Advertisement

Plant Molecular Biology

, Volume 93, Issue 1–2, pp 61–77 | Cite as

Five novel transcription factors as potential regulators of OsNHX1 gene expression in a salt tolerant rice genotype

  • Diego M. Almeida
  • Glenn B. Gregorio
  • M. Margarida Oliveira
  • Nelson J. M. SaiboEmail author
Article

Abstract

Key message

This manuscript reports the identification and characterization of five transcription factors binding to the promoter of OsNHX1 in a salt stress tolerant rice genotype (Hasawi). Although NHX1 encoding genes are known to be highly regulated at the transcription level by different abiotic stresses, namely salt and drought stress, until now only one transcription factor (TF) binding to its promoter has been reported. In order to unveil the TFs regulating NHX1 gene expression, which is known to be highly induced under salt stress, we have used a Y1H system to screen a salt induced rice cDNA expression library from Hasawi. This approach allowed us to identify five TFs belonging to three distinct TF families: one TCP (OsPCF2), one CPP (OsCPP5) and three NIN-like (OsNIN-like2, OsNIN-like3 and OsNIN-like4) binding to the OsNHX1 gene promoter. We have also shown that these TFs act either as transcriptional activators (OsPCF2, OsNIN-like4) or repressors (OsCPP5, OsNIN-like2) and their encoding genes are differentially regulated by salt and PEG-induced drought stress in two rice genotypes, Nipponbare (salt-sensitive) and Hasawi (salt-tolerant). The transactivation activity of OsNIN-like3 was not possible to determine. Increased soil salinity has a direct impact on the reduction of plant growth and crop yield and it is therefore fundamental to understand the molecular mechanisms underlying gene expression regulation under adverse environmental conditions.

Abstract

OsNHX1 is the most abundant K+-Na+/H+ antiporter localized in the tonoplast and its gene expression is induced by salt, drought and ABA. To investigate how OsNHX1 is transcriptionally regulated in response to salt stress in a salt-tolerant rice genotype (Hasawi), a salt-stress-induced cDNA expression library was constructed and subsequently screened using the yeast one-hybrid system and the OsNHX1 promoter as bait. Five transcription factors (TFs) belonging to three distinct TF families: one TCP (OsPCF2), one CPP (OsCPP5) and three NIN-like (OsNIN-like2, OsNIN-like3 and OsNIN-like4) were identified as binding to OsNHX1 promoter. Transactivation activity assays performed in Arabidopsis and rice protoplasts showed that OsPCF2 and OsNIN-like4 are activators of the OsNHX1 gene expression, while OsCPP5 and OsNIN-like2 act as repressors. The transactivation activity of OsNIN-like3 needs to be further investigated. Gene expression studies showed that OsNHX1 transcript level is highly induced by salt and PEG-induced drought stress in both shoots and roots in both Nipponbare and Hasawi rice genotypes. Nevertheless, OsNHX1 seems to play a particular role in shoots in response to drought. Most of the TFs binding to OsNHX1 promoter showed a modest transcriptional regulation under stress conditions, however, in response to most of the conditions studied, the OsPCF2 was induced earlier than OsNHX1, indicating that OsPCF2 may activate OsNHX1 gene expression. In addition, although the OsNHX1 response to salt and PEG-induced drought stress in either shoots or roots was quite similar in both rice genotypes, the expression of OsPCF2 in roots under salt stress and the OsNIN-like4 in roots subjected to PEG was mainly up-regulated in Hasawi, indicating that these TFs may be associated with the salt and drought stress tolerance observed for this genotype.

Keywords

Salt stress Drought NHX1 PCF2 CPP5 NIN-like 

Notes

Acknowledgments

DMA was financed by Fundação para a Ciência e Tecnologia (FCT) through the fellowship SFRH/BD/65229/2009. NS was supported by Programa Ciência 2007 and FCT Investigator, financed by POPH (QREN).

Funding

This work was funded by Research unit GREEN-it “Bioresources for Sustainability” (UID/Multi/04551/2013) and by FCT project PTDC/BIA_BCM/099836/2008.

