant Physiol 164(2):721–734CrossRefPubMedGoogle Scholar
  44. Hua Z, Vierstra RD (2011) The cullin-RING ubiquitin-protein ligases. Annu Rev Plant Biol 62:299–334CrossRefPubMedGoogle Scholar
  45. Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant cell 24(6):2546–2561CrossRefPubMedPubMedCentralGoogle Scholar
  46. Huizinga DH, Denton R, Koehler KG, Tomasello A, Wood L, Sen SE, Crowell DN (2010) Farnesylcysteine lyase is involved in negative regulation of abscisic acid signaling in Arabidopsis. Mol Plant 3(1):143–155CrossRefPubMedGoogle Scholar
  47. Humphrey SJ, James DE, Mann M (2015) Protein phosphorylation: a major switch mechanism for metabolic regulation. Trends Endocrinol Metab 26(12):676–687CrossRefPubMedGoogle Scholar
  48. Irigoyen ML, Iniesto E, Rodriguez L, Puga MI, Yanagawa Y, Pick E, Strickland E, Paz-Ares J, Wei N, De Jaeger G, Rodriguez PL, Deng XW, Rubio V (2014) Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis. Plant cell 26(2):712–728CrossRefPubMedPubMedCentralGoogle Scholar
  49. Jensen ON (2006) Interpreting the protein language using proteomics. Nat Rev Mol Cell Biol 7(6):391–403CrossRefPubMedGoogle Scholar
  50. Kim JH, Kim WT (2013) The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses. Plant Physiol 162(3):1733–1749CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kim TH, Bohmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591CrossRefPubMedPubMedCentralGoogle Scholar
  52. Kim H, Hwang H, Hong JW, Lee YN, Ahn IP, Yoon IS, Yoo SD, Lee S, Lee SC, Kim BG (2012) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63(2):1013–1024CrossRefPubMedGoogle Scholar
  53. Kim TW, Youn JH, Park TK, Kim EJ, Park CH, Wang ZY, Kim SK, Kim TW (2018) OST1 activation by the brassinosteroid-regulated kinase CDG1-LIKE1 in stomatal closure. Plant cell 30(8):1848–1863CrossRefPubMedGoogle Scholar
  54. Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci USA 107(36):15986–15991CrossRefPubMedGoogle Scholar
  55. Kong L, Cheng J, Zhu Y, Ding Y, Meng J, Chen Z, Xie Q, Guo Y, Li J, Yang S, Gong Z (2015) Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat Commun 6:8630CrossRefPubMedPubMedCentralGoogle Scholar
  56. Kurup S, Jones HD, Holdsworth MJ (2000) Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J 21(2):143–155CrossRefPubMedGoogle Scholar
  57. Lechner E, Leonhardt N, Eisler H, Parmentier Y, Alioua M, Jacquet H, Leung J, Genschik P (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev Cell 21(6):1116–1128CrossRefPubMedGoogle Scholar
  58. Lee HG, Seo PJ (2016) The Arabidopsis MIEL1 E3 ligase negatively regulates ABA signalling by promoting protein turnover of MYB96. Nat Commun 7:12525CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant cell 22(6):1716–1732CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lee K, Lee HG, Yoon S, Kim HU, Seo PJ (2015) The Arabidopsis MYB96 transcription factor is a positive regulator of ABSCISIC ACID-INSENSITIVE4 in the control of seed germination. Plant Physiol 168(2):677–689CrossRefPubMedPubMedCentralGoogle Scholar
  61. Li Y, Zhang L, Li D, Liu Z, Wang J, Li X, Yang Y (2016) The Arabidopsis F-box E3 ligase RIFP1 plays a negative role in abscisic acid signalling by facilitating ABA receptor RCAR3 degradation. Plant Cell Environ 39(3):571–582CrossRefPubMedGoogle Scholar
  62. Li D, Zhang L, Li X, Kong X, Wang X, Li Y, Liu Z, Wang J, Li X, Yang Y (2018a) AtRAE1 is involved in degradation of ABA receptor RCAR1 and negatively regulates ABA signalling in Arabidopsis. Plant Cell Environ 41(1):231–244CrossRefPubMedGoogle Scholar
