Advertisement

Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 138, Issue 2, pp 325–337 | Cite as

Overexpression of Sorghum plasma membrane-bound Na+/H+ antiporter-like protein (SbNHXLP) enhances salt tolerance in transgenic groundnut (Arachis hypogaea L.)

  • Venkatesh Kandula
  • Amareshwari Pudutha
  • P. Hima Kumari
  • S. Anil Kumar
  • P. B. Kavi Kishor
  • Roja Rani AnupalliEmail author
Original Article
  • 147 Downloads

Abstract

Soil salinity and water-deficit conditions often affect crop productivity in groundnut. Therefore, developing transgenic groundnut that can grow under such abiotic stress conditions is crucial to stabilize its yield. Sodium proton antiporter-like protein (NHXLP) is a plasma membrane-bound protein associated with Na+ exclusion and helps to maintain ion homeostasis under saline conditions. In the present study, salt tolerant transgenic groundnut variety JL-24 was developed by expressing SbNHXLP gene isolated from Sorghum bicolor. Molecular analysis of transgenics by PCR and Southern blot confirmed the integration of SbNHXLP gene. SbNHXLP expression at the transcript level was checked by reverse transcriptase (RT)-PCR. Homozygous T2 lines along with wild-type (WT) plants were evaluated for 150 mM NaCl stress tolerance. Biochemical analysis of transgenics under salt stress revealed higher chlorophyll content, superoxide dismutase, and catalase activities, accumulation of proline, and K+ accompanied by lower Na+ accumulation compared to WT plants. Additionally, transgenics displayed higher biomass and pod yield when compared with WT plants under stress. Our findings indicate that overexpression of SbNHXLP gene in groundnut results in enhanced tolerance to salinity stress. This highlights the potential of SbNHXLP as a target candidate gene to impart salt stress tolerance in groundnut.

Key message

A sodium proton antiporter-like protein isolated from Sorghum (SbNHXLP) was overexpressed in groundnut and stably integrated. Transgenics displayed higher chlorophyll, proline, K+, and better yields than WT plants under salt stress.

Keywords

Genetic transformation groundnut Sorghum plasma membrane Na+/H+ antiporter-like protein Salt tolerance 

Abbreviations

BAP

6-Benzylaminopurine

CAT

Catalase

DTT

Dithiothreitol

hptII

Hygromycin phosphotransferase

MDA

Malondialdehyde

MS

Murashige and Skoog

NAA

Naphthaleneacetic acid

NBT

Nitroblue tetrazolium

PEG

Polyethylene glycol

PCR

Polymerase chain reaction

PVP

Polyvinylpyrrolidone

ROS

Reactive oxygen species

SOS

Salt overly sensitive

NHXLP

Sodium proton antiporter-like protein

SOD

Superoxide dismutase

WT

Wild-type plants

Notes

Acknowledgements

VK is grateful to the University Grants Commission (UGC) and CSIR, New Delhi, for providing fellowship. RRA is thankful to the UGC, New Delhi for providing funds. PBK is grateful to the CSIR, New Delhi, for sanctioning CSIR-Emeritus Fellowship.

Author contributions

RRA and PBK conceived and designed the experiments. VK, AP carried out the experiments and analysed the data. VK, AP, and HP wrote the manuscript. AS, VK, AP, HP, RRA, PBK critically analyzed and refined the manuscript. All authors read and approved the manuscript.

Supplementary material

11240_2019_1628_MOESM1_ESM.doc (2.4 mb)
Supplementary material 1 (DOC 2444 kb)
11240_2019_1628_MOESM2_ESM.doc (130 kb)
Supplementary material 2 (DOC 130 kb)