Author contributions

D.M.A. performed all the experiments (rice treatments, cDNA library construction, Y1H screening, transctivation analysis, cellular localization, RT-qPCR), analyzed the data, and wrote the article. GG was involved in salt treatments and salt stress evaluation, GG, M.M.O. and N.J.M.S conceived the project and M.M.O. and N.J.M.S revised the article.

Supplementary material

11103_2016_547_MOESM1_ESM.pptx (540 kb)
Supplementary material 1 (PPTX 539 KB)
11103_2016_547_MOESM2_ESM.pptx (98 kb)
Supplementary material 2 (PPTX 98 KB)

References

  1. Adler G, Blumwald E, Bar-Zvi D (2010) The sugar beet gene encoding the sodium/proton exchanger 1 (BvNHX1) is regulated by a MYB transcription factor. Planta 232:187–195. doi: 10.1007/s00425-010-1160-7 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Almeida DM, Almadanim MC, Lourenço T, Abreu IA, Saibo NJ, Oliveira MM (2016) Screening for abiotic stress tolerance in rice: salt, cold and drought. In: P Duque (ed) Environmental responses in plants, methods in molecular biology. Springer, New York. doi: 10.1007/978-1-4939-3356-3_14 Google Scholar
  3. Andrés Z, Perez-Hormaeche J, Leidi EO, Schlucking K, Steinhorst L, McLachlan DH, Schumacher K, Hetherington AM, Kudla J, Cubero B, Pardo JM (2014) Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake. Proc Natl Acad Sci USA 111:E1806–E1814. DOI: 10.1073/pnas.1320421111 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581. DOI: 10.1038/sj.emboj.7600068 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239. DOI: 10.1046/j.1365-313X.2003.01871.x CrossRefPubMedGoogle Scholar
  6. Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–1142. doi: 10.1105/tpc.111.095273 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bassil E, Blumwald E (2014) The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters. Curr Opin Plant Biol 22:1–6. DOI: 10.1016/j.pbi.2014.08.002 CrossRefPubMedGoogle Scholar
  8. Bassil E, Tajima H, Liang YC, Ohto MA, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011a) 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. DOI: 10.1105/tpc.111.089581
  9. Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011b) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23:224–239. DOI: 10.1105/tpc.110.079426
  10. Bassil E, Coku A, Blumwald E (2012) Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot 63:5727–5740. DOI: 10.1093/jxb/ers250 CrossRefPubMedGoogle Scholar
  11. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernández E, Meyer C, Krapp A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435. DOI: 10.1111/j.1365-313X.2008.03695.x CrossRefPubMedGoogle Scholar
  12. Castaings L, Marchive C, Meyer C, Krapp A (2011) Nitrogen signalling in Arabidopsis: how to obtain insights into a complex signalling network. J Exp Bot 62:1391–1397. DOI: 10.1093/jxb/erq375 CrossRefPubMedGoogle Scholar
  13. Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222CrossRefPubMedGoogle Scholar
  14. Cvitanich C, Pallisgaard N, Nielsen KA, Hansen AC, Larsen K, Pihakaski-Maunsbach K, Marcker KA, Jensen EO (2000) CPP1, a DNA-binding protein involved in the expression of a soybean leghemoglobin c3 gene. Proc Natl Acad Sci USA 97:8163–8168. DOI: 10.1073/pnas.090468497 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Degenkolbe T, Do PT, Zuther E, Repsilber D, Walther D, Hincha DK, Köhl KI (2009) Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Mol Biol 2:133–153. doi: 10.1007/s11103-008-9412-7 CrossRefGoogle Scholar
  16. Djanaguiraman M, Prasad P.V.V. (2012) Effects of salinity on ion transport, water relations and oxidative damage. In: Springer-Verlag New, York Inc. (eds) Ecophysiology and responses of plants under salt stress. Springer, New YorkGoogle Scholar
  17. Fedorova E, Zink D (2008) Nuclear architecture and gene regulation. Biochim Biophys Acta 1783:2174–2184. doi: 10.1016/j.bbamcr.2008.07.018