  63. Li S, Lin M, Wang J, Zhang L, Lin M, Hu Z, Qi Z, Jiang H, Fu Y, Xin D, Liu C, Chen Q (2018b) Regulation of soybean SUMOylation system in response to Phytophthora sojae infection and heat shock. Plant Growth Regul 87(1):69–82CrossRefGoogle Scholar
  64. Lim CW, Baek W, Lee SC (2017) The pepper RING-type E3 ligase CaAIRF1 regulates ABA and drought signaling via CaADIP1 protein phosphatase degradation. Plant Physiol 173(4):2323–2339CrossRefPubMedPubMedCentralGoogle Scholar
  65. Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang JL, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J (2012) Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1. Nat Commun 3:752CrossRefPubMedPubMedCentralGoogle Scholar
  66. Lin Q, Wu F, Sheng P, Zhang Z, Zhang X, Guo X, Wang J, Cheng Z, Wang J, Wang H, Wan J (2015) The SnRK2-APC/C(TE) regulatory module mediates the antagonistic action of gibberellic acid and abscisic acid pathways. Nat Commun 6:7981CrossRefPubMedPubMedCentralGoogle Scholar
  67. Linster E, Stephan I, Bienvenut WV, Maple-Grodem J, Myklebust LM, Huber M, Reichelt M, Sticht C, Moller SG, Meinnel T, Arnesen T, Giglione C, Hell R, Wirtz M (2015) Downregulation of N-terminal acetylation triggers ABA-mediated drought responses in Arabidopsis. Nat Commun 6:7640CrossRefPubMedPubMedCentralGoogle Scholar
  68. Liu H, Stone SL (2010) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant cell 22(8):2630–2641CrossRefPubMedPubMedCentralGoogle Scholar
  69. Liu F, Wang X, Su M, Yu M, Zhang S, Lai J, Yang C, Wang Y (2015) Functional characterization of DnSIZ1, a SIZ/PIAS-type SUMO E3 ligase from Dendrobium. BMC Plant Biol 15:225CrossRefPubMedPubMedCentralGoogle Scholar
  70. Lois LM, Lima CD, Chua NH (2003) Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant cell 15(6):1347–1359CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17(3):410–418CrossRefPubMedPubMedCentralGoogle Scholar
  72. Luo J, Shen G, Yan J, He C, Zhang H (2006) AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. Plant J 46(4):649–657CrossRefPubMedGoogle Scholar
  73. Lyzenga WJ, Liu H, Schofield A, Muise-Hennessey A, Stone SL (2013) Arabidopsis CIPK26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J Exp Bot 64(10):2779–2791CrossRefPubMedPubMedCentralGoogle Scholar
  74. Lyzenga WJ, Sullivan V, Liu H, Stone SL (2017) The kinase activity of calcineurin B-like interacting protein kinase 26 (CIPK26) influences its own stability and that of the ABA-regulated ubiquitin ligase, keep on going (KEG). Front Plant Sci 8:502CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930):1064–1068PubMedGoogle Scholar
  76. Ma QJ, Sun MH, Lu J, Liu YJ, You CX, Hao YJ (2017) An apple CIPK protein kinase targets a novel residue of AREB transcription factor for ABA-dependent phosphorylation. Plant Cell Environ 40(10):2207–2219CrossRefPubMedGoogle Scholar
  77. Ma T, Yoo MJ, Zhang T, Liu L, Koh J, Song WY, Harmon AC, Sha W, Chen S (2018) Characterization of thiol-based redox modifications of Brassica napusSNF1-related protein kinase 2.6-2C. FEBS Open Bio 8(4):628–645CrossRefPubMedPubMedCentralGoogle Scholar
  78. Merilo E, Jalakas P, Laanemets K, Mohammadi O, Horak H, Kollist H, Brosche M (2015) Abscisic acid transport and homeostasis in the context of stomatal regulation. Mol Plant 8(9):1321–1333CrossRefPubMedGoogle Scholar
  79. Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant cell 18(10):2749–2766CrossRefPubMedPubMedCentralGoogle Scholar
  80. Minkoff BB, Stecker KE, Sussman MR (2015) Rapid phosphoproteomic effects of abscisic acid (ABA) on wild-type and ABA receptor-deficient A. thaliana mutants. Mol Cell Proteom 14(5):1169–1182CrossRefGoogle Scholar
