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Plant function and evolutionary biology
RESEARCH ARTICLE

Physiology and gene expression of the rice landrace Horkuch under salt stress

Laisa A. Lisa A D , Sabrina M. Elias A D , M. Sazzadur Rahman A B , Saima Shahid A , Tetsushi Iwasaki C , A. K. M. Mahbub Hasan A , Keiko Kosuge C , Yasuo Fukami C and Zeba I. Seraj A D E
+ Author Affiliations
- Author Affiliations

A Plant Biotechnology Laboratory, Department of Biochemistry and Molecular Biology, University of Dhaka, Dhaka-1000, Bangladesh.

B Plant Physiology Division, Bangladesh Rice Research Institute, Gazipur-1701, Bangladesh.

C Research Center for Environmental Genomics, Kobe University, 1-1 Rokkodai, Nada, Kobe 657-8501, Japan.

D These authors contributed equally to the work of this manuscript.

E Corresponding author. Email: zebai@univdhaka.edu

Functional Plant Biology 38(4) 282-292 https://doi.org/10.1071/FP10198
Submitted: 5 October 2010  Accepted: 23 February 2011   Published: 8 April 2011

Abstract

Good donors in breeding for salt tolerance are a prerequisite for food security under changing climatic conditions. Horkuch, a farmer-popular salt tolerant rice (Oryza sativa L.) variety from the south-west coast of Bangladesh was characterised up to maturity under NaCl stress, together with a modern variety (BRRI dhan41), a sensitive control (BRRI dhan29) and Pokkali, the salt-tolerant benchmark for rice. Horkuch had low reduction in shoot biomass, a low Na : K ratio in flag leaves, a low percent reduction in yield and good partitioning of Na in the older leaves, and maintained high levels of Ca and Mg in the flag leaves. In order to understand the physiology at the molecular level, the expression of salt-responsive genes was investigated using microarray analysis. Salt-stressed cDNA of Horkuch seedlings were hybridised with cDNA probes synthesised mainly from database sequences of Arabidopsis thaliana (L.) Heynh. The upregulated genes included transcription factors, signal transducers, metabolic enzymes, reactive oxygen species (ROS) scavengers, osmoprotectants and some specific salt-induced transcripts. An increase in expression of photosynthesis-related genes as well ROS scavengers suggested that this could be the reason for the better yield performance of Horkuch. The data therefore indicate Horkuch as a potential donor alternative to Pokkali in breeding programs for salt tolerance.

Additional keywords: Bangladesh, donor, gene expression, Oryza sativa L., salt response.


References

Akbar M, Yabuni T, Nakao S (1972) Breeding for saline-resistant varieties of rice. I. Variability for salt tolerance among some rice varieties. Japanese Journal of Breeding 5, 277–284.

Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and Rubisco oxygenase. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1433–1446.
Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and Rubisco oxygenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovFKgsbg%3D&md5=b0c5d40614fbc82bf87fe5e65c871535CAS | 11127997PubMed |

Bennett J, Khush GS (2003) Enhancing salt tolerance in crops through molecular breeding: a new strategy. Journal of Crop Production 7, 11–65.

Bhumbla D, Abrol I (1978) Saline and sodic soils. In ‘Soils and rice’. pp. 719–738. (International Rice Research Institute: Manila)

BRRI (2004) Adhunic Dhaner Chash (a bengali booklet for modern rice cultivation in Bangladesh), 11th edn. (Bangladesh Rice Research Institute, BRRI: Gazipur, Bangladesh)

Chao DY, Luo YH, Shi M, Luo D, Lin HX (2005) Salt-responsive genes in rice revealed by cDNA microarray analysis. Cell Research 15, 796–810.
Salt-responsive genes in rice revealed by cDNA microarray analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSgt7zK&md5=11f574d2914a03e3c99a30984081a09aCAS | 16246269PubMed |

Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. The Plant Cell 14, 559–574.
Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVegt7g%3D&md5=e63bff68b3e4438580191ffe1f91835bCAS | 11910004PubMed |

Chourey K, Ramani S, Apte SK (2003) Accumulation of LEA proteins in salt (NaCl) stressed young seedlings of rice (Oryza sativa L.) cultivar Bura Rata and their degradation during recovery from salinity stress. Journal of Plant Physiology 160, 1165–1174.
Accumulation of LEA proteins in salt (NaCl) stressed young seedlings of rice (Oryza sativa L.) cultivar Bura Rata and their degradation during recovery from salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpslGktLo%3D&md5=5c7d3eea57753768cb13d0066420a2e9CAS | 14610885PubMed |

Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualisation and analysis in functional genomics research. Bioinformatics 21, 3674–3676.
Blast2GO: a universal tool for annotation, visualisation and analysis in functional genomics research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFGqt70%3D&md5=c1aa233dcb50c658847906ddec7cfdedCAS | 16081474PubMed |

Darwish E, Testerink C, Khalil M, El-Shihy O, Munnik T (2009) Phospholipid signaling responses in salt-stressed rice leaves. Plant & Cell Physiology 50, 986–997.
Phospholipid signaling responses in salt-stressed rice leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSnsb4%3D&md5=fa31e5d57218eba500e106711e5c6705CAS | 19369274PubMed |

de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20, 1453–1454.

