Development and cell death domain-containing asparagine-rich protein (DCD/NRP): an essential protein in plant development and stress responses

  • Luiz Fernando de Camargos
  • Otto Teixeira Fraga
  • Celio Cabral Oliveira
  • Jose Cleydson Ferreira da Silva
  • Elizabeth Pacheco Batista Fontes
  • Pedro Augusto Braga ReisEmail author


Plants have evolved intriguing mechanisms to cope with environmental changes and developmental signals. These mechanisms are responsible for modulating the global gene expression in the cell and promoting a precise adjustment. The signaling pathways do not operate separately but display a complex network implicating the whole cell. The development and cell death (DCD) domain-containing asparagine-rich protein (NRP) plays a role in different stresses and developmental conditions; thereby, is considered an essential gene for plant adaptation and growth. The molecular functions of DCD/NRPs are not well characterized; however, they have been shown to be differentially expressed upon abiotic, biotic and developmental conditions. The evolution of omics approaches has generated data, which can be used to understand the function of NRPs and how they operate in different pathways. Using microarray and co-expression data, we identified that the expression of DCD/NRPs is strongly related to ER stress, ABA signaling, and the heterotrimeric G protein signaling. Interestingly, the involved pathways are also associated with plant development. Thus, NRPs may be a key factor in stress and developmental signaling.


NRPs UPR G signaling ABA Cell death response Osmotic stress 



This work was supported by FUNARBE and the Brazilian Government Agencies CNPq, FAPEMIG, and FINEP. L.F.C. is supported by CNPq, C.C.O. is supported by CAPES, O.T.F.N is supported by FAPEMIG graduate fellowships.


