Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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New Insights into the Protein Turnover Regulation in Ethylene Biosynthesis

  • Yoon, Gyeong Mee (Department of Botany and Plant Pathology, Purdue University)
  • Received : 2015.06.01
  • Accepted : 2015.06.08
  • Published : 2015.07.31
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Abstract

Biosynthesis of the phytohormone ethylene is under tight regulation to satisfy the need for appropriate levels of ethylene in plants in response to exogenous and endogenous stimuli. The enzyme 1-aminocyclopropane-1-carboxylic acid synthase (ACS), which catalyzes the rate-limiting step of ethylene biosynthesis, plays a central role to regulate ethylene production through changes in ACS gene expression levels and the activity of the enzyme. Together with molecular genetic studies suggesting the roles of post-translational modification of the ACS, newly emerging evidence strongly suggests that the regulation of ACS protein stability is an alternative mechanism that controls ethylene production, in addition to the transcriptional regulation of ACS genes. In this review, recent new insight into the regulation of ACS protein turnover is highlighted, with a special focus on the roles of phosphorylation, ubiquitination, and novel components that regulate the turnover of ACS proteins. The prospect of cross-talk between ethylene biosynthesis and other signaling pathways to control turnover of the ACS protein is also considered.

Keywords

References

  1. Abeles, F.B., Morgan, P.W., and Saltveit, M.E.J. (1992). Ethylene in plant biology. (San Diego, CA: Academic Press)
  2. Adams, D.O., and Yang, S.F. (1977). Methionine metabolism in apple tissue-implication of S-adenosylmethionine as an intermediate in conversion of methionine to ethylene. Plant Physiol. 60, 892-896. https://doi.org/10.1104/pp.60.6.892
  3. Aitken, A., Collinge, D.B., van Heusden, B.P., Isobe, T., Roseboom, P.H., Rosenfeld, G., and Soll, J. (1992). 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins. Trends Biochem Sci. 17, 498-501. https://doi.org/10.1016/0968-0004(92)90339-B
  4. Albagli, O., Dhordain, P., Deweindt, C., Lecocq, G., and Leprince, D. (1995). The BTB/POZ domain: a new protein-protein interaction motif common to DNA-and actin-binding proteins. Cell Growth Differ. 6, 1193-1198.
  5. Argueso, C.T., Hansen, M., and Kieber, J.J. (2007). Regulation of ethylene biosynthesis.. J. Plant Growth Regul. 26, 13.
  6. Arteca, R.N., and Arteca, J.M. (2008). Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants. J. Exp. Bot. 59, 3019-3026. https://doi.org/10.1093/jxb/ern159
  7. Ben-Nissan, G., Cui, W., Kim, D.J., Yang, Y., Yoo, B.C., and Lee, J.Y. (2008). Arabidopsis casein kinase 1-like 6 contains a microtubule-binding domain and affects the organization of cortical microtubules. Plant Physiol. 148, 1897-1907. https://doi.org/10.1104/pp.108.129346
  8. Blatch, G.L., and Lassle, M. (1999). The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. BioEssays 21, 932-939. https://doi.org/10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.0.CO;2-N
  9. Boller, T., Herner, R.C., and Kende, H. (1979). Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid. Planta 145, 293-303. https://doi.org/10.1007/BF00454455
  10. Bornke, F. (2005). The variable C-terminus of 14-3-3 proteins mediates isoform-specific interaction with sucrose-phosphate synthase in the yeast two-hybrid system. J. Plant Physiol. 162, 161-168. https://doi.org/10.1016/j.jplph.2004.09.006
  11. Bostick, M., Lochhead, S.R., Honda, A., Palmer, S., and Callis, J. (2004). Related to ubiquitin 1 and 2 are redundant and essential and regulate vegetative growth, auxin signaling, and ethylene production in Arabidopsis. Plant Cell 16, 2418-2432. https://doi.org/10.1105/tpc.104.024943
