Plant Cell Reports

, Volume 36, Issue 11, pp 1829–1839 | Cite as

An endoplasmic reticulum-localized Coffea arabica BURP domain-containing protein affects the response of transgenic Arabidopsis plants to diverse abiotic stresses

Original Article


Key message

The Coffea arabica BURP domain-containing gene plays an important role in the response of transgenic Arabidopsis plants to abiotic stresses via regulating the level of diverse proteins.


Although the functions of plant-specific BURP domain-containing proteins (BDP) have been determined for a few plants, their roles in the growth, development, and stress responses of most plant species, including coffee plant (Coffea arabica), are largely unknown. In this study, the function of a C. arabica BDP, designated CaBDP1, was investigated in transgenic Arabidopsis plants. The expression of CaBDP1 was highly modulated in coffee plants subjected to drought, cold, salt, or ABA. Confocal analysis of CaBDP1-GFP fusion proteins revealed that CaBDP1 is localized in the endoplasmic reticulum. The ectopic expression of CaBDP1 in Arabidopsis resulted in delayed germination of the transgenic plants under abiotic stress and in the presence of ABA. Cotyledon greening and seedling growth of the transgenic plants were inhibited in the presence of ABA due to the upregulation of ABA signaling-related genes like ABI3, ABI4, and ABI5. Proteome analysis revealed that the levels of several proteins are modulated in CaBDP1-expressing transgenic plants. The results of this study underscore the importance of BURP domain proteins in plant responses to diverse abiotic stresses.


Abiotic stress Arabidopsis thaliana BURP Coffea arabica Endoplasmic reticulum 



We thank Dr. Jung-Hyun Lee for technical assistance to grow coffee plants in a green house. This work was supported by a grant from the Next-Generation BioGreen21 Program (PJ01103601), Rural Development Administration, Republic of Korea.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Supplementary material

299_2017_2197_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1140 kb)