  1. Aalto MK, Helenius E, Kariola T, Pennanen V, Heino P, Hõrak H et al (2012) ERD15—an attenuator of plant ABA responses and stomatal aperture. Plant Sci 182:19–28. CrossRefGoogle Scholar
  2. Alves MS, Reis PA, Dadalto SP, Faria JA, Fontes EP, Fietto LG (2011) A novel transcription factor, ERD15 (early responsive to dehydration 15), connects endoplasmic reticulum stress with an osmotic stress-induced cell death signal. J Biol Chem 286:20020–20030. CrossRefGoogle Scholar
  3. Alvim FC, Carolino SMB, Cascardo JCM, Nunes CC, Martinez CA, Otoni WC, Fontes EPB (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126:1042–1054. CrossRefGoogle Scholar
  4. Bao Y, Howell SH (2017) The unfolded protein response supports plant development and defense as well as responses to abiotic stress. Front Plant Sci. 8:344. Google Scholar
  5. Belda-Palazon B, Rodriguez L, Fernandez MA, Castillo MC, Anderson EA, Gao C, Gonzalez-Guzman M, Peirats-Llobet M, Zhao Q, De Winne N et al (2016) FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. Plant Cell 10:e1004243. Google Scholar
  6. Bueso E, Rodriguez L, Lorenzo-Orts L, Gonzalez-Guzman M, Sayas E, Muñoz-Bertomeu J, Rodriguez PL et al (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 80:1057–1071. CrossRefGoogle Scholar
  7. Carvalho HH, Brustolini OJB, Pimenta MR, Mendes GC, Gouveia BC, Silva PA, Silva JCF, Mota CS, Soares-Ramos JRL, Fontes EPB (2014a) The molecular chaperone binding protein BiP prevents leaf dehydration-induced cellular homeostasis disruption. PLoS ONE 9:e86661. CrossRefGoogle Scholar
  8. Carvalho HH, Silva PA, Mendes GC, Brustolini OJB, Pimenta MR, Gouveia BC et al (2014b) The endoplasmic reticulum binding protein BiP displays dual function in modulating cell death events. Plant Physiol 164:654–670. CrossRefGoogle Scholar
  9. Cascardo JCM, Almeida RS, Buzeli RAA, Carolino SMB, Otoni WC, Fontes EPB (2000) The phosphorylation state and expression of soybean BiP isoforms are differentially regulated following abiotic stresses. J Biol Chem 275:14494–14500. CrossRefGoogle Scholar
  10. Chakravorty D, Gookin TE, Milner M, Yu Y, Assmann SM (2015) Extra-large G proteins (XLGs) expand the repertoire of subunits in Arabidopsis heterotrimeric G protein signaling. Plant Physiol. Google Scholar
  11. Chen Y, Brandizzi F (2012) AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis. Plant J 69:266–277. CrossRefGoogle Scholar
  12. Chen Y, Ji F, Xie H, Liang J (2006) Overexpression of the regulator of G-protein signalling protein enhances ABA-mediated inhibition of root elongation and drought tolerance in Arabidopsis. J Exp Bot 57:2101–2110CrossRefGoogle Scholar
  13. Cho Y, Yu CY, Iwasa T, Kanehara K (2015) Heterotrimeric G protein subunits differentially respond to endoplasmic reticulum stress in Arabidopsis. Plant Signal Behav 10:e1061162. CrossRefGoogle Scholar
  14. Colaneri AC, Tunc-Ozdemir M, Huang JP, Jones AM (2014) Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex. BMC Plant Biol 14:129. CrossRefGoogle Scholar
  15. Costa MDL, Reis PAB, Valente MAS, Irsigler AST, Carvalho CM, Loureiro ME et al (2008) A new branch of endoplasmic reticulum stress signaling and the osmotic signal converge on plant-specific asparagine-rich proteins to promote cell death. J Biol Chem 283:20209–20219. CrossRefGoogle Scholar
  16. Dai Q, Xue Q, McCray T, Margavage K, Chen F, Lee H, Nezames D, Guo Q, Terzaghi W, Wan JM et al (2013) The PP6 phosphatase regulates ABI5 phosphorylation and abscisic acid signaling in Arabidopsis. Plant Cell 25:517–534CrossRefGoogle Scholar
  17. Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108:7247–7252. CrossRefGoogle Scholar
  18. Deng Y, Srivastava R, Howell SH (2013) Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis. Proc Natl Acad Sci USA 110:19633–19638. CrossRefGoogle Scholar
  19. Deng Y, Srivastava R, Quilichini TD, Dong H, Bao Y, Horner HT, Howell SH (2016) IRE 1, a component of the unfolded protein response signaling pathway, protects pollen development in Arabidopsis from heat stress. Plant J. 88:193–204. CrossRefGoogle Scholar
  20. Ding L, Pandey S, Assmann SM (2008) Arabidopsis extra-large G proteins (XLGs) regulate root morphogenesis. Plant J 53:248–263. CrossRefGoogle Scholar
  21. Faria JAQA, Reis PAB, Reis MTB, Rosado GL, Pinheiro GL, Mendes GC, Fontes EPB (2011) The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress and osmotic stress-induced NRP-mediated cell-death signaling pathway. BMC Plant Biol 11:129. CrossRefGoogle Scholar
  22. Finkelstein R, Lynch J (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609. CrossRefGoogle Scholar