  81. Miricescu A, Goslin K, Graciet E (2018) Ubiquitylation in plants: signaling Hub for the integration of environmental signals. J Exp Bot 69(19):4511–4527CrossRefPubMedGoogle Scholar
  82. 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. Proc Natl Acad Sci USA 106(13):5418–5423CrossRefPubMedGoogle Scholar
  83. Mulekar JJ, Huq E (2014) Expanding roles of protein kinase CK2 in regulating plant growth and development. J Exp Bot 65(11):2883–2893CrossRefPubMedGoogle Scholar
  84. Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5:pls052CrossRefPubMedGoogle Scholar
  85. Nagashima Y, von Schaewen A, Koiwa H (2018) Function of N-glycosylation in plants. Plant Sci 274:70–79CrossRefPubMedGoogle Scholar
  86. Ng LM, Soon FF, Zhou XE, West GM, Kovach A, Suino-Powell KM, Chalmers MJ, Li J, Yong EL, Zhu JK, Griffin PR, Melcher K, Xu HE (2011) Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc Natl Acad Sci U S A 108(52):21259–21264CrossRefPubMedPubMedCentralGoogle Scholar
  87. Ni L, Fu X, Zhang H, Li X, Cai X, Zhang P, Liu L, Wang Q, Sun M, Wang Q, Zhang A, Zhang Z, Jiang M (2018) Abscisic acid inhibits rice protein phosphatase PP45 via H2O2 and relieves repression of the Ca2+/CaM-dependent protein kinase DMI3. Plant cell 31(1):128–152CrossRefPubMedGoogle Scholar
  88. Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136(1):136–148CrossRefPubMedGoogle Scholar
  89. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324(5930):1068–1071PubMedPubMedCentralGoogle Scholar
  90. Park HC, Kim H, Koo SC, Park HJ, Cheong MS, Hong H, Baek D, Chung WS, Kim DH, Bressan RA, Lee SY, Bohnert HJ, Yun DJ (2010) Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2 in rice. Plant Cell Environ 33(11):1923–1934CrossRefPubMedGoogle Scholar
  91. Peirats-Llobet M, Han SK, Gonzalez-Guzman M, Jeong CW, Rodriguez L, Belda-Palazon B, Wagner D, Rodriguez PL (2016) A direct link between abscisic acid sensing and the chromatin-remodeling ATPase BRAHMA via core ABA signaling pathway components. Mol Plant 9(1):136–147CrossRefPubMedGoogle Scholar
  92. Qi J, Song CP, Wang B, Zhou J, Kangasjarvi J, Zhu JK, Gong Z (2018) Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol 60(9):805–826CrossRefPubMedGoogle Scholar
  93. Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, Hoth S (2009) Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J 59(1):39–51CrossRefPubMedGoogle Scholar
  94. Rosenberger CL, Chen J (2018) To grow or not to grow: TOR and SnRK2 coordinate growth and stress response in Arabidopsis. Mol Cell 69(1):3–4CrossRefPubMedGoogle Scholar
  95. Saruhashi M, Kumar Ghosh T, Arai K, Ishizaki Y, Hagiwara K, Komatsu K, Shiwa Y, Izumikawa K, Yoshikawa H, Umezawa T, Sakata Y, Takezawa D (2015) Plant Raf-like kinase integrates abscisic acid and hyperosmotic stress signaling upstream of SNF1-related protein kinase2. Proc Natl Acad Sci USA 112(46):E6388–E6396CrossRefPubMedGoogle Scholar
  96. Sato A, Sato Y, Fukao Y, Fujiwara M, Umezawa T, Shinozaki K, Hibi T, Taniguchi M, Miyake H, Goto DB, Uozumi N (2009) Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem J 424(3):439–448CrossRefPubMedGoogle Scholar
  97. Seo KI, Lee JH, Nezames CD, Zhong S, Song E, Byun MO, Deng XW (2014) ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling. Plant Cell 26(2):695–711CrossRefPubMedPubMedCentralGoogle Scholar
  98. Seo DH, Ahn MY, Park KY, Kim EY, Kim WT (2016) The N-terminal UND motif of the Arabidopsis U-Box E3 ligase PUB18 is critical for the negative regulation of ABA-mediated stomatal movement and determines its ubiquitination specificity for exocyst subunit Exo70B1. Plant Cell 28(12):2952–2973CrossRefPubMedPubMedCentralGoogle Scholar