  1. Albertos P, Romero-Puertas MC, Tatematsu K, Mateos I, Sanchez-Vicente I, Nambara E et al (2015) S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat Commun 6:8669CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barsalobres-Cavallari CF, Severino FE, Maluf MP, Maia IG (2009) Identification of suitable internal control genes for expression studies in Coffea arabica under different experimental conditions. BMC Mol Biol 10:1CrossRefPubMedPubMedCentralGoogle Scholar
  3. Batchelor AK, Boutilier K, Miller SS, Hattori J, Bowman LA, Hu M et al (2002) SCB1, a BURP-domain protein gene, from developing soybean seed coats. Planta 215:523–532CrossRefPubMedGoogle Scholar
  4. Batista-Santos P, Lidon FC, Fortunato A, Leitao AE, Lopes E, Partelli F (2011) The impact of cold on photosynthesis in genotypes of Coffea spp.—photosystem sensitivity, photoprotective mechanisms and gene expression. J Plant Physiol 168:792–806CrossRefPubMedGoogle Scholar
  5. Baumlein H, Boerjan W, Nagy I, Bassuner R, Van Montagu M, Inze D et al (1991) A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Mol Gen Genet 225:459–467CrossRefPubMedGoogle Scholar
  6. Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266PubMedGoogle Scholar
  7. Boutilier KA, Gines MJ, DeMoor JM, Huang B, Baszczynski CL, Lyer VN et al (1994) Expression of the BnmNAP subfamily of napin genes coincides with the induction of Brassica microspore embryogenesis. Plant Mol Biol 26:1711–1723CrossRefPubMedGoogle Scholar
  8. Chang GG, Tong L (2003) Structure and function of malic enzymes, a new class of oxidative decarboxylases. Biochemistry 42:12721–12733CrossRefPubMedGoogle Scholar
  9. Chen Y, Brandizzi F (2013) Analysis of unfolded protein response in Arabidopsis. Methods Mol Biol 1043:73–80CrossRefPubMedPubMedCentralGoogle Scholar
  10. Choi MJ, Park YR, Park SJ, Kang H (2015) Stress-responsive expression patterns and functional characterization of cold shock domain proteins in cabbage (Brassica rapa) under abiotic stress conditions. Plant Physiol Biochem 96:132–140CrossRefPubMedGoogle Scholar
  11. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679CrossRefPubMedGoogle Scholar
  12. DaMatta FM, Ramalho JDC (2006) Impacts of drought and temperature stress on coffee physiology and production. Brazi J Plant Physiol 18:55–81CrossRefGoogle Scholar
  13. Ding X, Hou X, Xie K, Xiong L (2009) Genome-wide identification of BURP domain-containing genes in rice reveals a gene family with diverse structures and responses to abiotic stresses. Planta 230:149–163CrossRefPubMedGoogle Scholar
  14. 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 80:654–668CrossRefPubMedGoogle Scholar
  15. Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166CrossRefPubMedPubMedCentralGoogle Scholar
  16. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609CrossRefPubMedPubMedCentralGoogle Scholar
  17. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054PubMedPubMedCentralGoogle Scholar
  18. Fuentes D, Meneses M, Nunes-Nesi A, Araújo WL, Tapia R, Gómez I et al (2011) A deficiency in the flavoprotein of Arabidopsis mitochondrial complex II results in elevated photosynthesis and better growth in nitrogen-limiting conditions. Plant Physiol 157:1114–1127CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fujiwara T, Nambara E, Yamagishi K, Goto DB, Naito S (2002) Storage protein. Arabidopsis Book 1:e0020CrossRefPubMedPubMedCentralGoogle Scholar
  20. Galka MM, Rajagopalan N, Buhrow LM, Nelson KM, Switala J, Cutler AJ et al (2015) Identification of interactions between abscisic acid and ribulose-1,5-bisphosphate carboxylase/oxygenase. PLoS ONE 10:e0133033CrossRefPubMedPubMedCentralGoogle Scholar
  21. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gu L, Jung HJ, Kwak KJ, Nguyen Dinh S, Kim YO, Kang H (2016) An RRM-containing mei2-like MCT1 plays a negative role in the seed germination and seedling growth of Arabidopsis thaliana in the presence of ABA. Plant Physiol Biochem 109:273–279CrossRefPubMedGoogle Scholar
  23. Guzzo SD, Harakava R, Tsai SM (2009) Identification of coffee genes expressed during systemic acquired resistance and incompatible with Hemileia vastatrix. J Phytopathol 157:625–638CrossRefGoogle Scholar