  23. Gao H, Brandizzi F, Benning C, Larkin RM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA. 105:16398–16403. CrossRefGoogle Scholar
  24. Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8:404–408. CrossRefGoogle Scholar
  25. Hendershot LM (2004) The ER function BiP is a master regulator of ER function. Mt Sinai J Med 71:289–297Google Scholar
  26. Hoepflinger MC, Pieslinger AM, Tenhaken R (2011) Investigations on N-rich protein (NRP) of Arabidopsis thaliana under different stress conditions. Plant Physiol Biochem 49:293–302. CrossRefGoogle Scholar
  27. Hollien J (2013) Evolution of the unfolded protein response. Biochim Biophys Acta Mol Cell Res 1833:2458–2463. CrossRefGoogle Scholar
  28. Irsigler AST, Costa MDB, Zhang P, Reis PAB, Dewey RE, Boston RS, Fontes EPB (2007) Expression profiling on soybean leaves reveals integration of ER–and osmotic-stress pathways. BMC Genom 8:431CrossRefGoogle Scholar
  29. Iwata Y, Ashida M, Hasegawa C, Tabara K, Mishiba KI, Koizumi N (2017) Activation of the Arabidopsis membrane-bound transcription factor bZIP28 is mediated by site-2 protease, but not site-1 protease. Plant J 91:408–415. CrossRefGoogle Scholar
  30. Johnston CA, Taylor JP, Gao Y, Kimple AJ, Grigston JC, Chen JG et al (2007) GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling. Proc Natl Acad Sci USA 104:17317–17322. CrossRefGoogle Scholar
  31. Kim JS, Yamaguchi-Shinozaki K, Shinozaki K (2018) ER-anchored transcription factors bZIP17 and bZIP28 regulate root elongation. Plant Physiol 1:01414. Google Scholar
  32. Koizumi N, Martinez IM, Kimata Y, Kohno K, Sano H, Chrispeels MJ (2001) Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. Plant Physiol 127:949–962. CrossRefGoogle Scholar
  33. Kundu S, Gantait S (2017) Abscisic acid signal crosstalk during abiotic stress response. Plant Gene 11:61–69. CrossRefGoogle Scholar
  34. Liang Y, Gao Y, Jones AM (2017) Extra large G-protein interactome reveals multiple stress response function and partner-dependent XLG subcellular localization. Front Plant Sci 8:1015. CrossRefGoogle Scholar
  35. Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942. CrossRefGoogle Scholar
  36. Liu X, Stone L (2013) Cytoplasmic degradation of the Arabidopsis transcription factor ABSCISIC ACID INSENSITIVE 5 is mediated by the RING-type E3 ligase KEEP on GOING. J Biol Chem 288:20267–20279. CrossRefGoogle Scholar
  37. Liu JX, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909. CrossRefGoogle Scholar
  38. Ludwig AA, Tenhaken R (2001) A new cell wall located N-rich protein is strongly induced during the hypersensitive response in Glycine max L. Eur J Plant Pathol 107:323–336. CrossRefGoogle Scholar
  39. Malhotra JD, Kaufman RJ (2007) The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18:716–731. CrossRefGoogle Scholar
  40. Maruta N, Trusov Y, Brenyah E, Parekh U, Botella JR (2015) Membrane-localized extra-large G-proteins and Gβγ of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol 56:114. Google Scholar
  41. Mendes GC, Reis PAB, Calil IP, Carvalho HH, Aragão FJL, Fontes EPB (2013) GmNAC30 and GmNAC81NAC081 integrate the endoplasmic reticulum stress- and osmotic stress-induced cell death responses through a vacuolar processing enzyme. Proc Natl Acad Sci USA. 110:19627–19632. CrossRefGoogle Scholar
  42. Nagashima Y, Mishiba K, Suzuki E, Shimada Y, Iwata Y, Koizumi N (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1:29. CrossRefGoogle Scholar
  43. Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T et al (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363. CrossRefGoogle Scholar
  44. Pimenta MR, Silva PA, Mendes GC, Alves JR, Caetano HDN, Machado JPB, Brustolini OJB, Carpinetti PA, Melo BP, Silva JCF, Rosado GL, Ferreira MFF, Costa MDBL, Picoli EAT, Aragao FJL, Ramos HJO, Fontes EPB (2016) The stress-induced soybean NAC transcription factor GmNAC81 plays a positive role in developmentally programmed leaf senescence. Plant Cell Physiol 57:1098–1114. CrossRefGoogle Scholar
  45. Reis PAB, Fontes EPB (2012) N-rich protein (NRP)-mediated cell death signaling: a new branch of the ER stress response with implications for plant biotechnology. Plant Signal Behav 7:628–632. CrossRefGoogle Scholar
  46. Reis PAA, Rosado GL, Silva LAC, Oliveira LC, Oliveira LB, Costa MDBL, Alvim C, Fontes EPB (2011) The binding protein BiP attenuates stress-induced cell death in soybean via modulation of the N-rich. Plant Physiol 157:1853–1865. CrossRefGoogle Scholar
  47. Reis PAB, Carpinetti PA, Freitas PPJ, Santos EGD, Camargos LF, Oliveira IHT, Silva JCF, Carvalho HH, Costa DBM, Soares-Ramos JRL, Fontes EPB (2016) Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants. BMC Plant Biol 16:19CrossRefGoogle Scholar