  99. Shang Y, Dai C, Lee MM, Kwak JM, Nam KH (2016) BRI1-associated receptor kinase 1 regulates guard cell ABA signaling mediated by open stomata 1 in Arabidopsis. Mol Plant 9(3):447–460CrossRefPubMedGoogle Scholar
  100. Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823–826CrossRefPubMedGoogle Scholar
  101. Shi B, Ni L, Zhang A, Cao J, Zhang H, Qin T, Tan M, Zhang J, Jiang M (2012) OsDMI3 is a novel component of abscisic acid signaling in the induction of antioxidant defense in leaves of rice. Mol Plant 5(6):1359–1374CrossRefPubMedGoogle Scholar
  102. Shi B, Ni L, Liu Y, Zhang A, Tan M, Jiang M (2014) OsDMI3-mediated activation of OsMPK1 regulates the activities of antioxidant enzymes in abscisic acid signalling in rice. Plant Cell Environ 37(2):341–352CrossRefPubMedGoogle Scholar
  103. Sierla M, Horak H, Overmyer K, Waszczak C, Yarmolinsky D, Maierhofer T, Vainonen JP, Salojarvi J, Denessiouk K, Laanemets K, Toldsepp K, Vahisalu T, Gauthier A, Puukko T, Paulin L, Auvinen P, Geiger D, Hedrich R, Kollist H, Kangasjarvi J (2018) The receptor-like pseudokinase GHR1 is required for stomatal closure. Plant Cell 30(11):2813–2837PubMedPubMedCentralGoogle Scholar
  104. Singh D, Laxmi A (2015) Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front Plant Sci 6:895PubMedPubMedCentralGoogle Scholar
  105. Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583(18):2982–2986CrossRefPubMedGoogle Scholar
  106. 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(4):2378–2391CrossRefPubMedPubMedCentralGoogle Scholar
  107. 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(6):1031–1043CrossRefPubMedGoogle Scholar
  108. Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18(12):3415–3428CrossRefPubMedPubMedCentralGoogle Scholar
  109. Takahashi Y, Kinoshita T, Matsumoto M, K-i Shimazaki (2016) Inhibition of the Arabidopsis bHLH transcription factor by monomerization through abscisic acid-induced phosphorylation. Plant J 87(6):559–567CrossRefPubMedGoogle Scholar
  110. Takahashi S, Monda K, Higaki T, Hashimoto-Sugimoto M, Negi J, Hasezawa S, Iba K (2017a) Differential effects of phosphatidylinositol 4-kinase (PI4K) and 3-kinase (PI3K) inhibitors on stomatal responses to environmental signals. Front Plant Sci 8:677CrossRefPubMedPubMedCentralGoogle Scholar
  111. Takahashi Y, Ebisu Y, Shimazaki KI (2017b) Reconstitution of abscisic acid signaling from the receptor to DNA via bHLH transcription factors. Plant Physiol 174(2):815–822CrossRefPubMedPubMedCentralGoogle Scholar
  112. Tan W, Zhang D, Zhou H, Zheng T, Yin Y, Lin H (2018) Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genet 14(4):e1007336CrossRefPubMedPubMedCentralGoogle Scholar
  113. Tang N, Ma S, Zong W, Yang N, Lv Y, Yan C, Guo Z, Li J, Li X, Xiang Y, Song H, Xiao J, Li X, Xiong L (2016) MODD mediates deactivation and degradation of OsbZIP46 to negatively regulate ABA signaling and drought resistance in rice. Plant Cell 28(9):2161–2177CrossRefPubMedPubMedCentralGoogle Scholar
  114. Tian W, Hou C, Ren Z, Pan Y, Jia J, Zhang H, Bai F, Zhang P, Zhu H, He Y, Luo S, Li L, Luan S (2015) A molecular pathway for CO(2) response in Arabidopsis guard cells. Nat Commun 6:6057CrossRefPubMedGoogle Scholar
  115. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106(41):17588–17593CrossRefPubMedGoogle Scholar
  116. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51(11):1821–1839CrossRefPubMedPubMedCentralGoogle Scholar
