Plant Molecular Biology

, Volume 98, Issue 1–2, pp 137–152 | Cite as

Expression of the Arabidopsis ABF4 gene in potato increases tuber yield, improves tuber quality and enhances salt and drought tolerance

  • María Noelia Muñiz García
  • Juan Ignacio Cortelezzi
  • Marina Fumagalli
  • Daniela A. Capiati


Key message

In this study we show that expression of the Arabidopsis ABF4 gene in potato increases tuber yield under normal and abiotic stress conditions, improves storage capability and processing quality of the tubers, and enhances salt and drought tolerance.


Potato is the third most important food crop in the world. Potato plants are susceptible to salinity and drought, which negatively affect crop yield, tuber quality and market value. The development of new varieties with higher yields and increased tolerance to adverse environmental conditions is a main objective in potato breeding. In addition, tubers suffer from undesirable sprouting during storage that leads to major quality losses; therefore, the control of tuber sprouting is of considerable economic importance. ABF (ABRE-binding factor) proteins are bZIP transcription factors that regulate abscisic acid signaling during abiotic stress. ABF proteins also play an important role in the tuberization induction. We developed transgenic potato plants constitutively expressing the Arabidopsis ABF4 gene (35S::ABF4). In this study, we evaluated the performance of 35S::ABF4 plants grown in soil, determining different parameters related to tuber yield, tuber quality (carbohydrates content and sprouting behavior) and tolerance to salt and drought stress. Besides enhancing salt stress and drought tolerance, constitutive expression of ABF4 increases tuber yield under normal and stress conditions, enhances storage capability and improves the processing quality of the tubers.


Potato ABF bZIP Tuber yield Sprouting Salt stress Drought 



This work was supported by grants from the National Scientific and Technical Research Council (CONICET) (11220150100415CO) and the University of Buenos Aires (20020150100025BA). We would like to thank Dr. Edmundo Ploschuk and Instrumentalia S.A. for the assistance with the gas exchange measurements.

Author contributions

MNMG and JIC: characterization of the phenotype of 35S::ABF4 plants. MF: maintenance of the plants in greenhouse; planting and harvesting tubers; application of stress treatments. DAC: design, direction and coordination of the study; manuscript writing.

Supplementary material

11103_2018_769_MOESM1_ESM.pdf (477 kb)
Supplementary material 1 (PDF 477 KB)


