Isolation of Salt Stress Tolerance Genes from Roots of Mangrove Plant, Rhizophora stylosa Griff., Using PCR-Based Suppression Subtractive Hybridization

Plant Molecular Biology Reporter

Volumn 29, Issue 3, 2011, Pages 533-543

  Basyuni, Mohammad ^a,b   Kinjo, Yuji ^a   Baba, Shigeyuki ^a   Shinzato, Naoya ^a   Iwasaki, Hironori ^a   Siregar, Edy B M ^b   Oku, Hirosuke ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

^b UNIVERSITY OF SUMATERA UTARA   (Indonesia)

Author keywords

Expressed sequence tag; Isoprenoid biosynthesis; Mangrove; Rhizophora stylosa; Salt tolerance; Suppressive subtractive hybridization library

Indexed keywords

RHIZOPHORA STYLOSA;

EID: 79958744401     PISSN: 07359640     EISSN: 15729818     Source Type: Journal    
DOI: 10.1007/s11105-010-0257-2     Document Type: Article

References (65)

1. Altschul SF, Madden TL, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res 25: 3389-3402.
2. Arabidopsis Genome Initiative (2000) Arabidopsis genome initiative, analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
3. Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (-) - germacrene D synthase, PtdTPS1. Plant J 37: 603-616.
4. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8: 242. doi: 10. 1186/1471-2164-8-242.
5. Banzai T, Hershkovits G, Katcoff DJ, Hanagata N, Dubinsky Z, Karube I (2002) Identification and characterization of mRNA transcripts differentially display in the mangrove, Bruguiera gymnorrhiza. Plant Sci 162: 499-505.
6. Basyuni M, Oku H, Inafuku M, Baba S, Iwasaki H, Oshiro K, Okabe T, Shibuya M, Ebizuka Y (2006) Molecular cloning and functional expression of a multifunctional triterpene synthase cDNA from a mangrove species Kandelia candel (L.) Druce. Phytochemistry 67: 2517-2524.
7. Basyuni M, Oku H, Tsujimoto E, Kinjo K, Baba S, Takara T (2007) Triterpene synthases from the Okinawan mangrove tribe, Rhizophoraceae. FEBS J 274: 5028-5042.
8. Basyuni M, Baba S, Inafuku M, Iwasaki H, Kinjo K, Oku H (2009) Expression of terpenoid synthase mRNA and terpenoid content in salt stressed mangrove. J Plant Physiol 166: 1786-1800.
9. Bohnert HJ, Ayoubi P, Borchert C et al (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39: 295-311.
10. Boudsocq M, Laurière C (2005) Osmotic signaling in plants. Multiple pathways mediated by mediated by emerging kinase families. Plant Physiol 138: 1185-1194.
11. Brandle JE, Richman A, Swanson AK, Chapman BP (2002) Leaf ESTs from Stevia rebaudiana: a source for gene discovery in diterpene synthesis. Plant Mol Biol 50: 613-622.
12. Bunt JS, Williams WT, Clay HJ (1982) River water salinity and the distribution of mangrove species along several rivers in North Queensland. Aust J Bot 30: 401-412.
13. Chen N, Liu Y, Liu X, Chai J, Hu Z, Guo G, Liu H (2009) Enhanced tolerance to water deficit and salinity stress in transgenic Lycium barbarum L. plants ectopically expressing ATHK1, an Arabidopsis thaliana histidine kinase gene. Plant Mol Biol Rep 27: 321-333. doi: 10. 1007/s11105-008-0084-x.
14. Choi DW, Jung JD, Ha YI, Park HW, In DS, Chung HJ, Liu JR (2005) Analysis of transcripts in methyl jasmonate-treated ginseng hairy roots to identify genes involved in the biosynthesis of ginsenosides and other secondary metabolites. Plant Cell Rep 23: 557-566.
15. Cooper B, Clarke JD, Budworth P et al (2003) A nework of rice genes associated with stress response and seed development. Proc Natl Acad Sci USA 100: 4945-4950.
16. Davenport KR, Sohaskey M, Kamada Y, Levin DE, Gustin MC (1995) A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270: 30157-30161.
17. de Folter S, Angenent GC (2006) Trans meets cis in MADS science. Tends Plant Sci 11: 224-231.
18. de Nadal E, Casadomé L, Posas F (2003) Targeting the MEF2-like transcription factor Smp1 by the stress-activated Hog1 mitogen-activated protein kinase. Mol Cell Biol 23: 229-237.
19. Dodou E, Treisman R (1997) The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol Cell Biol 17: 1848-1859.
20. Droillard MJ, Boudsocq M, Barbier-Brygoo H, Laurière C (2002) Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett 11: 43-50.
21. Droillard MJ, Boudsocq M, Barbier-Brygoo H, Laurière C (2004) Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 10: 42-48.
22. Duan K, Yang H, Ran K, You S, Zhao H, Jiang Q (2009) Characterization of a novel stress-response member of the MAPK family in Malus hupehensis Rehd. Plant Mol Biol Rep 27: 69-78. doi: 10. 1007/s11105-008-0057-0.
23. Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt J, Miller B, Bohlmann J (2003) (E)-β-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15: 1227-1241.
24. Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Glob Ecol Biogeogr Lett 7: 27-47.
25. Ezawa S, Tada Y (2009) Identification of salt tolerance genes from the mangrove plant Bruguiera gymnorrhiza using Agrobacterium functional screening. Plant Sci 176: 272-278.
26. Fang Q, Xu Z, Song R (2006) Cloning, characterization and genetic engineering of FLC homolog in Thellungiella halophila. Biochem Biophys Res Commun 347: 707-714.
27. Fofonoff NP, Lewis EL (1979) A practical salinity scale. J Oceanogr Soc Japan 35: 63-64.
28. Fu XH, Huang YL, Deng SL, Zhou RC, Yang GL, Ni XW, Li WJ, Shi SH (2005) Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Plant Sci 169: 147-154.