  12. Catala, R., Lopez-Cobollo, R., Mar Castellano, M., Angosto, T., Alonso, J.M., Ecker, J.R., and Salinas, J. (2014). The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links lowtemperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation. Plant Cell 26, 3326-3342. https://doi.org/10.1105/tpc.114.127605
  13. Chae, H.S., and Kieber, J.J. (2005). Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci. 10, 291-296. https://doi.org/10.1016/j.tplants.2005.04.006
  14. Chae, H.S., Faure, F., and Kieber, J.J. (2003). The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15, 545-559. https://doi.org/10.1105/tpc.006882
  15. Christians, M.J., Gingerich, D.J., Hansen, M., Binder, B.M., Kieber, J.J., and Vierstra, R.D. (2009). The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 57, 332-345. https://doi.org/10.1111/j.1365-313X.2008.03693.x
  16. Crocker, W., and Knight, L.I. (1908). Effect of illuminating gas and ethylene upon flowering carnation. Bot. Gaz 46, 259-276. https://doi.org/10.1086/329718
  17. Dai, C., and Xue, H.W. (2010). Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J. 29, 1916-1927. https://doi.org/10.1038/emboj.2010.75
  18. Darling, D.L., Yingling, J., and Wynshaw-Boris, A. (2005). Role of 14-3-3 proteins in eukaryotic signaling and development. Curr. Top. Dev. Biol. 68, 281-315. https://doi.org/10.1016/S0070-2153(05)68010-6
  19. De Boer, A.H., van Kleeff, P.J., and Gao, J. (2013). Plant 14-3-3 proteins as spiders in a web of phosphorylation. Protoplasma 250, 425-440. https://doi.org/10.1007/s00709-012-0437-z
  20. De Grauwe, L., Chaerle, L., Dugardeyn, J., Decat, J., Rieu, I., Vriezen, W.H., Baghour, M., Moritz, T., Beemster, G.T., Phillips, A.L., et al. (2008a). Reduced gibberellin response affects ethylene biosynthesis and responsiveness in the Arabidopsis gai eto2-1 double mutant. New Phytol. 177, 128-141.
  21. De Grauwe, L., Dugardeyn, J., and Van Der Straeten, D. (2008b). Novel mechanisms of ethylene-gibberellin crosstalk revealed by the gai eto2-1 double mutant. Plant Signal. Behav. 3, 1113-1115. https://doi.org/10.4161/psb.3.12.7037
  22. Denison, F.C., Paul, A.L., Zupanska, A.K., and Ferl, R.J. (2011). 14-3-3 proteins in plant physiology. Semin. Cell Dev. Biol. 22, 720-727. https://doi.org/10.1016/j.semcdb.2011.08.006
  23. Dong, J.G., Fernandez-Maculet, J.C., and Yang, S.F. (1992). Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. Proc. Natl. Acad. Sci. USA 89, 9789-9793. https://doi.org/10.1073/pnas.89.20.9789
  24. Dougherty, M.K., and Morrison, D.K. (2004). Unlocking the code of 14-3-3. J. Cell Sci. 117, 1875-1884. https://doi.org/10.1242/jcs.01171
  25. Freeman, A.K., and Morrison, D.K. (2011). 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin. Cell Dev. Biol. 22, 681-687. https://doi.org/10.1016/j.semcdb.2011.08.009
  26. Fu, H., Subramanian, R.R., and Masters, S.C. (2000). 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40, 617-647. https://doi.org/10.1146/annurev.pharmtox.40.1.617
  27. Gane, R. (1934). Production of ethylene by some ripening fruits. Nature 134, 1008-1008
  28. Ganguly, S., Weller, J.L., Ho, A., Chemineau, P., Malpaux, B., and Klein, D.C. (2005). Melatonin synthesis: 14-3-3-dependent activation and inhibition of arylalkylamine N-acetyltransferase mediated by phosphoserine-205. Proc. Natl. Acad. Sci. USA 102, 1222-1227. https://doi.org/10.1073/pnas.0406871102
  29. Guzman, P., and Ecker, J.R. (1990). Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523. https://doi.org/10.1105/tpc.2.6.513
  30. Hansen, M., Chae, H.S., and Kieber, J.J. (2009). Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J. 57, 606-614. https://doi.org/10.1111/j.1365-313X.2008.03711.x
  31. Harpaz-Saad, S., Yoon, G.M., Matto, A.K., and Kieber, J.J. (2012). The formation of ACC and competition between polyamines and ethylene for SAM. Annu. Plant Rev. 44, 53-81.