References

  1. Adem GD, Roy SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biol 14:113.  https://doi.org/10.1186/1471-2229-14-113 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Adem GD, Roy SJ, Plett DC, Zhoul M, Bowman JP, Shabala S (2015) Expressing AtNHX1 in barley (Hordeum vulgare L.) does not improve plant performance under saline conditions. Plant Growth Regul 77:289–297.  https://doi.org/10.1007/s10725-015-0063-9 CrossRefGoogle Scholar
  3. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126.  https://doi.org/10.1016/S0076-6879(84)05016-3 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Afzal M, Ahmad A, Alderfasi AA, Ghoneim A, Saqib M (2014) Physiological tolerance and cation accumulation of different genotypes of Capsicum annum under varying salinity stress. Proc Int Acad Ecol Environ Sci 4:39–49Google Scholar
  5. Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131.  https://doi.org/10.1093/jxb/ern251 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Anjaneyulu E, Reddy PS, Sunita MS, Kishor PBK, Meriga B (2014) Salt tolerance and activity of antioxidative enzymes of transgenic finger millet overexpressing a vacuolar H+-pyrophosphatase gene (SbVPPase) from Sorghum bicolor. J Plant Physiol 171:789–798.  https://doi.org/10.1016/j.jplph.2014.02.001 CrossRefPubMedGoogle Scholar
  7. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15.  https://doi.org/10.1104/pp.24.1.1 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Asif MA, Zafar AY, Iqbal J, Iqbal MM, Rashid U, Ali GM, Arif A, Nazir F (2011) Enhanced expression of AtNHX1, in transgenic groundnut (Arachis hypogaea L.) improves salt and drought tolerance. Mol Biotechnol 49:250–256.  https://doi.org/10.1007/s12033-011-9399-1 CrossRefPubMedGoogle Scholar
  9. Baker CM, Durham RE, Burns JA, Parrott WA, Wetzstein HY (1995) High frequency somatic embryogenesis in peanut (Arachis hypogaea L.) using mature, dry seed. Plant Cell Rep 15:38–42.  https://doi.org/10.1007/BF01690250 CrossRefPubMedGoogle Scholar
  10. Banavath JN, Chakradhar T, Pandit V, Konduru S, Guduru KK, Akila CS et al (2018) Stress inducible overexpression of AtHDG11 leads to improved drought and salt stress tolerance in peanut (Arachis hypogaea L.). Front Chem 6:34.  https://doi.org/10.1038/nrmicro280 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Banjara M, Zhu L, Shen G (2012) Expression of an Arabidopsis sodium/proton antiporter gene (AtNHX1) in peanut to improve salt tolerance. Plant Biotechnol Rep 6:59–67.  https://doi.org/10.1007/s11816-011-0200-5 CrossRefGoogle Scholar
  12. Bassil E, Ohto M, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011a) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23:224–239.  https://doi.org/10.1105/tpc.110.079426 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bassil E, Tajima H, Liang YC, Ohto MA, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011b) The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23:3482–3497.  https://doi.org/10.1105/tpc.111.089581 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207.  https://doi.org/10.1007/BF00018060 CrossRefGoogle Scholar
  15. Ben RK, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284.  https://doi.org/10.1016/j.plaphy.2014.04.007 CrossRefGoogle Scholar
  16. Bhatia CR, Murty GSS, Mathews VH (1985) Regeneration from “de-embryonated” peanut cotyledons cultured without nutrients and agar. ZeitschriftfürPflanzenzuchtung 94:149–155Google Scholar
  17. Bhatnagar-Mathur P, Devi MJ, Reddy DS, Lavanya M, Vadez V, Serraj R et al (2007) Stress-inducible expression of AtDREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep 26:2071–2082CrossRefPubMedGoogle Scholar
  18. Bhatnagar-Mathur P, Devi MJ, Vadez V, Sharma KK (2009) Differential antioxidative responses in transgenic peanut bear no relationship to their superior transpiration efficiency under drought stress. J Plant Physiol 166:1207–1217.  https://doi.org/10.1016/j.jplph.2009.01.001 CrossRefPubMedGoogle Scholar