  24. Harshavardhan VT, Van Son L, Seiler C, Junker A, Weigelt-Fischer K, Klukas C et al (2014) AtRD22 and AtUSPL1, members of the plant-specific BURP domain family involved in Arabidopsis thaliana drought tolerance. PLoS ONE 9:e110065CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hattori J, Boutilier KA, van Lookeren CMM, Miki BL (1998) A conserved BURP domain defines a novel group of plant proteins with unusual primary structures. Mol Gen Genet 259:424–428CrossRefPubMedGoogle Scholar
  26. ICO Annual Review 2012/13. ISSN 1473-3331, 1-36Google Scholar
  27. Jiang T, Zhang XF, Wang XF, Zhang DP (2011) Arabidopsis 3-ketoacyl-coa thiolase-2 (KAT2), an enzyme of fatty acid β-oxidation, is involved in ABA signal transduction. Plant Cell Physiol 52:528–538CrossRefPubMedGoogle Scholar
  28. Jung JH, Kim H, Go YS, Lee SB, Hur CG, Kim HU et al (2011) Identification of functional BrFAD2-1 gene encoding microsomal delta-12 fatty acid desaturase from Brassica rapa and development of Brassica napus containing high oleic acid contents. Plant Cell Rep 30:1881–1892CrossRefPubMedGoogle Scholar
  29. Jung HJ, Kim MK, Kang H (2013) An ABA-regulated putative RNA-binding protein affects seed germination of Arabidopsis under ABA or abiotic stress conditions. J Plant Physiol 170:179–184CrossRefPubMedGoogle Scholar
  30. Kang BS, Baek JH, Macoy DM, Chakraborty R, Cha J-Y, Hwang D-Y et al (2015) N-glycosylation process in both ER and Golgi plays pivotal role in plant immunity. J Plant Biol 58:374–382CrossRefGoogle Scholar
  31. Kim YO, Kang H (2006) The role of a zinc finger-containing glycine rich RNA-binding protein during the cold adaptation process in Arabidopsis thaliana. Plant Cell Physiol 47:793–798CrossRefPubMedGoogle Scholar
  32. Kim YO, Pan O, Jung CH, Kang H (2007) A zinc finger-containing glycine-rich RNA-binding protein, AtRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions. Plant Cell Physiol 48:1170–1181CrossRefPubMedGoogle Scholar
  33. Kramer D, Breitenstein B, Kleinwächter M, Selmar D (2010) Stress metabolism in green coffee bean (Coffea arabica L.): expression of dehydrins and accumulation of GABA during drying. Plant Cell Physiol 5:546–553CrossRefGoogle Scholar
  34. Laporte MM, Shen B, Tarczynski MC (2002) Engineering for drought avoidance: expression of maize NADP-malic enzyme in tobacco results in altered stomatal function. J Exp Bot 53:699–705CrossRefPubMedGoogle Scholar
  35. Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lopez-Molina L, Chua NH (2000) A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol 41:541–547CrossRefPubMedGoogle Scholar
  37. Marraccini P, Freire LP, Alves GSC, Vieira NG, Vinecky F, Elbelt S et al (2011) RBCS1 expression in coffee: coffea orthologs, Coffea arabica homeologs, and expression variability between genotypes and under drought stress. BMC Plant Biol 11:85CrossRefPubMedPubMedCentralGoogle Scholar
  38. Matus JT, Aquea F, Espinoza C, Vega A, Cavallini E, Santo SD et al (2014) Inspection of the grapevine BURP superfamily highlights an expansion of RD22 genes with distinctive expression features in berry development and ABA-mediated stress responses. PLoS ONE 9:e110372CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mishra MK, Slater A (2012) Recent advances in the genetic transformation of coffee. Biotechnol Res Internat 2012:580857CrossRefGoogle Scholar
  40. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nguyen Dinh S, Sai TZT, Nawaz G, Lee K, Kang H (2016) Abiotic stresses affect differently the intron splicing and expression of chloroplast genes in coffee plants (Coffea arabica) and rice (Oryza sativa). J Plant Physiol 201:85–94CrossRefPubMedGoogle Scholar
  42. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Deleseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 61:1567–1582CrossRefGoogle Scholar
  43. Park J, Cui Y, Kang BH (2015) AtPGL3 is an Arabidopsis BURP domain protein that is localized to the cell wall and promotes cell enlargement. Frontier Plant Sci 6:412Google Scholar