  18. Ferdose J, Kawasaki M, Taniguchi M, Miyake H (2009) Differential sensitivity of rice cultivars to salinity and its relation to ion accumulation and root tip structure. Plant Prod Sci 4:453–461. doi: 10.1626/pps.12.453 CrossRefGoogle Scholar
  19. Figueiredo DD, Barros PM, Cordeiro AM, Serra TS, Lourenço T, Chander S, Oliveira MM, Saibo NJ (2012) Seven zinc-finger transcription factors are novel regulators of the stress responsive gene OsDREB1B. J Exp Bot 63:3643–3656. doi: 10.1093/jxb/ers035 CrossRefPubMedGoogle Scholar
  20. Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155. doi: 10.1016/S0167-4781(99)00065-2 CrossRefPubMedGoogle Scholar
  21. Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233:175–188. doi: 10.1007/s00425-010-1289-4 CrossRefPubMedGoogle Scholar
  22. Gao J-P, Chao D-Y, Lin H-X (2007) Understanding abiotic stress tolerance mechanisms: Recent studies on stress response in rice. J Integr Plant Biol 49:742–750. doi: 10.1111/j.1744-7909.2007.00495.x CrossRefGoogle Scholar
  23. Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA 96:1480–1485. DOI: 10.1073/pnas.96.4.1480 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gong Q, Li P, Ma S, Indu RS, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 445:826–839. doi: 10.1111/j.1365-313X.2005.02587.x CrossRefGoogle Scholar
  25. Gregorio GB, Senadhira D, Mendoza RD (1997) Screening rice for salinity tolerance. IRRI Discussion Paper Series No. 22Google Scholar
  26. Gregorio GB, Senadhira D, Mendoza RD, Manigbas NL, Roxas JP, Guerta CQ (2002) Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crops Res 76:91–101. doi: 10.1016/S0378-4290(02)00031-X CrossRefGoogle Scholar
  27. Hamada A, Shono M, Xia T, Ohta M, Hayashi Y, Tanaka A, Hayakawa T (2001) Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol Biol 46:35–42. doi: 10.1023/A:1010603222673 CrossRefPubMedGoogle Scholar
  28. Hauser B, He J, SO P, Gasser C (2000) TSO1 is a novel protein that modulates cytokinesis and cell expansion in Arabidopsis. Development 127:2219–26PubMedGoogle Scholar
  29. Jiang X, Leidi EO, Pardo JM (2010) How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal Behav. doi: 10.4161/psb.5.7.11767 Google Scholar
  30. Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182–D1187. doi: 10.1093/nar/gkt1016 CrossRefPubMedGoogle Scholar
  31. Konishi M, Yanagisawa S (2011) Roles of the transcriptional regulation mediated by the nitrate-responsive cis-element in higher plants. Biochem Biophys Res Commun 411:708–713. doi: 10.1016/j.bbrc.2011.07.008 CrossRefPubMedGoogle Scholar
  32. Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun. doi: 10.1038/ncomms2621 PubMedCentralGoogle Scholar
  33. Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619. doi: 10.1105/tpc.9.9.1607 CrossRefGoogle Scholar
  34. Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348. doi: 10.1046/j.1365-313X.2002.01294.x CrossRefPubMedGoogle Scholar
  35. Kosugi S, Hasebe M, Tomita M, Yanagawa H (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA 106:10171–10176. DOI: 10.1073/pnas.0900604106 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kumari S, Sabharwal VP, Kushwaha HR, Sopory SK, Singla-Pareek SL, Pareek A (2009) Transcriptome map for seedling stage specific salinity stress response indicates a specific set of genes as candidate for saline tolerance in Oryza sativa L. Funct Integr Genomics 9:109–123. doi: 10.1007/s10142-008-0088-5 CrossRefPubMedGoogle Scholar
  37. Leidi EO, Barragán V, Rubio L, El-Hamdaoui A, Ruiz MT, Cubero B, Fernández JA, Bressan RA, Hasegawa PM, Quintero FJ, Pardo JM (2010) The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J 61:495–506. doi: 10.1111/j.1365-313X.2009.04073.x CrossRefPubMedGoogle Scholar