  19. Bhauso TD, Radhakrishnan T, Kumar A, Mishra GP, Dobaria JR, Patel K et al (2014) Overexpression of bacterial mtlDgene in peanut improves drought tolerance through accumulation of mannitol. Sci World J.  https://doi.org/10.1155/2014/125967 CrossRefGoogle Scholar
  20. Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–444.  https://doi.org/10.1016/S0955-0674(00)00112-5 CrossRefPubMedGoogle Scholar
  21. Blumwald E, Poole R (1987) Salt tolerance in suspension cultures of sugar beet: induction of Na+/H+ antiport activity at the tonoplast by growth in salt. Plant Physiol 83:884–887.  https://doi.org/10.1104/pp.83.4.884 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chen X, Lu X, Shu N, Wang D, Wang S, Wang J, Guo L, Guo X, Fan W, Lin Z, Ye W (2017) GhSOS1, a plasma membrane Na+/H+ antiporter gene from upland cotton, enhances salt tolerance in transgenic Arabidopsis thaliana. PLoS ONE.  https://doi.org/10.1371/journal.pone.0181450 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cheng M, Jarret RL, Li Z, Demski JW (1997) Expression and inheritance of foreign genes in transgenic peanut plants generated by Agrobacterium-mediated transformation. Plant Cell Rep 16:541–544.  https://doi.org/10.1007/BF01142320 CrossRefPubMedGoogle Scholar
  25. Chengalrayan K, Mhaske VB, Hazra S (1998) Genotypic control of peanut somatic embryogenesis. Plant Cell Rep 17:522–525.  https://doi.org/10.1007/s002990050435 CrossRefPubMedGoogle Scholar
  26. Desikan R (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172.  https://doi.org/10.1104/pp.127.1.159 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Dhindsa RS, Plumb-dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101.  https://doi.org/10.1093/jxb/32.1.93 CrossRefGoogle Scholar
  28. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15.  https://doi.org/10.2307/4119796 CrossRefGoogle Scholar
  29. Eckardt NA, Berkowitz GA (2011) Functional analysis of Arabidopsis NHX antiporters: the role of the vacuole in cellular turgor and growth. Plant Cell 23:3087–3098.  https://doi.org/10.1105/tpc.111.230914 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Egnin M, Mora A, Prakash CS (1998) Factors enhancing Agrobacterium tumefaciens-mediated gene transfer in peanut (Arachis hypogaea L.). In Vitro Cell Dev Biol Plant 34:310–318.  https://doi.org/10.1007/BF02822740 CrossRefPubMedGoogle Scholar
  31. Fahramand M, Mahmoody M, Keykha A, Noori M, Rigi K (2014) Influence of abiotic stress on proline, photosynthetic enzymes and growth. Int Res J Appl Basic Sci 8:257–265Google Scholar
  32. Feki K, Tounsi S, Masmoudi K, Brini F (2017) The durum wheat plasma membrane Na+/H+ antiporter SOS1 is involved in oxidative stress response. Protoplasma 254:1725–1734.  https://doi.org/10.1007/s00709-016-1066-8 CrossRefPubMedGoogle Scholar
  33. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112.  https://doi.org/10.1146/64.070195.000525 CrossRefPubMedGoogle Scholar
  34. Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K (2012) Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiol Biochem 51:109–115.  https://doi.org/10.1016/j.plaphy.2011.10.012 CrossRefPubMedGoogle Scholar
  35. Gao X, Ren Z, Zhao Y, Zhang H (2003) Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol 133:1873–1881.  https://doi.org/10.1104/pp.103.026062 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Garciadeblás B, Haro R, Benito B (2007) Cloning of two SOS1 transporters from the seagrass Cymodocea nodosa. SOS1 transporters from Cymodocea and Arabidopsis mediate potassium uptake in bacteria. Plant Mol Biol 63:479–490.  https://doi.org/10.1007/s11103-006-9102-2 CrossRefPubMedGoogle Scholar
  37. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449.  https://doi.org/10.1073/pnas.191389398 CrossRefPubMedGoogle Scholar
  38. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314.  https://doi.org/10.1104/pp.59.2.309 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom.  https://doi.org/10.1155/2014/701596 CrossRefGoogle Scholar
