Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots

Planta

Volumn 238, Issue 4, 2013, Pages 669-681

  Nguyen, Minh Xuan ^a   Moon, Sunok ^a   Jung, Ki Hong ^a  

^a Kyung Hee University   (South Korea)

Author keywords

Drought stress in root; Functional gene network; Gene redundancy; Meta profiling analysis

Indexed keywords

AQUAPORIN; WATER;

ARTICLE; DROUGHT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT ROOT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; VALIDATION STUDY;

AQUAPORINS; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; ORYZA SATIVA; PHYLOGENY; PLANT ROOTS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL; WATER;

EID: 84884674556     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1918-9     Document Type: Article

References (66)

1. Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59: 469-484.
2. Boursiac Y, Prak S, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Santoni V, Maurel C (2008) The response of Arabidopsis root water transport to a challenging environment implicates reactive oxygen species- and phosphorylation-dependent internalization of aquaporins. Plant Signal Behav 3: 1096-1098.
3. Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125: 1206-1215.
4. Denker BM, Smith BL, Kuhajda FP, Agre P (1988) Identification, purification, and partial characterization of a novel Mr 28, 000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263: 15634-15642.
5. Eynard A, Lal R, Wiebe K (2005) Crop response in salt-affected soils. J Sustain Agric 27: 5-50.
6. Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15.
7. Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16: 277-286.
8. Hayano-Kanashiro C, Calderon-Vazquez C, Ibarra-Laclette E, Herrera-Estrella L, Simpson J (2009) Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS ONE 4: e7531.
9. 2 transport facilitator. Plant J 67: 795-804.
10. Ishibashi K, Kondo S, Hara S, Morishita Y (2011) The evolutionary aspects of aquaporin family. Am J Physiol Regul Integr Comp Physiol 300: R566-R576.
11. Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579: 5814-5820.
12. 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.
13. Jang JY, Lee SH, Rhee JY, Chung GC, Ahn SJ, Kang H (2007) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol Biol 64: 621-632.
14. Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schaffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15: 509-522.
15. Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153: 185-197.
16. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126: 1358-1369.
17. Johnson BD, Schumacher RJ, Ross ED, Toft DO (1998) Hop modulates Hsp70/Hsp90 interactions in protein folding. J Biol Chem 273: 3679-3686.
18. Jolivet P, Roux E, D'Andrea S, Davanture M, Negroni L, Zivy M, Chardot T (2004) Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 42: 501-509.
19. Josine TL, Ji J, Wang G, Guan CF (2011) Advances in genetic engineering for plants abiotic stress control. Afr J Biotechnol 10: 5402-5413.
20. Jung KH, Lee J, Dardick C, Seo YS, Cao P, Canlas P, Phetsom J, Xu X, Ouyang S, An K, Cho YJ, Lee GC, Lee Y, An G, Ronald PC (2008) Identification and functional analysis of light-responsive unique genes and gene family members in rice. PLoS Genet 4: e1000164.
21. Kaldenhoff R, Fischer M (2006) Aquaporins in plants. Acta Physiol (Oxf) 187: 169-176.
22. Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284: 2114-2120.
23. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
24. Lee I, Seo YS, Coltrane D, Hwang S, Oh T, Marcotte EM, Ronald PC (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc Natl Acad Sci USA 108: 18548-18553.
25. Li GW, Peng YH, Yu X, Zhang MH, Cai WM, Sun WN, Su WA (2008a) Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice. J Plant Physiol 165: 1879-1888.
26. Li GW, Zhang MH, Cai WM, Sun WN, Su WA (2008b) Characterization of OsPIP2;7, a water channel protein in rice. Plant Cell Physiol 49: 1851-1858.
27. Lian HL, Yu X, Ye Q, Ding X, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45: 481-489.
28. Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA (2006) Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 16: 651-660.
29. Liang G, He H, Li Y, Yu D (2012) A new strategy for construction of artificial miRNA vectors in Arabidopsis. Planta 235: 1421-1429.
30. Liu C, Fukumoto T, Matsumoto T, Gena P, Frascaria D, Kaneko T, Katsuhara M, Zhong S, Sun X, Zhu Y, Iwasaki I, Ding X, Calamita G, Kitagawa Y (2013) Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol Biochem 63: 151-158.
31. Lu HA, Sun TX, Matsuzaki T, Yi XH, Eswara J, Bouley R, McKee M, Brown D (2007) Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking. J Biol Chem 282: 28721-28732.
32. Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28: 85-96.
33. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440: 688-691.
34. Matsumoto T, Lian HL, Su WA, Tanaka D, Liu C, Iwasaki I, Kitagawa Y (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50: 216-229.
35. Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol Plant Mol Biol 48: 399-429.
36. Maurel C, Javot H, Lauvergeat V, Gerbeau P, Tournaire C, Santoni V, Heyes J (2002) Molecular physiology of aquaporins in plants. Int Rev Cytol 215: 105-148.
37. Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59: 595-624.
38. Mendonca AG, Alves RJ, Pereira-Leal JB (2011) Loss of genetic redundancy in reductive genome evolution. PLoS Comput Biol 7: e1001082.
39. Mihara M, Itoh T, Izawa T (2010) SALAD database: a motif-based database of protein annotations for plant comparative genomics. Nucleic Acids Res 38: D835-D842.
40. Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138: 1903-1913.
41. Miller EW, Dickinson BC, Chang CJ (2010) Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci USA 107: 15681-15686.
42. Mitani-Ueno N, Yamaji N, Zhao FJ, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62: 4391-4398.
43. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497.
44. Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150: 1368-1379.
45. 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.
46. Pandey S, Bhandari H, Hardy B (2007) Economic costs of drought and rice farmers' coping mechanisms: a cross-country comparative analysis. International Rice Research Institute, Los Baños, p 203.
47. Pang Y, Li L, Ren F, Lu P, Wei P, Cai J, Xin L, Zhang J, Chen J, Wang X (2010) Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J Genet Genomics 37(389-397): 381-382.
48. Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schaffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152: 1418-1430.
49. Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci USA 88: 11110-11114.
50. Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2002) From genome to function: the Arabidopsis aquaporins. Genome Biol 3: RESEARCH0001.
51. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696.
52. Rouard M, Guignon V, Aluome C, Laporte MA, Droc G, Walde C, Zmasek CM, Perin C, Conte MG (2011) GreenPhylDB v2. 0: comparative and functional genomics in plants. Nucleic Acids Res 39: D1095-D1102.
53. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
54. Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46: 1568-1577.
55. Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49: 30-39.
56. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
57. Soto G, Alleva K, Mazzella MA, Amodeo G, Muschietti JP (2008) AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett 582: 4077-4082.
58. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
59. Torres GAM, Gimenes MA, de Rosa Jr VE, Quecini V (2007) Identifying water stress-response mechanisms in citrus by in silico transcriptome analysis. Genet Mol Biol 30: 888-905.
60. van der Schoot C, Paul LK, Paul SB, Rinne PL (2011) Plant lipid bodies and cell-cell signaling: a new role for an old organelle? Plant Signal Behav 6: 1732-1738.
61. Weaver CD, Shomer NH, Louis CF, Roberts DM (1994) Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem 269: 17858-17862.
62. Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114: 1347-1357.
63. Yamaji N, Ma JF (2009) A transporter at the node responsible for intervascular transfer of silicon in rice. Plant Cell 21: 2878-2883.
64. Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20: 1381-1389.
65. Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res 16: 599-608.
66. Zardoya R, Villalba S (2001) A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 52: 391-404.