  32. Hernandez Sebastia, C., Hardin, S.C., Clouse, S.D., Kieber, J.J., and Huber, S.C. (2004). Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch. Biochem. Biophys. 428, 81-91. https://doi.org/10.1016/j.abb.2004.04.025
  33. Ho, M.S., Ou, C., Chan, Y.R., Chien, C.T., and Pi, H. (2008). The utility F-box for protein destruction. Cell. Mol. Life Sci. 65, 1977-2000. https://doi.org/10.1007/s00018-008-7592-6
  34. Holt, L.J., Tuch, B.B., Villen, J., Johnson, A.D., Gygi, S.P., and Morgan, D.O. (2009). Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325, 1682-1686. https://doi.org/10.1126/science.1172867
  35. Joo, S., Liu, Y., Lueth, A., and Zhang, S. (2008). MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J. 54, 129-140. https://doi.org/10.1111/j.1365-313X.2008.03404.x
  36. Kamiyoshihara, Y., Iwata, M., Fukaya, T., Tatsuki, M., and Mori, H. (2010). Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J. 64, 140-150.
  37. Kende, H. (1993). Ethylene biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 283-307. https://doi.org/10.1146/annurev.pp.44.060193.001435
  38. Kim, C.Y., Liu, Y., Thorne, E.T., Yang, H., Fukushige, H., Gassmann, W., Hildebrand, D., Sharp, R.E., and Zhang, S. (2003). Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15, 2707-2718. https://doi.org/10.1105/tpc.011411
  39. Knight, L.I., Rose, R.C., and Crocker, W. (1910). Effects of various gases and vapors upon etiolated seedlings of the sweet pea. Science 31, 635-636.
  40. Lara, I., and Vendrell, M. (2000). Development of ethylenesynthesizing capacity in preclimacteric apples: interaction between abscisic acid and ethylene. J. Am. Soc. Hortic. Sci. 125, 505-512.
  41. Larsen, P.B., and Cancel, J.D. (2004). A recessive mutation in the RUB1-conjugating enzyme, RCE1, reveals a requirement for RUB modification for control of ethylene biosynthesis and proper induction of basic chitinase and PDF1.2 in Arabidopsis. Plant J. 38, 626-638. https://doi.org/10.1111/j.1365-313X.2004.02068.x
  42. Li, C.H., Wang, G., Zhao, J.L., Zhang, L.Q., Ai, L.F., Han, Y.F., Sun, D.Y., Zhang, S.W., and Sun, Y. (2014). The Receptor-Like Kinase SIT1 Mediates Salt Sensitivity by Activating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell 26, 2538-2553. https://doi.org/10.1105/tpc.114.125187
  43. Lieberman, M., and Mapson, L.W. (1964). Genesis and biogenesis of ethylene. Nature 204, 343-345. https://doi.org/10.1038/204343a0
  44. Liu, Y., and Zhang, S. (2004). Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stressresponsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386-3399. https://doi.org/10.1105/tpc.104.026609
  45. Liu, W., Xu, Z.H., Luo, D., and Xue, H.W. (2003). Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J. 36, 189-202. https://doi.org/10.1046/j.1365-313X.2003.01866.x
  46. Lyzenga, W.J., Booth, J.K., and Stone, S.L. (2012). The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7. Plant J. 71, 23-34. https://doi.org/10.1111/j.1365-313X.2012.04965.x
  47. Mattoo, A.K., and Suttle, J.C. (1991). The Plant Hormone Ethylene. (Boca Raton: CRC Press).
  48. Mayfield, J.D., Folta, K.M., Paul, A.L., and Ferl, R.J. (2007). The 14-3-3 Proteins mu and upsilon influence transition to flowering and early phytochrome response. Plant Physiol. 145, 1692-1702. https://doi.org/10.1104/pp.107.108654
  49. McClellan, C.A., and Chang, C.L. (2008). The role of protein turnover in ethylene biosynthesis and response. Plant Sci. 175, 24-31. https://doi.org/10.1016/j.plantsci.2008.01.004
  50. Murr, D.P., and Yang, S.F. (1975). Conversion of 5-methylthioadenosine to methionine by apple tissue. Phytochemistry 14, 1291-1292. https://doi.org/10.1016/S0031-9422(00)98613-8
  51. Neljubov, D. (1901). Uber die horizontale Nutation der Stengel von Pisum sativum und einiger Anderer. Pflanzen Beih. Bot. Zentralb 10, 128-139.