  38. Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102:12978–12983. doi: 10.1073/pnas.0504039102 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Liu Z., Running M.P., Meyerowitz E.M. (1997) TSO1 functions in cell division during Arabidopsis flower development. Development 124:665–72PubMedGoogle Scholar
  40. Liu P, Yang G-D, Li H, Zheng C-C, Wu C-A (2010) Overexpression of NHX1 in transgenic Arabidopsis enhances photoprotection capacity in high salinity and drought conditions. Acta Physiol Plant 32:81–90. doi: 10.1007/s11738-009-0383-3 CrossRefGoogle Scholar
  41. Liu C, Mao B, Ou S, Wang W, Liu L, Wu Y, Chu C, Wang X (2014) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84:19–36. doi: 10.1007/s11103-013-0115-3 CrossRefPubMedGoogle Scholar
  42. Maggio A, Zhu J-K, Hasegawa PM, Bressan RA (2006) Osmogenetics: Aristotle to Arabidopsis. Plant Cell 18:1542–1557. doi: 10.1105/tpc.105.040501
  43. Manassero NGU, Viola IL, Welchen E, Gonzalez DH (2013) TCP transcription factors: architecture of plants form. Biomol Concepts. 4:111–27. doi: 10.1515/bmc-2012-0051 CrossRefPubMedGoogle Scholar
  44. Marchive C, Roudier F, Castaings L, Brehaut V, Blondet E, Colot V, Meyer C, Krapp A (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4:1713. doi: 10.1038/ncomms2650 CrossRefPubMedGoogle Scholar
  45. Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu J-K, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:2. doi: 10.1104/pp.106.092635 Google Scholar
  46. Michael G, André L (2002) Global impact of salinity and agricultural ecosystems. In: Läuchli A, Lüttge U (eds), Salinity: environment—plants—molecules. Kluwer Academic Publishers, Dodrecht, pp 3–20Google Scholar
  47. Mohammadi-Nejad G, Arzani A, Reza AM, Singh RK, Gregorio GB (2008) Assessment of rice genotypes for salt tolerance using microsatellite markers associated with the saltol QTL. Afr J Biotechnol 6:730–736Google Scholar
  48. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi: 10.1146/annurev.arplant.59.032607.092911 CrossRefPubMedGoogle Scholar
  49. Negrão S, Almadanim MC, Pires IS, Abreu IA, Maroco J, Courtois B, Gregorio GB, McNally KL, Oliveira MM (2013) New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol J 11:87–100. doi: 10.1111/pbi.12010 CrossRefPubMedGoogle Scholar
  50. Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282. doi: 10.1016/S0014-5793(02)03679-7 CrossRefPubMedGoogle Scholar
  51. Ouwerkerk P.B., Meijer A.H. (2001) Yeast one-hybrid screening for DNA–protein interactions. Curr Protoc Mol Biol Chap. doi: 10.1002/0471142727.mb1212s55 Google Scholar
  52. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887. doi: 10.1093/nar/gkl976 CrossRefPubMedGoogle Scholar
  53. Pires IS, Negrão S, Oliveira MM, Purugganan MD (2015) Comprehensive phenotypic analysis of rice (Oryza sativa) response to salinity stress. Physiol Plant. doi: 10.1111/ppl.12356 PubMedGoogle Scholar
  54. Reguera M, Bassil E, Tajima H, Wimmer M, Chanoca A, Otegui MS, Paris N, Blumwald E (2015) pH regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis. Plant Cell 27:1200–1217. doi: 10.1105/tpc.114.135699 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rodríguez-Rosales MP, Galvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O, Venema K (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4:265–276CrossRefPubMedPubMedCentralGoogle Scholar
  56. Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124. doi: 10.1016/j.copbio.2013.12.004 CrossRefPubMedGoogle Scholar
  57. Santos AP, Serra T, Figueiredo DD, Barros P, Lourenço T, Chander S, Oliveira MM, Saibo NJ (2011) Transcription regulation of abiotic stress responses in rice: a combined action of transcription factors and epigenetic mechanisms. OMICS 15:839–857. doi: 10.1089/omi.2011.0095 CrossRefPubMedGoogle Scholar
  58. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195. doi: 10.1038/46058 CrossRefPubMedGoogle Scholar
