3 Biotech

, 9:176 | Cite as

Matrix attachment regions as a tool to influence plant transgene expression

  • Anna Sergeevna DolgovaEmail author
  • Sergey Vladimirovich Dolgov
Review Article


The inclusion of special regulatory sequences known as matrix attachment regions (MARs) in transgene constructs has been suggested as a possible approach to stabilise the expression of foreign heterological genes. The present review provides a brief summary regarding the MARs that have been used in investigations studying their influence on plant transgene expression in different plants with different promoters and reporter genes, and the comparison of these investigations.


Transgenic plant Matrix attachment regions MAR Transgene expression 



This study was supported by the Russian Science Foundation Grant #17-75-10093.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.


  1. Able JA, Rathus CO, Carroll BJ, Godwin ID (2004) Enhancing transgene expression levels in sorghum: current status and future goals. In: Seetharama N, Godwin ID (eds) Sorghum tissue culture and transformation. Oxford Publishers, New Delhi, pp 85–96Google Scholar
  2. Abranches R, Shultz RW, Thompson WF, Allen GC (2005) Matrix attachment regions and regulated transcription increase and stabilize transgene expression. Plant Biotechnol J 3:535–543. CrossRefPubMedGoogle Scholar
  3. Allen GC, Hall GE Jr, Childs LC, Weissinger AK, Spiker S, Thompson WF (1993) Scaffold attachment regions increase reporter gene expression in stably transformed plant cells. Plant Cell 5:603–613CrossRefGoogle Scholar
  4. Allen GC, Hall G Jr, Michalowski S, Newman W, Spiker S, Weissinger AK, Thompson WF (1996) High-level transgene expression in plant cells: effects of a strong scaffold attachment region from tobacco. Plant Cell 8:899–913CrossRefGoogle Scholar
  5. Bennet J (1993) Genes for crop improvement. In: Setlow JK (ed) Genetic engineering, vol 15. Plenum, New York, pp 165–189CrossRefGoogle Scholar
  6. Bhat SR, Srinivasan S (2002) Molecular and genetic analyses of transgenic plants: considerations and approaches. Plant Sci 164:673–681CrossRefGoogle Scholar
  7. Birch RG (1997) Plant transformation: problems and strategies for practical application. Annu Rev Plant Physiol Plant Mol Biol 48:297–326CrossRefGoogle Scholar
  8. Breyne P, Van Montagu M, Depicker A, Gheysen G (1992) Characterization of a plant scaffold attachment region in a DNA fragment that normalizes transgene expression in tobacco. Plant Cell 4:463–471CrossRefGoogle Scholar
  9. Brouwer C, Bruce W, Maddock S, Avramova Z, Bowen B (2002) Suppression of transgene silencing by matrix attachment regions in maize: a dual role for the maize 5′ ADH1 matrix attachment region. Plant Cell 14:2251–2264CrossRefGoogle Scholar
  10. Buising CM, Benbow RM (1994) Molecular analysis of transgenic plants generated by microprojectile bombardment: effect of petunia transformation booster sequence. Mol Gen Genet 243:71–81CrossRefGoogle Scholar
  11. Butaye K, Goderis I, Wouters P, Pues J, Delauré S, Broekaert W, Depicker A, Cammue B, De Bolle M (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J 39:440–449CrossRefGoogle Scholar
  12. Cheng Z, Targolli J, Wu R (2001) Tobacco matrix attachment region sequence increased transgene expression levels in rice plants. Mol Breed 7:317–327CrossRefGoogle Scholar
  13. Conkling MA, Cheng C-L, Yamamoto YT, Goodman HM (1990) lsolation of transcriptionally regulated root-specific genes from tobacco. Plant Physiol 93:1203–1211CrossRefGoogle Scholar
  14. De Bolle MFC, Butaye KMJ, Coucke WJW, Goderis IJWM, Wouters PFJ, van Boxel N, Broekaert WF, Cammue BPA (2003) Analysis of the influence of promoter elements and a matrix attachment region on the inter-individual variation of transgene expression in populations of Arabidopsis thaliana. Plant Sci 165:169–179CrossRefGoogle Scholar
  15. De Bolle MF, Butaye KM, Goderis IJ, Wouters PF, Jacobs A, Delauré SL, Depicker A, Cammue BP (2007) The influence of matrix attachment regions on transgene expression in Arabidopsis thaliana wild type and gene silencing mutants. Plant Mol Biol 634:533–543CrossRefGoogle Scholar