  40. Hichri I, Muhovski Y, Žižková E, Dobrev PI, Gharbi E, Franco-Zorrilla JM, Lopez-Vidriero I, Solano R, Clippe A, Errachid A, Motyka V, Lutts S (2017) The Solanum lycopersicum WRKY3 transcription factor SlWRKY3 is involved in salt stress tolerance in tomato. Front Plant Sci 8:1343.  https://doi.org/10.1126/science.aaa6743 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334.  https://doi.org/10.1139/b79-163 CrossRefGoogle Scholar
  42. Hsieh YF, Jain M, Wang J, Gallo M (2017) Direct organogenesis from cotyledonary node explants suitable for Agrobacterium-mediated transformation in peanut (Arachis hypogaea L.). Plant Cell Tissue Organ Cult 128:161–175.  https://doi.org/10.1007/s11240-016-1095-1 CrossRefGoogle Scholar
  43. Jamil M, Rehman S, Rha ES (2014) Response of growth, PSII photochemistry and chlorophyll content to salt stress in four Brassica species. Life Sci J 11:139–145.  https://doi.org/10.1086/115371 CrossRefGoogle Scholar
  44. Janila P, Nigam SN, Pandey MK, Nagesh P, Varshney RK (2013) Groundnut improvement: use of genetic and genomic tools. Front Plant Sci 4:23.  https://doi.org/10.1086/115371 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Jha B, Mishra A, Jha A, Joshi M (2013) Developing transgenic Jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS ONE.  https://doi.org/10.1371/journal.pone.0071136 CrossRefPubMedPubMedCentralGoogle Scholar
  46. KaviKishor PB, Himakumari P, Sunita MSL, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:544.  https://doi.org/10.3389/fpls.2015.00544 CrossRefGoogle Scholar
  47. Kiranmai K, Lokanadha RG, Pandurangaiah M, Nareshkumar A, Amaranatha RV, Lokesh U et al (2018) A novel WRKY transcription factor, MuWRKY3 (Macrotyloma uniflorum Lam. Verdc.) enhances drought stress tolerance in transgenic groundnut (Arachis hypogaea L.) plants. Front Plant Sci.  https://doi.org/10.3389/fpls.2018.00346 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608.  https://doi.org/10.1093/jxb/err460 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Krishna G, Singh BK, Kim EK, Morya VK, Ramteke PW (2015) Progress in genetic engineering of peanut (Arachis hypogaea L.)—a review. Plant Biotechnol J 13:147–162.  https://doi.org/10.1111/pbi.12339 CrossRefPubMedGoogle Scholar
  50. Kumar K, Kumar M, Kim SR, Ryu H, Cho YG (2013) Insights into genomics of salt stress response in rice. Rice 6:27.  https://doi.org/10.1186/1939-8433-6-27 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kumari PH, Kumar SA, Sivan P, Katam R, Suravajhala P, Rao KS, Varshney RK, Kishor PBK (2017) Overexpression of a plasma membrane bound Na+/H+ antiporter-like protein (SbNHXLP) confers salt tolerance and improves fruit yield in tomato by maintaining ion homeostasis. Front Plant Sci 7:2027.  https://doi.org/10.3389/fpls.2016.02027 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lawlor DW (1995) The effects of water deficit on photosynthesis. In: Smirnoff N (ed) Environment and plant metabolism flexibility and acclimation. Oxford Bios Scientific Publishers, Oxford, pp 129–160Google Scholar
  53. Ma DM, Xu WR, Li HW, Jin FX, Guo LN, Wang J, Dai HJ, Xu X (2014) Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma 251:219–231.  https://doi.org/10.1007/s00709-013-0540-9 CrossRefPubMedGoogle Scholar
  54. Mallikarjuna G, Rao TSRB, Kirti PB (2016) Genetic engineering for peanut improvement: current status and prospects. Plant Cell Tissue Organ Cult 125:399.  https://doi.org/10.1007/s11240-016-0966-9 CrossRefGoogle Scholar
  55. Martinez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012.  https://doi.org/10.1104/pp.106.092635 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Maughan PJ, Turner TB, Coleman CE, Elzinga DB, Jellen EN, Morales JA, Udall JA, Fairbanks DJ, Bonifacio A (2009) Characterization of salt overly sensitive 1 (SOS1) gene homoeologs in quinoa (Chenopodium quinoa Willd.). Genome 52:647–657.  https://doi.org/10.1139/G09-041 CrossRefPubMedGoogle Scholar