  59. Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60:229–237. doi: 10.1007/s00239-004-0144-2 CrossRefPubMedGoogle Scholar
  60. Schmit F, Cremer S, Gaubatz S (2009) LIN54 is an essential core subunit of the DREAM/LINC complex that binds to the cdc2 promoter in a sequence-specific manner. FEBS J 219:5703–5716. doi: 10.1111/j.1742-4658.2009.07261 CrossRefGoogle Scholar
  61. Sorokin AV, Kim ER, Ovchinnikov LP (2007) Nucleocytoplasmic transport of proteins. BioChemistry 72:1439–1457. doi: 10.1134/S0006297907130032 PubMedGoogle Scholar
  62. Sottosanto JB, Gelli A, Blumwald E (2004) DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na+/H+ antiporter: impact of AtNHX1 on gene expression. Plant J 40:752–771. doi: 10.1186/1471-2229-7-18 CrossRefPubMedGoogle Scholar
  63. Tavares B, Domingos P, Dias PN, Feijo JA, Bicho A (2011) The essential role of anionic transport in plant cells: the pollen tube as a case study. J Exp Bot 62:2273–2298. doi: 10.1093/jxb/err036 CrossRefPubMedGoogle Scholar
  64. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139:822–835. doi: 10.1104/pp.105.065961 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, Close TJ (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63:609–623. doi: 10.1007/s11103-006-9112-0 CrossRefPubMedGoogle Scholar
  66. Xia T, Apse MP, Aharon GS, Blumwald E (2002) Identification and characterization of a NaCl-inducible vacuolar Na+/H + antiporter in Beta vulgaris. Physiol Plant 116:206–212. doi: 10.1034/j.1399-3054.2002.1160210.x CrossRefPubMedGoogle Scholar
  67. Xiao B-Z, Chen X, Xiang C-B, Tang N, Zhang Q-F, Xionga L-Z (2008) Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol Plant 2:73–83. doi: 10.1093/mp/ssn068 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Xuea Z-Y, Zhia D-Y, Xueb G-P, Zhangc H, Zhaoc Y-X, Xiaa G-M (2004) Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci 167:849–859CrossRefGoogle Scholar
  69. Yang Z, Gu S, Wang X, Li W, Tang Z, Xu C (2008) Molecular evolution of the CPP-like gene family in plants: insights from comparative genomics of Arabidopsis and rice. J Mol Evol 67:266–277. doi: 10.1007/s00239-008-9143-z CrossRefPubMedGoogle Scholar
  70. Yao X, Ma H, Wang J, Zhang D (2007) Genome-wide comparative analysis and expression pattern of TCP gene families in Arabidopsis thaliana and Oryza sativa. J Integr Plant Biol 49:885–897. DOI: 10.1111/j.1744-7909.2007.00509.x CrossRefGoogle Scholar
  71. Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539. doi: 10.1046/j.1365-313X.2002.01309.x CrossRefPubMedGoogle Scholar
  72. Yoshida S, Forno D, Cock J, Gomez K (1976) Laboratory manual for physiological studies of rice. Internationa Rice Research Instirute (IRRI), ManilaGoogle Scholar
  73. Zhang H-X, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768. doi: 10.1038/90824 CrossRefPubMedGoogle Scholar
  74. Zhang GH, Su Q, An LJ, Wu S (2008) Characterization and expression of a vacuolar Na+/H+ antiporter gene from the monocot halophyte Aeluropus littoralis. Plant Physiol Biochem 462:117–126. doi: 10.1016/j.plaphy.2007.10.022 CrossRefGoogle Scholar
  75. Zhang T, Hu S, Zhang G, Pan L, Zhang X, Al-Mssallem IS, Yu J (2012) The organelle genomes of Hassawi rice (Oryza sativa L.) and its hybrid in saudi arabia: genome variation, rearrangement, and origins. PLOS ONE 7:e42041. doi: 10.1371/journal.pone.0042041 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Diego M. Almeida
    • 1
  • Glenn B. Gregorio
    • 2
    • 3
  • M. Margarida Oliveira
    • 1
  • Nelson J. M. Saibo
    • 1
    Email author
  1. 1.Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António XavierUniversidade Nova de Lisboa and Instituto de Biologia Experimental e TecnológicaOeirasPortugal
  2. 2.International Rice Research InstituteMetro ManilaPhilippines
  3. 3.East-West Seed Company (EWS)San RafaelPhilippines

Personalised recommendations