  16. Depicker A, Stachel S, Dhaese P, Zambryski P, Goodman HM (1982) Nopaline synthase: transcript mapping and DNA sequence. J Mol Appl Genet 1:561–573PubMedGoogle Scholar
  17. Diamos AG, Mason HS (2018) Chimeric 3′ flanking regions strongly enhance gene expression in plants. Plant Biotechnol J. [Epub ahead of print] CrossRefPubMedPubMedCentralGoogle Scholar
  18. Diamos AG, Rosenthal SH, Mason HS (2016) 5′ and 3′ untranslated regions strongly enhance performance of geminiviral replicons in Nicotiana benthamiana Leaves. Front Plant Sci 7:200. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dietz-Pfeilstetter A, Arndt N, Manske U (2016) Effects of a petunia scaffold/matrix attachment region on copy number dependency and stability of transgene expression in Nicotiana tabacum. Transgenic Res 25(2):149–162. CrossRefPubMedGoogle Scholar
  20. Dolgova AS, Dolgov SV, Nazipova NN, Maksimenko OG, Georgiev PG (2015) Arabidopsis termination elements increase transgene expression in tobacco plants. Plant Cell Tissue Organ Cult 120(3):1107–1116. CrossRefGoogle Scholar
  21. Elmayan T, Vaucheret H (1996) Expression of single copies of a strongly expressed 35S transgene can be silenced posttranscriptionally. Plant J 9:787–797CrossRefGoogle Scholar
  22. Festa M, Brun P, Piccinini R, Castagliuolo I, Basso B, Zecconi A (2013) Staphylococcus aureus Efb protein expression in Nicotiana tabacum and immune response to oral administration. Res Vet Sci 94(3):484–489. CrossRefPubMedGoogle Scholar
  23. Fukuda Y, Nishikawa S (2003) Matrix attachment regions enhance transcription of a downstream transgene and the accessibility of its promoter region to micrococcal nuclease. Plant Mol Biol 51:665–675CrossRefGoogle Scholar
  24. Galliano H, Müller AE, Lucht JM, Meyer P (1995) The transformation booster sequence from Petunia hybrida is a retrotransposon derivative that binds to the nuclear scaffold. Mol Gen Genet 247:614–622. CrossRefPubMedGoogle Scholar
  25. Halweg C, Thompson WF, Spiker S (2005) The Rb7 matrix attachment region increases the likelihood and magnitude of transgene expression in tobacco cells: a flow cytometric study. Plant Cell 17:418–429CrossRefGoogle Scholar
  26. Han KH, Ma C, Strauss SH (1997) Matrix attachment regions (MARs) enhance transformation frequency and transgene expression in poplar. Transgenic Res 6:415–420CrossRefGoogle Scholar
  27. Hily JM, Singer SD, Yang Y, Liu Z (2009) A transformation booster sequence (TBS) from Petunia hybrida functions as an enhancer-blocking insulator in Arabidopsis thaliana. Plant Cell Rep 28(7):1095–1104. CrossRefPubMedGoogle Scholar
  28. Hobbs SLA, Warketin TD, DeLong CMO (1993) Transgene copy number can be positively or negatively associated with transgene expression. Plant Mol Biol 21:17–26CrossRefGoogle Scholar
  29. Holmes-Davis R, Comai L (2002) The matrix attachment regions (MARs) associated with the Heat Shock Cognate 80 gene (HSC80) of tomato represent specific regulatory elements. Mol Genet Genom 266:891–898CrossRefGoogle Scholar
  30. Holmes-Davis R, Luca C (1998) Nuclear matrix attachment regions and plant gene expression. Trends Plant Sci 3(3):91–97CrossRefGoogle Scholar
  31. Ji L, Xu R, Lu L, Zhang J, Yang G, Huang J, Wu C, Zheng C (2013) TM6, a novel nuclear matrix attachment region, enhances its flanking gene expression through influencing their chromatin structure. Mol Cells 36(2):127–137. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kalos M, Fournier REK (1995) Position-independent transgene expression mediated by boundary elements from the apolipoprotein B chromatin domain. Mol Cell Biol 15:198–207CrossRefGoogle Scholar
  33. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61(6):909–921. CrossRefPubMedGoogle Scholar
  34. Kusaba M (2004) RNA interference in crop plants. Curr Opin Biotechnol 15:139–143CrossRefGoogle Scholar
  35. Lanfranco L (2003) Engineering crops, a deserving venture. Riv Biol 96:31–54PubMedGoogle Scholar
  36. Levee V, Garin E, Klimaszewska K, Seguin A (1999) Stable genetic transformation of white pine (Pinus strobus L.) after cocultivation of embryogenic tissues with Agrobacterium tumefaciens. Mol Breed 5:429–440CrossRefGoogle Scholar