  1. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bastías A, López-Climent M, Valcárcel M, Rosello S, Gómez-Cadenas A, Casaretto JA (2011) Modulation of organic acids and sugar content in tomato fruits by an abscisic acid-regulated transcription factor. Physiol Plant 141:215–226. CrossRefPubMedGoogle Scholar
  3. Bastías A, Yañez M, Osorio S, Arbona V, Gómez-Cadenas A, Fernie AR, Casaretto JA (2014) The transcription factor AREB1 regulates primary metabolic pathways in tomato fruit. J Exp Bot 65:2351–2363. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207. CrossRefGoogle Scholar
  5. Bayat F, Shiran B, Belyaev DV, Yur’eva NO, Sobol’kova GI, Alizadeh H, Khodambashi M, Babakov V (2010) Potato plants bearing a vacuolar Na+/H+ antiporter HvNHX2 from barley are characterized by improved salt tolerance. Russ J Plant Physiol 57:696. CrossRefGoogle Scholar
  6. Birch PRJ, Bryan G, Fenton B, Gilroy EM, Hein I, Jones JT, Prashar A, Taylor MA, Torrance L, Toth IK (2012) Crops that feed the world 8: potato: are the trends of increased global production sustainable. Food Secur 4:477–508. CrossRefGoogle Scholar
  7. Boneh U, Biton I, Schwartz A, Ben-Ari G (2012) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Sci 187:89–96. CrossRefPubMedGoogle Scholar
  8. Bouaziz D, Pirrello J, Ben Amor H, Hammami A, Charfeddine M, Dhieb A, Bouzayen M, Gargouri-Bouzid R (2012) Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. Plant Physiol Biochem 60:98–108. CrossRefPubMedGoogle Scholar
  9. Bouaziz D, Pirrello J, Charfeddine M, Hammami A, Jbir R, Dhieb A, Bouzayen M, Gargouri-Bouzid R (2013) Overexpression of StDREB1 transcription factor increases tolerance to salt in transgenic potato plants. Mol Biotechnol 54:803–817. CrossRefPubMedGoogle Scholar
  10. Camire ME, Kubow S, Donnelly DJ (2009) Potatoes and human health. Crit Rev Food Sci Nutr 49:823–840. CrossRefPubMedGoogle Scholar
  11. Capiati DA, País SM, Téllez-Iñón MT (2006) Wounding increases salt tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross-tolerance signalling. J Exp Bot 57:2391–2400. CrossRefPubMedGoogle Scholar
  12. Casaretto JA, Ho TH (2005) Transcriptional regulation by abscisic acid in barley (Hordeum vulgare L.) seeds involves autoregulation of the transcription factor HvABI5. Plant Mol Biol 57:21–34. CrossRefPubMedGoogle Scholar
  13. Celebi-Toprak F, Behnam B, Serrano G, Kasuga M, Yamaguchi-Shinozaki K, Naka H, Watanabe J, Yamanaka S, Watanabe KN (2005) Tolerance to salt stress of the transgenic tetrasomic tetraploid potato, Solanum tuberosum cv. Desiree appears to be induced by the DREB1A gene and rd29A promoter of Arabidopsis thaliana. Breed Sci 55:311–319. CrossRefGoogle Scholar
  14. Cheng YJ, Kim MD, Deng XP, Kwak SS, Chen W (2013) Enhanced salt stress tolerance in transgenic potato plants expressing IbMYB1, a sweet potato transcription factor. J Microbiol Biotechnol 23:1737–1746. CrossRefPubMedGoogle Scholar
  15. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730. CrossRefPubMedGoogle Scholar
  16. Destefano-Beltran L, Knauber D, Huckle L, Suttle JC (2006) Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. Plant Mol Biol 61:687–697. CrossRefPubMedGoogle Scholar
  17. Dutt S, Manjul AS, Raigond P, Singh B, Siddappa S, Bhardwaj V, Kawar PG, Patil VU, Kardile HB (2017) Key players associated with tuberization in potato: potential candidates for genetic engineering. Crit Rev Biotechnol 37:942–957. CrossRefPubMedGoogle Scholar
  18. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074. CrossRefGoogle Scholar
  19. Eltayeb AE, Yamamoto S, Eltayeb Habora ME, Yin L, Tsujimoto H, Tanaka K (2011) Transgenic potato overexpressing Arabidopsis cytosolic AtDHAR1 showed higher tolerance to herbicide, drought and salt stresses. Breed Sci 61:3–10. CrossRefGoogle Scholar
  20. Fang Z, Bouwkamp JC, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Bot 49:503–510. CrossRefGoogle Scholar
  21. Fujino K, Koda Y, Kikuta Y (1995) Reorientation of cortical microtubules in the sub-apical region during tuberization in single-node stem segments of potato in culture. Plant Cell Physiol 36:891–895. CrossRefGoogle Scholar
  22. Gangadhar BH, Sajeesh K, Venkatesh J, Baskar V, Abhinandan K, Yu JW, Prasad R, Mishra RK (2016) Enhanced tolerance of transgenic potato plants over-expressing non-specific lipid transfer protein-1 (StnsLTP1) against multiple abiotic stresses. Front Plant Sci 7:1228. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (2016) ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant 9:1272–1285. CrossRefPubMedGoogle Scholar