Downie B, Gurusinghe S, Dahal P, Thacker RR, Snyder JC, Nonogaki H, Yim K, Fukanaga K, Alvarado V, Bradford KJ (2003) Expression of a galactinol synthase gene in tomato seeds is upregulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiology 131, 1347–1359.
Expression of a galactinol synthase gene in tomato seeds is upregulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFels7g%3D&md5=d0fbd5771879b3e00b2a4e0997793a38CAS | 12644684PubMed |

Forster BP, Ellis RP, Thomas WT, Newton AC, Tuberosa R, This D, el-Enein RA, Bahri MH, Ben Salem M (2000) The development and application of molecular markers for abiotic stress tolerance in barley. Journal of Experimental Botany 51, 19–27.
The development and application of molecular markers for abiotic stress tolerance in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXpslKjsw%3D%3D&md5=c79de4a74e57353b28b806bd05aa7868CAS | 10938792PubMed |

Fujiwara M, Umemura K, Kawasaki T, Shimamoto K (2006) Proteomics of Rac GTPase signaling reveals its predominant role in elicitor-induced defense response of cultured rice cells. Plant Physiology 140, 734–745.
Proteomics of Rac GTPase signaling reveals its predominant role in elicitor-induced defense response of cultured rice cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsV2iu70%3D&md5=799bc8707c010791a6a006c44042d156CAS | 16384895PubMed |

Gregorio G, Senadhira D, Mendoza R (1997) ‘Screening rice for salinity tolerance.’ International Rice Research Institute (IRRI) discussion paper series no. 22. (IRRI: Los Banos, Philippines)

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 Research 76, 91–101.
Progress in breeding for salinity tolerance and associated abiotic stresses in rice.Crossref | GoogleScholarGoogle Scholar |

Gu R, Fonseca S, Puskas LG, Hackler L, Zvara A, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiology 24, 265–276.

Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiology 132, 578–596.
Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslersbo%3D&md5=db5382bdfa5e8e2cd03413c6ea5dacf1CAS | 12805589PubMed |

IRRI (2007) ‘CROPSTAT, Version 6.1.’ (IRRI: Los Banos, Philippines)

Ismail A (2008) ‘Speeding the development of salt-tolerant rice varieties through marker-assisted selection and their dissemination in salt-affected areas of Bangladesh.’ Project abstract: commissioned project. (Generation Challenge Program: Mexico City)

Jagendorf AT, Takabe T (2001) Inducers of glycinebetaine synthesis in barley. Plant Physiology 127, 1827–1835.
Inducers of glycinebetaine synthesis in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVWksw%3D%3D&md5=72df9b8bf09349fdb5361e3140ae7bffCAS | 11743126PubMed |

Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. The Plant Cell 13, 889–905.

Khatun S, Rizzo CA, Flowers TJ (1995) Genotypic variation in the effect of salinity on fertility in rice. Plant and Soil 173, 239–250.
Genotypic variation in the effect of salinity on fertility in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnvVelu7s%3D&md5=7248f76a528402f8e38b15b07feb01b2CAS |

Kim YO, Pan S, Jung CH, Kang H (2007) A zinc finger-containing glycine-rich RNA-binding protein, atRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions. Plant & Cell Physiology 48, 1170–1181.
A zinc finger-containing glycine-rich RNA-binding protein, atRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKlsrvI&md5=403ff116920f867edda3cd243f7ec8bcCAS | 17602187PubMed |

Kumar A, Altabella T, Taylor M (1997) Recent advances in polyamines research. Trends in Plant Science 2, 124–130.
Recent advances in polyamines research.Crossref | GoogleScholarGoogle Scholar |

Lisa LA, Seraj ZI, Elahi1 CMF, Das KC, Biswas K, Islam MR, Salam MA, Gomosta AR (2004) Genetic variation in microsatellite DNA, physiology and morphology of coastal saline rice (Oryza sativa L.) landraces of Bangladesh. Plant and Soil 263, 213–228.
Genetic variation in microsatellite DNA, physiology and morphology of coastal saline rice (Oryza sativa L.) landraces of Bangladesh.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsF2ks7w%3D&md5=d465f07ca4fb9477060677a4a7221e75CAS |

Liu Q, Wang H, Zhang Z, Wu J, Feng Y, Zhu Z (2009) Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics 10, 313
Divergence in function and expression of the NOD26-like intrinsic proteins in plants.Crossref | GoogleScholarGoogle Scholar | 19604350PubMed |

Moons A, Bauw G, Prinsen E, Van Montagu M, Van der Straeten D (1995) Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant indica rice varieties. Plant Physiology 107, 177–186.
Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant indica rice varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVOmsLs%3D&md5=df38fe3f37dba7f0d774f911b086ad8aCAS | 7870812PubMed |

Moradi F, Ismail AM, Egdane J, Gregorio GB (2003) Salinity tolerance of rice during reproductive development and association with tolerance at the seedling stage. Indian Journal of Plant Physiology 8, 105–116.