  37. Levin JS, Thompson WF, Csinos AS, Stephenson MG, Weissinger AK (2005) Matrix attachment regions increase the efficiency and stability of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco. Transgenic Res 14:193–206. CrossRefPubMedGoogle Scholar
  38. Li X, Zhu Z, Xu J, Wu Q, Xu H (2001) Isolation of pea matrix attachment region and study on its function in transgenic tobaccos. Sci China 44(4):400–408CrossRefGoogle Scholar
  39. Li J, Brunner AM, Meilan R, Strauss SH (2008) Matrix attachment region elements have small and variable effects on transgene expression and stability in field-grown Populus. Plant Biotechnol J 6(9):887–896CrossRefGoogle Scholar
  40. Liu JW, Tabe LM (1998) The influences of two plant nuclear matrix attachment regions (MARs) on gene expression in transgenic plants. Plant Cell Physiol 39:115–123CrossRefGoogle Scholar
  41. Lloyd A (2003) Vector construction for gene overexpression as a tool to elucidate gene function. Methods Mol Biol 236:329–344PubMedGoogle Scholar
  42. Loc PV, Strätling WH (1988) The matrix attachment regions of the chicken lysozyme gene co-map with the boundaries of the chromatin domain. EMBO J 7(3):655–664CrossRefGoogle Scholar
  43. Mankin SL, Allen GC, Phelan T, Spiker S, Thompson WF (2003) Elevation of transgene expression level by flanking matrix attachment regions (MAR) is promoter dependent: a study of the interactions of six promoters with the RB7 3´MAR. Transgenic Res 12:3–12CrossRefGoogle Scholar
  44. Maximova S, Miller C, Antúnez de Mayolo G, Pishak S, Young A, Guiltinan MJ (2003) Stable transformation of Theobroma cacao L. and influence of matrix attachment regions on GFP expression. Plant Cell Rep 21(9):872–883PubMedGoogle Scholar
  45. Meyer P, Kartzke S, Niedenhof I, Heidmann I, Bussmann K, Saedler H (1988) A genomic DNA segment from Petunia hybrida leads to increased transformation frequencies and simple integration patterns. Proc Natl Acad Sci USA 85(22):8568–8572CrossRefGoogle Scholar
  46. Mlynarova L, Loonen A, Heldens J, Jansen RC, Keizer P, Stiekema WJ, Nap JP (1994) Reduced position effect in mature transgenic plants conferred by the chicken lysozyme matrixassociated region. Plant Cell 6:417–426CrossRefGoogle Scholar
  47. Mlynarova L, Jansen RC, Conner AJ, Stiekema WJ, Nap JP (1995) The MAR-mediated reduction in position effect can be uncoupled from copy number–dependent expression in transgenic plants. Plant Cell 7:599–609CrossRefGoogle Scholar
  48. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–479CrossRefGoogle Scholar
  49. Nowak W, Gawlowska M, Jarmolowski A, Augustyniak J (2001) Effect of nuclear matrix attachment regions on transgene expression in tobacco plants. Acta Biochim Pol 48:637–646PubMedGoogle Scholar
  50. Odell JT and Krebbers E (1998). Enhanced transgene expression in a population of monocot cells employing scaffold attachment regions. World Patent OfficeGoogle Scholar
  51. Oh SJ, Jeong JS, Kim EH, Yi NR, Yi SI, Jang IC, Kim YS, Suh SC, Nahm BH, Kim JK (2005) Matrix attachment region from the chicken lysozyme locus reduces variability in transgene expression and confers copy number-dependence in transgenic rice plants. Plant Cell Rep 24:145–154CrossRefGoogle Scholar
  52. Peach C, Velten J (1991) Transgene expression variability (position effect) of CAT and GUS reporter genes driven by linked divergent T-DNA promoters. Plant Mol Biol 17:49–60CrossRefGoogle Scholar
  53. Petersen K, Leah R, Knudsen S, Cameron-Mills V (2002) Matrix attachment regions (MARs) enhance transformation frequencies and reduce variance of transgene expression in barley. Plant Mol Biol 49:45–58CrossRefGoogle Scholar
  54. Poljak L, Seum C, Mattioni T, Laemmli UK (1994) SARs stimulate but do not confer position independent gene expression. Nucleic Acids Res 22:4386–4394CrossRefGoogle Scholar
  55. Scheid OM, Paszkowski J, Potrykus I (1991) Reversible inactivation of a transgene in Arabidopsis thaliana. Mol Gen Genet 228:104–112CrossRefGoogle Scholar
  56. Schöffl F, Schröder G, Kliem M, Rieping M (1993) An SAR sequence containing 395 bp DNA fragment mediates enhanced, gene-dosage-correlated expression of a chimaeric heat shock gene in transgenic tobacco plants. Transgenic Res 2:93–100CrossRefGoogle Scholar