  117. Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y, Peck SC, Shinozaki K (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci Signal 6(270):rs8CrossRefPubMedGoogle Scholar
  118. Umezawa T, Takahashi F, Shinozaki K (2014) Phosphorylation networks in the abscisic acid signaling pathway. Enzymes 35:27–56CrossRefPubMedGoogle Scholar
  119. Vandelle E, Delledonne M (2011) Peroxynitrite formation and function in plants. Plant Sci 181(5):534–539CrossRefPubMedGoogle Scholar
  120. Vilela B, Najar E, Lumbreras V, Leung J, Pages M (2015) Casein kinase 2 negatively regulates abscisic acid-activated SnRK2s in the core abscisic acid-signaling module. Mol Plant 8(5):709–721CrossRefPubMedGoogle Scholar
  121. Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161PubMedPubMedCentralGoogle Scholar
  122. Waadt R, Manalansan B, Rauniyar N, Munemasa S, Booker MA, Brandt B, Waadt C, Nusinow DA, Kay SA, Kunz HH, Schumacher K, DeLong A, Yates JR 3rd, Schroeder JI (2015) Identification of open stomata1-interacting proteins reveals interactions with sucrose non-fermenting1-related protein kinases2 and with type 2A protein phosphatases that function in abscisic acid responses. Plant Physiol 169(1):760–779CrossRefPubMedPubMedCentralGoogle Scholar
  123. Wang H, Wang X (2018) GSK3-like kinases are a class of positive components in the core ABA signaling pathway. Mol Plant 11(6):761–763CrossRefPubMedGoogle Scholar
  124. Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci USA 112(2):613–618CrossRefPubMedGoogle Scholar
  125. Wang H, Tang J, Liu J, Hu J, Liu J, Chen Y, Cai Z, Wang X (2018a) Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol Plant 11(2):315–325CrossRefPubMedGoogle Scholar
  126. Wang P, Zhao Y, Li Z, Hsu CC, Liu X, Fu L, Hou YJ, Du Y, Xie S, Zhang C, Gao J, Cao M, Huang X, Zhu Y, Tang K, Wang X, Tao WA, Xiong Y, Zhu JK (2018b) Reciprocal Regulation of the TOR Kinase and ABA Receptor Balances Plant Growth and Stress Response. Mol Cell 69(1):100–112 e106CrossRefPubMedGoogle Scholar
  127. Wang Q, Qu GP, Kong X, Yan Y, Li J, Jin JB (2018c) Arabidopsis small ubiquitin-related modifier protease ASP1 positively regulates abscisic acid signaling during early seedling development. J Integr Plant Biol 60(10):924–937CrossRefPubMedGoogle Scholar
  128. Wang X, Guo C, Peng J, Li C, Wan F, Zhang S, Zhou Y, Yan Y, Qi L, Sun K, Yang S, Gong Z, Li J (2018d) ABRE-BINDING FACTORS play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol 221(1):341–355CrossRefPubMedGoogle Scholar
  129. Withers J, Dong X (2017) Post-translational regulation of plant immunity. Curr Opin Cell Biol 38:124–132CrossRefGoogle Scholar
  130. Wu Q, Zhang X, Peirats-Llobet M, Belda-Palazon B, Wang X, Cui S, Yu X, Rodriguez PL, An C (2016) Ubiquitin ligases RGLG1 and RGLG5 regulate abscisic acid signaling by controlling the turnover of phosphatase PP2CA. Plant Cell 28(9):2178–2196CrossRefPubMedPubMedCentralGoogle Scholar
  131. Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ 38(1):35–49CrossRefPubMedGoogle Scholar
  132. Yu F, Wu Y, Xie Q (2015) Precise protein post-translational modifications modulate ABI5 activity. Trends Plant Sci 20(9):569–575CrossRefPubMedGoogle Scholar
  133. Yu F, Lou L, Tian M, Li Q, Ding Y, Cao X, Wu Y, Belda-Palazon B, Rodriguez PL, Yang S, Xie Q (2016a) ESCRT-I component VPS23A affects ABA signaling by recognizing ABA receptors for endosomal degradation. Mol Plant 9(12):1570–1582CrossRefPubMedGoogle Scholar
  134. Yu F, Wu Y, Xie Q (2016b) Ubiquitin-proteasome system in ABA signaling: from perception to action. Mol Plant 9(1):21–33CrossRefPubMedGoogle Scholar