Pandhal J, Noirel J, Wright PC, Biggs CA (2009) A systems biology approach to investigate the response of Synechocystis sp. PCC6803 to a high salt environment. Saline Systems 5, 8
A systems biology approach to investigate the response of Synechocystis sp. PCC6803 to a high salt environment.Crossref | GoogleScholarGoogle Scholar | 19735556PubMed |

Pearce DW, Warford J (1994) World without end, economics environment and sustainable development. (Oxford University Press: New York)

Peng S, Cassman KG, Virmani SS, Sheehy J, Khush GS (1999) Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Science 39, 1552–1559.
Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential.Crossref | GoogleScholarGoogle Scholar |

Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. The Plant Cell 16, 2128–2150.
Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVantrw%3D&md5=0d1cc2c20223ddc045d5407582a39f77CAS | 15273295PubMed |

Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, Mackinlay J, Loake GJ, Mundy J, Morris PC (2008) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiology 148, 212–222.
Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKmsbvL&md5=7f5261a1dcca3de1fd3988db4ce83c86CAS | 18599650PubMed |

Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiology 133, 1755–1767.
Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFCr&md5=909cdf99eda6288d447d9f9391f82607CAS | 14645724PubMed |

Rhoades JD, Loveday J (1990) Salinity in irrigated agriculture. In ‘American Society of Civil Engineers, irrigation of agricultural crops’. (Eds BA Steward, DR Nielsen) pp. 1089–1142. Monograph 30. (American Society of Agronomists: Madison, WI)

Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends in Plant Science 15, 247–258.
WRKY transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVaqsbk%3D&md5=fabb2da0df49388cdb6d93637437ebedCAS | 20304701PubMed |

Saibo NJ, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals of Botany 103, 609–623.
Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7c%3D&md5=979111fa47ece6bd67959ab8fbfad39dCAS | 19010801PubMed |

Senadheera P, Singh RK, Maathuis FJ (2009) Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. Journal of Experimental Botany 60, 2553–2563.
Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlGisb0%3D&md5=5e8ae59f6dd1cb6c0651126f489b5cd7CAS | 19395386PubMed |

Sengupta S, Majumder AL (2009) Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 229, 911–929.
Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agsb0%3D&md5=420434aa7ef5232430d763dffe98b395CAS | 19130079PubMed |

Silva P, Geros H (2009) Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signaling & Behavior 4, 718–726.
Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1Knsb4%3D&md5=e2b6da69e98a5b16dbb72f0b6a1b6869CAS | 19820346PubMed |

Singh S, Cornilescu CC, Tyler RC, Cornilescu G, Tonelli M, Lee MS, Markley JL (2005) Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress-related protein. Protein Science 14, 2601–2609.
Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress-related protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOrur%2FI&md5=c1febd993efd2e949fc9fa999d382c16CAS | 16155204PubMed |

Suarez DL, (1996) Beryllium, magnesium, calcium, strontium and barium. In: ‘Methods of Soil Analysis. Part 3. Chemical Methods.’ (Ed. DL Sparks) pp. 583–584. (Soil Science Society of America, Inc. American Society of Agronomy, Inc.: Madison, WI)

Thornalley PJ, Vasak M (1985) Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochimica et Biophysica Acta 827, 36–44.
Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXptFKhtA%3D%3D&md5=36e197a9778d234f753fd5ad77228b83CAS | 2981555PubMed |

Wang E, Miller LD, Ohnmacht GA, Liu ET, Marincola FM (2000) High-fidelity mRNA amplification for gene profiling. Nature Biotechnology 18, 457–459.
High-fidelity mRNA amplification for gene profiling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXis1GlsLo%3D&md5=c029c9a2e0cb99055ddd3662cbd6402bCAS | 10748532PubMed |

Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, Tang HJ, Zhang HS (2008) Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Letters 582, 1037–1043.
Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1Khsb8%3D&md5=c7b44b71fa7a0f02e11a92c57d7c226dCAS | 18325341PubMed |

Yoshida S, Forno DA, Cock JH, Gomez KA (1976) ‘Laboratory manual for physiological studies of rice.’ 3rd edition. (IRRI: Los Banos, Philippines)

Zhang X, Liu S, Takano T (2008) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Molecular Biology 68, 131–143.
Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVGltLc%3D&md5=5699640c689a39262bd67521471b0623CAS | 18523728PubMed |