  57. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681.  https://doi.org/10.1146/annurev.arplant.59.032607.092911 CrossRefPubMedGoogle Scholar
  58. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497.  https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  59. Murillo-Amador B, Yamada S, Yamaguchi T, Rueda-Puente E, Ávila-Serrano N, García-Hernández JL, López-Aguilar R, Troyo-Diéguez E, Nieto-Garibay A (2007) Influence of calcium silicate on growth, physiological parameters and mineral nutrition in two legume species under salt stress. J Agron Crop Sci 193:413–421.  https://doi.org/10.1111/j.1439-037X.2007.00273.x CrossRefGoogle Scholar
  60. Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742CrossRefPubMedPubMedCentralGoogle Scholar
  61. Oh DH, Gong Q, Ulanov A, Zhang Q, Li Y, Ma W, Yun DJ, Bressan RA, Bohnert HJ (2007) Sodium stress in the halophyte Thellungiella halophila and transcriptional changes in a thsos1-RNA interference line. J Integr Plant Biol 49:1484–1496.  https://doi.org/10.1111/j.1672-9072.2007.00548.x CrossRefGoogle Scholar
  62. Oh D-H, Leidi E, Zhang Q, Hwang SM, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Lee SY, Zhao Y, Bahk JD, Bressan RA, Yun DJ, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222.  https://doi.org/10.1104/pp.109.137802 CrossRefPubMedPubMedCentralGoogle Scholar
  63. OlÍas R, Eljakaoui Z, Li J, Morales P (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916.  https://doi.org/10.1111/j.1365-3040.2009.01971.x CrossRefPubMedGoogle Scholar
  64. Pandey MK, Monyo E, Ozias-Akins P, Liang X, Guimarães P, Nigam SN, Upadhyaya HD, Janila P, Zhang X, Guo B, Cook DR, Bertioli DJ, Michelmore R, Varshney RK (2012) Advances in Arachis genomics for peanut improvement. Biotechnol Adv 30:639–651.  https://doi.org/10.1016/j.biotechadv.2011.11.001 CrossRefPubMedGoogle Scholar
  65. Pandey S, Patel MK, Mishra A, Jha B (2016) In planta transformed cumin (Cuminum cyminum L.) plants, overexpressing the SbNHX1 gene showed enhanced salt endurance. PLoS ONE.  https://doi.org/10.1371/journal.pone.0159349 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199.  https://doi.org/10.1093/jxb/erj114 CrossRefPubMedGoogle Scholar
  67. Pasapula V, Shen G, Kuppu S, Paez-Valencia J, Mendoza M, Hou P, Chen J, Qiu X, Zhu L, Zhang X, Auld D, Blumwald E, Zhang H, Gaxiola R, Payton P (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J 9:88–99.  https://doi.org/10.1111/j.1467-7652.2010.00535.x CrossRefPubMedGoogle Scholar
  68. Patel KG, Mandaliya VB, Mishra GP, Jentilal R, Dobaria JR, Thankappa R (2016) Transgenic peanut overexpressing mtlD gene confers enhanced salinity stress tolerance via mannitol accumulation and differential antioxidative responses. Acta Physiol Plant 38:181.  https://doi.org/10.1007/s11738-016-2200-0 CrossRefGoogle Scholar
  69. Patel KG, Thankappan R, Mishra GP, Mandaliya VB, Kumar A, Dobaria JR (2017) Transgenic peanut (Arachis hypogaea L.) overexpressing mtlD gene showed improved photosynthetic, physio-biochemical, and yield-parameters under soil-moisture deficit stress in lysimeter system. Front Plant Sci 8:1881.  https://doi.org/10.3389/fpls.2017.01881 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Payton P, Webb R, Kornyeyev D, Allen R, Holaday AS (2001) Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity. J Exp Bot 52:2345–2354.  https://doi.org/10.1093/jexbot/52.365.2345 CrossRefPubMedGoogle Scholar
  71. Pruthvi V, Narasimhan R, Nataraja KN (2014) Simultaneous expression of abiotic stress responsive transcription factors, AtDREB2A, AtHB7 and AtABF3 improves salinity and drought tolerance in peanut (Arachis hypogaea L.). PLoS ONE.  https://doi.org/10.1371/journal.pone.0111152 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+-H+ antiporter during salinity stress. Plant Physiol 136:2548–2555.  https://doi.org/10.1104/pp.104.049213 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Qin H, Gu Q, Zhang J, Sun L, Kuppu S, Zhang Y et al (2011) Regulated expression of isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions. Plant Cell Physiol 52:1904–1914CrossRefPubMedGoogle Scholar