  135. Zhang X, Garreton V, Chua NH (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19(13):1532–1543CrossRefPubMedPubMedCentralGoogle Scholar
  136. Zhang S, Qi Y, Liu M, Yang C (2013) SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana (F). J Integr Plant Biol 55(1):83–95CrossRefPubMedGoogle Scholar
  137. Zhang H, Cui F, Wu Y, Lou L, Liu L, Tian M, Ning Y, Shu K, Tang S, Xie Q (2015) The RING finger ubiquitin E3 ligase SDIR1 targets SDIR1-INTERACTING PROTEIN1 for degradation to modulate the salt stress response and ABA signaling in Arabidopsis. Plant Cell 27(1):214–227CrossRefPubMedPubMedCentralGoogle Scholar
  138. 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 198:69–80CrossRefPubMedGoogle Scholar
  139. Zhang S, Hou B, Chai L, Yang A, Yu X, Shen Y (2017a) Sigma factor FaSigE positively regulates strawberry fruit ripening by ABA. Plant Growth Regul 83(3):417–427CrossRefGoogle Scholar
  140. Zhang S, Zhuang K, Wang S, Lv J, Ma N, Meng Q (2017b) A novel tomato SUMO E3 ligase, SlSIZ1, confers drought tolerance in transgenic tobacco. J Integr Plant Biol 59(2):102–117CrossRefPubMedGoogle Scholar
  141. Zhang L, Li X, Li D, Sun Y, Li Y, Luo Q, Liu Z, Wang J, Li X, Zhang H, Lou Z, Yang Y (2018a) CARK1 mediates ABA signaling by phosphorylation of ABA receptors. Cell Discov 4:30CrossRefPubMedPubMedCentralGoogle Scholar
  142. Zhang L, Liang X-G, Shen S, Yin H, Zhou L-L, Gao Z, Lv X-Y, Zhou S-L (2018b) Increasing the abscisic acid level in maize grains induces precocious maturation by accelerating grain filling and dehydration. Plant Growth Regul 86(1):65–79CrossRefGoogle Scholar
  143. Zhao C, Wang P, Si T, Hsu CC, Wang L, Zayed O, Yu Z, Zhu Y, Dong J, Tao WA, Zhu JK (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43(5):618–629 e615CrossRefPubMedPubMedCentralGoogle Scholar
  144. 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. Proc Natl Acad Sci USA 109(31):12822–12827CrossRefPubMedGoogle Scholar
  145. Zheng Y, Chen Z, Ma L, Liao C (2018) The ubiquitin E3 ligase RHA2b promotes degradation of MYB30 in abscisic acid signaling. Plant Physiol 178(1):428–440CrossRefPubMedGoogle Scholar
  146. Zhou X, Hao H, Zhang Y, Bai Y, Zhu W, Qin Y, Yuan F, Zhao F, Wang M, Hu J, Xu H, Guo A, Zhao H, Zhao Y, Cao C, Yang Y, Schumaker KS, Guo Y, Xie CG (2015) SOS2-LIKE PROTEIN KINASE5, an SNF1-RELATED PROTEIN KINASE3-type protein kinase, is important for abscisic acid responses in Arabidopsis through phosphorylation of ABSCISIC ACID-INSENSITIVE5. Plant Physiol 168(2):659–676CrossRefPubMedPubMedCentralGoogle Scholar
  147. Zhu M, Zhu N, Song WY, Harmon AC, Assmann SM, Chen S (2014) Thiol-based redox proteins in abscisic acid and methyl jasmonate signaling in Brassica napus guard cells. Plant J 78(3):491–515CrossRefPubMedPubMedCentralGoogle Scholar
  148. Zhuang X, Cui Y, Gao C, Jiang L (2015) Endocytic and autophagic pathways crosstalk in plants. Curr Opin Cell Biol 28:39–47CrossRefGoogle Scholar
  149. Zong W, Tang N, Yang J, Peng L, Ma S, Xu Y, Li G, Xiong L (2016) Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought resistance related genes. Plant Physiol 171(4):2810–2825PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute of Cell Biology, School of Life SciencesLanzhou UniversityLanzhouPeople’s Republic of China
  2. 2.Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life SciencesLanzhou UniversityLanzhouPeople’s Republic of China
  3. 3.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingPeople’s Republic of China

Personalised recommendations