  52. Nodzon, L.A., Xu, W.H., Wang, Y., Pi, L.Y., Chakrabarty, P.K., and Song, W.Y. (2004). The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J. 40, 996-1006. https://doi.org/10.1111/j.1365-313X.2004.02266.x
  53. Paul, A.L., Folta, K.M., and Ferl, R.J. (2008). 14-3-3 proteins, red light and photoperiodic flowering: a point of connection? Plant Signal. Behav. 3, 511-515. https://doi.org/10.4161/psb.3.8.5717
  54. Paul, A.L., Denison, F.C., Schultz, E.R., Zupanska, A.K., and Ferl, R.J. (2012). 14-3-3 phosphoprotein interaction networks-does isoform diversity present functional interaction specification? Front. Plant Sci. 3, 190.
  55. Pintard, L., Willems, A., and Peter, M. (2004). Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23, 1681-1687. https://doi.org/10.1038/sj.emboj.7600186
  56. Prasad, M.E., Schofield, A., Lyzenga, W., Liu, H., and Stone, S.L. (2010). Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol. 153, 1587-1596. https://doi.org/10.1104/pp.110.156976
  57. Purwestri, Y.A., Ogaki, Y., Tamaki, S., Tsuji, H., and Shimamoto, K. (2009). The 14-3-3 protein GF14c acts as a negative regulator of flowering in rice by interacting with the florigen Hd3a. Plant Cell Physiol. 50, 429-438. https://doi.org/10.1093/pcp/pcp012
  58. Sauter, M., Moffatt, B., Saechao, M.C., Hell, R., and Wirtz, M. (2013). Methionine salvage and Sadenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. Biochem. J. 451, 145-154. https://doi.org/10.1042/BJ20121744
  59. Skottke, K.R., Yoon, G.M., Kieber, J.J., and DeLong, A. (2011). Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet. 7, e1001370. https://doi.org/10.1371/journal.pgen.1001370
  60. Su, C.H., Zhao, R., Zhang, F., Qu, C., Chen, B., Feng, Y.H., Phan, L., Chen, J., Wang, H., Wang, H., et al. (2011). 14-3-3sigma exerts tumor-suppressor activity mediated by regulation of COP1 stability. Cancer Res. 71, 884-894. https://doi.org/10.1158/0008-5472.CAN-10-2518
  61. Tan, S.T., and Xue, H.W. (2014). Casein kinase 1 regulates ethylene synthesis by phosphorylating and promoting the turnover of ACS5. Cell Rep. 9, 1692-1702. https://doi.org/10.1016/j.celrep.2014.10.047
  62. Tan, S.T., Dai, C., Liu, H.T., and Xue, H.W. (2013). Arabidopsis casein kinase1 proteins CK1.3 and CK1.4 phosphorylate cryptochrome2 to regulate blue light signaling. Plant Cell 25, 2618-2632. https://doi.org/10.1105/tpc.113.114322
  63. Tari, I., and Nagy, M. (1996). Abscisic acid and ethrel abolish the inhibition of adventitious root formation of pacrobutrazol-treated bean primary leaf cuttings. Biol. Plant. 38, 369-375. https://doi.org/10.1007/BF02896664
  64. Tseng, T.S., Whippo, C., Hangarter, R.P., and Briggs, W.R. (2012). The role of a 14-3-3 protein in stomatal opening mediated by PHOT2 in Arabidopsis. Plant Cell 24, 1114-1126. https://doi.org/10.1105/tpc.111.092130
  65. Tsuchisaka, A., and Theologis, A. (2004). Unique and overlapping expression patterns among the Arabidopsis 1-aminocyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 136, 2982-3000. https://doi.org/10.1104/pp.104.049999
  66. Van de Poel, B., and Van Der Straeten, D. (2014). 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front. Plant Sci. 5, 640.