  74. Qin H, Gu Q, Kuppu S, Sun L, Zhu X, Mishra N, Hu R, Shen G, Zhang J, Zhang Y, Zhu L, Zhang X, Burow M, Payton P, Zhang H (2013) Expression of the Arabidopsis vacuolar H+-pyrophosphatase gene AVP1 in peanut to improve drought and salt tolerance. Plant Biotechnol Rep 7:345–355.  https://doi.org/10.1007/s11816-012-0269-5 CrossRefGoogle Scholar
  75. Rana K, Mohanty IC (2012) In vitro regeneration and genetic transformation in peanut (Arachis hypogaea L. cv. Smruti) for abiotic stress tolerance mediated by Agrobacterium tumifaciens. J Today’s Biol Sci: Res Rev 1:62–85Google Scholar
  76. Ravikumar G, Manimaran P, Voleti SR, Subrahmanyam D, Sundaram RM, Bansal KC, Viraktamath BC, Balachandran SM (2014) Stress-inducible expression of AtDREB1A transcription factor greatly improves drought stress tolerance in transgenic indica rice. Transgenic Res 23:421–439.  https://doi.org/10.1007/s11248-013-9776-6 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Reddy MSS, Dinkins RD, Collins GB (2003) Gene silencing in transgenic soybean plants transformed via particle bombardment. Plant Cell Rep 21:676–683.  https://doi.org/10.1007/s00299-002-0567-4 CrossRefPubMedGoogle Scholar
  78. Reddy SP, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kavi Kishor PB (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113.  https://doi.org/10.1016/j.plaphy.2015.05.014 CrossRefPubMedGoogle Scholar
  79. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  80. Santosh RBRT, Vijaya NJ, Sudhakar RP, Reddy MK, Mallikarjuna G (2017) Expression of Pennisetum glaucum eukaryotic translational initiation factor 4A (PgeIF4A) confers improved drought, salinity, and oxidative stress tolerance in groundnut. Front Plant Sci 8:453.  https://doi.org/10.3389/fpls.2017.00453 CrossRefGoogle Scholar
  81. Sarkar T, Thankappan R, Kumar A, Mishra GP, Dobaria JR (2014) Heterologous expression of the AtDREB1A gene in transgenic peanut-conferred tolerance to drought and salinity stresses. PLoS ONE.  https://doi.org/10.1371/journal.pone.0110507 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Sarkar T, Thankappan R, Kumar A, Mishra GP, Dobaria JR (2016) Stress inducible expression of AtDREB1A transcription factor in transgenic peanut (Arachis hypogaea L.) conferred tolerance to soil-moisture deficit stress. Front Plant Sci 7:935.  https://doi.org/10.3389/fpls.2016.00935 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Shabala S (2017) Signalling by potassium: another second messenger to add to the list? J Exp Bot 68:4003–4007.  https://doi.org/10.1093/jxb/erx238 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Shabala L, Cuin TA, Newman IA, Shabala S (2005) Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222:1041–1050.  https://doi.org/10.1007/s00425-005-0074-2 CrossRefPubMedGoogle Scholar
  85. Sharma KK, Anjaiah V (2000) An efficient method for the production of transgenic plants of peanut (Arachis hypogaea L.) through Agrobacterium tumefaciens-mediated genetic transformation. Plant Sci 159:7–19.  https://doi.org/10.1016/S0168-9452(00)00294-6 CrossRefPubMedGoogle Scholar
  86. Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477.  https://doi.org/10.1105/tpc.010371 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85.  https://doi.org/10.1038/nbt766 CrossRefPubMedGoogle Scholar
  88. Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131.  https://doi.org/10.1016/j.sjbs.2014.12.001 CrossRefPubMedGoogle Scholar
  89. Sun YG, Wang B, Jin SH, Qu XX, Li YJ, Hou BK (2013) Ectopic expression of Arabidopsis glycosyltransferase UGT85A5 enhances salt stress tolerance in tobacco. PLoS ONE.  https://doi.org/10.1371/journal.pone.0059924 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270.  https://doi.org/10.1111/j.1365-3040.2011.02336.x CrossRefPubMedGoogle Scholar
  91. Swathi Anuradha T, Divya K, Jami SK, Kirti PB (2008) Transgenic tobacco and peanut plants expressing a mustard defensin show resistance to fungal pathogens. Plant Cell Rep 27:1777–1786.  https://doi.org/10.1007/s00299-008-0596-8 CrossRefPubMedGoogle Scholar
