, Volume 243, Issue 1, pp 1–12 | Cite as

Plant abiotic stress-related RCI2/PMP3s: multigenes for multiple roles

  • Pedro S. C. F. RochaEmail author


Main conclusion

RCI2 / PMP3 s participate in abiotic stress responses and impact the expression of other genes. Their multifunctionality is determined by differential expression and by distinct activities of their structurally different proteins.

In plants, RCI2/PMP3 genes, which encode small membrane proteins of the PMP3 family, are closely associated with abiotic stress responses. Their involvement in mediating stress tolerance is supported by genetic evidence and overexpression studies. RCI2/PMP3s occur as multigenes in plant genomes and their encoded proteins belong to distinct and conserved structural groups. In addition, different isoforms appear to be targeted to the plasma membrane or to distinct endomembrane compartments in cells. Several studies have revealed that RCI2/PMP3 proteins participate in cell ion homeostasis, and in regulation of membrane stability and polarization. They also appear to potentiate plant transcriptional responses to abiotic stresses. However, their mechanisms of action remain unknown. This paper reviews the current knowledge of the multiple roles of plant RCI2/PMP3 genes resulting from their differential expression under normal and stress conditions. The structural diversity of RCI2/PMP3 proteins is analyzed and evidence supporting their functional specialization and possible activity mechanisms is examined. Finally, strategies are discussed for exploiting new and established technologies to overcome the difficulties posed by the multigene status of RCI2s and the integral membrane character of their proteins, enabling the probing of their individual functions and collective significance.


Cell ion homeostasis Membrane stability Integral membrane protein Stress tolerance Gene family 



PSCFR research has been funded by the National Natural Science Foundation of China, Grant numbers 31071151 and 30771211. The author wishes to thank the anonymous reviewer for the helpful suggestions.

Supplementary material

425_2015_2386_MOESM1_ESM.pdf (126 kb)
Supplementary material 1 (PDF 125 kb)
425_2015_2386_MOESM2_ESM.pdf (43 kb)
Supplementary material 2 (PDF 43 kb)
425_2015_2386_MOESM3_ESM.pdf (159 kb)
Supplementary material 3 (PDF 160 kb)