  57. Sels J, Delauré SL, Aerts AM, Proost P, Cammue BP, De Bolle MF (2007) Use of a PTGS-MAR expression system for efficient in planta production of bioactive Arabidopsis thaliana plant defensins. Transgenic Res 16:531–538. CrossRefPubMedGoogle Scholar
  58. Sidorenko L, Bruce W, Maddock S, Tagliani L, Li X, Daniels M, Peterson T (2003) Functional analysis of two matrix attachment region (MAR) elements in transgenic maize plants. Transgenic Res 12:137–154CrossRefGoogle Scholar
  59. Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symp Soc Exp Biol 11:118–130PubMedGoogle Scholar
  60. Tetko IV, Haberer G, Rudd S, Meyers B, Mewes H-W, Mayer KFX (2006) Spatiotemporal expression control correlates with intragenic scaffold matrix attachment regions (S/MARs) in Arabidopsis thaliana. PLoS Comput Biol 2(3):e21. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Torney F, Partier A, Says-Lesage V, Nadaud I, Barret P, Beckert M (2004) Heritable transgene expression pattern imposed onto maize ubiquitin promoter by maize adh-1 matrix attachment regions: tissue and developmental specificity in maize transgenic plants. Plant Cell Rep 22(12):931–938CrossRefGoogle Scholar
  62. Ülker B, Allen GC, Thompson WF, Spiker S, Weissinger AK (1999) A tobacco matrix attachment region reduces the loss of transgene expression in the progeny of transgenic tobacco plants. Plant J 18:253–263CrossRefGoogle Scholar
  63. Vain P, Worland B, Kohli A, Snape JW, Christou P, Allen GC, Thompson WF (1999) Matrix attachment regions increase transgene expression levels and stability in transgenic rice plants and their progeny. Plant J 18:233–242CrossRefGoogle Scholar
  64. Vain P, James A, Worland B, Snape W (2002) Transgene behaviour across two generations in a large random population of transgenic rice plants produced by particle bombardment. Theor Appl Genet 105:878–889CrossRefGoogle Scholar
  65. van der Geest AH, Hall TC (1997) The β-phaseolin 5′ matrix attachment region acts as an enhancer facilitator. Plant Mol Biol 33:553. CrossRefPubMedGoogle Scholar
  66. van der Geest AHY, Hall GE Jr, Spiker S, Hall TC (1994) The β-phaseolin gene is flanked by matrix attachment regions. Plant Mol Biol 6:413–423Google Scholar
  67. van der Geest AH, Welter ME, Woosley AT, Pareddy DR, Pavelko SE, Skokut M, Ainley WM (2004) A short synthetic MAR positively affects transgene expression in rice and Arabidopsis. Plant Biotechnol J 2:13–26. CrossRefPubMedGoogle Scholar
  68. van Leeuwen W, Mlynárová L, Nap JP, van der Plas LHW, van der Krol AR (2001) The effect of MAR elements on variation in spatial and temporal regulation of transgene expression. Plant Mol Biol 47:543–554CrossRefGoogle Scholar
  69. Wang T, Xue L, Hou W, Yang B, Chai Y, Ji X, Wang Y (2007) Increased expression of transgene in stably transformed cells of Dunaliella salina by matrix attachment regions. Appl Microbiol Biotechnol 76:651–657. CrossRefPubMedGoogle Scholar
  70. Xu MY, Zhang X, Zhang L, Luo YZ, Fan YL, Wang L (2011) Functional analysis of BnMAR element in transgenic tobacco plants. Mol Biol Rep 38(5):3285–3291. CrossRefPubMedGoogle Scholar
  71. Xue H, Yang YT, Wu CA, Yang GD, Zhang MM, Zheng CC (2005) TM2, a novel strong matrix attachment region. isolated from tobacco, increases transgene expression in transgenic rice calli and plants. Theor Appl Genet 110:620–627CrossRefGoogle Scholar
  72. Zhang K, Wang J, Yang G, Guo X, Wen F, Cui D, Zheng C (2002) Isolation of a strong matrix attachment region (MAR) and identification of its function in vitro and in vivo. Chin Sci Bull 47(23):1999–2005CrossRefGoogle Scholar
  73. Zhang J, Lu L, Ji L, Yang G, Zheng C (2009) Functional characterization of a tobacco matrix attachment region-mediated enhancement of transgene expression. Transgenic Res 18:377–385CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  1. 1.Central Research Institute of EpidemiologyMoscowRussia
  2. 2.Saint-Petersburg Pasteur InstituteSt. PetersburgRussia
  3. 3.Biotron, Branch of Shemyakin and Ovchinnikov Institute of Bioorganic ChemistryPuschinoRussia

Personalised recommendations