  44. Partelli FL, Vieira HD, Viana AP, Batista-Santos P, Rodrigues AP, Leião AE et al (2009) Low temperature impact on photosynthetic parameters in coffee genotypes. Pesq Agropec Brasília 44:1404–1415CrossRefGoogle Scholar
  45. Pattison RJ, Amtmann A (2009) N-glycan production in the endoplasmic reticulum of plants. Trends Plant Sci 14:92–99CrossRefPubMedGoogle Scholar
  46. Reeves WM, Lynch TJ, Mobin R, Finkelstein RR (2011) Direct targets of the transcription factors ABA-Insensitive (ABI4 and ABI5) reveal synergistic action by ABI4 and several bZIP ABA response factors. Plant Mol Biol 75:347–363CrossRefPubMedPubMedCentralGoogle Scholar
  47. Santos AB, Mazzafera P (2012) Dehydrins are highly expressed in water-stressed plants of two coffee species. Tropical Plant Biol 5:218–232CrossRefGoogle Scholar
  48. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025CrossRefPubMedGoogle Scholar
  49. Tang Y, Cao Y, Qiu J, Gao Z, Ou Z, Wang Y et al (2014) Expression of a vacuole-localized BURP-domain protein from soybean (SALI3-2) enhances tolerance to cadmium and copper stresses. PLoS ONE 9:e98830CrossRefPubMedPubMedCentralGoogle Scholar
  50. Teerawanichpan P, Xia Q, Caldwell SJ, Datla R, Selvaraj G (2009) Protein storage vacuoles of Brassica napus zygotic embryos accumulate a BURP domain protein and perturbation of its production distorts the PSV. Plant Mol Biol 71:331–343CrossRefPubMedGoogle Scholar
  51. Treacy BK, Hattori J, Prudhomme I, Barbour E, Boutilier K, Baszczynski CL et al (1997) Bnm1, a Brassica pollen-specific gene. Plant Mol Biol 34:603–611CrossRefPubMedGoogle Scholar
  52. Van Son L, Tiedemann J, Rutten T, Hillmer S, Hinz G, Zank T et al (2009) The BURP domain protein AtUSPL1 of Arabidopsis thaliana is destined to the protein storage vacuoles and overexpression of the cognate gene distorts seed development. Plant Mol Biol 71:319–329CrossRefPubMedGoogle Scholar
  53. Vitale A, Denecke J (1999) The endoplasmic reticulum-gateway to the secretory pathway. Plant Cell 11:615–628PubMedPubMedCentralGoogle Scholar
  54. Vitale A, Ceriotti A, Denecke J (1993) The role of the endoplasmic reticulum in protein synthesis, modification and intracellular transport. J Exp Bot 44:1417–1444CrossRefGoogle Scholar
  55. Wang HM, Zhou L, Fu YP, Cheung MY, Wong FL, Phang TH et al (2012) Expression of an apoplast-localized BURP-domain protein from soybean (GmRD22) enhances tolerance towards abiotic stress. Plant, Cell Environ 35:1932–1947CrossRefGoogle Scholar
  56. Watson CF, Zheng L, DellaPenna D (1994) Reduction of tomato polygalacturonase beta subunit expression affects pectin solubilization and degradation during fruit ripening. Plant Cell 6:1623–1634PubMedPubMedCentralGoogle Scholar
  57. Xu H, Li Y, Yan Y, Wang K, Gao Y, Hu Y (2010) Genome scale identification of soybean BURP domain-containing genes and their expression under stress treatments. BMC Plant Biol 10:197CrossRefPubMedPubMedCentralGoogle Scholar
  58. Xu ZY, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y et al (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199CrossRefPubMedPubMedCentralGoogle Scholar
  59. Xu T, Gu L, Choi MJ, Kim RJ, Suh MC, Kang H (2014a) Comparative functional analysis of wheat (Triticum aestivum) zinc finger-containing glycine-rich RNA-binding proteins in response to abiotic stresses. PLoS ONE 9:e96877CrossRefPubMedPubMedCentralGoogle Scholar
  60. Xu T, Sy ND, Lee HJ, Kwak KJ, Gu L, Kim JI et al (2014b) Functional characterization of a chloroplast-targeted RNA-binding protein CRP1 in Arabidopsis thaliana under abiotic stress conditions. J Plant Biol 57:349–356CrossRefGoogle Scholar
  61. 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 21:133–139CrossRefPubMedGoogle Scholar
  62. Zheng L, Heupel RC, DellaPenna D (1992) The β-subunit of tomato fruit polygalacturonase isoenzyme 1: isolation, characterization, and identification of unique structural features. Plant Cell 4:1147–1156PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Plant Biotechnology, College of Agriculture and Life SciencesChonnam National UniversityGwangjuKorea
  2. 2.Institute of Environment and BiotechnologyTaynguyen UniversityBuon Ma ThuotVietnam

Personalised recommendations