  1. Baisakh N, Subudhi PK (2009) Heat stress alters the expression of salt stress induced genes in smooth cordgrass (Spartina alterniflora L.). Plant Physiol Biochem 47:232–235. doi: 10.1016/j.plaphy.2008.11.010 CrossRefPubMedGoogle Scholar
  2. Baisakh N, Subudhi PK, Varadwaj P (2008) Primary responses to salt stress in a halophyte, smooth cordgrass (Spartina alterniflora Loisel.). Funct Integr Genomics 8:287–300. doi: 10.1007/s10142-008-0075-x CrossRefPubMedGoogle Scholar
  3. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84. doi: 10.1016/j.copbio.2014.11.007 CrossRefPubMedGoogle Scholar
  4. Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434. doi: 10.1016/s0955-0674(00)00112-5 CrossRefPubMedGoogle Scholar
  5. Brown APC, Dunn MA, Goddard NJ, Hughes MA (2001) Identification of a novel low-temperature-response element in the promoter of the barley (Hordeum vulgare L) gene blt101.1. Planta 213:770–780. doi: 10.1007/s004250100549 CrossRefPubMedGoogle Scholar
  6. Capel J, Jarillo JA, Salinas J, Martinez-Zapater JM (1997) Two homologous low-temperature-inducible genes from Arabidopsis encode highly hydrophobic proteins. Plant Physiol 115:569–576. doi: 10.1104/pp.115.2.569 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451. doi: 10.1016/j.tplants.2007.07.002 CrossRefPubMedGoogle Scholar
  8. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. doi: 10.1016/j.tplants.2014.02.001 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Feng D-R, Liu B, Li W-Y, He Y-M, Qi K-B, Wang H-B, Wang J-F (2009) Over-expression of a cold-induced plasma membrane protein gene (MpRCI) from plantain enhances low temperature-resistance in transgenic tobacco. Environ Exper Bot 6:395–402. doi: 10.1016/j.envexpbot.2008.12.009 CrossRefGoogle Scholar
  10. Fu J, Zhang D, Liu Y, Ying S, Shi Y, Song Y, Li Y, Wang T (2012) Isolation and characterization of maize PMP3 genes involved in salt stress tolerance. PLoS ONE. doi: 10.1371/journal.pone.0031101 Google Scholar
  11. Gahl RF, Tekle E, Zhu GA, Taraska JW, Tjandra N (2015) Acquiring snapshots of the orientation of trans-membrane protein domains using a hybrid FRET pair. FEBS Lett 589:885–889. doi: 10.1016/j.febslet.2015.02.030 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Galvez AF, Gulick PJ, Dvorak J (1993) Characterization of the early stages of genetic salt-stress responses in salt-tolerant Lophopyrum elongatum, salt-sensitive wheat, and their amphiploid. Plant Physiol 103:257–265PubMedPubMedCentralGoogle Scholar
  13. Gao C, Cai Y, Wang Y, Kang B-H, Aniento F, Robinson DG, Jiang L (2014) Retention mechanisms for ER and Golgi membrane proteins. Trends Plant Sci 19:508–515. doi: 10.1016/j.tplants.2014.04.004 CrossRefPubMedGoogle Scholar
  14. Gimeno J, Gadea J, Forment J, Perez-Valle J, Santiago J, Martinez-Godoy MA, Yenush L, Belles JM, Brumos J, Colmenero-Flores JM, Talon M, Serrano R (2009) Shared and novel molecular responses of mandarin to drought. Plant Mol Biol 70:403–420. doi: 10.1007/s11103-009-9481-2 CrossRefPubMedGoogle Scholar
  15. Goddard NJ, Dunn MA, Zhang L, White AJ, Jack PL, Hughes MA (1993) Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, blt101. Plant Mol Biol 23:871–879. doi: 10.1007/bf00021541 CrossRefPubMedGoogle Scholar
  16. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci. doi: 10.3389/fpls.2014.00151 PubMedPubMedCentralGoogle Scholar
  17. Gulick PJ, Dvorak J (1992) Coordinate gene response to salt stress in Lophopyrum elongatum. Plant Physiol 100:1384–1388. doi: 10.1104/pp.100.3.1384 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gulick PJ, Shen W, An HY (1994) ESI3, a stress-induced gene from Lophopyrum elongatum. Plant Physiol 104:799–800. doi: 10.1104/pp.104.2.799 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gusta LV, Trischuk R, Weiser CJ (2005) Plant cold acclimation: The role of abscisic acid. J Plant Growth Regul 24:308–318. doi: 10.1007/s00344-005-0079-x CrossRefGoogle Scholar
  20. Hu CD, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZip and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9:789–798. doi: 10.1016/s1097-2765(02)00496-3 CrossRefPubMedGoogle Scholar
  21. Huang G-T, Ma S-L, Bai L-P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z-F (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987. doi: 10.1007/s11033-011-0823-1 CrossRefPubMedGoogle Scholar
  22. Imai R, Koike M, Sutoh K, Kawakami A, Torada A, Oono K (2005) Molecular characterization of a cold-induced plasma membrane protein gene from wheat. Mol Genet Genomics 274:445–453. doi: 10.1007/s00438-005-0050-3 CrossRefPubMedGoogle Scholar