  92. Taffouo VD, Wamba OF, Youmbi E, Nono GV, Akoa A (2010) Growth, yield, water status and ionic distribution response of three bambara groundnut (Vignas ubterranea (L.) Verdc.) landraces grown under saline conditions. Int J Bot 6:53–58.  https://doi.org/10.3923/ijb.2010.53.58 CrossRefGoogle Scholar
  93. Tang W, Newton RJ, Weidner DA (2007) Genetic transformation and gene silencing mediated by multiple copies of a transgene in eastern white pine. J Exp Bot 58:545–554.  https://doi.org/10.1093/jxb/erl228 CrossRefPubMedGoogle Scholar
  94. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527.  https://doi.org/10.1093/aob/mcg058 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Tian F, Chang E, Li Y, Sun P, Hu J, Zhang J (2017) Expression and integrated network analyses revealed functional divergence of NHX-type Na+/H+ exchanger genes in poplar. Sci Rep 7:2607.  https://doi.org/10.1038/s41598-017-02894-8 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Tiwari S, Tuli R (2012) Optimization of factors for efficient recovery of transgenic peanut (Arachis hypogaea L.). Plant Cell, Tissue Organ Cult 109:111–121.  https://doi.org/10.1007/s11240-011-0079-4 CrossRefGoogle Scholar
  97. Tiwari S, Mishra DK, Singh A, Singh PK, Tuli R (2008) Expression of a synthetic cry1EC gene for resistance against Spodoptera litura in transgenic peanut (Arachis hypogaea L.). Plant Cell Rep 27:1017–1025.  https://doi.org/10.1007/s00299-008-0525-x CrossRefPubMedGoogle Scholar
  98. Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236.  https://doi.org/10.1093/53.372.1227 CrossRefPubMedGoogle Scholar
  99. Wang X, Yang R, Wang B, Liu G, Yang C, Cheng Y (2011) Functional characterization of a plasma membrane Na+/H+ antiporter from alkali grass (Puccinellia tenuiflora). Mol Biol Rep 38:4813–4822.  https://doi.org/10.1007/s11033-010-0624-y CrossRefPubMedGoogle Scholar
  100. Wu L, Fan Z, Guo L, Li Y, Chen ZL, Qu LJ (2005) Over-expression of the bacterial nhaA gene in rice enhances salt and drought tolerance. Plant Sci 168:297–302.  https://doi.org/10.1016/j.plantsci.2004.05.033 CrossRefGoogle Scholar
  101. Xu K, Huang B, Liu K, Qi F, Tan G, Li C, Zhang X (2016) Peanut regeneration by somatic embryogenesis (SE), involving bulbil-like body (BLB), a new type of SE structure. Plant Cell Tissie Org Cult 125:321–328.  https://doi.org/10.1007/s11240-016-0952-2 CrossRefGoogle Scholar
  102. Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol 12:188.  https://doi.org/10.1186/1471-2229-12-188 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (salt overly sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31.  https://doi.org/10.1093/mp/ssn058 CrossRefPubMedGoogle Scholar
  104. Yue Y, Zhang M, Zhang J, Duan L, Li Z (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. J Plant Physiol 169:255–261.  https://doi.org/10.1016/j.jplph.2011.10.007 CrossRefPubMedGoogle Scholar
  105. Zhang YM, Zhang HM, Liu ZH, Li HC, Guo XL, Li GL (2014) The wheat NHX antiporter gene TaNHX2 confers salt tolerance in transgenic alfalfa by increasing the retention capacity of intracellular potassium. Plant Mol Biol 87:317327.  https://doi.org/10.1007/s11103-014-0278-6 CrossRefGoogle Scholar
  106. Zhang WD, Wang P, Bao Z, Ma Q, Duan LJ, Bao AK, Zhang JL, Wang SM (2017) SOS1, HKT1;5, and NHX1 synergistically modulate Na+ homeostasis in the halophytic grass Puccinellia tenuiflora. Front Plant Sci 8:576.  https://doi.org/10.3389/fpls.2017.00576 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Venkatesh Kandula
    • 1
  • Amareshwari Pudutha
    • 1
  • P. Hima Kumari
    • 1
  • S. Anil Kumar
    • 2
  • P. B. Kavi Kishor
    • 1
  • Roja Rani Anupalli
    • 1
    Email author
  1. 1.Department of GeneticsOsmania UniversityHyderabadIndia
  2. 2.Department of BiotechnologyVignan’s Foundation for Science, Technology & ResearchGunturIndia

Personalised recommendations