  24. Hartmann A, Senning M, Hedden P, Sonnewald U, Sonnewald S (2011) Reactivation of meristem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol 155:776–796. CrossRefPubMedGoogle Scholar
  25. Hijmans RJ (2003) The effect of climate change on global potato production. Am J Pot Res 80:271–280. CrossRefGoogle Scholar
  26. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052. CrossRefPubMedGoogle Scholar
  27. Hossain MA, Cho JI, Han M, Ahn CH, Jeon JS, An G, Park PB (2010a) The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signalling in rice. J Plant Physiol 167:1512–1520. CrossRefPubMedGoogle Scholar
  28. Hossain MA, Lee Y, Cho JI, Ahn CH, Lee SK, Jeon JS, Kang H, Lee CH, An G, Park PB (2010b) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signalling in rice. Plant Mol Biol 72:557–566. CrossRefGoogle Scholar
  29. Hsieh TH, Li CW, Su RC, Cheng CP, Tsai YC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473. CrossRefPubMedGoogle Scholar
  30. Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ipcc (2008) Climate change and water. In: Bates BC, Kundzewicz ZW, Palutikof J, Wu S (eds.) Technical paper of the intergovernmental panel on climate change, IPCC Secretariat, GenevaGoogle Scholar
  32. ISAAA (2016) Global Status of Commercialized Biotech/GM Crops: 2016. ISAAA Brief No. 52. ISAAA, Ithaca. ISBN: 978-1-892456-66-4Google Scholar
  33. Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kerr TC, Abdel-Mageed H, Aleman L, Lee J, Payton P, Cryer D, Allen RD (2017) Ectopic expression of two AREB/ABF orthologs increases drought tolerance in cotton (Gossypium hirsutum). Plant Cell Environ. CrossRefPubMedGoogle Scholar
  35. Kim S, Kang JY, Cho DI, Park JH, Kim SY (2004) ABF2, an ABRE binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40:75–87. CrossRefPubMedGoogle Scholar
  36. Kloosterman B, Navarro C, Bijsterbosch G, Lange T, Prat S, Visser RG, Bachem CW (2007) StGA2ox1 is induced prior to stolon swelling and controls GA levels during potato tuber development. Plant J 52:362–373. CrossRefPubMedGoogle Scholar
  37. Kobayashi F, Maeta E, Terashima A, Takumi S (2008) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134:74–86. CrossRefPubMedGoogle Scholar
  38. Levine RL, Willians JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–363. CrossRefPubMedGoogle Scholar
  39. Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19:998–1011. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Liang C, Meng Z, Meng Z, Malik W, Yan R, Lwin KM, Lin F, Wang Y, Sun G, Zhou T, Zhu T, Li J, Jin S, Guo S, Zhang R (2016) GhABF2, a bZIP transcription factor, confers drought and salinity tolerance in cotton (Gossypium hirsutum L.). Sci Rep 6:35040. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Moon SJ, Han SY, Kim DY, Yoon IS, Shin D, Byun MO, Kwon HB, Kim BG (2015) Ectopic expression of a hot pepper bZIP-like transcription factor in potato enhances drought tolerance without decreasing tuber yield. Plant Mol Biol 89:421–431. CrossRefPubMedGoogle Scholar
  42. Movahedi S, Tabatabaei BS, Alizade H, Ghobadi C, Yamchi A, Khaksar G (2012) Constitutive expression of Arabidopsis DREB1B in transgenic potato enhances drought and freezing tolerance. Biol Plant 56:37. CrossRefGoogle Scholar
  43. Muñiz García MN, Giammaria V, Grandellis C, Téllez-Iñón MT, Ulloa RM, Capiati DA (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235:761–778. CrossRefPubMedGoogle Scholar
  44. Muñiz García MN, Stritzler M, Capiati DA (2014) Heterologous expression of Arabidopsis ABF4 gene in potato enhances tuberization through ABA-GA crosstalk regulation. Planta 239:615–631. CrossRefPubMedGoogle Scholar
  45. Nelson N (1994) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380Google Scholar
  46. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Orellana S, Yañez M, Espinoza A, Verdugo I, González E, Ruiz-Lara S, Casaretto JA (2010) The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2208. CrossRefPubMedGoogle Scholar
  48. Rahnama H, Vakilian H, Fahimi H, Ghareyazie B (2011) Enhanced salt stress tolerance in transgenic potato plants (Solanum tuberosum L.) expressing a bacterial mtlD gene. Acta Physiol Plant 33:1521–1532. CrossRefGoogle Scholar