  23. Inada M, Ueda A, Shi W, Takabe T (2005) A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na + and K + accumulation under salt stress. Planta 220:395–402. doi: 10.1007/s00425-004-1358-7 CrossRefPubMedGoogle Scholar
  24. Johnsson N, Varshavsky A (1994) Split ubiquitin as a sensor of protein interactions in vivo. Proc Natl Acad Sci USA 91:10340–10344. doi: 10.1073/pnas.91.22.10340 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jones DT (2007) Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23:538–544. doi: 10.1093/bioinformatics/btl677 CrossRefPubMedGoogle Scholar
  26. Käll L, Krogh A, Sonnhammer ELL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036. doi: 10.1016/j.jmb.2004.03.016 CrossRefPubMedGoogle Scholar
  27. Kim S-H, Kim J-Y, Kim S-J, An K-S, An G, Kim S-R (2007) Isolation of cold stress-responsive genes in the reproductive organs, and characterization of the OsLti6b gene from rice (Oryza sativa L.). Plant Cell Rep 26:1097–1110. doi: 10.1007/s00299-006-0297-0 CrossRefPubMedGoogle Scholar
  28. Kroemer K, Reski R, Frank W (2004) Abiotic stress response in the moss Physcomitrella patens: evidence for an evolutionary alteration in signaling pathways in land plants. Plant Cell Rep 22:864–870. doi: 10.1007/s00299-004-0785-z CrossRefPubMedGoogle Scholar
  29. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305:567–580. doi: 10.1006/jmbi.2000.4315 CrossRefPubMedGoogle Scholar
  30. Li IT, Pham E, Truong K (2006) Protein biosensors based on the principle of fluorescence resonance energy transfer for monitoring cellular dynamics. Biotechnol Lett 28:1971–1982. doi: 10.1007/s10529-006-9193-5 CrossRefPubMedGoogle Scholar
  31. Li L, Li N, Song SF, Li YX, Xia XJ, Fu XQ, Chen GH, Deng HF (2014) Cloning and characterization of the drought-resistance OsRCI2-5 gene in rice (Oryza sativa L.). Genetics Mol Res 13:4022–4035. doi: 10.4238/2014.May.23.13 CrossRefGoogle Scholar
  32. Liu SH, Lee H, Kang PS, Huang XH, Yim JH, Lee HK, Kim IC (2010) Complementary DNA library construction and expressed sequence tag analysis of an Arctic moss, Aulacomnium turgidum. Polar Biol 33:617–626. doi: 10.1007/s00300-009-0737-8 CrossRefGoogle Scholar
  33. Liu B, Feng D, Zhang B, Mu P, Zhang Y, He Y, Qi K, Wang J, Wang H (2012) Musa paradisica RCI complements AtRCI and confers Na + tolerance and K +sensitivity in Arabidopsis. Plant Sci 184:102–111. doi: 10.1016/j.plantsci.2011.12.004 CrossRefPubMedGoogle Scholar
  34. Long R, Zhang F, Li Z, Li M, Cong L, Kang J, Zhang T, Zhao Z, Sun Y, Yang Q (2015) Isolation and functional characterization of salt-stress induced RCI2-like genes from Medicago sativa and Medicago truncatula. J Plant Res 128:697–707. doi: 10.1007/s10265-015-0715-x CrossRefPubMedGoogle Scholar
  35. Medina J, Catala R, Salinas J (2001) Developmental and stress regulation of RCI2A and RCI2B, two cold-inducible genes of Arabidopsis encoding highly conserved hydrophobic proteins. Plant Physiol 125:1655–1666. doi: 10.1104/pp.125.4.1655 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Medina J, Ballesteros M, Salinas J (2007) Phylogenetic and functional analysis of Arabidopsis RCI2 genes. J Exp Bot 58:4333–4346. doi: 10.1093/jxb/erm285 CrossRefPubMedGoogle Scholar
  37. Miller JP, Lo RS, Ben-Hur A, Desmarais C, Stagljar I, Noble WS, Fields S (2005) Large-scale identification of yeast integral membrane protein interactions. Proc Natl Acad Sci USA 102:12123–12128. doi: 10.1073/pnas.0505482102 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mitsuya S, Taniguchi M, Miyake H, Takabe T (2005) Disruption of RCI2A leads to over-accumulation of Na + and increased salt sensitivity in Arabidopsis thaliana plants. Planta 222:1001–1009. doi: 10.1007/s00425-005-0043-9 CrossRefPubMedGoogle Scholar
  39. Mitsuya S, Taniguchi M, Miyake H, Takabe T (2006) Overexpression of RC12A decreases Na + uptake and mitigates salinity-induced damages in Arabidopsis thaliana plants. Physiol Plant 128:95–102. doi: 10.1111/j.1399-3054.2006.00714.x CrossRefGoogle Scholar
  40. Morsy MR, Almutairi AM, Gibbons J, Yun SJ, de los Reyes BG (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180. doi: 10.1016/j.gene.2004.09.033 CrossRefPubMedGoogle Scholar
  41. Navarre C, Goffeau A (2000) Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J 19:2515–2524. doi: 10.1093/emboj/19.11.2515 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ndong C, Ouellet F, Houde M, Sarhan F (1997) Gene expression during cold acclimation in strawberry. Plant Cell Physiol 38:863–870CrossRefPubMedGoogle Scholar