29. Gao C, Wang Y, Liu G, Wang C, Jiang J, Yang C (2010) Cloning of ten peroxidase (POD) genes from Tamarix Hispida and characterization of their responses to abiotic stress. Plant Mol Biol Rep 28: 77-89.
30. Gosti F, Bertauche N, Vartanian N, Giraudat J (1995) Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246: 10-18.
31. 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 Physiol 24: 265-276.
32. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463-499.
33. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinase ATMPK4 and ATMPK6. Plant J 24: 655-665.
34. Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E (2004) Characterization of geraniol synthase from the peltate glands of Sweet basil. Plant Physiol 134: 370-379.
35. Jack T (2001) Plant development going MADS. Plant Mol Biol 46: 515-520.
36. Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54: 713-725.
37. Jin S, Xu R, Wei Y, Goodwin PH (1999) Increased expression of a plant actin gene during a biotrophic interaction between round-leaved mallow, Malva pusilla, and Colletotrichum gloeosporioides f. sp. malvae. Planta 209: 487-494.
38. Jung US, Levin DE (1999) Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signaling pathway. Mol Microbiol 34: 1049-1057.
39. Jung US, Sobering AK, Romeo MJ, Levin DE (2002) Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase. Mol Microbiol 46: 781-789.
40. Kaufmann K, Melzer R, Theissen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347: 183-198.
41. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141.
42. Larionov A, Krause A, Miller WA (2005) Standard curve based method for relative real time PCR data processing. BMC Bioinform 6: 62. doi: 10. 1186/1471-2105-6-62.
43. Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphotase 2C mutant. Plant Cell 16: 596-615.
44. Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res 16: 414-427.
45. Lorenzo LD, Merchan F, Laporte P, Thomson R, Clarke J, Sousa C, Crespi M (2009) A novel plant leucine-rich repeat receptor kinase regulates the response of Medicago truncatula roots to salt stress. Plant Cell 21: 668-680.
46. Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 100: 9061-9066.
47. Matsuoka D, Nanmori T, Sato K, Fukami Y, Kikkawa U, Yasuda T (2002) Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant J 29: 637-647.
48. Mehta PA, Sivaprakash K, Parani M, Venkatarama G, Parida AK (2005) Generation and analysis of expressed sequence tags from the salt-tolerant mangrove species Avicennia marina (Forsk) Vierh. Ther Appl Genet 110: 416-424.
49. Miller B, Madilao LL, Ralph S, Bohlmann J (2005) Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol 137: 369-382.
50. Miyama M, Tada Y (2008) Transcriptional and physiological study of the response of Burma mangrove (Bruguiera gymnorrhiza) to salt and osmotic stress. Plant Mol Biol 68: 119-129.
51. Munns R (2005) Genes and salt tolerance: bring them together. New Phytol 167: 645-663.
52. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165-185.
53. Nguyen PD, Ho CL, Harikrishna JA, Wong MCVL, Rahim RA (2006) Generation and analysis of expressed sequence tags from the mangrove plant, Acanthus ebracteatus Vahl. Tree Genet Genomes 2: 196-201.
54. Osbourn AE, Qi X, Townsend B, Qin B (2003) Dissecting plant secondary metabolism-constitutive chemical defenses in cereals. New Phytol 159: 101-108.
55. Park JS, Kim JB, Hahn BS, Kim KH, Ha SH, Kim JB, Kim YH (2004) EST analysis of genes involved in secondary metabolism in Camellia sinensis (tea), using suppression subtractive hybridization. Plant Sci 166: 953-961.
56. Ralph SG, Chun HJ, Cooper D et al (2008) Analysis of 4, 664 high-quality sequence-finished poplar full-length cDNA clones and their utility for the discovery of genes responding to insect feeding. BMC Genomics 9: 57. doi: 10. 1186/1471-2164-9-57.
57. Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters: novel plant salt stress tolerance-related genes from transcriptional profiling data. Physiol Plant 127: 1-9.
58. Seki M, Ishida J, Narusaka M et al (2002) Monitoring the expression pattern of around 7, 000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Plant J 31: 279-292.
59. Shimada T, Endo T, Fujii H, Hara M, Ueda T, Kita M, Omura M (2004) Molecular cloning and functional characterization of four monoterpene synthase genes from Citrus unshiu Marc. Plant Sci 166: 49-58.
60. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221-227.
61. Wakushima S, Kuraishi S, Sakurai N (1994) Soil salinity and pH in Japanese mangrove forests and growth of cultivated mangrove plants in different soil conditions. J Plant Res 107: 39-46.
62. Watanabe Y, Irie K, Matsumoto K (1995) Yeast RLM1 encodes a serum response factor-like protein that may function downstream of the Mpk 1 (Slt2) mitogen-activated protein kinase pathway. Mol Cell Biol 15: 5740-5749.
63. Watanabe Y, Takaesu G, Hagiwara M, Irie K, Matsumoto K (1997) Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol Cell Biol 17: 2615-2623.
64. Wong YY, Ho CL, Nguyen PD, Teo SS, Harikrishna JA, Rahim RA, Wong MCVL (2007) Isolation of salinity tolerant genes from the mangrove plant, Bruguiera cylindrica by using suppression subtractive hybridization (SSH) and bacterial functional screening. Aquat Bot 86: 117-122.
65. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781-803.