  49. Rommens CM, Shakya R, Heap M, Fessenden K (2010) Tastier and healthier alternatives to French Fries. J Food Sci 75:109–115. CrossRefGoogle Scholar
  50. Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45:527–544. CrossRefGoogle Scholar
  51. Shin D, Moon SJ, Han S, Kim BG, Park SR, Lee SK, Yoon HJ, Lee HE, Kwon HB, Baek D, Yi BY, Byun MO (2011) Expression of StMYB1R-1, a novel potato single MYB-like domain transcription factor, increases drought tolerance. Plant Physiol 155:421–432. CrossRefPubMedGoogle Scholar
  52. Somogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23Google Scholar
  53. Sonnewald U (2001) Control of potato tuber sprouting. Trends Plant Sci 6:333–335. CrossRefPubMedGoogle Scholar
  54. Sonnewald S, Sonnewald U (2014) Regulation of potato tuber sprouting. Planta 239:27–38. CrossRefPubMedGoogle Scholar
  55. Stiller I, Dulai S, Kondrák M, Tarnai R, Szabó L, Toldi O, Bánfalvi Z (2008) Effects of drought on water content and photosynthetic parameters in potato plants expressing the trehalose-6-phosphate synthase gene of Saccharomyces cerevisiae. Planta 227:299–308. CrossRefPubMedGoogle Scholar
  56. Stritzler M, Muñiz García MN, Schlesinger M, Cortelezzi JI, Capiati DA (2017) The plasma membrane H+-ATPase gene family in Solanum tuberosum L. Role of PHA1 in tuberization. J Exp Bot 68:4821–4837. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Suárez-López P (2013) A critical appraisal of phloem-mobile signals involved in tuber induction. Front Plant Sci 4:253CrossRefPubMedPubMedCentralGoogle Scholar
  58. Suttle JC, Hultstrand J (1994) Role of endogenous abscisic acid in potato microtuber dormancy. Plant Physiol 105:891–896. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Szalonek M, Sierpien B, Rymaszewski W, Gieczewska K, Garstka M, Lichocka M, Sass L, Paul K, Vass I, Vankova R, Dobrev P, Szczesny P, Marczewski W, Krusiewicz D, Strzelczyk-Zyta D, Hennig J, Konopka-Postupolska D (2015) Potato annexin STANN1 promotes drought tolerance and mitigates light stress in transgenic Solanum tuberosum L. plants. PLoS ONE 10:e0132683. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Teixeira AI, Ribeiro LF, Rezende ST, Barros EG, Moreira MA (2012) Development of a method to quantify sucrose in soybean grains. Food Chem 130:1134–1136. CrossRefGoogle Scholar
  61. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637. CrossRefPubMedGoogle Scholar
  62. Upadhyaya CP, Venkatesh J, Gururani MA, Asnin L, Sharma K, Ajappala H, Park SW (2011) Transgenic potato overproducing L-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol Lett 33:2297–2307. CrossRefPubMedGoogle Scholar
  63. Vasquez Robinet C, Mane SP, Ulanov AV, Watkinson JI, Stromberg VK, De Koeyer D, Schafleitner R, Willmot DB, Bonierbale M, Bohnert HJ, Grene R (2008) Physiological and molecular adaptations to drought in Andean potato genotypes. J Exp Bot 59:2109–2123. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wang-Pruski G, Nowak J (2004) Potato after-cooking darkening. Am J Pot Res 81:7–16. CrossRefGoogle Scholar
  65. Xu X, Vreugdenhil D, van Lammeren AMM (1998) Cell division and cell enlargement during potato tuber formation. J Exp Bot 49:573–582. CrossRefGoogle Scholar
  66. Yáñez M, Cáceres S, Orellana S, Bastías A, Verdugo I, Ruiz-Lara S, Casaretto JA (2009) An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep 28:1497–1507. CrossRefPubMedGoogle Scholar
  67. Yeo AR (1999) Predicting the interaction between the effects of salinity and climate change on crop plants. Sci Hortic 78:159–174. CrossRefGoogle Scholar
  68. Zhang N, Si HJ, Wen G, Du HH, Liu BL, Wang D (2011) Enhanced drought and salinity tolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol Rep 5:71–77. CrossRefGoogle Scholar
  69. Zhang Q, Wang M, Hu J, Wang W, Fu X, Liu JH (2015) PtrABF of Poncirus trifoliata functions in dehydration tolerance by reducing stomatal density and maintaining reactive oxygen species homeostasis. J Exp Bot 66:5911–5927. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Institute of Genetic Engineering and Molecular Biology “Dr. Héctor Torres” (INGEBI)National Scientific and Technical Research Council (CONICET)Buenos AiresArgentina
  2. 2.Biochemistry Department, School of Exact and Natural SciencesUniversity of Buenos AiresBuenos AiresArgentina

Personalised recommendations