  43. Nugent T, Jones DT (2012) Detecting pore-lining regions in transmembrane protein sequences. BMC Bioinformatics 13:169. doi: 10.1186/1471-2105-13-169 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nylander M, Heino P, Helenius E, Palva ET, Ronne H, Welin BV (2001) The low-temperature- and salt-induced RCI2A gene of Arabidopsis complements the sodium sensitivity caused by a deletion of the homologous yeast gene SNA1. Plant Mol Biol 45:341–352. doi: 10.1023/a:1006451914231 CrossRefPubMedGoogle Scholar
  45. Pokrzywa W, Guerriat B, Dodzian J, Morsomme P (2009) Dual sorting of the Saccharomyces cerevisiae vacuolar protein Sna4p. Eukaryot Cell 8:278–286. doi: 10.1128/ec.00363-08 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Reggiori F, Pelham HRB (2001) Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J 20:5176–5186. doi: 10.1093/emboj/20.18.5176 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nature Biotechnol 17:1030–1032. doi: 10.1038/13732 CrossRefGoogle Scholar
  48. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2:905–909. doi: 10.1038/nmeth819 CrossRefPubMedGoogle Scholar
  49. Sivankalyani V, Geetha M, Subramanyam K, Girija S (2015) Ectopic expression of Arabidopsis RCI2A gene contributes to cold tolerance in tomato. Transgenic Res 24:237–251. doi: 10.1007/s11248-014-9840-x CrossRefPubMedGoogle Scholar
  50. Stagljar I, Korostensky C, Johnsson N, te Heesen S (1998) A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc Natl Acad Sci USA 95:5187–5192. doi: 10.1073/pnas.95.9.5187 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Tamura K, Shimada T, Ono E, Tanaka Y, Nagatani A, Higashi S, Watanabe M, Nishimura M, Hara-Nishimura I (2003) Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J 35:545–555. doi: 10.1046/j.1365-313X.2003.01822.x CrossRefPubMedGoogle Scholar
  52. Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi WM, Takabe T, Bennett J (2004) Osmotic stress in barley regulates expression of a different set of genes than salt stress does. J Exp Bot 55:2213–2218. doi: 10.1093/jxb/erh242 CrossRefPubMedGoogle Scholar
  53. Ueda A, Kathiresan A, Bennett J, Takabe T (2006) Comparative transcriptome analyses of barley and rice under salt stress. Theor Appl Genet 112:1286–1294. doi: 10.1007/s00122-006-0231-4 CrossRefPubMedGoogle Scholar
  54. Van Zeebroeck G, Kimpe M, Vandormael P, Thevelein JM (2011) A split-ubiquitin two-hybrid screen for proteins physically interacting with the yeast amino acid transceptor Gap1 and ammonium transceptor Mep2. PLoS ONE. doi: 10.1371/journal.pone.0024275 PubMedPubMedCentralGoogle Scholar
  55. Viklund H, Elofsson A (2008) OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar. Bioinformatics 24:1662–1668. doi: 10.1093/bioinformatics/btn221 CrossRefPubMedGoogle Scholar
  56. Wang DH, Chen YQ, Wang Y, Wang ZZ (2013) Molecular cloning and expression of two plasma membrane protein 3 (SmPMP3) genes from Salvia miltiorrhiza. Russ J Plant Physiol 60:155–164. doi: 10.1134/s1021443712060179 CrossRefGoogle Scholar
  57. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE. doi: 10.1371/journal.pone.0000718 Google Scholar
  58. Xiang L, Etxeberria E, Van den Ende W (2013) Vacuolar protein sorting mechanisms in plants. FEBS J 280:979–993. doi: 10.1111/febs.12092 CrossRefPubMedGoogle Scholar
  59. Xu Y, Piston DW, Johnson CH (1999) A bioluminescence resonance energy transfer (BRET) system: Application to interacting circadian clock proteins. Proc Natl Acad Sci USA 96:151–156. doi: 10.1073/pnas.96.1.151 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139. doi: 10.1016/j.pbi.2014.07.009 CrossRefPubMedGoogle Scholar
  61. Zhang C-Q, Nishluchi S, Liu S, Takano T (2008) Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice. BMB Rep 41:448–454CrossRefGoogle Scholar
  62. Zhao Y, Tong H, Cai R, Peng X, Li X, Gan D, Zhu S (2014) Identification and characterization of the RCI2 gene family in maize (Zea mays). J Genetics 93:655–666. doi: 10.1007/s12041-014-0421-9 CrossRefGoogle Scholar
  63. Zouhar J, Rojo E (2009) Plant vacuoles: where did they come from and where are they heading? Curr Opin Plant Biol 12:677–684. doi: 10.1016/j.pbi.2009.08.004 CrossRefPubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Institute of Subtropical AgricultureChinese Academy of SciencesChangshaPeople’s Republic of China

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