  48. Ruberti C, Kim SJ, Stefano G, Brandizzi F (2015) Unfolded protein response in plants: one master, many questions. Curr Opin Plant Biol 27:59–66. CrossRefGoogle Scholar
  49. Song L, Huang SSC, Wise A, Castanon R, Nery JR, Chen H, Watanabe M, Thomas J, Bar-Joseph Z, Ecker JR (2016) A transcription factor hierarchy defines an environmental stress response network. Science 354:p.aag1550. CrossRefGoogle Scholar
  50. Srivastava R, Deng Y, Shah S, Rao AG, Howell SH (2013) BINDING PROTEIN is a master regulator of the endoplasmic reticulum stress sensor/transducer bZIP28 in Arabidopsis. Plant Cell 25:1416–1429. CrossRefGoogle Scholar
  51. Staehelin LA (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11:1151–1165. CrossRefGoogle Scholar
  52. Sun L, Yang ZT, Song ZT, Wang MJ, Sun L, Lu SJ, Liu JX (2013) The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J 76:274–286. Google Scholar
  53. Sun L, Zhang SS, Lu SJ, Liu JX (2015) Site-1 protease cleavage site is important for the ER stress-induced activation of membrane-associated transcription factor bZIP28 in Arabidopsis. Sci China Life Sci 58:270–275. CrossRefGoogle Scholar
  54. Tenhaken R, Doerks T, Bork P (2005) DCD—a novel plant specific domain in proteins involved in development and programmed cell death. BMC Bioinform 6:169. CrossRefGoogle Scholar
  55. Tunc-Ozdemir M, Urano D, Jaiswal DK, Clouse SD, Jones AM (2016) Direct modulation of a heterotrimeric G protein-coupled signaling by a receptor kinase complex. J Biol Chem. Google Scholar
  56. Tunc-Ozdemir M, Li B, Jaiswal DK, Urano D, Jones AM, Torres MP (2017) Predicted functional implications of phosphorylation of regulator of G protein signaling protein in plants. Front Plant Sci 8:1456. CrossRefGoogle Scholar
  57. Urano D, Chen JG, Botella JR, Jones AM (2013) Heterotrimeric G protein signalling in the plant kingdom. Open Biol 3:120186. CrossRefGoogle Scholar
  58. Urano D, Maruta N, Trusov Y, Stoian R, Wu Q, Liang Y, Jones AM et al (2016) Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom. Sci Signal 9:ra-93. CrossRefGoogle Scholar
  59. Valente MAS, Faria JAQA, Ramos JRLS, Reis PAB, Pinheiro GL, Piovesan ND et al (2009) The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco. J Exp Bot 60:533–546. CrossRefGoogle Scholar
  60. Vitale A, Denecke J (1999) The endoplasmic reticulum: gateway of the secretory pathway. Plant Cell 11:615–628. Google Scholar
  61. Wang D, Gao Z, Du P, Xiao W, Tan Q, Chen X, Li L, Gao D (2016) Expression of ABA metabolism-related genes suggests similarities and differences between seed dormancy and bud dormancy of peach (Prunus persica). Front Plant Sci 6:1248. Google Scholar
  62. Xu DB, Chen M, Ma YN, Xu ZS, Li LC, Chen YF, Ma YZ (2015) A G-protein β subunit, AGB1, negatively regulates the ABA response and drought tolerance by down-regulating AtMPK6-related pathway in Arabidopsis. PLoS ONE 10:e0116385CrossRefGoogle Scholar
  63. Yang ZT, Lu SJ, Wang MJ, Bi DL, Sun L, Zhou SF, Song ZT, Liu JX (2014a) A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis. Plant J 79:1033–1043. CrossRefGoogle Scholar
  64. Yang Z-T, Wang M-J, Sun L, Lu S-J, Bi D-L, Sun L, Song Z-T, Zhang S-S, Zhou S-F, Liu J-X (2014b) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet 10:e1004243. CrossRefGoogle Scholar
  65. Yu F, Xie Q (2017) Non-26S proteasome endomembrane trafficking pathways in ABA signaling. Trends Plant Sci 22:976–985. CrossRefGoogle Scholar
  66. Zhou R, Zhu T, Han L, Liu M, Xu M, Liu Y et al (2017) The asparagine-rich protein NRP interacts with the Verticillium effector PevD1 and regulates the subcellular localization of cryptochrome 2. J Exp Bot 68:3427–3440. CrossRefGoogle Scholar
  67. Zhu T, Wu Y, Yang X, Chen W, Gon Q, Liu X (2018) The asparagine-rich protein NRP facilitates the degradation of the PP6-type phosphatase FyPP3 to promote ABA response in Arabidopsis. Mol Plant 11:257–268. CrossRefGoogle Scholar

Copyright information

© Brazilian Society of Plant Physiology 2018

Authors and Affiliations

  • Luiz Fernando de Camargos
    • 1
    • 2
  • Otto Teixeira Fraga
    • 1
    • 2
  • Celio Cabral Oliveira
    • 1
    • 2
  • Jose Cleydson Ferreira da Silva
    • 1
    • 2
  • Elizabeth Pacheco Batista Fontes
    • 1
    • 2
  • Pedro Augusto Braga Reis
    • 1
    • 2
    Email author
  1. 1.Departamento de Bioquímica e Biologia MolecularUniversidade Federal de ViçosaViçosaBrazil
  2. 2.National Institute of Science and Technology in Plant-Pest Interactions, BioagroUniversidade Federal de ViçosaViçosaBrazil

Personalised recommendations