  67. Vogel, J.P., Woeste, K.E., Theologis, A., and Kieber, J.J. (1998). Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl. Acad. Sci. USA 95, 4766-4771. https://doi.org/10.1073/pnas.95.8.4766
  68. Vriezen, W.H., Hulzink, R., Mariani, C., and Voesenek, L.A. (1999). 1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence. Plant Physiol. 121, 189-196. https://doi.org/10.1104/pp.121.1.189
  69. Wang, K.L., Yoshida, H., Lurin, C., and Ecker, J.R. (2004). Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428, 945-950. https://doi.org/10.1038/nature02516
  70. Wee, S., Geyer, R.K., Toda, T., and Wolf, D.A. (2005). CSN facilitates Cullin-RING ubiquitin ligase function by counteracting autocatalytic adapter instability. Nat. Cell Biol. 7, 387-391. https://doi.org/10.1038/ncb1241
  71. Woeste, K.E., Vogel, J.P., and Kieber, J.J. (1999a). Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings. Physiol. Plant. 105, 478-484. https://doi.org/10.1034/j.1399-3054.1999.105312.x
  72. Woeste, K.E., Ye, C., and Kieber, J.J. (1999b). Two Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol. 119, 521-530. https://doi.org/10.1104/pp.119.2.521
  73. Xiong, L., Xiao, D., Xu, X., Guo, Z., and Wang, N.N. (2014). The non-catalytic N-terminal domain of ACS7 is involved in the posttranslational regulation of this gene in Arabidopsis. J. Exp. Bot. 65, 4397-4408. https://doi.org/10.1093/jxb/eru211
  74. Yang, S.F., and Hoffman, N.E. (1984). Ethylene biosynthesis and its regulation in higher plants.. Ann. Rev. Plant Physiol. 34, 34.
  75. Yang, H.Y., Wen, Y.Y., Lin, Y.I., Pham, L., Su, C.H., Yang, H., Chen, J., and Lee, M.H. (2007). Roles for negative cell regulator 14-3-3sigma in control of MDM2 activities. Oncogene 26, 7355-7362. https://doi.org/10.1038/sj.onc.1210540
  76. Yi, H.C., Joo, S., Nam, K.H., Lee, J.S., Kang, B.G., and Kim, W.T. (1999). Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol. Biol. 41, 443-454. https://doi.org/10.1023/A:1006372612574
  77. Yoon, G.M., and Kieber, J.J. (2013a). 14-3-3 regulates 1-aminocyclopropane-1-carboxylate synthase protein turnover in Arabidopsis. Plant Cell 25, 1016-1028. https://doi.org/10.1105/tpc.113.110106
  78. Yoon, G.M., and Kieber, J.J. (2013b). ACC synthase and its cognate E3 ligase are inversely regulated by light. Plant Signal. Behav. 8, e26478. https://doi.org/10.4161/psb.26478
  79. Yoshida, H., Nagata, M., Saito, K., Wang, K.L., and Ecker, J.R. (2005). Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol. 5, 14. https://doi.org/10.1186/1471-2229-5-14
  80. Yoshida, H., Wang, K.L., Chang, C.M., Mori, K., Uchida, E., and Ecker, J.R. (2006). The ACC synthase TOE sequence is required for interaction with ETO1 family proteins and destabilization of target proteins. C 62, 427-437. https://doi.org/10.1007/s11103-006-9029-7
  81. Zarembinski, T.I., and Theologis, A. (1994). Ethylene biosynthesis and action: a case of conservation. The 26, 1579-1597. https://doi.org/10.1007/BF00016491
  82. Zhang, M., Yuan, B., and Leng, P. (2009). The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J. Exp. Bot. 60, 1579-1588. https://doi.org/10.1093/jxb/erp026

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  19. The regulation of ethylene biosynthesis: a complex multilevel control circuitry vol.229, pp.2, 2015, https://doi.org/10.1111/nph.16873
  20. Reciprocal antagonistic regulation of E3 ligases controls ACC synthase stability and responses to stress vol.118, pp.34, 2015, https://doi.org/10.1073/pnas.2011900118
  21. Plants Saline Environment in Perception with Rhizosphere Bacteria Containing 1-Aminocyclopropane-1-Carboxylate Deaminase vol.22, pp.21, 2021, https://doi.org/10.3390/ijms222111461